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Neural Mechanisms of Binaural Processing in the Auditory Brainstem

Tom C.T. Yin, Phil H. Smith, Philip X. Joris

10.1002/cphy.c180036

Source: Volume 9, Issue 4, October 2019

Published online: September 2019

Full Article on Wiley Online Library



Abstract

Spatial hearing, and more specifically the ability to localize sounds in space, is one of the most studied and best understood aspects of hearing. Because there is no coding of acoustic space at the receptor organ, physiological sensitivity to spatial aspects of sounds first emerges in the central nervous system. Much progress has been made in the identification and characterization of the circuits in the auditory brainstem that create sensitivity to binaural and monaural cues toward acoustic space. We review the progress over the past third of a century, with a focus on the mammalian brainstem and on the anatomy and cellular physiology underlying the physiological tuning of monaural and binaural circuits to acoustic cues toward spatial hearing. In addition to examining the detailed mechanisms involved in the processing of the three main spatial cues, we also review the integration of these cues and their use toward behavior. © 2019 American Physiological Society. Compr Physiol 9:1503‐1575, 2019.

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Figure 1. Figure 1. Comparison of FTCs and PSTHs of ANFs with different rates of spontaneous activity. (A) FTCs recorded from cats raised in a low‐noise environment arranged by SR in columns with high SR to the left and low SR to the right and by CF in rows with low at the top and high at the bottom. Low CF are all fibers between 1.9 and 2.2 kHz) and high CFs are between 4.4 and 5 kHz. Each curve is from a different fiber, and each panel plots curves from three to seven different fibers. The individual fibers show remarkable uniformity in shape. The far‐right panel illustrates this uniformity by replotting each of the curves after shifting the medium‐ and low‐SR fibers so the tips of the tuning curves coincide. The amount of shift can be seen from the arrows to the left. Modified, with permission, from Liberman MC, 1978 362. (B) Poststimulus‐time histograms of three ANFs of low (left), medium (middle), and high CF (right) as indicated. The fiber plotted in the middle has high spontaneous activity, while the one to the right has low spontaneous activity. The differences in the initial onset response and adaptation are evident in the PSTHs. The low‐frequency fiber on the left shows the multiple modes corresponding to the frequency of the tone, characteristic of phase‐locking. Modified, with permission, from Kiang NYS, 1984 313.
Figure 2. Figure 2. Phase‐locking of inner hair cell (left) and ANF (right) responses. (A) Intracellular receptor potentials for an inner hair cell of the anesthetized guinea pig to tones at 80 dB SPL varying in frequency from 100 to 5000 Hz. At low frequencies, the cyclic AC component dominates the response, but at higher frequencies, the DC component becomes larger as the AC component disappears above about 3 kHz. The oscillating AC component is responsible for the ANF phase‐locking at low frequencies. The 25‐mV scale bar applies for 100 to 900 Hz; the 12.5 mV applies for the 1000 to 5000 Hz waveforms. Reused, with permission, from Palmer AR and Russell IJ, 1986 489. (B) Period histograms of an auditory‐nerve fiber of the anesthetized squirrel monkey when stimulated with tones from 300 to 1403 Hz, as labeled. The abscissae represent one cycle of the tone, here labeled as the period in microseconds. The vector strength or synchronization index is indicated by its magnitude R and corresponding phase, indicated by the small arrow under each histogram. Note that the decline in R value mirrors the decrease in the AC component in the receptor potential of the IHC (A). The CF of the fiber was about 1100 Hz. Modified, with permission, from Anderson DJ, et al., 1971 19.
Figure 3. Figure 3. Temporal analysis of ANF spike trains in response to multiple repetitions of a broadband noise (70 dB), based on counting of interspike intervals. Each column shows displays for one ANF, ordered from low (left) to high CF (right). The top row (same abscissa as second row) shows all‐order interspike‐interval histograms, in which the time between spikes is measured for all spikes within a spike train (i.e. for each response to a single stimulus repetition). Because these intervals respect a refractory time, the intervals are never shorter than a minimal duration (∼1 ms), resulting in a gap without intervals. This gap obscures the temporal patterning, but it can be appreciated at the lowest CF (550 Hz) that there is a periodicity consistent with the characteristic period (CF−1, here 1.8 ms) and multiples thereof, indicated with dots under the abscissa. The second row shows the complementary histogram, in which all‐order interspike intervals are counted across spiketrains. There is no refractoriness across spiketrains, and a clear temporal pattern is now visible for all CFs, which is dominantly oscillatory (at CF−1) for CFs below 5 kHz and consists of a broad peak for CFs > 5 kHz. These two components reflect phase‐locking to the fine structure of motion of the organ of Corti at low CFs and to envelopes at high CFs. These shuffled autocorrelograms are much smoother than the all‐order interspike‐interval histograms because they allow many permutations between spike trains for the extraction of intervals. The bottom row shows the shuffled autocorrelograms in a format allowing easier comparison with binaural ITD functions by showing the histogram as a function for both forward and backward interspike intervals and by normalizing the ordinate to the total number of spikes. Numbers in top row indicate CF and spontaneous rate. Reused, with permission, from Louage DH, et al., 2004 386.
Figure 4. Figure 4. Coding of stimulus intensity by ANFs in the anesthetized cat. Rate‐level curves of 13 ANFs of tones at CF as indicated in each plot and arranged by CF from top (low) to bottom (high) and with sloping (left) or flat (right) saturation. The spontaneous rate of the fiber and the threshold can be deduced from the lowest SPL used and its discharge rate at that SPL. There is a tendency for cells with flat saturation to have low threshold and high spontaneous activity. Reused, with permission, from Sachs MB and Abbas PJ, 1974 550.
Figure 5. Figure 5. Schematic diagram of the primary cell types and their connections in the cochlear nucleus with its two major subdivisions, the ventral (VCN) and dorsal cochlear nucleus (DCN). Excitatory glutamatergic synaptic endings are shown in green, inhibitory glycinergic terminals in yellow, and inhibitory gamma‐aminobutyric acid (GABAergic) terminals in red. Auditory inputs to the nucleus arrive as type I auditory‐nerve fibers (ANFs, lower right), and the major output projection pathways are the trapezoid body (TB) and the dorsal and intermediate acoustic stria (DAS/IAS), on the left. Electrical synaptic connections are indicated by resistive symbols in the molecular domain of the DCN. Cell types: SBC, spherical bushy cell; GBC, globular bushy cell; RN, nerve root neuron; TS, T‐stellate; DS, D‐stellate; OC, octopus cell; FC, fusiform cell; GC, giant cell; VC, vertical cell; CW, cartwheel cell; BC, basket cell; GoC, Golgi cell; GrC, granule cell; SC, superficial stellate cell; and UBC, unipolar brush cell.
Figure 6. Figure 6. Transformations of the ANF response (on the left) by the five major projection neurons of the cochlear nucleus (right). The PSTHs show the responses to tones at CF, in some cases for both low (phase‐locked) and high CF. The frequency‐tuning curve (FTC) shows areas of excitation (black) and inhibition (dotted lines). In the AVCN, the spherical bushy cells have a primary‐like response, the globular bushy cells have a primary‐like‐with‐notch response, T‐stellate cells have a chopper response with prominent inhibitory side bands in the FTC, octopus cells have an onset response with a wide FTC, and fusiform cells can have pauser or buildup responses and a complex FTC with prominent inhibitory areas.
Figure 7. Figure 7. Circuits in the superior olivary complex (SOC) for computing the interaural cues. (A) The EE circuit involving the MSO that encodes ITDs from excitatory inputs from SBCs of both sides. MSO neurons also receive inhibitory inputs from the contralateral ear relayed through the ipsilateral MNTB and from the ipsilateral ear through the ipsilateral LNTB. (B) The IE circuit involving the LSO that computes ILDs from excitatory inputs from spherical bushy cells on the ipsilateral side and inhibitory inputs from the MNTB. The red to green shading shows the tonotopic organization from low to high frequencies, respectively, in each of the major nuclei. Excitatory glutamatergic cells are shown in green and inhibitory glycinergic cells in red. For simplicity, cell types include principal and nonprincipal cells. The PSTHs show typical responses to tones at CF for the cells adjacent to the histograms. In some cases, two histograms are shown for low and high CF. Abbreviations: MSO, medial superior olive; LSO, lateral superior olive; MNTB, medial nucleus of the trapezoid body; LNTB, lateral nucleus of the trapezoid body; VNTB, ventral nucleus of the trapezoid body.
Figure 8. Figure 8. Drawings of Golgi‐impregnated axons/neurons in coronal sections through the superior olivary complex of the cat. Modified, with permission, from Figures 343, 344, and 345 of Ramon y Cajal S, 1909 516. (A) Axons projecting to the SOC. Midline is to the right edge of the drawing. The prominent calyces of Held in the MNTB are seen near (a), terminals in VNTB near (b), in MSO near (c), in the S‐shaped LSO near (d), and VNTB near (e). (B) Neurons in the LSO. The bipolar principal cells are shown near (a) and an example of a marginal cell near (b). (C) Neurons in the MSO. The bipolar principal cells are shown near (a) and a marginal cell near (b).
Figure 9. Figure 9. Head‐related transfer functions (HRTFs) for the cat. (A) HRTFs for five positions in space varying in azimuth at 0° elevation. At each position, the top traces show the time domain recordings from the left (blue trace) and right (red) ear to a click stimulus from the azimuthal position indicated. The bottom traces are the Fourier transforms of the time domain signal showing the frequency spectrum. (B) HRTFs for five positions varying in elevation at 0° azimuth. Here, the time domain traces are to the left and the spectra to the right in each pair. The midfrequency notch in each spectral plot is indicated by the asterisk. Dotted vertical lines in spectra traces are at 10 kHz for reference. Reused, with permission, from Musicant AD, et al., 1990 449.
Figure 10. Figure 10. The Jeffress model for computing ITDs. Reused, with permission, from Goldberg JM and Brown PB, 1969 199.
Figure 11. Figure 11. Comparison of phase‐locking of ANFs to bushy cells from the anesthetized cat. (A, B) Responses of an ANF to tones at CF (350 Hz) at 70 dB SPL plotted as dot rasters in (A) and period histogram in (B). Each dot indicates the time of occurrence of an action potential relative to stimulus onset at 0 time. Each row represents the response to one of the 200 stimulus presentations of tones of 25 ms duration (waveform seen below C), repeated every 100 ms. Period histograms in (B) of the same responses showing the probability of spikes to occur over a narrow range of stimulus phase angles. The histogram has been shifted on the phase axis so that the mean phase is 0.0 for ease of comparison with (D). Panels (C) and (D): dot rasters and period histograms for a bushy cell recorded from its axon in the trapezoid body with a CF of 340 Hz at 69 dB SPL. (E) Comparison of the maximum synchronization index over stimulus level for ANFs and bushy cells. The two lines indicate the range of Rmax in ANFs reported by Johnson 272, and the data points are for all the bushy cells recorded in the trapezoid body. The bushy cells are designated by SBC or GBC if there were anatomical data on the course of their axons (e.g. GBC projecting to MNTB as calyces of Held and SBC projecting bilaterally to MSO). Otherwise, they are called phase‐locked (PHL) since it is not possible to distinguish primary‐like from primary‐like‐with‐notch responses when they are phase‐locked. The ordinate is plotted on an expansive scale to emphasize the values greater than 0.9, which no ANF ever exceeds. Redrawn, with permission, from Joris PX, et al., 1994 277.
Figure 12. Figure 12. Coincidence detection in the MSO of the anesthetized cat. (A) ITD sensitivity to pure tones at CF (1000 Hz). Positive ITDs represent delays of the ipsilateral tone. Stimulus was 1 repetition of a 5‐s long tone at 60 dB SPL. The arrows labeled C and I on the ordinate indicate the level of response to monaural stimulation of the contralateral and ipsilateral ear, respectively. Downward arrow marks the mean interaural phase φd of the delay curve. Examples of waveform timing are shown below the plot. (B) Period histogram of responses to the same monaural tones to the contralateral ear. Downward arrow marks the mean monaural phase. (C) Period histogram of responses to monaural tones to the ipsilateral ear. Modified, with permission, from Yin TC and Chan JC, 1990 722.
Figure 13. Figure 13. Schematic diagram of the characteristic delay analysis. Each row is meant to illustrate a different type of response. For illustrative purposes, the ITD responses are idealized as linear, triangular responses on the left. Each curve is the response to a different stimulus frequency as shown by the different symbols. To the right is the interaural phase versus frequency plot. (A) Peak response type with CP = 0.0 and CD = +300 μs. (B) Trough response type with CP = 0.5 and CD = −100 μs. (C) Intermediate response type (tweener) with CP = 0.2 and CD = 200 μs. Reused, with permission, from Yin TC and Kuwada S, 1983 727.
Figure 14. Figure 14. Responses of three cells (rows) in the ICC of anesthetized cat that illustrate the three cell types commonly seen. On the left are the superimposed and normalized ITD curves at different frequencies, and on the right are the interaural phase versus frequency plots. CD and CP are as indicated. (A) Peak‐type cell. (B) Trough‐type cell. (C) Intermediate‐type cell. Reused, with permission, from Yin TC and Kuwada S, 1983 727.
Figure 15. Figure 15. Binaural‐beat stimulus and analysis. (A) Plots of the tone stimuli to the ipsilateral and contralateral ears during a binaural‐beat stimulus showing how the interaural phase (φ) changes continuously during the duration of the stimulus. In this case, the contralateral stimulus is higher by fb, so it leads the ipsilateral stimulus during the first half cycle and lags during the second half cycle. The cycle repeats every fb. (B) Schematic diagram of how the stimuli would be perceived, though the perceived position is inside the head rather than externalized as diagrammed. (C) Responses of a cell in the ICC to the binaural‐beat stimulus, in this case with fb = 1 Hz added to the ipsilateral tone. (D) Response of the same cell to ITDs of the same tone. (E) Comparison of the interaural‐phase sensitivity of the cell computed using ITDs (D) and binaural beats (C) plotted as interaural period histograms. Modified, with permission, from Yin TC and Kuwada S, 1983 726.
Figure 16. Figure 16. Comparison of ITD sensitivity to tones and noise in an MSO cell of the anesthetized cat. (A) ITD functions for eight frequencies plotted on a common ITD axis. (B) Response of the same cell to ITDs of noise (asterisks) and to tones (triangles) as computed by the composite curve, which is the sum of its responses to all frequencies. For comparison, the two curves are normalized to their peak response. (C) Characteristic delay analysis of the same cell showing its peak‐type response with CP = 0.63 and CD = 33 μs. Reused, with permission, from Yin TC and Chan JC, 1990 722.
Figure 17. Figure 17. Comparison, for nine ICC cells, of ITDs of noise (solid line, *) and tone composite curves (dashed line, Δ) from the anesthetized cat. Reused, with permission, from Yin TC, et al., 1986 724.
Figure 18. Figure 18. Responses of four ICC cells in the anesthetized cat to ITDs of noise with different interaural correlations. The interaural noise correlation for each curve is indicated in the key. Reused, with permission, from Yin TC, et al., 1987 723.
Figure 19. Figure 19. Stylized distributions (yellow surfaces) of optimal delays (ODs) with a hard boundary (dashed line) at the edge of the physiological range (A) or with a hard π‐limit (B). The middle panels represent a population of MSO (or ICC) neurons: each neuron (circle) is represented according to its OD (abscissa) and best frequency (BF) (ordinate). The top and bottom panels illustrate the corresponding ITD functions for a high‐ and lower BF neuron, respectively, at the edge of the distribution, as would be obtained in response to broadband noise (Figures 16,17,18). The distribution in (A) predicts that neurons with high BF would have a secondary maximum (slipped cycle) that is closer to 0 ITD than the primary maximum at the OD: this is only rarely observed. Experimentally, the largest ODs observed are such that the primary peak of the ITD function (at the OD) is usually the peak closest to 0 ITD. This results in the π‐limit. Modified, with permission, from Joris P and Yin TC, 2007 273.
Figure 20. Figure 20. Intracellular recording from gerbil MSO, in vivo, using the whole‐cell patch recording technique. The top panels show monaural responses to a long ipsilateral (200 Hz) or contralateral (201 Hz) tone at 70 dB SPL. Note that the EPSPs are spike‐like in duration and are subthreshold. There are no obvious IPSPs. The lower panels show two segments of the response when the two tones are now delivered as a binaural‐beat stimulus. When the tones are nearly in‐phase (left), spikes are triggered. When the tones are nearly out‐of‐phase (right), the EPSPs are smaller and remain subthreshold. Reused, with permission, from Franken TP, et al., 2015 177 and unpublished data.
Figure 21. Figure 21. ILD sensitivity of an LSO nonprincipal cell of the anesthetized cat. (A‐D) Dot rasters (top) and PSTHs (bottom) to 20 repetitions of CF tones with four combinations of ILDs obtained by holding the ipsilateral stimulus constant at 30 dB SPL, while the contralateral level varied between 5 dB (A) and 45 dB (D). The 16‐kHz tone was on during the first 300 ms. The inset in (A) shows the first 40 ms of a monaural ipsilateral tone at CF to show the chopping response. (E) Plot of the ILD sensitivity of the cell as mean discharge rate and +1 SEM. Points labeled (A‐D) correspond to the responses above. Dotted line labeled Spon indicates the spontaneous activity, and the vertical dotted line shows the half‐maximal ILD. Reused, with permission, from Tollin DJ and Yin TC, 2002 651.
Figure 22. Figure 22. Spatial receptive field in azimuth of the same LSO cell as in Figure 21 studied using VAS to simulate different spatial positions in azimuth at 0° elevation. (A) At each position, a broadband noise was filtered with the HRTF appropriate for that position in space and delivered to both the ipsilateral and contralateral ears. The dot rasters for 21 azimuthal positions spaced at 4.5° are stacked together and plotted as a function of poststimulus time. The duration of the stimulus was 0 to 200 ms. (B) Same stimulus as in (A) except that the input to the contralateral ear was turned off. (C) Plots of azimuthal receptive field derived from (A) and (B) showing the clear suppressive effect of the contralateral input at all azimuthal positions. Reused, with permission, from Tollin DJ and Yin TC, 2002 651.
Figure 23. Figure 23. Responses of an LSO cell in the anesthetized cat to ITDs and ILDs of clicks. The level of the excitatory ipsilateral click was held constant at 50 dB SPL, while the level of the contralateral click was varied from 30 to 70 dB SPL. Positive ITDs correspond to the excitatory ipsilateral click delayed in time, as shown by the schematic EPSP from the ipsilateral side and IPSP from the contralateral side at the top. The CF of the cell was 5.2 kHz. Traces above the plot illustrate the timing of the ipsilateral EPSP and contralateral IPSP during the three conditions. This cell gave a transient response to ipsilateral tones, and was therefore likely a principal cell. Reused, with permission, from Joris PX and Yin TC, 1995 290.
Figure 24. Figure 24. Test of the latency hypothesis from responses to bilateral click stimuli of cells in the LSO of the anesthetized rat. (A) ILD (or what they call IID) sensitivity function (open circles) and monaural rate‐level curve (solid circles, labeled ipsi alone). The ILD function was obtained with the contralateral SPL at the base level 75 dB and varying the ipsilateral SPL from 50 to 100 dB SPL as shown by the bottom axis. (B) ITD sensitivity of the same cell at 75 dB base in both ears. Positive ITDs indicate that the contralateral inhibitory stimulus leads in time. The ITDs used were chosen from the latency changes recorded from rate‐level curves for the ipsilateral excitatory stimulus (not shown). From this latency‐level function, the equivalent ITDs (ITDe) can be calculated for changes in SPL from the base (top axis in C). (C) Comparison of the ILD function (IID, open circles), with the equivalent ITD function (ITDe, closed circles) and delay‐cancelled ILD (IIDdc, open diamonds) for a cell in which the ILD sensitivity appears to be primarily derived from ITD through the changes in latency with level since the ILD and ITDe curves are similar, while the ILDdc curve is flat. (D) Same comparisons as in (C) for a different cell for which ITD appears not to be important in establishing the ILD sensitivity since the ILD and ILDdc curves are similar, while the ITDe curve is flat. Redrawn, with permission, from Figures 3 and 4 of Irvine DR, et al., 2001 260.
Figure 25. Figure 25. ILD functions in the LSO of the awake mustache bat, Pteronotus parnellii, showing the variation in the threshold for spike inhibition due to the inhibitory contralateral input. The ILD functions were obtained by holding the ipsilateral tone at CF constant, while varying the level of the contralateral inhibitory tone. Reused, with permission, from Park TJ, et al., 1997 498.
Figure 26. Figure 26. Topographic distribution of ILDs in the inferior colliculus of the mustache bat, Pteronotus parnellii. Reconstructions of four electrode penetrations in four different animals showing the systematic change in inhibitory threshold (numbers to the right of symbols) with increasing depth. ILD functions were obtained by setting the contralateral excitatory CF tone to 15 dB above threshold and varying the ipsilateral level. The inhibitory threshold was defined as the half‐maximal ILD. The CFs of multiunit cluster recordings are plotted on the abscissae. The approximate locations of the penetrations on a surface view of the IC are shown to the right, but all penetrations were in different animals. Reused, with permission, from Wenstrup JJ, et al., 1986 688.
Figure 27. Figure 27. Circuitry in DCN to account for the type IV response map. (A) DCN circuitry with respect to inputs to the type IV (fusiform) cells. The heavy horizontal line at the bottom represents the tonotopic input from ANFs with low frequencies to the left. The type II cell is thought to be the vertical cell and the wideband inhibitor (WBI) the D‐stellate cell in Figure 5. MSN (medullary somatic nuclei) represents the somatosensory input from the dorsal column and spinal trigeminal nuclei. Modified, with permission, from Figure 12 of Davis KA and Young ED, 2000 130. (B) Schematic of the tuning curves of the three inputs to the type IV cell that carry acoustic information from ANFs. Inhibitory input from type II cell is shown in red and from the WBI in green, while excitatory input from ANFs is shown in black. Drawn, with permission, from Young ED, et al., 1992 735. (C) Response map of a typical type IV neuron in the DCN of a decerebrate cat. Plots of spike activity as a function of frequency for nine different attenuation levels are shown modulated about the spontaneous activity (horizontal line in each plot). Inhibition is plotted below the spontaneous rate and is coded by the same shading as in (B). The CF of the neuron is 7.41 kHz. Modified, with permission, from Figure 2C of Spirou GA and Young ED, 1991 622.
Figure 28. Figure 28. Sensitivity of a type IV neuron in the DCN of a decerebrate cat to the frequency of a spectral notch. (A) Power spectrum of three stimuli of broadband noise filtered through a simulated HRTF spectral notch at different notch frequencies. (B) Response map of a type IV neuron tested with the notch filtered noises. The stimulus labeled c has a notch frequency that corresponds to the CF (11.6 kHz) of the type IV cell, shown by the downward arrow. Shading convention same as in Figure 27. (A) and (B) have a common frequency axis. (C, D) Responses of the cell to variations in stimulus level for the five different spectral notch frequencies. Modified, with permission, from Figure 5 of Young ED, et al., 1997 733.
Figure 29. Figure 29. Study of an IC neuron in the anesthetized guinea pig to test for convergent input. (A) Interaural phase versus frequency plot showing an intermediate CP = 0.2. (B) Superimposed ITD plots at 10 different frequencies. (C) PSTH of the responses to a 3‐s binaural beat at the CF of 250 Hz (histogram) and in the presence of suppressor tones at the two ears of 100 Hz (heavy line). The suppressor tone was chosen to have an unfavorable ITD at 100 Hz. (D‐H) Similar responses as in (C) at five other frequencies with the same suppressor tones. Here, the data are plotted as interaural‐phase period histograms for the binaural‐beat stimulus at the indicated frequencies. The 100‐Hz tone at an unfavorable ITD suppresses the interaural‐phase sensitivity at the lowest frequencies (E, 150 Hz) and phaseshifts the responses at higher frequencies. (I) Interaural phase versus frequency plot for the original unsuppressed responses (open squares and closed circles) and in the presence of the 100‐Hz suppressor (open circles). (J) ITD curves for the five highest frequencies in the presence of the low‐frequency suppressor show a peak‐type response as suggested by the phase‐frequency plot for these frequencies in (I). Reused, with permission, from McAlpine D, et al., 1998 420.
Figure 30. Figure 30. The precedence effect (PE). (A) Typical arrangement of studies of the PE using free field stimuli. A cat is positioned between two speakers (a) and (b). Identical stimuli, usually clicks or transients, are delivered to the speakers with an interstimulus delay (ISD) between the stimuli. When ISD = 0, the subject perceives the click to arise from a phantom source directly in front. (B) Plots of the perceived azimuth as a function of ISD. Three intervals of ISD are identified: summing localization, the period of the PE, and ISDs longer than the echo threshold (breakdown of fusion) when both clicks are heard and localized. Adapted, with permission, from Blauert J, 1997 51. (C) Behavioral measurements of localization in cats trained to direct their gaze to the location of sound sources. In this case, the speakers (a) and (b) were positioned at +18° and −18°, respectively, as shown by the arrows to the far right. With the head restrained, cats undershoot the acoustic targets. In this case, the apparent locations of “a” and “b” show the degree of undershoot. All three components of the PE are seen in cats. Reused, with permission, from Tollin DJ, et al., 2004 648.
Figure 31. Figure 31. Responses of a cell in the ICC of the anesthetized cat to stimuli mimicking the PE. (A) Spatial receptive field of the cell for single clicks varying in azimuth in the frontal hemifield. The locations of the two speakers used during PE stimuli are shown by the downward arrows. (B) Plots of the responses of the cell to PE stimuli, with a click to speakers at ±45° with variable interclick delays (ICDs). Positive ICDs correspond to the click to speaker (a) leading. Spikes during two different time periods are plotted: those occurring from 12 to 18 ms following the leading click (dashed line) and those during the 0 to 150 ms period (solid line). Error bars indicate +1 SEM over 50 repetitions. (C) Dot rasters of the responses to the PE stimuli. The ICD for each set of stimuli is indicated to the right. When the (b) speaker is leading (negative ICDs in lower section), the suppression of the lagging click to speaker (a) is apparent as the ICD is decreased from 100 to 2 ms. When the (a) speaker is leading, there is partial suppression of the response to the lagging (b) speaker even when the ICD is 100 ms and complete suppression for all other ICDs shown. Reused, with permission, from Yin TC, 1994 720.
Figure 32. Figure 32. Binaural masking‐level differences (BMLDs). Schematic diagram of the BMLD and its counterintuitive results from adding noise (bottom trace) or signal (tone trace). The frowning subject indicates difficulty in detecting the tone signal, while smiling means the signal is more easily detected. The nomenclature for describing the different stimulus conditions is shown in the right column, where N stands for noise, S for signal, the subscript m designates monaural, and o and π mean either in‐phase or out‐of‐phase, respectively. (A) Monaural signal and noise to one ear is difficult to detect. (B) Adding noise to the other ear now makes the signal more detectable. (C) Adding the signal to the other ear makes the signal difficult to detect. (D) Inverting the phase of the signal makes it detectable. Adapted, with permission, from Moore BCJ, 1982 436.
Figure 33. Figure 33. Studies of BMLDs in the ICC of anesthetized guinea pigs. Responses from three different cells (rows) are shown. In each row, the left‐hand plot is the ITD sensitivity for broadband noise. In the middle are interaural period histograms of the responses to binaural beats at CF. On the right are responses to stimuli mimicking the BMLD paradigm showing the responses plotted as D′ values of the detectability of the 500‐Hz tone with a constant noise masker as a function of the level of the tone. The two plots in each graph show the NoSo (solid circles) and NoSπ (open circles) configurations. (A) Cell shows a positive BMLD in which adding signal in‐phase causes an increase in discharge, while adding signal out‐of‐phase causes a decrease. (B) Cell shows a positive BMLD, where adding signal in‐ or out‐of‐phase both causes an increase in response. (C) Cell shows a negative BMLD, where adding signal in‐ or out‐of‐phase causes an increase in discharge. Modified, with permission, from Figures 4,5,6 of Jiang D, et al., 1997 270.
Figure 34. Figure 34. Studies of spatial release from masking in the ICC of anesthetized cats. Virtual acoustic space techniques were used to simulate sounds in free field but delivered over head phones. The top row shows the stimulus configuration. The stimulus (S) was a train of broadband chirps at 40 Hz repetition, while the noise (N) was broadband and continuous. The virtual positions of S and N are either at +90° or −90°. This cell had a CF of 740 Hz and responded best at +90°. Bottom row shows dot rasters as a function of noise level. In each condition, the signal was on from 0 to 200 ms, while the noise was continuous. Reused, with permission, from Lane CC and Delgutte B, 2005 351.


Figure 1. Comparison of FTCs and PSTHs of ANFs with different rates of spontaneous activity. (A) FTCs recorded from cats raised in a low‐noise environment arranged by SR in columns with high SR to the left and low SR to the right and by CF in rows with low at the top and high at the bottom. Low CF are all fibers between 1.9 and 2.2 kHz) and high CFs are between 4.4 and 5 kHz. Each curve is from a different fiber, and each panel plots curves from three to seven different fibers. The individual fibers show remarkable uniformity in shape. The far‐right panel illustrates this uniformity by replotting each of the curves after shifting the medium‐ and low‐SR fibers so the tips of the tuning curves coincide. The amount of shift can be seen from the arrows to the left. Modified, with permission, from Liberman MC, 1978 362. (B) Poststimulus‐time histograms of three ANFs of low (left), medium (middle), and high CF (right) as indicated. The fiber plotted in the middle has high spontaneous activity, while the one to the right has low spontaneous activity. The differences in the initial onset response and adaptation are evident in the PSTHs. The low‐frequency fiber on the left shows the multiple modes corresponding to the frequency of the tone, characteristic of phase‐locking. Modified, with permission, from Kiang NYS, 1984 313.


Figure 2. Phase‐locking of inner hair cell (left) and ANF (right) responses. (A) Intracellular receptor potentials for an inner hair cell of the anesthetized guinea pig to tones at 80 dB SPL varying in frequency from 100 to 5000 Hz. At low frequencies, the cyclic AC component dominates the response, but at higher frequencies, the DC component becomes larger as the AC component disappears above about 3 kHz. The oscillating AC component is responsible for the ANF phase‐locking at low frequencies. The 25‐mV scale bar applies for 100 to 900 Hz; the 12.5 mV applies for the 1000 to 5000 Hz waveforms. Reused, with permission, from Palmer AR and Russell IJ, 1986 489. (B) Period histograms of an auditory‐nerve fiber of the anesthetized squirrel monkey when stimulated with tones from 300 to 1403 Hz, as labeled. The abscissae represent one cycle of the tone, here labeled as the period in microseconds. The vector strength or synchronization index is indicated by its magnitude R and corresponding phase, indicated by the small arrow under each histogram. Note that the decline in R value mirrors the decrease in the AC component in the receptor potential of the IHC (A). The CF of the fiber was about 1100 Hz. Modified, with permission, from Anderson DJ, et al., 1971 19.


Figure 3. Temporal analysis of ANF spike trains in response to multiple repetitions of a broadband noise (70 dB), based on counting of interspike intervals. Each column shows displays for one ANF, ordered from low (left) to high CF (right). The top row (same abscissa as second row) shows all‐order interspike‐interval histograms, in which the time between spikes is measured for all spikes within a spike train (i.e. for each response to a single stimulus repetition). Because these intervals respect a refractory time, the intervals are never shorter than a minimal duration (∼1 ms), resulting in a gap without intervals. This gap obscures the temporal patterning, but it can be appreciated at the lowest CF (550 Hz) that there is a periodicity consistent with the characteristic period (CF−1, here 1.8 ms) and multiples thereof, indicated with dots under the abscissa. The second row shows the complementary histogram, in which all‐order interspike intervals are counted across spiketrains. There is no refractoriness across spiketrains, and a clear temporal pattern is now visible for all CFs, which is dominantly oscillatory (at CF−1) for CFs below 5 kHz and consists of a broad peak for CFs > 5 kHz. These two components reflect phase‐locking to the fine structure of motion of the organ of Corti at low CFs and to envelopes at high CFs. These shuffled autocorrelograms are much smoother than the all‐order interspike‐interval histograms because they allow many permutations between spike trains for the extraction of intervals. The bottom row shows the shuffled autocorrelograms in a format allowing easier comparison with binaural ITD functions by showing the histogram as a function for both forward and backward interspike intervals and by normalizing the ordinate to the total number of spikes. Numbers in top row indicate CF and spontaneous rate. Reused, with permission, from Louage DH, et al., 2004 386.


Figure 4. Coding of stimulus intensity by ANFs in the anesthetized cat. Rate‐level curves of 13 ANFs of tones at CF as indicated in each plot and arranged by CF from top (low) to bottom (high) and with sloping (left) or flat (right) saturation. The spontaneous rate of the fiber and the threshold can be deduced from the lowest SPL used and its discharge rate at that SPL. There is a tendency for cells with flat saturation to have low threshold and high spontaneous activity. Reused, with permission, from Sachs MB and Abbas PJ, 1974 550.


Figure 5. Schematic diagram of the primary cell types and their connections in the cochlear nucleus with its two major subdivisions, the ventral (VCN) and dorsal cochlear nucleus (DCN). Excitatory glutamatergic synaptic endings are shown in green, inhibitory glycinergic terminals in yellow, and inhibitory gamma‐aminobutyric acid (GABAergic) terminals in red. Auditory inputs to the nucleus arrive as type I auditory‐nerve fibers (ANFs, lower right), and the major output projection pathways are the trapezoid body (TB) and the dorsal and intermediate acoustic stria (DAS/IAS), on the left. Electrical synaptic connections are indicated by resistive symbols in the molecular domain of the DCN. Cell types: SBC, spherical bushy cell; GBC, globular bushy cell; RN, nerve root neuron; TS, T‐stellate; DS, D‐stellate; OC, octopus cell; FC, fusiform cell; GC, giant cell; VC, vertical cell; CW, cartwheel cell; BC, basket cell; GoC, Golgi cell; GrC, granule cell; SC, superficial stellate cell; and UBC, unipolar brush cell.


Figure 6. Transformations of the ANF response (on the left) by the five major projection neurons of the cochlear nucleus (right). The PSTHs show the responses to tones at CF, in some cases for both low (phase‐locked) and high CF. The frequency‐tuning curve (FTC) shows areas of excitation (black) and inhibition (dotted lines). In the AVCN, the spherical bushy cells have a primary‐like response, the globular bushy cells have a primary‐like‐with‐notch response, T‐stellate cells have a chopper response with prominent inhibitory side bands in the FTC, octopus cells have an onset response with a wide FTC, and fusiform cells can have pauser or buildup responses and a complex FTC with prominent inhibitory areas.


Figure 7. Circuits in the superior olivary complex (SOC) for computing the interaural cues. (A) The EE circuit involving the MSO that encodes ITDs from excitatory inputs from SBCs of both sides. MSO neurons also receive inhibitory inputs from the contralateral ear relayed through the ipsilateral MNTB and from the ipsilateral ear through the ipsilateral LNTB. (B) The IE circuit involving the LSO that computes ILDs from excitatory inputs from spherical bushy cells on the ipsilateral side and inhibitory inputs from the MNTB. The red to green shading shows the tonotopic organization from low to high frequencies, respectively, in each of the major nuclei. Excitatory glutamatergic cells are shown in green and inhibitory glycinergic cells in red. For simplicity, cell types include principal and nonprincipal cells. The PSTHs show typical responses to tones at CF for the cells adjacent to the histograms. In some cases, two histograms are shown for low and high CF. Abbreviations: MSO, medial superior olive; LSO, lateral superior olive; MNTB, medial nucleus of the trapezoid body; LNTB, lateral nucleus of the trapezoid body; VNTB, ventral nucleus of the trapezoid body.


Figure 8. Drawings of Golgi‐impregnated axons/neurons in coronal sections through the superior olivary complex of the cat. Modified, with permission, from Figures 343, 344, and 345 of Ramon y Cajal S, 1909 516. (A) Axons projecting to the SOC. Midline is to the right edge of the drawing. The prominent calyces of Held in the MNTB are seen near (a), terminals in VNTB near (b), in MSO near (c), in the S‐shaped LSO near (d), and VNTB near (e). (B) Neurons in the LSO. The bipolar principal cells are shown near (a) and an example of a marginal cell near (b). (C) Neurons in the MSO. The bipolar principal cells are shown near (a) and a marginal cell near (b).


Figure 9. Head‐related transfer functions (HRTFs) for the cat. (A) HRTFs for five positions in space varying in azimuth at 0° elevation. At each position, the top traces show the time domain recordings from the left (blue trace) and right (red) ear to a click stimulus from the azimuthal position indicated. The bottom traces are the Fourier transforms of the time domain signal showing the frequency spectrum. (B) HRTFs for five positions varying in elevation at 0° azimuth. Here, the time domain traces are to the left and the spectra to the right in each pair. The midfrequency notch in each spectral plot is indicated by the asterisk. Dotted vertical lines in spectra traces are at 10 kHz for reference. Reused, with permission, from Musicant AD, et al., 1990 449.


Figure 10. The Jeffress model for computing ITDs. Reused, with permission, from Goldberg JM and Brown PB, 1969 199.


Figure 11. Comparison of phase‐locking of ANFs to bushy cells from the anesthetized cat. (A, B) Responses of an ANF to tones at CF (350 Hz) at 70 dB SPL plotted as dot rasters in (A) and period histogram in (B). Each dot indicates the time of occurrence of an action potential relative to stimulus onset at 0 time. Each row represents the response to one of the 200 stimulus presentations of tones of 25 ms duration (waveform seen below C), repeated every 100 ms. Period histograms in (B) of the same responses showing the probability of spikes to occur over a narrow range of stimulus phase angles. The histogram has been shifted on the phase axis so that the mean phase is 0.0 for ease of comparison with (D). Panels (C) and (D): dot rasters and period histograms for a bushy cell recorded from its axon in the trapezoid body with a CF of 340 Hz at 69 dB SPL. (E) Comparison of the maximum synchronization index over stimulus level for ANFs and bushy cells. The two lines indicate the range of Rmax in ANFs reported by Johnson 272, and the data points are for all the bushy cells recorded in the trapezoid body. The bushy cells are designated by SBC or GBC if there were anatomical data on the course of their axons (e.g. GBC projecting to MNTB as calyces of Held and SBC projecting bilaterally to MSO). Otherwise, they are called phase‐locked (PHL) since it is not possible to distinguish primary‐like from primary‐like‐with‐notch responses when they are phase‐locked. The ordinate is plotted on an expansive scale to emphasize the values greater than 0.9, which no ANF ever exceeds. Redrawn, with permission, from Joris PX, et al., 1994 277.


Figure 12. Coincidence detection in the MSO of the anesthetized cat. (A) ITD sensitivity to pure tones at CF (1000 Hz). Positive ITDs represent delays of the ipsilateral tone. Stimulus was 1 repetition of a 5‐s long tone at 60 dB SPL. The arrows labeled C and I on the ordinate indicate the level of response to monaural stimulation of the contralateral and ipsilateral ear, respectively. Downward arrow marks the mean interaural phase φd of the delay curve. Examples of waveform timing are shown below the plot. (B) Period histogram of responses to the same monaural tones to the contralateral ear. Downward arrow marks the mean monaural phase. (C) Period histogram of responses to monaural tones to the ipsilateral ear. Modified, with permission, from Yin TC and Chan JC, 1990 722.


Figure 13. Schematic diagram of the characteristic delay analysis. Each row is meant to illustrate a different type of response. For illustrative purposes, the ITD responses are idealized as linear, triangular responses on the left. Each curve is the response to a different stimulus frequency as shown by the different symbols. To the right is the interaural phase versus frequency plot. (A) Peak response type with CP = 0.0 and CD = +300 μs. (B) Trough response type with CP = 0.5 and CD = −100 μs. (C) Intermediate response type (tweener) with CP = 0.2 and CD = 200 μs. Reused, with permission, from Yin TC and Kuwada S, 1983 727.


Figure 14. Responses of three cells (rows) in the ICC of anesthetized cat that illustrate the three cell types commonly seen. On the left are the superimposed and normalized ITD curves at different frequencies, and on the right are the interaural phase versus frequency plots. CD and CP are as indicated. (A) Peak‐type cell. (B) Trough‐type cell. (C) Intermediate‐type cell. Reused, with permission, from Yin TC and Kuwada S, 1983 727.


Figure 15. Binaural‐beat stimulus and analysis. (A) Plots of the tone stimuli to the ipsilateral and contralateral ears during a binaural‐beat stimulus showing how the interaural phase (φ) changes continuously during the duration of the stimulus. In this case, the contralateral stimulus is higher by fb, so it leads the ipsilateral stimulus during the first half cycle and lags during the second half cycle. The cycle repeats every fb. (B) Schematic diagram of how the stimuli would be perceived, though the perceived position is inside the head rather than externalized as diagrammed. (C) Responses of a cell in the ICC to the binaural‐beat stimulus, in this case with fb = 1 Hz added to the ipsilateral tone. (D) Response of the same cell to ITDs of the same tone. (E) Comparison of the interaural‐phase sensitivity of the cell computed using ITDs (D) and binaural beats (C) plotted as interaural period histograms. Modified, with permission, from Yin TC and Kuwada S, 1983 726.


Figure 16. Comparison of ITD sensitivity to tones and noise in an MSO cell of the anesthetized cat. (A) ITD functions for eight frequencies plotted on a common ITD axis. (B) Response of the same cell to ITDs of noise (asterisks) and to tones (triangles) as computed by the composite curve, which is the sum of its responses to all frequencies. For comparison, the two curves are normalized to their peak response. (C) Characteristic delay analysis of the same cell showing its peak‐type response with CP = 0.63 and CD = 33 μs. Reused, with permission, from Yin TC and Chan JC, 1990 722.


Figure 17. Comparison, for nine ICC cells, of ITDs of noise (solid line, *) and tone composite curves (dashed line, Δ) from the anesthetized cat. Reused, with permission, from Yin TC, et al., 1986 724.


Figure 18. Responses of four ICC cells in the anesthetized cat to ITDs of noise with different interaural correlations. The interaural noise correlation for each curve is indicated in the key. Reused, with permission, from Yin TC, et al., 1987 723.


Figure 19. Stylized distributions (yellow surfaces) of optimal delays (ODs) with a hard boundary (dashed line) at the edge of the physiological range (A) or with a hard π‐limit (B). The middle panels represent a population of MSO (or ICC) neurons: each neuron (circle) is represented according to its OD (abscissa) and best frequency (BF) (ordinate). The top and bottom panels illustrate the corresponding ITD functions for a high‐ and lower BF neuron, respectively, at the edge of the distribution, as would be obtained in response to broadband noise (Figures 16,17,18). The distribution in (A) predicts that neurons with high BF would have a secondary maximum (slipped cycle) that is closer to 0 ITD than the primary maximum at the OD: this is only rarely observed. Experimentally, the largest ODs observed are such that the primary peak of the ITD function (at the OD) is usually the peak closest to 0 ITD. This results in the π‐limit. Modified, with permission, from Joris P and Yin TC, 2007 273.


Figure 20. Intracellular recording from gerbil MSO, in vivo, using the whole‐cell patch recording technique. The top panels show monaural responses to a long ipsilateral (200 Hz) or contralateral (201 Hz) tone at 70 dB SPL. Note that the EPSPs are spike‐like in duration and are subthreshold. There are no obvious IPSPs. The lower panels show two segments of the response when the two tones are now delivered as a binaural‐beat stimulus. When the tones are nearly in‐phase (left), spikes are triggered. When the tones are nearly out‐of‐phase (right), the EPSPs are smaller and remain subthreshold. Reused, with permission, from Franken TP, et al., 2015 177 and unpublished data.


Figure 21. ILD sensitivity of an LSO nonprincipal cell of the anesthetized cat. (A‐D) Dot rasters (top) and PSTHs (bottom) to 20 repetitions of CF tones with four combinations of ILDs obtained by holding the ipsilateral stimulus constant at 30 dB SPL, while the contralateral level varied between 5 dB (A) and 45 dB (D). The 16‐kHz tone was on during the first 300 ms. The inset in (A) shows the first 40 ms of a monaural ipsilateral tone at CF to show the chopping response. (E) Plot of the ILD sensitivity of the cell as mean discharge rate and +1 SEM. Points labeled (A‐D) correspond to the responses above. Dotted line labeled Spon indicates the spontaneous activity, and the vertical dotted line shows the half‐maximal ILD. Reused, with permission, from Tollin DJ and Yin TC, 2002 651.


Figure 22. Spatial receptive field in azimuth of the same LSO cell as in Figure 21 studied using VAS to simulate different spatial positions in azimuth at 0° elevation. (A) At each position, a broadband noise was filtered with the HRTF appropriate for that position in space and delivered to both the ipsilateral and contralateral ears. The dot rasters for 21 azimuthal positions spaced at 4.5° are stacked together and plotted as a function of poststimulus time. The duration of the stimulus was 0 to 200 ms. (B) Same stimulus as in (A) except that the input to the contralateral ear was turned off. (C) Plots of azimuthal receptive field derived from (A) and (B) showing the clear suppressive effect of the contralateral input at all azimuthal positions. Reused, with permission, from Tollin DJ and Yin TC, 2002 651.


Figure 23. Responses of an LSO cell in the anesthetized cat to ITDs and ILDs of clicks. The level of the excitatory ipsilateral click was held constant at 50 dB SPL, while the level of the contralateral click was varied from 30 to 70 dB SPL. Positive ITDs correspond to the excitatory ipsilateral click delayed in time, as shown by the schematic EPSP from the ipsilateral side and IPSP from the contralateral side at the top. The CF of the cell was 5.2 kHz. Traces above the plot illustrate the timing of the ipsilateral EPSP and contralateral IPSP during the three conditions. This cell gave a transient response to ipsilateral tones, and was therefore likely a principal cell. Reused, with permission, from Joris PX and Yin TC, 1995 290.


Figure 24. Test of the latency hypothesis from responses to bilateral click stimuli of cells in the LSO of the anesthetized rat. (A) ILD (or what they call IID) sensitivity function (open circles) and monaural rate‐level curve (solid circles, labeled ipsi alone). The ILD function was obtained with the contralateral SPL at the base level 75 dB and varying the ipsilateral SPL from 50 to 100 dB SPL as shown by the bottom axis. (B) ITD sensitivity of the same cell at 75 dB base in both ears. Positive ITDs indicate that the contralateral inhibitory stimulus leads in time. The ITDs used were chosen from the latency changes recorded from rate‐level curves for the ipsilateral excitatory stimulus (not shown). From this latency‐level function, the equivalent ITDs (ITDe) can be calculated for changes in SPL from the base (top axis in C). (C) Comparison of the ILD function (IID, open circles), with the equivalent ITD function (ITDe, closed circles) and delay‐cancelled ILD (IIDdc, open diamonds) for a cell in which the ILD sensitivity appears to be primarily derived from ITD through the changes in latency with level since the ILD and ITDe curves are similar, while the ILDdc curve is flat. (D) Same comparisons as in (C) for a different cell for which ITD appears not to be important in establishing the ILD sensitivity since the ILD and ILDdc curves are similar, while the ITDe curve is flat. Redrawn, with permission, from Figures 3 and 4 of Irvine DR, et al., 2001 260.


Figure 25. ILD functions in the LSO of the awake mustache bat, Pteronotus parnellii, showing the variation in the threshold for spike inhibition due to the inhibitory contralateral input. The ILD functions were obtained by holding the ipsilateral tone at CF constant, while varying the level of the contralateral inhibitory tone. Reused, with permission, from Park TJ, et al., 1997 498.


Figure 26. Topographic distribution of ILDs in the inferior colliculus of the mustache bat, Pteronotus parnellii. Reconstructions of four electrode penetrations in four different animals showing the systematic change in inhibitory threshold (numbers to the right of symbols) with increasing depth. ILD functions were obtained by setting the contralateral excitatory CF tone to 15 dB above threshold and varying the ipsilateral level. The inhibitory threshold was defined as the half‐maximal ILD. The CFs of multiunit cluster recordings are plotted on the abscissae. The approximate locations of the penetrations on a surface view of the IC are shown to the right, but all penetrations were in different animals. Reused, with permission, from Wenstrup JJ, et al., 1986 688.


Figure 27. Circuitry in DCN to account for the type IV response map. (A) DCN circuitry with respect to inputs to the type IV (fusiform) cells. The heavy horizontal line at the bottom represents the tonotopic input from ANFs with low frequencies to the left. The type II cell is thought to be the vertical cell and the wideband inhibitor (WBI) the D‐stellate cell in Figure 5. MSN (medullary somatic nuclei) represents the somatosensory input from the dorsal column and spinal trigeminal nuclei. Modified, with permission, from Figure 12 of Davis KA and Young ED, 2000 130. (B) Schematic of the tuning curves of the three inputs to the type IV cell that carry acoustic information from ANFs. Inhibitory input from type II cell is shown in red and from the WBI in green, while excitatory input from ANFs is shown in black. Drawn, with permission, from Young ED, et al., 1992 735. (C) Response map of a typical type IV neuron in the DCN of a decerebrate cat. Plots of spike activity as a function of frequency for nine different attenuation levels are shown modulated about the spontaneous activity (horizontal line in each plot). Inhibition is plotted below the spontaneous rate and is coded by the same shading as in (B). The CF of the neuron is 7.41 kHz. Modified, with permission, from Figure 2C of Spirou GA and Young ED, 1991 622.


Figure 28. Sensitivity of a type IV neuron in the DCN of a decerebrate cat to the frequency of a spectral notch. (A) Power spectrum of three stimuli of broadband noise filtered through a simulated HRTF spectral notch at different notch frequencies. (B) Response map of a type IV neuron tested with the notch filtered noises. The stimulus labeled c has a notch frequency that corresponds to the CF (11.6 kHz) of the type IV cell, shown by the downward arrow. Shading convention same as in Figure 27. (A) and (B) have a common frequency axis. (C, D) Responses of the cell to variations in stimulus level for the five different spectral notch frequencies. Modified, with permission, from Figure 5 of Young ED, et al., 1997 733.


Figure 29. Study of an IC neuron in the anesthetized guinea pig to test for convergent input. (A) Interaural phase versus frequency plot showing an intermediate CP = 0.2. (B) Superimposed ITD plots at 10 different frequencies. (C) PSTH of the responses to a 3‐s binaural beat at the CF of 250 Hz (histogram) and in the presence of suppressor tones at the two ears of 100 Hz (heavy line). The suppressor tone was chosen to have an unfavorable ITD at 100 Hz. (D‐H) Similar responses as in (C) at five other frequencies with the same suppressor tones. Here, the data are plotted as interaural‐phase period histograms for the binaural‐beat stimulus at the indicated frequencies. The 100‐Hz tone at an unfavorable ITD suppresses the interaural‐phase sensitivity at the lowest frequencies (E, 150 Hz) and phaseshifts the responses at higher frequencies. (I) Interaural phase versus frequency plot for the original unsuppressed responses (open squares and closed circles) and in the presence of the 100‐Hz suppressor (open circles). (J) ITD curves for the five highest frequencies in the presence of the low‐frequency suppressor show a peak‐type response as suggested by the phase‐frequency plot for these frequencies in (I). Reused, with permission, from McAlpine D, et al., 1998 420.


Figure 30. The precedence effect (PE). (A) Typical arrangement of studies of the PE using free field stimuli. A cat is positioned between two speakers (a) and (b). Identical stimuli, usually clicks or transients, are delivered to the speakers with an interstimulus delay (ISD) between the stimuli. When ISD = 0, the subject perceives the click to arise from a phantom source directly in front. (B) Plots of the perceived azimuth as a function of ISD. Three intervals of ISD are identified: summing localization, the period of the PE, and ISDs longer than the echo threshold (breakdown of fusion) when both clicks are heard and localized. Adapted, with permission, from Blauert J, 1997 51. (C) Behavioral measurements of localization in cats trained to direct their gaze to the location of sound sources. In this case, the speakers (a) and (b) were positioned at +18° and −18°, respectively, as shown by the arrows to the far right. With the head restrained, cats undershoot the acoustic targets. In this case, the apparent locations of “a” and “b” show the degree of undershoot. All three components of the PE are seen in cats. Reused, with permission, from Tollin DJ, et al., 2004 648.


Figure 31. Responses of a cell in the ICC of the anesthetized cat to stimuli mimicking the PE. (A) Spatial receptive field of the cell for single clicks varying in azimuth in the frontal hemifield. The locations of the two speakers used during PE stimuli are shown by the downward arrows. (B) Plots of the responses of the cell to PE stimuli, with a click to speakers at ±45° with variable interclick delays (ICDs). Positive ICDs correspond to the click to speaker (a) leading. Spikes during two different time periods are plotted: those occurring from 12 to 18 ms following the leading click (dashed line) and those during the 0 to 150 ms period (solid line). Error bars indicate +1 SEM over 50 repetitions. (C) Dot rasters of the responses to the PE stimuli. The ICD for each set of stimuli is indicated to the right. When the (b) speaker is leading (negative ICDs in lower section), the suppression of the lagging click to speaker (a) is apparent as the ICD is decreased from 100 to 2 ms. When the (a) speaker is leading, there is partial suppression of the response to the lagging (b) speaker even when the ICD is 100 ms and complete suppression for all other ICDs shown. Reused, with permission, from Yin TC, 1994 720.


Figure 32. Binaural masking‐level differences (BMLDs). Schematic diagram of the BMLD and its counterintuitive results from adding noise (bottom trace) or signal (tone trace). The frowning subject indicates difficulty in detecting the tone signal, while smiling means the signal is more easily detected. The nomenclature for describing the different stimulus conditions is shown in the right column, where N stands for noise, S for signal, the subscript m designates monaural, and o and π mean either in‐phase or out‐of‐phase, respectively. (A) Monaural signal and noise to one ear is difficult to detect. (B) Adding noise to the other ear now makes the signal more detectable. (C) Adding the signal to the other ear makes the signal difficult to detect. (D) Inverting the phase of the signal makes it detectable. Adapted, with permission, from Moore BCJ, 1982 436.


Figure 33. Studies of BMLDs in the ICC of anesthetized guinea pigs. Responses from three different cells (rows) are shown. In each row, the left‐hand plot is the ITD sensitivity for broadband noise. In the middle are interaural period histograms of the responses to binaural beats at CF. On the right are responses to stimuli mimicking the BMLD paradigm showing the responses plotted as D′ values of the detectability of the 500‐Hz tone with a constant noise masker as a function of the level of the tone. The two plots in each graph show the NoSo (solid circles) and NoSπ (open circles) configurations. (A) Cell shows a positive BMLD in which adding signal in‐phase causes an increase in discharge, while adding signal out‐of‐phase causes a decrease. (B) Cell shows a positive BMLD, where adding signal in‐ or out‐of‐phase both causes an increase in response. (C) Cell shows a negative BMLD, where adding signal in‐ or out‐of‐phase causes an increase in discharge. Modified, with permission, from Figures 4,5,6 of Jiang D, et al., 1997 270.


Figure 34. Studies of spatial release from masking in the ICC of anesthetized cats. Virtual acoustic space techniques were used to simulate sounds in free field but delivered over head phones. The top row shows the stimulus configuration. The stimulus (S) was a train of broadband chirps at 40 Hz repetition, while the noise (N) was broadband and continuous. The virtual positions of S and N are either at +90° or −90°. This cell had a CF of 740 Hz and responded best at +90°. Bottom row shows dot rasters as a function of noise level. In each condition, the signal was on from 0 to 200 ms, while the noise was continuous. Reused, with permission, from Lane CC and Delgutte B, 2005 351.
References
 1. Adam TJ , Finlayson PG , Schwarz DW . Membrane properties of principal neurons of the lateral superior olive. J Neurophysiol 86: 922‐934, 2001.
 2. Adam TJ , Schwarz DW , Finlayson PG . Firing properties of chopper and delay neurons in the lateral superior olive of the rat. Exp Brain Res 124: 489‐502, 1999.
 3. Adams JC . Ascending projections to the inferior colliculus. J Comp Neurol 183: 519‐538, 1979. DOI: 10.1002/cne.901830305.
 4. Adams JC . Cytology of periolivary cells and the organization of their projections in the cat. J Comp Neurol 215: 275‐289, 1983. DOI: 10.1002/cne.902150304.
 5. Adams JC . Neural circuits in the human auditory brainstem. In: Ainsworth WA , Greenberg S , editors. Auditory Basis of Speech Perception. Keele, UK: Keele University, 1996, p. 39‐44.
 6. Adams JC , Mugnaini E . Dorsal nucleus of the lateral lemniscus: a nucleus of GABAergic projection neurons. Brain Res Bull 13: 585‐590, 1984.
 7. Adams JC , Mugnaini E . Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear Res 49: 281‐298, 1990.
 8. Adams JC , Warr WB . Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J Comp Neurol 170: 107‐121, 1976. DOI: 10.1002/cne.901700108.
 9. Agapiou JP , McAlpine D . Low‐frequency envelope sensitivity produces asymmetric binaural tuning curves. J Neurophysiol 100: 2381‐2396, 2008. DOI: 10.1152/jn.90393.2008.
 10. Agar E , Green GG , Sanders DJ . Membrane properties of mouse dorsal cochlear nucleus neurons in vitro. J Basic Clin Physiol Pharmacol 8: 157‐179, 1997.
 11. Agmon‐Snir H , Carr CE , Rinzel J . The role of dendrites in auditory coincidence detection. Nature 393: 268‐272, 1998. DOI: 10.1038/30505.
 12. Aitkin LM . Medial geniculate body of the cat: responses to tonal stimuli of neurons in medial division. J Neurophysiol 36: 275‐283, 1973.
 13. Aitkin LM , Irvine DRF , Webster WR . Central neural mechanisms of hearing. In: Brookhart JM , Mountcastle VB , editors. Handbook of Physiology, the Nervous System, Sensory Processes. Bethesda, MD: American Physiological Society, 1984, p. 675‐737.
 14. Aitkin LM , Webster WR . Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. J Neurophysiol 35: 365‐380, 1972.
 15. Alabi AA , Tsien RW . Synaptic vesicle pools and dynamics. Cold Spring Harb Perspect Biol 4: a013680, 2012. DOI: 10.1101/cshperspect.a013680.
 16. Albrecht O , Dondzillo A , Mayer F , Thompson JA , Klug A . Inhibitory projections from the ventral nucleus of the trapezoid body to the medial nucleus of the trapezoid body in the mouse. Front Neural Circuits 8: 83, 2014. DOI: 10.3389/fncir.2014.00083.
 17. Alibardi L . Fine structure, synaptology and immunocytochemistry of large neurons in the rat dorsal cochlear nucleus connected to the inferior colliculus. J Hirnforsch 39: 429‐439, 1999.
 18. Andersen RA , Roth GL , Aitkin LM , Merzenich MM . The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol 194: 649‐662, 1980. DOI: 10.1002/cne.901940311.
 19. Anderson DJ , Rose JE , Hind JE , Brugge JF . Temporal position of discharges in single auditory nerve fibers within the cycle of a sine‐wave stimulus: frequency and intensity effects. J Acoust Soc Am 49: 1131‐1139, 1971.
 20. Apostolides PF , Trussell LO . Chemical synaptic transmission onto superficial stellate cells of the mouse dorsal cochlear nucleus. J Neurophysiol 111: 1812‐1822, 2014. DOI: 10.1152/jn.00821.2013.
 21. Apostolides PF , Trussell LO . Superficial stellate cells of the dorsal cochlear nucleus. Front Neural Circuits 8: 63, 2014. DOI: 10.3389/fncir.2014.00063.
 22. Arnott RH , Wallace MN , Shackleton TM , Palmer AR . Onset neurones in the anteroventral cochlear nucleus project to the dorsal cochlear nucleus. J Assoc Res Otolaryngol 5: 153‐170, 2004. DOI: 10.1007/s10162‐003‐4036‐8.
 23. Aschoff A , Ostwald J . Distribution of cochlear efferents and olivo‐collicular neurons in the brainstem of rat and guinea pig. A double labeling study with fluorescent tracers. Exp Brain Res 71: 241‐251, 1988.
 24. Baizer JS , Wong KM , Paolone NA , Weinstock N , Salvi RJ , Manohar S , Witelson SF , Baker JF , Sherwood CC , Hof PR . Laminar and neurochemical organization of the dorsal cochlear nucleus of the human, monkey, cat, and rodents. Anat Rec (Hoboken) 297: 1865‐1884, 2014. DOI: 10.1002/ar.23000.
 25. Bal R , Oertel D . Hyperpolarization‐activated, mixed‐cation current (I(h)) in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 84: 806‐817, 2000.
 26. Bal R , Oertel D . Potassium currents in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 86: 2299‐2311, 2001.
 27. Banks MI , Smith PH . Intracellular recordings from neurobiotin‐labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12: 2819‐2837, 1992.
 28. Barker M , Solinski HJ , Hashimoto H , Tagoe T , Pilati N , Hamann M . Acoustic overexposure increases the expression of VGLUT‐2 mediated projections from the lateral vestibular nucleus to the dorsal cochlear nucleus. PLoS One 7: e35955, 2012. DOI: 10.1371/journal.pone.0035955.
 29. Barnes‐Davies M , Barker MC , Osmani F , Forsythe ID . Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19: 325‐333, 2004.
 30. Batra R , Kuwada S , Fitzpatrick DC . Sensitivity to interaural temporal disparities of low‐ and high‐frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J Neurophysiol 78: 1222‐1236, 1997.
 31. Batra R , Kuwada S , Fitzpatrick DC . Sensitivity to interaural temporal disparities of low‐ and high‐frequency neurons in the superior olivary complex. II. Coincidence detection. J Neurophysiol 78: 1237‐1247, 1997.
 32. Batra R , Kuwada S , Stanford TR . High‐frequency neurons in the inferior colliculus that are sensitive to interaural delays of amplitude‐modulated tones: evidence for dual binaural influences. J Neurophysiol 70: 64‐80, 1993. DOI: 10.1152/jn.1993.70.1.64.
 33. Batteau DW . The role of the pinna in human localization. Proc R Soc Lond B Biol Sci 168: 158‐180, 1967.
 34. Baumann VJ , Lehnert S , Leibold C , Koch U . Tonotopic organization of the hyperpolarization‐activated current (Ih) in the mammalian medial superior olive. Front Neural Circuits 7: 117, 2013. DOI: 10.3389/fncir.2013.00117.
 35. Baydyuk M , Xu J , Wu LG . The calyx of Held in the auditory system: structure, function, and development. Hear Res 338: 22‐31, 2016. DOI: 10.1016/j.heares.2016.03.009.
 36. Bazwinsky I , Hilbig H , Bidmon HJ , Rubsamen R . Characterization of the human superior olivary complex by calcium binding proteins and neurofilament H (SMI‐32). J Comp Neurol 456: 292‐303, 2003. DOI: 10.1002/cne.10526.
 37. Beckius GE , Batra R , Oliver DL . Axons from anteroventral cochlear nucleus that terminate in medial superior olive of cat: observations related to delay lines. J Neurosci 19: 3146‐3161, 1999.
 38. Behrend O , Brand A , Kapfer C , Grothe B . Auditory response properties in the superior paraolivary nucleus of the gerbil. J Neurophysiol 87: 2915‐2928, 2002.
 39. Bender KJ , Trussell LO . Axon initial segment Ca2+ channels influence action potential generation and timing. Neuron 61: 259‐271, 2009. DOI: 10.1016/j.neuron.2008.12.004.
 40. Bender KJ , Uebele VN , Renger JJ , Trussell LO . Control of firing patterns through modulation of axon initial segment T‐type calcium channels. J Physiol 590: 109‐118, 2012. DOI: 10.1113/jphysiol.2011.218768.
 41. Benichoux V , Fontaine B , Franken TP , Karino S , Joris PX , Brette R . Neural tuning matches frequency‐dependent time differences between the ears. Elife 4: 2015. DOI: 10.7554/eLife.06072.
 42. Benichoux V , Rebillat M , Brette R . On the variation of interaural time differences with frequency. J Acoust Soc Am 139: 1810, 2016. DOI: 10.1121/1.4944638.
 43. Benson TE , Brown MC . Postsynaptic targets of type II auditory nerve fibers in the cochlear nucleus. J Assoc Res Otolaryngol 5: 111‐125, 2004. DOI: 10.1007/s10162‐003‐4012‐3.
 44. Benson TE , Brown MC . Ultrastructure of synaptic input to medial olivocochlear neurons. J Comp Neurol 499: 244‐257, 2006. DOI: 10.1002/cne.21118.
 45. Berrebi AS , Morgan JI , Mugnaini E . The Purkinje cell class may extend beyond the cerebellum. J Neurocytol 19: 643‐654, 1990.
 46. Berrebi AS , Mugnaini E . Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat Embryol (Berl) 183: 427‐454, 1991.
 47. Beyerl BD . Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145: 209‐223, 1978.
 48. Bianchi F , Verhulst S , Dau T . Experimental evidence for a cochlear source of the precedence effect. J Assoc Res Otolaryngol 14: 767‐779, 2013. DOI: 10.1007/s10162‐013‐0406‐z.
 49. Blackburn CC , Sachs MB . Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. J Neurophysiol 62: 1303‐1329, 1989.
 50. Blackburn CC , Sachs MB . The representations of the steady‐state vowel sound /e/ in the discharge patterns of cat anteroventral cochlear nucleus neurons. J Neurophysiol 63: 1191‐1212, 1990.
 51. Blauert J . Spatial Hearing: The Psychophysics of Human Sound Localization. Cambridge, MA: MIT Press, 1997.
 52. Bledsoe SC Jr , Snead CR , Helfert RH , Prasad V , Wenthold RJ , Altschuler RA . Immunocytochemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trapezoid body to the lateral superior olive is glycinergic. Brain Res 517: 189‐194, 1990.
 53. Bonham BH , Lewis ER . Localization by interaural time difference (ITD): effects of interaural frequency mismatch. J Acoust Soc Am 106: 281‐290, 1999.
 54. Borges‐Merjane C , Trussell LO . ON and OFF unipolar brush cells transform multisensory inputs to the auditory system. Neuron 85: 1029‐1042, 2015. DOI: 10.1016/j.neuron.2015.02.009.
 55. Borst JG , Soria van Hoeve J . The calyx of Held synapse: from model synapse to auditory relay. Annu Rev Physiol 74: 199‐224, 2012. DOI: 10.1146/annurev‐physiol‐020911‐153236.
 56. Boudreau JC , Tsuchitani C . Binaural interaction in the cat superior olive S segment. J Neurophysiol 31: 442‐454, 1968.
 57. Boudreau JC , Tsuchitani C . Cat superior olive S‐segment cell discharge to tonal stimulation. Contrib Sens Physiol 4: 143‐213, 1970.
 58. Bourk TR . Electrical Responses of Neural Units in the Anteroventral Cochlear Nucleus of the Cat. Cambridge, MA: MIT Press, 1976.
 59. Bourk TR , Mielcarz JP , Norris BE . Tonotopic organization of the anteroventral cochlear nucleus of the cat. Hear Res 4: 215‐241, 1981.
 60. Brand A , Behrend O , Marquardt T , McAlpine D , Grothe B . Precise inhibition is essential for microsecond interaural time difference coding. Nature 417: 543‐547, 2002. DOI: 10.1038/417543a.
 61. Brawer JR , Morest DK , Kane EC . The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155: 251‐300, 1974. DOI: 10.1002/cne.901550302.
 62. Bremen P , Joris PX . Axonal recordings from medial superior olive neurons obtained from the lateral lemniscus of the chinchilla (Chinchilla laniger). J Neurosci 33: 17506‐17518, 2013. DOI: 10.1523/JNEUROSCI.1518‐13.2013.
 63. Brette R . On the interpretation of sensitivity analyses of neural responses. J Acoust Soc Am 128: 2965‐2972, 2010. DOI: 10.1121/1.3488311.
 64. Brew HM , Forsythe ID . Two voltage‐dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15: 8011‐8022, 1995.
 65. Bronkhorst A . The cocktail party phenomenon: a review of research on speech intelligibility in multiple‐talker conditions. Acta Acust united Ac 86: 117‐128, 2000.
 66. Bronkhorst AW . Localization of real and virtual sound sources. J Acoust Soc Am 98: 2542‐2553, 1995.
 67. Bronkhorst AW , Houtgast T . Auditory distance perception in rooms. Nature 397: 517‐520, 1999. DOI: 10.1038/17374.
 68. Brown AD , Jones HG , Kan A , Thakkar T , Stecker GC , Goupell MJ , Litovsky RY . Evidence for a neural source of the precedence effect in sound localization. J Neurophysiol 114: 2991‐3001, 2015. DOI: 10.1152/jn.00243.2015.
 69. Brown AD , Stecker GC , Tollin DJ . The precedence effect in sound localization. J Assoc Res Otolaryngol 16: 1‐28, 2015. DOI: 10.1007/s10162‐014‐0496‐2.
 70. Brown CH , Beecher MD , Moody DB , Stebbins WC . Localization of primate calls by old world monkeys. Science 201: 753‐754, 1978.
 71. Brown CH , Beecher MD , Moody DB , Stebbins WC . Localization of noise bands by Old World monkeys. J Acoust Soc Am 68: 127‐132, 1980.
 72. Brown MC . Morphology of labeled afferent fibers in the guinea pig cochlea. J Comp Neurol 260: 591‐604, 1987. DOI: 10.1002/cne.902600411.
 73. Brown MC . Antidromic responses of single units from the spiral ganglion. J Neurophysiol 71: 1835‐1847, 1994.
 74. Brown MC , Drottar M , Benson TE , Darrow K . Commissural axons of the mouse cochlear nucleus. J Comp Neurol 521: 1683‐1696, 2013. DOI: 10.1002/cne.23257.
 75. Brown MC , Ledwith JV 3rd. Projections of thin (type‐II) and thick (type‐I) auditory‐nerve fibers into the cochlear nucleus of the mouse. Hear Res 49: 105‐118, 1990.
 76. Brugge JF , Anderson DJ , Aitkin LM . Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. J Neurophysiol 33: 441‐458, 1970.
 77. Brunso‐Bechtold JK , Henkel CK , Linville C . Synaptic organization in the adult ferret medial superior olive. J Comp Neurol 294: 389‐398, 1990. DOI: 10.1002/cne.902940308.
 78. Brunso‐Bechtold JK , Thompson GC , Masterton RB . HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197: 705‐722, 1981. DOI: 10.1002/cne.901970410.
 79. Bukowska D . Morphological evidence for secondary vestibular afferent connections to the dorsal cochlear nucleus in the rabbit. Cells Tissues Organs 170: 61‐68, 2002. DOI: 10.1159/000047921.
 80. Burger RM , Pollak GD . Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats. J Neurosci 21: 4830‐4843, 2001.
 81. Burian M , Gstoettner W . Projection of primary vestibular afferent fibres to the cochlear nucleus in the guinea pig. Neurosci Lett 84: 13‐17, 1988.
 82. Butler RA . The bandwidth effect on monaural and binaural localization. Hear Res 21: 67‐73, 1986.
 83. Butler RA , Humanski RA . Localization of sound in the vertical plane with and without high‐frequency spectral cues. Percept Psychophys 51: 182‐186, 1992.
 84. Butts DA , Goldman MS . Tuning curves, neuronal variability, and sensory coding. PLoS Biol 4: e92, 2006. DOI: 10.1371/journal.pbio.0040092.
 85. Cai Y , McGee J , Walsh EJ . Contributions of ion conductances to the onset responses of octopus cells in the ventral cochlear nucleus: simulation results. J Neurophysiol 83: 301‐314, 2000.
 86. Caicedo A , Herbert H . Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 328: 377‐392, 1993. DOI: 10.1002/cne.903280305.
 87. Caird D , Klinke R . Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52: 385‐399, 1983.
 88. Caird D , Klinke R . Processing of interaural time and intensity differences in the cat inferior colliculus. Exp Brain Res 68: 379‐392, 1987.
 89. Caird D , Pillmann F , Klinke R . Responses of single cells in the cat inferior colliculus to binaural masking level difference signals. Hear Res 43: 1‐23, 1989.
 90. Caird DM , Palmer AR , Rees A . Binaural masking level difference effects in single units of the guinea pig inferior colliculus. Hear Res 57: 91‐106, 1991.
 91. Calford MB , Webster WR . Auditory representation within principal division of cat medial geniculate body: an electrophysiology study. J Neurophysiol 45: 1013‐1028, 1981.
 92. Campagnola L , Manis PB . A map of functional synaptic connectivity in the mouse anteroventral cochlear nucleus. J Neurosci 34: 2214‐2230, 2014. DOI: 10.1523/JNEUROSCI.4669‐13.2014.
 93. Cant NB . The fine structure of two types of stellate cells in the anterior division of the anteroventral cochlear nucleus of the cat. Neuroscience 6: 2643‐2655, 1981.
 94. Cant NB , Casseday JH . Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J Comp Neurol 247: 457‐476, 1986. DOI: 10.1002/cne.902470406.
 95. Cant NB , Gaston KC . Pathways connecting the right and left cochlear nuclei. J Comp Neurol 212: 313‐326, 1982. DOI: 10.1002/cne.902120308.
 96. Cant NB , Hyson RL . Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear Res 58: 26‐34, 1992.
 97. Cao XJ , Oertel D . The magnitudes of hyperpolarization‐activated and low‐voltage‐activated potassium currents co‐vary in neurons of the ventral cochlear nucleus. J Neurophysiol 106: 630‐640, 2011. DOI: 10.1152/jn.00015.2010.
 98. Cariani PA , Delgutte B . Neural correlates of the pitch of complex tones. I. Pitch and pitch salience. J Neurophysiol 76: 1698‐1716, 1996. DOI: 10.1152/jn.1996.76.3.1698.
 99. Carlile S , Leong P , Hyams S . The nature and distribution of errors in sound localization by human listeners. Hear Res 114: 179‐196, 1997.
 100. Carney LH . Sensitivities of cells in anteroventral cochlear nucleus of cat to spatiotemporal discharge patterns across primary afferents. J Neurophysiol 64: 437‐456, 1990.
 101. Carney LH . Supra‐threshold Hearing and fluctuation profiles: implications for sensorineural and hidden hearing loss. J Assoc Res Otolaryngol 19: 331‐352, 2018. DOI: 10.1007/s10162‐018‐0669‐5.
 102. Carney LH , McDuffy MJ , Shekhter I . Frequency glides in the impulse responses of auditory‐nerve fibers. J Acoust Soc Am 105: 2384‐2391, 1999.
 103. Carney LH , Yin TC . Temporal coding of resonances by low‐frequency auditory nerve fibers: single‐fiber responses and a population model. J Neurophysiol 60: 1653‐1677, 1988. DOI: 10.1152/jn.1988.60.5.1653.
 104. Carney LH , Yin TC . Responses of low‐frequency cells in the inferior colliculus to interaural time differences of clicks: excitatory and inhibitory components. J Neurophysiol 62: 144‐161, 1989.
 105. Carr CE , Konishi M . A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10: 3227‐3246, 1990.
 106. Caspary DM , Hughes LF , Schatteman TA , Turner JG . Age‐related changes in the response properties of cartwheel cells in rat dorsal cochlear nucleus. Hear Res 216‐217: 207‐215, 2006. DOI: 10.1016/j.heares.2006.03.005.
 107. Casseday JH , Neff WD . Localization of pure tones. J Acoust Soc Am 54: 365‐372, 1973.
 108. Champoux F , Paiement P , Mercier C , Lepore F , Lassonde M , Gagne JP . Auditory processing in a patient with a unilateral lesion of the inferior colliculus. Eur J Neurosci 25: 291‐297, 2007. DOI: 10.1111/j.1460‐9568.2006.05260.x.
 109. Cheatham MA , Huynh KH , Gao J , Zuo J , Dallos P . Cochlear function in Prestin knockout mice. J Physiol 560: 821‐830, 2004. DOI: 10.1113/jphysiol.2004.069559.
 110. Cherry EC . Some experiments on the recognition of speech with one and with two ears. J Acoust Soc Am 25: 975‐979, 1953.
 111. Cherry EC , Sayers BM . “Human crosscorrelator” – a technique for measuring certain parameters of speech perception. J Acoust Soc Am 28: 889‐895, 1956.
 112. Chirila FV , Rowland KC , Thompson JM , Spirou GA . Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature. J Physiol 584: 167‐190, 2007. DOI: 10.1113/jphysiol.2007.137976.
 113. Clarey JC , Barone P , Irons WA , Samson FK , Imig TJ . Comparison of noise and tone azimuth tuning of neurons in cat primary auditory cortex and medical geniculate body. J Neurophysiol 74: 961‐980, 1995.
 114. Coffey CS , Ebert CS Jr , Marshall AF , Skaggs JD , Falk SE , Crocker WD , Pearson JM , Fitzpatrick DC . Detection of interaural correlation by neurons in the superior olivary complex, inferior colliculus and auditory cortex of the unanesthetized rabbit. Hear Res 221: 1‐16, 2006. DOI: 10.1016/j.heares.2006.06.005.
 115. Colburn HS . Theory of binaural interaction based on auditory‐nerve data. II. Detection of tones in noise. J Acoust Soc Am 61: 525‐533, 1977.
 116. Colburn HS , Durlach NI . Binaural phenomena. In: Carterette EC , Friedman MP , editors. Handbook of Perception. New York: Academic Press, vol. 4: 1978, p. 365‐466.
 117. Colburn HS , Han YA , Culotta CP . Coincidence model of MSO responses. Hear Res 49: 335‐346, 1990.
 118. Coleman JR , Clerici WJ . Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262: 215‐226, 1987. DOI: 10.1002/cne.902620204.
 119. Coomes DL , Schofield BR . Projections from the auditory cortex to the superior olivary complex in guinea pigs. Eur J Neurosci 19: 2188‐2200, 2004. DOI: 10.1111/j.0953‐816X.2004.03317.x.
 120. Couchman K , Grothe B , Felmy F . Medial superior olivary neurons receive surprisingly few excitatory and inhibitory inputs with balanced strength and short‐term dynamics. J Neurosci 30: 17111‐17121, 2010. DOI: 10.1523/JNEUROSCI.1760‐10.2010.
 121. Couchman K , Grothe B , Felmy F . Functional localization of neurotransmitter receptors and synaptic inputs to mature neurons of the medial superior olive. J Neurophysiol 107: 1186‐1198, 2012. DOI: 10.1152/jn.00586.2011.
 122. Covey E , Jones DR , Casseday JH . Projections from the superior olivary complex to the cochlear nucleus in the tree shrew. J Comp Neurol 226: 289‐305, 1984. DOI: 10.1002/cne.902260212.
 123. Cranford JL . Localization of paired sound sources in cats: effects of variable arrival times. J Acoust Soc Am 72: 1309‐1311, 1982.
 124. Crow G , Rupert AL , Moushegian G . Phase locking in monaural and binaural medullary neurons: implications for binaural phenomena. J Acoust Soc Am 64: 493‐501, 1978.
 125. Darrow KN , Benson TE , Brown MC . Planar multipolar cells in the cochlear nucleus project to medial olivocochlear neurons in mouse. J Comp Neurol 520: 1365‐1375, 2012. DOI: 10.1002/cne.22797.
 126. Darrow KN , Maison SF , Liberman MC . Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9: 1474‐1476, 2006. DOI: 10.1038/nn1807.
 127. Davis KA , Ramachandran R , May BJ . Single‐unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J Neurophysiol 82: 164‐175, 1999.
 128. Davis KA , Ramachandran R , May BJ . Auditory processing of spectral cues for sound localization in the inferior colliculus. J Assoc Res Otolaryngol 4: 148‐163, 2003. DOI: 10.1007/s10162‐002‐2002‐5.
 129. Davis KA , Young ED . Granule cell activation of complex‐spiking neurons in dorsal cochlear nucleus. J Neurosci 17: 6798‐6806, 1997.
 130. Davis KA , Young ED . Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 83: 926‐940, 2000.
 131. Day ML , Delgutte B . Decoding sound source location and separation using neural population activity patterns. J Neurosci 33: 15837‐15847, 2013. DOI: 10.1523/JNEUROSCI.2034‐13.2013.
 132. Day ML , Koka K , Delgutte B . Neural encoding of sound source location in the presence of a concurrent, spatially separated source. J Neurophysiol 108: 2612‐2628, 2012. DOI: 10.1152/jn.00303.2012.
 133. Day ML , Semple MN . Frequency‐dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J Neurophysiol 106: 1985‐1999, 2011. DOI: 10.1152/jn.00131.2011.
 134. de Boer E , de Jongh HR . On cochlear encoding: potentialities and limitations of the reverse‐correlation technique. J Acoust Soc Am 63: 115‐135, 1978.
 135. Dean I , Harper NS , McAlpine D . Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8: 1684‐1689, 2005. DOI: 10.1038/nn1541.
 136. Dean I , Robinson BL , Harper NS , McAlpine D . Rapid neural adaptation to sound level statistics. J Neurosci 28: 6430‐6438, 2008. DOI: 10.1523/JNEUROSCI.0470‐08.2008.
 137. Dehmel S , Kopp‐Scheinpflug C , Dorrscheidt GJ , Rubsamen R . Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil. Hear Res 172: 18‐36, 2002.
 138. Dehmel S , Kopp‐Scheinpflug C , Weick M , Dorrscheidt GJ , Rubsamen R . Transmission of phase‐coupling accuracy from the auditory nerve to spherical bushy cells in the Mongolian gerbil. Hear Res 268: 234‐249, 2010. DOI: 10.1016/j.heares.2010.06.005.
 139. Delgutte B , Joris PX , Litovsky RY , Yin TC . Receptive fields and binaural interactions for virtual‐space stimuli in the cat inferior colliculus. J Neurophysiol 81: 2833‐2851, 1999.
 140. Dent ML , Dooling RJ . Investigations of the precedence effect in budgerigars: effects of stimulus type, intensity, duration, and location. J Acoust Soc Am 113: 2146‐2158, 2003.
 141. Dent ML , Dooling RJ . Investigations of the precedence effect in budgerigars: the perceived location of auditory images. J Acoust Soc Am 113: 2159‐2169, 2003.
 142. Dent ML , Tollin DJ , Yin TC . Influence of sound source location on the behavior and physiology of the precedence effect in cats. J Neurophysiol 102: 724‐734, 2009. DOI: 10.1152/jn.00129.2009.
 143. Devore S , Delgutte B . Effects of reverberation on the directional sensitivity of auditory neurons across the tonotopic axis: influences of interaural time and level differences. J Neurosci 30: 7826‐7837, 2010. DOI: 10.1523/JNEUROSCI.5517‐09.2010.
 144. Devore S , Ihlefeld A , Hancock K , Shinn‐Cunningham B , Delgutte B . Accurate sound localization in reverberant environments is mediated by robust encoding of spatial cues in the auditory midbrain. Neuron 62: 123‐134, 2009. DOI: 10.1016/j.neuron.2009.02.018.
 145. Ding J , Benson TE , Voigt HF . Acoustic and current‐pulse responses of identified neurons in the dorsal cochlear nucleus of unanesthetized, decerebrate gerbils. J Neurophysiol 82: 3434‐3457, 1999.
 146. Dong W , Olson ES . Detection of cochlear amplification and its activation. Biophys J 105: 1067‐1078, 2013. DOI: 10.1016/j.bpj.2013.06.049.
 147. Doucet JR , Ross AT , Gillespie MB , Ryugo DK . Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus. J Comp Neurol 408: 515‐531, 1999.
 148. Doucet JR , Ryugo DK . Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385: 245‐264, 1997.
 149. Englitz B , Tolnai S , Typlt M , Jost J , Rubsamen R . Reliability of synaptic transmission at the synapses of Held in vivo under acoustic stimulation. PLoS One 4: e7014, 2009. DOI: 10.1371/journal.pone.0007014.
 150. Evans EF . Frequency selectivity at high signal levels of single units in cochlear nerve and nucleus. In: Evans EF , Wilson JP , editors. Psychophysics and Physiology of Hearing. London: Academic Press, 1977, p. 185‐192.
 151. Evans EF , Nelson PG . On the functional relationship between the dorsal and ventral divisions of the cochlear nucleus of the cat. Exp Brain Res 17: 428‐442, 1973.
 152. Faye‐Lund H . Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol (Berl) 175: 35‐52, 1986.
 153. Fekete DM , Rouiller EM , Liberman MC , Ryugo DK . The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229: 432‐450, 1984. DOI: 10.1002/cne.902290311.
 154. Felix RA 2nd , Fridberger A , Leijon S , Berrebi AS , Magnusson AK . Sound rhythms are encoded by postinhibitory rebound spiking in the superior paraolivary nucleus. J Neurosci 31: 12566‐12578, 2011. DOI: 10.1523/JNEUROSCI.2450‐11.2011.
 155. Felix RA 2nd , Kadner A , Berrebi AS . Effects of ketamine on response properties of neurons in the superior paraolivary nucleus of the mouse. Neuroscience 201: 307‐319, 2012. DOI: 10.1016/j.neuroscience.2011.11.027.
 156. Felix RA 2nd , Magnusson AK . Development of excitatory synaptic transmission to the superior paraolivary and lateral superior olivary nuclei optimizes differential decoding strategies. Neuroscience 334: 1‐12, 2016. DOI: 10.1016/j.neuroscience.2016.07.039.
 157. Felix RA 2nd , Vonderschen K , Berrebi AS , Magnusson AK . Development of on‐off spiking in superior paraolivary nucleus neurons of the mouse. J Neurophysiol 109: 2691‐2704, 2013. DOI: 10.1152/jn.01041.2012.
 158. Ferragamo MJ , Golding NL , Oertel D . Synaptic inputs to stellate cells in the ventral cochlear nucleus. J Neurophysiol 79: 51‐63, 1998.
 159. Ferragamo MJ , Oertel D . Octopus cells of the mammalian ventral cochlear nucleus sense the rate of depolarization. J Neurophysiol 87: 2262‐2270, 2002. DOI: 10.1152/jn.00587.2001.
 160. Fettiplace R . Hair cell transduction, tuning, and synaptic transmission in the mammalian cochlea. Compr Physiol 7: 1197‐1227, 2017. DOI: 10.1002/cphy.c160049.
 161. Finlayson PG , Caspary DM . Synaptic potentials of chinchilla lateral superior olivary neurons. Hear Res 38: 221‐228, 1989.
 162. Finlayson PG , Caspary DM . Low‐frequency neurons in the lateral superior olive exhibit phase‐sensitive binaural inhibition. J Neurophysiol 65: 598‐605, 1991.
 163. Fischl MJ , Burger RM , Schmidt‐Pauly M , Alexandrova O , Sinclair JL , Grothe B , Forsythe ID , Kopp‐Scheinpflug C . Physiology and anatomy of neurons in the medial superior olive of the mouse. J Neurophysiol 116: 2676‐2688, 2016. DOI: 10.1152/jn.00523.2016.
 164. Fitzpatrick DC , Batra R , Stanford TR , Kuwada S . A neuronal population code for sound localization. Nature 388: 871‐874, 1997. DOI: 10.1038/42246.
 165. Fitzpatrick DC , Kuwada S . Tuning to interaural time differences across frequency. J Neurosci 21: 4844‐4851, 2001.
 166. Fitzpatrick DC , Kuwada S , Batra R . Neural sensitivity to interaural time differences: beyond the Jeffress model. J Neurosci 20: 1605‐1615, 2000.
 167. Fitzpatrick DC , Kuwada S , Batra R , Trahiotis C . Neural responses to simple simulated echoes in the auditory brain stem of the unanesthetized rabbit. J Neurophysiol 74: 2469‐2486, 1995.
 168. Fitzpatrick DC , Kuwada S , Kim DO , Parham K , Batra R . Responses of neurons to click‐pairs as simulated echoes: auditory nerve to auditory cortex. J Acoust Soc Am 106: 3460‐3472, 1999.
 169. Flores EN , Duggan A , Madathany T , Hogan AK , Marquez FG , Kumar G , Seal RP , Edwards RH , Liberman MC , Garcia‐Anoveros J . A non‐canonical pathway from cochlea to brain signals tissue‐damaging noise. Curr Biol 25: 606‐612, 2015. DOI: 10.1016/j.cub.2015.01.009.
 170. Fontaine B , Brette R . Neural development of binaural tuning through Hebbian learning predicts frequency‐dependent best delays. J Neurosci 31: 11692‐11696, 2011. DOI: 10.1523/JNEUROSCI.0237‐11.2011.
 171. Ford MC , Alexandrova O , Cossell L , Stange‐Marten A , Sinclair J , Kopp‐Scheinpflug C , Pecka M , Attwell D , Grothe B . Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing. Nat Commun 6: 8073, 2015. DOI: 10.1038/ncomms9073.
 172. Forsythe ID , Barnes‐Davies M . The binaural auditory pathway: excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc Biol Sci 251: 151‐157, 1993. DOI: 10.1098/rspb.1993.0022.
 173. Forsythe ID , Barnes‐Davies M . The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc Biol Sci 251: 143‐150, 1993. DOI: 10.1098/rspb.1993.0021.
 174. Francis NA , Guinan JJ Jr . Acoustic stimulation of human medial olivocochlear efferents reduces stimulus‐frequency and click‐evoked otoacoustic emission delays: implications for cochlear filter bandwidths. Hear Res 267: 36‐45, 2010. DOI: 10.1016/j.heares.2010.04.009.
 175. Franken TP , Bremen P , Joris PX . Coincidence detection in the medial superior olive: mechanistic implications of an analysis of input spiking patterns. Front Neural Circuits 8: 42, 2014. DOI: 10.3389/fncir.2014.00042.
 176. Franken TP , Joris PX , Smith PH . Principal cells of the brainstem's interaural sound level detector are temporal differentiators rather than integrators. Elife 7: 2018. DOI: 10.7554/eLife.33854.
 177. Franken TP , Roberts MT , Wei L , Golding NL , Joris PX . In vivo coincidence detection in mammalian sound localization generates phase delays. Nat Neurosci 18: 444‐452, 2015. DOI: 10.1038/nn.3948.
 178. Franken TP , Smith PH , Joris PX . In vivo whole‐cell recordings combined with electron microscopy reveal unexpected morphological and physiological properties in the lateral nucleus of the trapezoid body in the auditory brainstem. Front Neural Circuits 10: 69, 2016. DOI: 10.3389/fncir.2016.00069.
 179. Franken TP , Smith PH , Joris PX . Microsecond interaural time differences of acoustic transients are decoded by inhibitory‐excitatory interaction in neurons of the lateral superior olive. J Acoust Soc Am 141: 3570‐3571, 2017.
 180. Frens MA , Van Opstal AJ . A quantitative study of auditory‐evoked saccadic eye movements in two dimensions. Exp Brain Res 107: 103‐117, 1995.
 181. Friauf E , Ostwald J . Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra‐axonal injection of horseradish peroxidase. Exp Brain Res 73: 263‐284, 1988.
 182. Fujino K , Oertel D . Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J Neurosci 21: 7372‐7383, 2001.
 183. Gacek RR , Rasmussen GL . Fiber analysis of the statoacoustic nerve of guinea pig, cat, and monkey. Anat Rec 139: 455‐463, 1961.
 184. Gai Y , Carney LH . Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99: 1077‐1095, 2008. DOI: 10.1152/jn.00708.2007.
 185. Gai Y , Ruhland JL , Yin TC . Localization of click trains and speech by cats: the negative level effect. J Assoc Res Otolaryngol 15: 789‐800, 2014. DOI: 10.1007/s10162‐014‐0469‐5.
 186. Gai Y , Ruhland JL , Yin TC , Tollin DJ . Behavioral and modeling studies of sound localization in cats: effects of stimulus level and duration. J Neurophysiol 110: 607‐620, 2013. DOI: 10.1152/jn.01019.2012.
 187. Galambos R , Schwartzkopff J , Rupert A . Microelectrode study of superior olivary nuclei. Am J Phys 197: 527‐536, 1959.
 188. Gao F , Kadner A , Felix RA 2nd , Chen L , Berrebi AS . Forward masking in the superior paraolivary nucleus of the rat. Brain Struct Funct 222: 365‐379, 2017. DOI: 10.1007/s00429‐016‐1222‐0.
 189. Gardner MB , Gardner RS . Problem of localization in the median plane: effect of pinnae cavity occlusion. J Acoust Soc Am 53: 400‐408, 1973.
 190. Gardner SM , Trussell LO , Oertel D . Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input. J Neurosci 19: 8721‐8729, 1999.
 191. Gerstein GL , Kiang NY . An approach to the quantitative analysis of electrophysiological data from single neurons. Biophys J 1: 15‐28, 1960.
 192. Glendenning KK , Baker BN , Hutson KA , Masterton RB . Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSO. J Comp Neurol 319: 100‐122, 1992. DOI: 10.1002/cne.903190110.
 193. Glendenning KK , Hutson KA , Nudo RJ , Masterton RB . Acoustic chiasm II: anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol 232: 261‐285, 1985. DOI: 10.1002/cne.902320210.
 194. Glendenning KK , Masterton RB . Acoustic chiasm: efferent projections of the lateral superior olive. J Neurosci 3: 1521‐1537, 1983.
 195. Glenn JF , Oatman LC . Stimulation studies in the descending auditory pathway. Brain Res 196: 258‐261, 1980.
 196. Godfrey DA , Kiang NYS , Norris BE . Single unit activity in the dorsal cochlear nucleus of the cat. J Comp Neurol 162: 269‐284, 1975. DOI: 10.1002/cne.901620207.
 197. Godfrey DA , Kiang NYS , Norris BE . Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162: 247‐268, 1975. DOI: 10.1002/cne.901620206.
 198. Goldberg JM , Brown PB . Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31: 639‐656, 1968.
 199. Goldberg JM , Brown PB . Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32: 613‐636, 1969.
 200. Golding NL , Ferragamo MJ , Oertel D . Role of intrinsic conductances underlying responses to transients in octopus cells of the cochlear nucleus. J Neurosci 19: 2897‐2905, 1999.
 201. Golding NL , Oertel D . Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J Neurophysiol 78: 248‐260, 1997.
 202. Golding NL , Oertel D . Synaptic integration in dendrites: exceptional need for speed. J Physiol 590: 5563‐5569, 2012. DOI: 10.1113/jphysiol.2012.229328.
 203. Golding NL , Robertson D , Oertel D . Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J Neurosci 15: 3138‐3153, 1995.
 204. Goldwyn JH , McLaughlin M , Verschooten E , Joris PX , Rinzel J . Signatures of somatic inhibition and dendritic excitation in auditory brainstem field potentials. J Neurosci 37: 10451‐10467, 2017. DOI: 10.1523/JNEUROSCI.0600‐17.2017.
 205. Gomez‐Alvarez M , Saldana E . Different tonotopic regions of the lateral superior olive receive a similar combination of afferent inputs. J Comp Neurol 524: 2230‐2250, 2016. DOI: 10.1002/cne.23942.
 206. Gomez‐Nieto R , Rubio ME . A bushy cell network in the rat ventral cochlear nucleus. J Comp Neurol 516: 241‐263, 2009. DOI: 10.1002/cne.22139.
 207. Gomez‐Nieto R , Sinex DG , Horta‐Junior Jde A , Castellano O , Herrero‐Turrion JM , Lopez DE . A fast cholinergic modulation of the primary acoustic startle circuit in rats. Brain Struct Funct 219: 1555‐1573, 2014. DOI: 10.1007/s00429‐013‐0585‐8.
 208. Gonzalez‐Hernandez T , Mantolan‐Sarmiento B , Gonzalez‐Gonzalez B , Perez‐Gonzalez H . Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372: 309‐326, 1996. DOI: 10.1002/(SICI)1096‐9861(19960819)372:2<309::AID‐CNE11>3.0.CO;2‐E.
 209. Goodman DF , Benichoux V , Brette R . Decoding neural responses to temporal cues for sound localization. Elife 2: e01312, 2013. DOI: 10.7554/eLife.01312.
 210. Goyer D , Kurth S , Gillet C , Keine C , Rubsamen R , Kuenzel T . Slow cholinergic modulation of spike probability in ultra‐fast time‐coding sensory neurons. eNeuro 3: 2016. DOI: 10.1523/ENEURO.0186‐16.2016.
 211. Grantham DW . Detectability of time‐varying interaural correlation in narrow‐band noise stimuli. J Acoust Soc Am 72: 1178‐1184, 1982.
 212. Grantham DW , Wightman FL . Detectability of varying interaural temporal differences. J Acoust Soc Am 63: 511‐523, 1978.
 213. Grothe B . Interaction of excitation and inhibition in processing of pure tone and amplitude‐modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71: 706‐721, 1994. DOI: 10.1152/jn.1994.71.2.706.
 214. Grothe B . New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4: 540‐550, 2003. DOI: 10.1038/nrn1136.
 215. Grothe B , Carr CE , Casseday JH , Fritzsch B , Koppl C . The evolution of central pathways and their neural processing patterns. In: Manley GA , Popper AN , Fay RR , editors. Springer Handbook of Auditory Research: Evolution of the Vertebrate System. New York: Springer, 2004, p. 28‐359.
 216. Grothe B , Pecka M . The natural history of sound localization in mammals – a story of neuronal inhibition. Front Neural Circuits 8: 116, 2014. DOI: 10.3389/fncir.2014.00116.
 217. Grothe B , Pecka M , McAlpine D . Mechanisms of sound localization in mammals. Physiol Rev 90: 983‐1012, 2010. DOI: 10.1152/physrev.00026.2009.
 218. Grothe B , Sanes DH . Bilateral inhibition by glycinergic afferents in the medial superior olive. J Neurophysiol 69: 1192‐1196, 1993.
 219. Grothe B , Sanes DH . Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an in vitro study. J Neurosci 14: 1701‐1709, 1994.
 220. Guinan JJ . Physiology of the medial and lateral olivocochlear systems. In: Ryugo DK , Fay RR , Popper AN , editors. Auditory and Vestibular Efferents. New York: Springer, 2011, p. 39‐81.
 221. Guinan JJ , Guinan SS , Norris BE . Single auditory units in the superior olivary complex. I. Responses to sounds and classification based on physiological properties. Int J Neurosci 4: 101‐120, 1972.
 222. Guinan JJ Jr , Li RY . Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hear Res 49: 321‐334, 1990.
 223. Guinan JJ , Norris BE , Guinan SS . Single auditory units in the superior olivary complex. II. Locations of unit categories and tonotopic organization. Int J Neurosci 4: 147‐166, 1972.
 224. Guinan JJ Jr , Warr WB , Norris BE . Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex. J Comp Neurol 221: 358‐370, 1983. DOI: 10.1002/cne.902210310.
 225. Hancock KE . A physiologically‐based population rate code for interaural time differences (ITDs) predicts bandwidth‐dependent lateralization. In: Kollmeier B , Klump G , Hohmann V , Langemann U , Mauermann M , Uppenkamp S , Verhey J , editors. Hearing – From Sensory Processing to Perception. Berlin: Springer‐Verlag, 2007.
 226. Hancock KE , Delgutte B . A physiologically based model of interaural time difference discrimination. J Neurosci 24: 7110‐7117, 2004. DOI: 10.1523/JNEUROSCI.0762‐04.2004.
 227. Hancock KE , Voigt HF . Intracellularly labeled fusiform cells in dorsal cochlear nucleus of the gerbil. I. Physiological response properties. J Neurophysiol 87: 2505‐2519, 2002.
 228. Hancock KE , Voigt HF . Intracellularly labeled fusiform cells in dorsal cochlear nucleus of the gerbil. II. Comparison of physiology and anatomy. J Neurophysiol 87: 2520‐2530, 2002.
 229. Harper NS , McAlpine D . Optimal neural population coding of an auditory spatial cue. Nature 430: 682‐686, 2004. DOI: 10.1038/nature02768.
 230. Hartmann WM , Rakerd B . Auditory spectral discrimination and the localization of clicks in the sagittal plane. J Acoust Soc Am 94: 2083‐2092, 1993.
 231. Hartung K , Trahiotis C . Peripheral auditory processing and investigations of the “precedence effect” which utilize successive transient stimuli. J Acoust Soc Am 110: 1505‐1513, 2001.
 232. Hebrank J , Wright D . Are two ears necessary for localization of sound sources on the median plane? J Acoust Soc Am 56: 935‐938, 1974.
 233. Hebrank J , Wright D . Spectral cues used in the localization of sound sources on the median plane. J Acoust Soc Am 56: 1829‐1834, 1974.
 234. Heeringa AN , Wu C , Shore SE . Multisensory integration enhances temporal coding in ventral cochlear nucleus bushy cells. J Neurosci 38: 2832‐2843, 2018. DOI: 10.1523/JNEUROSCI.2244‐17.2018.
 235. Heffner RS , Heffner HE , Koay G . Sound localization in chinchillas. II. Front/back and vertical localization. Hear Res 88: 190‐198, 1995.
 236. Heffner RS , Koay G , Heffner HE . Sound localization in chinchillas, III: effect of pinna removal. Hear Res 99: 13‐21, 1996.
 237. Heil P . Further observations on the threshold model of latency for auditory neurons. Behav Brain Res 95: 233‐236, 1998.
 238. Heil P , Peterson AJ . Basic response properties of auditory nerve fibers: a review. Cell Tissue Res 361: 129‐158, 2015. DOI: 10.1007/s00441‐015‐2177‐9.
 239. Helfert RH , Bonneau JM , Wenthold RJ , Altschuler RA . GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res 501: 269‐286, 1989.
 240. Helfert RH , Juiz JM , Bledsoe SC Jr , Bonneau JM , Wenthold RJ , Altschuler RA . Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J Comp Neurol 323: 305‐325, 1992. DOI: 10.1002/cne.903230302.
 241. Helfert RH , Schwartz IR . Morphological evidence for the existence of multiple neuronal classes in the cat lateral superior olivary nucleus. J Comp Neurol 244: 533‐549, 1986. DOI: 10.1002/cne.902440409.
 242. Helfert RH , Schwartz IR . Morphological features of five neuronal classes in the gerbil lateral superior olive. Am J Anat 179: 55‐69, 1987. DOI: 10.1002/aja.1001790108.
 243. Henkel CK , Spangler KM . Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods. J Comp Neurol 221: 416‐428, 1983. DOI: 10.1002/cne.902210405.
 244. Hill PA , Nelson PA , Kirkeby O , Hamada H . Resolution of front‐back confusion in virtual acoustic imaging systems. J Acoust Soc Am 108: 2901‐2910, 2000.
 245. Hind JE , Anderson DJ , Brugge JF , Rose JE . Coding of information pertaining to paired low‐frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30: 794‐816, 1967.
 246. Hirsch JA , Chan JC , Yin TC . Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. J Neurophysiol 53: 726‐745, 1985.
 247. Hirsh IJ . The influence of interaural phase on interaural summation and inhibition. J Acoust Soc Am 20: 536‐544, 1948.
 248. Hofman M , Van Opstal J . Binaural weighting of pinna cues in human sound localization. Exp Brain Res 148: 458‐470, 2003. DOI: 10.1007/s00221‐002‐1320‐5.
 249. Hofman PM , Van Opstal AJ . Spectro‐temporal factors in two‐dimensional human sound localization. J Acoust Soc Am 103: 2634‐2648, 1998.
 250. Hofman PM , Van Riswick JG , Van Opstal AJ . Relearning sound localization with new ears. Nat Neurosci 1: 417‐421, 1998. DOI: 10.1038/1633.
 251. Hormigo S , Gomez‐Nieto R , Castellano O , Herrero‐Turrion MJ , Lopez DE , de Anchieta de Castro E Horta‐Júnior J . The noradrenergic projection from the locus coeruleus to the cochlear root neurons in rats. Brain Struct Funct 220: 1477‐1496, 2015. DOI: 10.1007/s00429‐014‐0739‐3.
 252. Huang AY , May BJ . Sound orientation behavior in cats. II. Mid‐frequency spectral cues for sound localization. J Acoust Soc Am 100: 1070‐1080, 1996.
 253. Hutson KA , Glendenning KK , Masterton RB . Acoustic chiasm. IV: eight midbrain decussations of the auditory system in the cat. J Comp Neurol 312: 105‐131, 1991. DOI: 10.1002/cne.903120109.
 254. Imig TJ , Adrian HO . Binaural columns in the primary field (A1) of cat auditory cortex. Brain Res 138: 241‐257, 1977.
 255. Imig TJ , Bibikov NG , Poirier P , Samson FK . Directionality derived from pinna‐cue spectral notches in cat dorsal cochlear nucleus. J Neurophysiol 83: 907‐925, 2000.
 256. Ingham NJ , Bleeck S , Winter IM . Contralateral inhibitory and excitatory frequency response maps in the mammalian cochlear nucleus. Eur J Neurosci 24: 2515‐2529, 2006. DOI: 10.1111/j.1460‐9568.2006.05134.x.
 257. Inoue J . Effects of stimulus intensity on sound localization in the horizontal and upper‐hemispheric median plane. J UOEH 23: 127‐138, 2001.
 258. Irvine DR , Gago G . Binaural interaction in high‐frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences. J Neurophysiol 63: 570‐591, 1990.
 259. Irvine DR , Park VN , Mattingley JB . Responses of neurons in the inferior colliculus of the rat to interaural time and intensity differences in transient stimuli: implications for the latency hypotheses. Hear Res 85: 127‐141, 1995.
 260. Irvine DR , Park VN , McCormick L . Mechanisms underlying the sensitivity of neurons in the lateral superior olive to interaural intensity differences. J Neurophysiol 86: 2647‐2666, 2001.
 261. Irvine DR , Rajan R , Aitkin LM . Sensitivity to interaural intensity differences of neurons in primary auditory cortex of the cat. I. types of sensitivity and effects of variations in sound pressure level. J Neurophysiol 75: 75‐96, 1996. DOI: 10.1152/jn.1996.75.1.75.
 262. Ivarsson C , De Ribaupierre Y , De Ribaupierre F . Influence of auditory localization cues on neuronal activity in the auditory thalamus of the cat. J Neurophysiol 59: 586‐606, 1988.
 263. Javel E . Coding of AM tones in the chinchilla auditory nerve: implications for the pitch of complex tones. J Acoust Soc Am 68: 133‐146, 1980.
 264. Jay MF , Sparks DL . Localization of auditory and visual targets for the initiation of saccadic eye movements. In: Berkley MA , Stebbins WC , editors. Wiley Series in Neuroscience, Vol 2 Comparative Perception, Vo 1 Basic Mechanisms. Oxford, UK: John Wiley & Sons, 1990, p. 351‐374.
 265. Jeffress LA . A place theory of sound localization. J Comp Physiol Psychol 41: 35‐39, 1948.
 266. Jenkins WM , Masterton RB . Sound localization: effects of unilateral lesions in central auditory system. J Neurophysiol 47: 987‐1016, 1982.
 267. Jenkins WM , Merzenich MM . Role of cat primary auditory cortex for sound‐localization behavior. J Neurophysiol 52: 819‐847, 1984.
 268. Jercog PE , Svirskis G , Kotak VC , Sanes DH , Rinzel J . Asymmetric excitatory synaptic dynamics underlie interaural time difference processing in the auditory system. PLoS Biol 8: e1000406, 2010. DOI: 10.1371/journal.pbio.1000406.
 269. Jiang D , McAlpine D , Palmer AR . Detectability index measures of binaural masking level difference across populations of inferior colliculus neurons. J Neurosci 17: 9331‐9339, 1997.
 270. Jiang D , McAlpine D , Palmer AR . Responses of neurons in the inferior colliculus to binaural masking level difference stimuli measured by rate‐versus‐level functions. J Neurophysiol 77: 3085‐3106, 1997.
 271. Johannesma PIM . Dynamical aspects of the transmission of stochastic neural signals. In: Broda E , Locker A , Springer‐Lederer H , editors. Proceedings First European Biophysics Congress. Vienna: Verlag der Medizinische Akademie, 1971, p. 329‐333.
 272. Johnson DH . The relationship between spike rate and synchrony in responses of auditory‐nerve fibers to single tones. J Acoust Soc Am 68: 1115‐1122, 1980.
 273. Joris P , Yin TC . A matter of time: internal delays in binaural processing. Trends Neurosci 30: 70‐78, 2007. DOI: 10.1016/j.tins.2006.12.004.
 274. Joris PX . Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. J Neurophysiol 76: 2137‐2156, 1996.
 275. Joris PX . Response classes in the dorsal cochlear nucleus and its output tract in the chloralose‐anesthetized cat. J Neurosci 18: 3955‐3966, 1998.
 276. Joris PX . Interaural time sensitivity dominated by cochlea‐induced envelope patterns. J Neurosci 23: 6345‐6350, 2003.
 277. Joris PX , Carney LH , Smith PH , Yin TC . Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71: 1022‐1036, 1994.
 278. Joris PX , Louage DH , Cardoen L , van der Heijden M . Correlation index: a new metric to quantify temporal coding. Hear Res 216‐217: 19‐30, 2006. DOI: 10.1016/j.heares.2006.03.010.
 279. Joris PX , Michelet P , Franken TP , McLaughlin M . Variations on a Dexterous theme: peripheral time‐intensity trading. Hear Res 238: 49‐57, 2008. DOI: 10.1016/j.heares.2007.11.011.
 280. Joris PX , Schreiner CE , Rees A . Neural processing of amplitude‐modulated sounds. Physiol Rev 84: 541‐577, 2004. DOI: 10.1152/physrev.00029.2003.
 281. Joris PX , Smith PH . Temporal and binaural properties in dorsal cochlear nucleus and its output tract. J Neurosci 18: 10157‐10170, 1998.
 282. Joris PX , Smith PH . The volley theory and the spherical cell puzzle. Neuroscience 154: 65‐76, 2008. DOI: 10.1016/j.neuroscience.2008.03.002.
 283. Joris PX , Smith PH , Yin TC . Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J Neurophysiol 71: 1037‐1051, 1994.
 284. Joris PX , Smith PH , Yin TC . Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21: 1235‐1238, 1998.
 285. Joris PX , Trussell LO . The calyx of Held: a hypothesis on the need for reliable timing in an intensity‐difference encoder. Neuron 100: 534‐549, 2018. DOI: 10.1016/j.neuron.2018.10.026.
 286. Joris PX , Van de Sande B , Louage DH , van der Heijden M . Binaural and cochlear disparities. Proc Natl Acad Sci U S A 103: 12917‐12922, 2006. DOI: 10.1073/pnas.0601396103.
 287. Joris PX , van de Sande B , Recio‐Spinoso A , van der Heijden M . Auditory midbrain and nerve responses to sinusoidal variations in interaural correlation. J Neurosci 26: 279‐289, 2006. DOI: 10.1523/JNEUROSCI.2285‐05.2006.
 288. Joris PX , Van De Sande B , van der Heijden M . Temporal damping in response to broadband noise. I. Inferior colliculus. J Neurophysiol 93: 1857‐1870, 2005. DOI: 10.1152/jn.00962.2004.
 289. Joris PX , Yin TC . Responses to amplitude‐modulated tones in the auditory nerve of the cat. J Acoust Soc Am 91: 215‐232, 1992.
 290. Joris PX , Yin TC . Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73: 1043‐1062, 1995.
 291. Joris PX , Yin TC . Envelope coding in the lateral superior olive. III. Comparison with afferent pathways. J Neurophysiol 79: 253‐269, 1998.
 292. Juiz JM , Helfert RH , Bonneau JM , Wenthold RJ , Altschuler RA . Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig. J Comp Neurol 373: 11‐26, 1996. DOI: 10.1002/(SICI)1096‐9861(19960909)373:1<11::AID‐CNE2>3.0.CO;2‐G.
 293. Kadner A , Berrebi AS . Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat. Neuroscience 151: 868‐887, 2008. DOI: 10.1016/j.neuroscience.2007.11.008.
 294. Kadner A , Kulesza RJ Jr , Berrebi AS . Neurons in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat may play a role in sound duration coding. J Neurophysiol 95: 1499‐1508, 2006. DOI: 10.1152/jn.00902.2005.
 295. Kalmykova IV . Investigation of the precedence effect in the cat auditory system. Sens Syst 7: 208‐211, 1993.
 296. Kandler K , Friauf E . Development of electrical membrane properties and discharge characteristics of superior olivary complex neurons in fetal and postnatal rats. Eur J Neurosci 7: 1773‐1790, 1995.
 297. Kane EC . Octopus cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons. Int J Neurosci 5: 251‐279, 1973.
 298. Kane ES , Puglisi SG , Gordon BS . Neuronal types in the deep dorsal cochlear nucleus of the cat: I. Giant neurons. J Comp Neurol 198: 483‐513, 1981. DOI: 10.1002/cne.901980308.
 299. Kanold PO , Manis PB . Transient potassium currents regulate the discharge patterns of dorsal cochlear nucleus pyramidal cells. J Neurosci 19: 2195‐2208, 1999.
 300. Kanold PO , Manis PB . A physiologically based model of discharge pattern regulation by transient K+ currents in cochlear nucleus pyramidal cells. J Neurophysiol 85: 523‐538, 2001.
 301. Kanold PO , Young ED . Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21: 7848‐7858, 2001.
 302. Kapfer C , Seidl AH , Schweizer H , Grothe B . Experience‐dependent refinement of inhibitory inputs to auditory coincidence‐detector neurons. Nat Neurosci 5: 247‐253, 2002. DOI: 10.1038/nn810.
 303. Karino S , Smith PH , Yin TC , Joris PX . Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re‐examination. J Neurosci 31: 3016‐3031, 2011. DOI: 10.1523/JNEUROSCI.5175‐10.2011.
 304. Kavanagh GL , Kelly JB . Midline and lateral field sound localization in the ferret (Mustela putorius): contribution of the superior olivary complex. J Neurophysiol 67: 1643‐1658, 1992.
 305. Keine C , Rubsamen R . Inhibition shapes acoustic responsiveness in spherical bushy cells. J Neurosci 35: 8579‐8592, 2015. DOI: 10.1523/JNEUROSCI.0133‐15.2015.
 306. Keine C , Rubsamen R , Englitz B . Signal integration at spherical bushy cells enhances representation of temporal structure but limits its range. Elife 6: 2017. DOI: 10.7554/eLife.29639.
 307. Keller CH , Takahashi TT . Responses to simulated echoes by neurons in the barn owl's auditory space map. J Comp Physiol A 178: 499‐512, 1996.
 308. Kelly JB . Localization of paired sound sources in the rat: small time differences. J Acoust Soc Am 55: 1277‐1284, 1974.
 309. Kelly JB , Buckthought AD , Kidd SA . Monaural and binaural response properties of single neurons in the rat's dorsal nucleus of the lateral lemniscus. Hear Res 122: 25‐40, 1998.
 310. Kelly JB , Kavanagh GL . Sound localization after unilateral lesions of inferior colliculus in the ferret (Mustela putorius). J Neurophysiol 71: 1078‐1087, 1994.
 311. Khurana S , Liu Z , Lewis AS , Rosa K , Chetkovich D , Golding NL . An essential role for modulation of hyperpolarization‐activated current in the development of binaural temporal precision. J Neurosci 32: 2814‐2823, 2012. DOI: 10.1523/JNEUROSCI.3882‐11.2012.
 312. Khurana S , Remme MW , Rinzel J , Golding NL . Dynamic interaction of Ih and IK‐LVA during trains of synaptic potentials in principal neurons of the medial superior olive. J Neurosci 31: 8936‐8947, 2011. DOI: 10.1523/JNEUROSCI.1079‐11.2011.
 313. Kiang NYS . Peripheral neural processing of auditory information. In: Brookhart JM , Mountcastle VB , editors. Handbook of Physiology, The Nervous System III, Sensory Processes. Bethesda, MD: American Physiological Society, 1984, p. 639‐674.
 314. Kim DO , Bishop B , Kuwada S . Acoustic cues for sound source distance and azimuth in rabbits, a racquetball and a rigid spherical model. J Assoc Res Otolaryngol 11: 541‐557, 2010. DOI: 10.1007/s10162‐010‐0221‐8.
 315. Kim DO , Moiseff A , Turner JB , Gull J . Acoustic cues underlying auditory distance in barn owls. Acta Otolaryngol 128: 382‐387, 2008. DOI: 10.1080/00016480701840114.
 316. Kim DO , Zahorik P , Carney LH , Bishop BB , Kuwada S . Auditory distance coding in rabbit midbrain neurons and human perception: monaural amplitude modulation depth as a cue. J Neurosci 35: 5360‐5372, 2015. DOI: 10.1523/JNEUROSCI.3798‐14.2015.
 317. Kim PJ , Young ED . Comparative analysis of spectro‐temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory‐nerve fibers. J Acoust Soc Am 95: 410‐422, 1994.
 318. King AJ , Palmer AR . Cells responsive to free‐field auditory stimuli in guinea‐pig superior colliculus: distribution and response properties. J Physiol 342: 361‐381, 1983.
 319. Kiss A , Majorossy K . Neuron morphology and synaptic architecture in the medial superior olivary nucleus. Light‐ and electron microscope studies in the cat. Exp Brain Res 52: 315‐327, 1983.
 320. Klumpp RG , Eady HR . Some measurements of interaural time difference thresholds. J Acoust Soc Am 28: 859‐860, 1956.
 321. Knudsen EI . Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2: 1177‐1194, 1982.
 322. Koch U , Braun M , Kapfer C , Grothe B . Distribution of HCN1 and HCN2 in rat auditory brainstem nuclei. Eur J Neurosci 20: 79‐91, 2004. DOI: 10.1111/j.0953‐816X.2004.03456.x.
 323. Kolston J , Osen KK , Hackney CM , Ottersen OP , Storm‐Mathisen J . An atlas of glycine‐ and GABA‐like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol (Berl) 186: 443‐465, 1992.
 324. Kopp‐Scheinpflug C , Lippe WR , Dorrscheidt GJ , Rubsamen R . The medial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre‐ and postsynaptic activity. J Assoc Res Otolaryngol 4: 1‐23, 2003. DOI: 10.1007/s10162‐002‐2010‐5.
 325. Kopp‐Scheinpflug C , Pigott BM , Forsythe ID . Nitric oxide selectively suppresses IH currents mediated by HCN1‐containing channels. J Physiol 593: 1685‐1700, 2015. DOI: 10.1113/jphysiol.2014.282194.
 326. Kopp‐Scheinpflug C , Tozer AJ , Robinson SW , Tempel BL , Hennig MH , Forsythe ID . The sound of silence: ionic mechanisms encoding sound termination. Neuron 71: 911‐925, 2011. DOI: 10.1016/j.neuron.2011.06.028.
 327. Kotak VC , Sanes DH . Long‐lasting inhibitory synaptic depression is age‐ and calcium‐dependent. J Neurosci 20: 5820‐5826, 2000.
 328. Kotak VC , Sanes DH . Developmental expression of inhibitory synaptic long‐term potentiation in the lateral superior olive. Front Neural Circuits 8: 67, 2014. DOI: 10.3389/fncir.2014.00067.
 329. Kramer F , Griesemer D , Bakker D , Brill S , Franke J , Frotscher E , Friauf E . Inhibitory glycinergic neurotransmission in the mammalian auditory brainstem upon prolonged stimulation: short‐term plasticity and synaptic reliability. Front Neural Circuits 8: 14, 2014. DOI: 10.3389/fncir.2014.00014.
 330. Kuenzel T , Borst JG , van der Heijden M . Factors controlling the input‐output relationship of spherical bushy cells in the gerbil cochlear nucleus. J Neurosci 31: 4260‐4273, 2011. DOI: 10.1523/JNEUROSCI.5433‐10.2011.
 331. Kulesza RJ Jr . Cytoarchitecture of the human superior olivary complex: nuclei of the trapezoid body and posterior tier. Hear Res 241: 52‐63, 2008. DOI: 10.1016/j.heares.2008.04.010.
 332. Kulesza RJ Jr . Cytoarchitecture of the human superior olivary complex: medial and lateral superior olive. Hear Res 225: 80‐90, 2007. DOI: 10.1016/j.heares.2006.12.006.
 333. Kulesza RJ Jr . Characterization of human auditory brainstem circuits by calcium‐binding protein immunohistochemistry. Neuroscience 258: 318‐331, 2014. DOI: 10.1016/j.neuroscience.2013.11.035.
 334. Kulesza RJ Jr , Berrebi AS . Superior paraolivary nucleus of the rat is a GABAergic nucleus. J Assoc Res Otolaryngol 1: 255‐269, 2000.
 335. Kulesza RJ Jr , Kadner A , Berrebi AS . Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 97: 1610‐1620, 2007. DOI: 10.1152/jn.00613.2006.
 336. Kulesza RJ Jr , Spirou GA , Berrebi AS . Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 89: 2299‐2312, 2003. DOI: 10.1152/jn.00547.2002.
 337. Kulkarni A , Colburn HS . Role of spectral detail in sound‐source localization. Nature 396: 747‐749, 1998. DOI: 10.1038/25526.
 338. Kuo SP , Lu HW , Trussell LO . Intrinsic and synaptic properties of vertical cells of the mouse dorsal cochlear nucleus. J Neurophysiol 108: 1186‐1198, 2012. DOI: 10.1152/jn.00778.2011.
 339. Kuwabara N , DiCaprio RA , Zook JM . Afferents to the medial nucleus of the trapezoid body and their collateral projections. J Comp Neurol 314: 684‐706, 1991. DOI: 10.1002/cne.903140405.
 340. Kuwabara N , Zook JM . Classification of the principal cells of the medial nucleus of the trapezoid body. J Comp Neurol 314: 707‐720, 1991. DOI: 10.1002/cne.903140406.
 341. Kuwabara N , Zook JM . Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J Comp Neurol 324: 522‐538, 1992. DOI: 10.1002/cne.903240406.
 342. Kuwabara N , Zook JM . Local collateral projections from the medial superior olive to the superior paraolivary nucleus in the gerbil. Brain Res 846: 59‐71, 1999.
 343. Kuwada S , Batra R . Coding of sound envelopes by inhibitory rebound in neurons of the superior olivary complex in the unanesthetized rabbit. J Neurosci 19: 2273‐2287, 1999.
 344. Kuwada S , Batra R , Yin TC , Oliver DL , Haberly LB , Stanford TR . Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17: 7565‐7581, 1997.
 345. Kuwada S , Bishop B , Alex C , Condit DW , Kim DO . Spatial tuning to sound‐source azimuth in the inferior colliculus of unanesthetized rabbit. J Neurophysiol 106: 2698‐2708, 2011. DOI: 10.1152/jn.00532.2011.
 346. Kuwada S , Bishop B , Kim DO . Approaches to the study of neural coding of sound source location and sound envelope in real environments. Front Neural Circuits 6: 1‐12, 2012. DOI: 10.3389/fncir.2012.00042.
 347. Kuwada S , Bishop B , Kim DO . Azimuth and envelope coding in the inferior colliculus of the unanesthetized rabbit: effect of reverberation and distance. J Neurophysiol 112: 1340‐1355, 2014. DOI: 10.1152/jn.00826.2013.
 348. Kuwada S , Stanford TR , Batra R . Interaural phase‐sensitive units in the inferior colliculus of the unanesthetized rabbit: effects of changing frequency. J Neurophysiol 57: 1338‐1360, 1987.
 349. Kuwada S , Yin TC . Binaural interaction in low‐frequency neurons in inferior colliculus of the cat. I. Effects of long interaural delays, intensity, and repetition rate on interaural delay function. J Neurophysiol 50: 981‐999, 1983.
 350. Kuwada S , Yin TC , Wickesberg RE . Response of cat inferior colliculus neurons to binaural beat stimuli: possible mechanisms for sound localization. Science 206: 586‐588, 1979.
 351. Lane CC , Delgutte B . Neural correlates and mechanisms of spatial release from masking: single‐unit and population responses in the inferior colliculus. J Neurophysiol 94: 1180‐1198, 2005. DOI: 10.1152/jn.01112.2004.
 352. Langford TL . Responses elicited from medial superior olivary neurons by stimuli associated with binaural masking and unmasking. Hear Res 15: 39‐50, 1984.
 353. Larsen E , Liberman MC . Contralateral cochlear effects of ipsilateral damage: no evidence for interaural coupling. Hear Res 260: 70‐80, 2010. DOI: 10.1016/j.heares.2009.11.011.
 354. Lavine RA . Phase‐locking in response of single neurons in cochlear nucler complex of the cat to low‐frequency tonal stimuli. J Neurophysiol 34: 467‐483, 1971.
 355. Leao KE , Leao RN , Walmsley B . Modulation of dendritic synaptic processing in the lateral superior olive by hyperpolarization‐activated currents. Eur J Neurosci 33: 1462‐1470, 2011. DOI: 10.1111/j.1460‐9568.2011.07627.x.
 356. Lee Y , Lopez DE , Meloni EG , Davis M . A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J Neurosci 16: 3775‐3789, 1996.
 357. Leijon SC , Peyda S , Magnusson AK . Temporal processing capacity in auditory‐deprived superior paraolivary neurons is rescued by sequential plasticity during early development. Neuroscience 337: 315‐330, 2016. DOI: 10.1016/j.neuroscience.2016.09.014.
 358. Lesica NA , Lingner A , Grothe B . Population coding of interaural time differences in gerbils and barn owls. J Neurosci 30: 11696‐11702, 2010. DOI: 10.1523/JNEUROSCI.0846‐10.2010.
 359. Levine RA , Gardner JC , Fullerton BC , Stufflebeam SM , Carlisle EW , Furst M , Rosen BR , Kiang NY . Effects of multiple sclerosis brainstem lesions on sound lateralization and brainstem auditory evoked potentials. Hear Res 68: 73‐88, 1993.
 360. Levine RA , Gardner JC , Stufflebeam SM , Fullerton BC , Carlisle EW , Furst M , Rosen BR , Kiang NY . Binaural auditory processing in multiple sclerosis subjects. Hear Res 68: 59‐72, 1993.
 361. Li L , Kelly JB . Binaural responses in rat inferior colliculus following kainic acid lesions of the superior olive: interaural intensity difference functions. Hear Res 61: 73‐85, 1992.
 362. Liberman MC . Auditory‐nerve response from cats raised in a low‐noise chamber. J Acoust Soc Am 63: 442‐455, 1978.
 363. Liberman MC . Morphological differences among radial afferent fibers in the cat cochlea: an electron‐microscopic study of serial sections. Hear Res 3: 45‐63, 1980.
 364. Liberman MC . The cochlear frequency map for the cat: labeling auditory‐nerve fibers of known characteristic frequency. J Acoust Soc Am 72: 1441‐1449, 1982.
 365. Liberman MC . Central projections of auditory‐nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J Comp Neurol 313: 240‐258, 1991. DOI: 10.1002/cne.903130205.
 366. Liberman MC . Central projections of auditory nerve fibers of differing spontaneous rate, II: posteroventral and dorsal cochlear nuclei. J Comp Neurol 327: 17‐36, 1993. DOI: 10.1002/cne.903270103.
 367. Liberman MC , Gao J , He DZ , Wu X , Jia S , Zuo J . Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419: 300‐304, 2002. DOI: 10.1038/nature01059.
 368. Liberman MC , Oliver ME . Morphometry of intracellularly labeled neurons of the auditory nerve: correlations with functional properties. J Comp Neurol 223: 163‐176, 1984. DOI: 10.1002/cne.902230203.
 369. Licklider JC . The influence of interaural phase relations upon the masking of speech by white noise. J Acoust Soc Am 20: 150‐159, 1948.
 370. Licklider JC . A duplex theory of pitch perception. Experientia 7: 128‐134, 1951.
 371. Lindemann W . Extension of a binaural cross‐correlation model by contralateral inhibition. I. Simulation of lateralization for stationary signals. J Acoust Soc Am 80: 1608‐1622, 1986.
 372. Lindsey BG . Fine structure and distribution of axon terminals from the cochlear nucleus on neurons in the medial superior olivary nucleus of the cat. J Comp Neurol 160: 81‐103, 1975. DOI: 10.1002/cne.901600106.
 373. Litovsky RY , Colburn HS , Yost WA , Guzman SJ . The precedence effect. J Acoust Soc Am 106: 1633‐1654, 1999.
 374. Litovsky RY , Delgutte B . Neural correlates of the precedence effect in the inferior colliculus: effect of localization cues. J Neurophysiol 87: 976‐994, 2002.
 375. Litovsky RY , Fligor BJ , Tramo MJ . Functional role of the human inferior colliculus in binaural hearing. Hear Res 165: 177‐188, 2002.
 376. Litovsky RY , Yin TC . Physiological studies of the precedence effect in the inferior colliculus of the cat. I. Correlates of psychophysics. J Neurophysiol 80: 1285‐1301, 1998.
 377. Litovsky RY , Yin TC . Physiological studies of the precedence effect in the inferior colliculus of the cat. II. Neural mechanisms. J Neurophysiol 80: 1302‐1316, 1998.
 378. Liu C , Glowatzki E , Fuchs PA . Unmyelinated type II afferent neurons report cochlear damage. Proc Natl Acad Sci U S A 112: 14723‐14727, 2015. DOI: 10.1073/pnas.1515228112.
 379. Loftus WC , Bishop DC , Saint Marie RL , Oliver DL . Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472: 330‐344, 2004. DOI: 10.1002/cne.20070.
 380. Lomber SG , Malhotra S . Double dissociation of ‘what’ and ‘where’ processing in auditory cortex. Nat Neurosci 11: 609‐616, 2008. DOI: 10.1038/nn.2108.
 381. Lopez DE , Merchan MA , Bajo VM , Saldana E . The cochlear root neurons in the rat, mouse, and gerbil. In: Merchan MA , Juis JM , Godfrey DA , editors. The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum Press, 1993, p. 291‐301.
 382. Lopez DE , Saldana E , Nodal FR , Merchan MA , Warr WB . Projections of cochlear root neurons, sentinels of the rat auditory pathway. J Comp Neurol 415: 160‐174, 1999.
 383. Lorente de No R . The Primary Acoustic Nuclei. Ann Arbor, MI: Raven Press, 1981, p. 177.
 384. Lorteije JA , Rusu SI , Kushmerick C , Borst JG . Reliability and precision of the mouse calyx of Held synapse. J Neurosci 29: 13770‐13784, 2009. DOI: 10.1523/JNEUROSCI.3285‐09.2009.
 385. Louage DH , Joris PX , van der Heijden M . Decorrelation sensitivity of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise. J Neurosci 26: 96‐108, 2006. DOI: 10.1523/JNEUROSCI.2339‐05.2006.
 386. Louage DH , van der Heijden M , Joris PX . Temporal properties of responses to broadband noise in the auditory nerve. J Neurophysiol 91: 2051‐2065, 2004. DOI: 10.1152/jn.00816.2003.
 387. Louage DH , van der Heijden M , Joris PX . Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise. J Neurosci 25: 1560‐1570, 2005. DOI: 10.1523/JNEUROSCI.4742‐04.2005.
 388. Lu HW , Smith PH , Joris PX . Submillisecond monaural coincidence detection by octopus cells. Acta Acust united Ac 104: 852‐855, 2018.
 389. Lu HW , Trussell LO . Spontaneous activity defines effective convergence ratios in an inhibitory circuit. J Neurosci 36: 3268‐3280, 2016. DOI: 10.1523/JNEUROSCI.3499‐15.2016.
 390. Luling H , Siveke I , Grothe B , Leibold C . Frequency‐invariant representation of interaural time differences in mammals. PLoS Comput Biol 7: e1002013, 2011. DOI: 10.1371/journal.pcbi.1002013.
 391. Ma WL , Brenowitz SD . Single‐neuron recordings from unanesthetized mouse dorsal cochlear nucleus. J Neurophysiol 107: 824‐835, 2012. DOI: 10.1152/jn.00427.2011.
 392. Macpherson EA , Middlebrooks JC . Localization of brief sounds: effects of level and background noise. J Acoust Soc Am 108: 1834‐1849, 2000.
 393. Magnusson AK , Kapfer C , Grothe B , Koch U . Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset. J Physiol 568: 497‐512, 2005. DOI: 10.1113/jphysiol.2005.094763.
 394. Mahendrasingam S , Wallam CA , Polwart A , Hackney CM . An immunogold investigation of the distribution of GABA and glycine in nerve terminals on the somata of spherical bushy cells in the anteroventral cochlear nucleus of guinea pig. Eur J Neurosci 19: 993‐1004, 2004.
 395. Maison S , Liberman LD , Liberman MC . Type II cochlear ganglion neurons do not drive the olivocochlear reflex: re‐examination of the cochlear phenotype in peripherin knock‐out mice. eNeuro 3: 2016. DOI: 10.1523/ENEURO.0207‐16.2016.
 396. Makous JC , Middlebrooks JC . Two‐dimensional sound localization by human listeners. J Acoust Soc Am 87: 2188‐2200, 1990.
 397. Malhotra S , Hall AJ , Lomber SG . Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas. J Neurophysiol 92: 1625‐1643, 2004. DOI: 10.1152/jn.01205.2003.
 398. Malhotra S , Lomber SG . Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat. J Neurophysiol 97: 26‐43, 2007. DOI: 10.1152/jn.00720.2006.
 399. Malhotra S , Stecker GC , Middlebrooks JC , Lomber SG . Sound localization deficits during reversible deactivation of primary auditory cortex and/or the dorsal zone. J Neurophysiol 99: 1628‐1642, 2008. DOI: 10.1152/jn.01228.2007.
 400. Manis PB . Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J Neurosci 10: 2338‐2351, 1990.
 401. Manis PB , Marx SO . Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11: 2865‐2880, 1991.
 402. Manis PB , Spirou GA , Wright DD , Paydar S , Ryugo DK . Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J Comp Neurol 348: 261‐276, 1994. DOI: 10.1002/cne.903480208.
 403. Manis PB , Xie R , Wang Y , Marrs GS , Spirou GA . The endbulbs of Held. In: Trussell LO , Popper AN , Fay RR , editors. Synaptic Mechanisms in the Auditory System. New York: Springer, 2012, p. 61‐93.
 404. Manley GA , Koppl C , Konishi M . A neural map of interaural intensity differences in the brain stem of the barn owl. J Neurosci 8: 2665‐2676, 1988.
 405. Mao J , Carney LH . Binaural detection with narrowband and wideband reproducible noise maskers. IV. Models using interaural time, level, and envelope differences. J Acoust Soc Am 135: 824‐837, 2014. DOI: 10.1121/1.4861848.
 406. Marquardt T , McApline D . A pi‐limit for coding ITDs, implications for binaural models. In: Kollmeier B , Klump GM , Homann V , Langemann U , Mauermann M , Uppenkamp S , Verhey J , editors. Hearing – From Sensory Processing to Perception. Berlin: Springer‐Verlag, 2007, p. 407‐416.
 407. Mast TE . Binaural interaction and contralateral inhibition in dorsal cochlear nucleus of the chinchilla. J Neurophysiol 33: 108‐115, 1970. DOI: 10.1152/jn.1970.33.1.108.
 408. Mast TE . Dorsal cochlear nucleus of the chinchilla: excitation by contralateral sound. Brain Res 62: 61‐70, 1973.
 409. Masterton RB , Granger EM . Role of the acoustic striae in hearing: contribution of dorsal and intermediate striae to detection of noises and tones. J Neurophysiol 60: 1841‐1860, 1988.
 410. Masterton RB , Granger EM , Glendenning KK . Role of acoustic striae in hearing: mechanism for enhancement of sound detection in cats. Hear Res 73: 209‐222, 1994.
 411. Mathews PJ , Jercog PE , Rinzel J , Scott LL , Golding NL . Control of submillisecond synaptic timing in binaural coincidence detectors by K(v)1 channels. Nat Neurosci 13: 601‐609, 2010. DOI: 10.1038/nn.2530.
 412. May BJ . Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear Res 148: 74‐87, 2000.
 413. May BJ , Prell GS , Sachs MB . Vowel representations in the ventral cochlear nucleus of the cat: effects of level, background noise, and behavioral state. J Neurophysiol 79: 1755‐1767, 1998.
 414. Mayer F , Albrecht O , Dondzillo A , Klug A . Glycinergic inhibition to the medial nucleus of the trapezoid body shows prominent facilitation and can sustain high levels of ongoing activity. J Neurophysiol 112: 2901‐2915, 2014. DOI: 10.1152/jn.00864.2013.
 415. Mc Laughlin M , van der Heijden M , Joris PX . How secure is in vivo synaptic transmission at the calyx of Held? J Neurosci 28: 10206‐10219, 2008. DOI: 10.1523/JNEUROSCI.2735‐08.2008.
 416. Mc Laughlin M , Verschooten E , Joris PX . Oscillatory dipoles as a source of phase shifts in field potentials in the mammalian auditory brainstem. J Neurosci 30: 13472‐13487, 2010. DOI: 10.1523/JNEUROSCI.0294‐10.2010.
 417. McAlpine D , Jiang D , Palmer AR . Binaural masking level differences in the inferior colliculus of the guinea pig. J Acoust Soc Am 100: 490‐503, 1996.
 418. McAlpine D , Jiang D , Palmer AR . Interaural delay sensitivity and the classification of low best‐frequency binaural responses in the inferior colliculus of the guinea pig. Hear Res 97: 136‐152, 1996.
 419. McAlpine D , Jiang D , Palmer AR . A neural code for low‐frequency sound localization in mammals. Nat Neurosci 4: 396‐401, 2001. DOI: 10.1038/86049.
 420. McAlpine D , Jiang D , Shackleton TM , Palmer AR . Convergent input from brainstem coincidence detectors onto delay‐sensitive neurons in the inferior colliculus. J Neurosci 18: 6026‐6039, 1998.
 421. McAlpine D , Palmer AR . Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci 22: 1443‐1453, 2002.
 422. McFadden D . Letter: precedence effects and auditory cells with long characteristic delays. J Acoust Soc Am 54: 528‐530, 1973.
 423. Merchan MA , Collia F , Lopez DE , Saldana E . Morphology of cochlear root neurons in the rat. J Neurocytol 17: 711‐725, 1988.
 424. Meredith MA , Stein BE . Descending efferents from the superior colliculus relay integrated multisensory information. Science 227: 657‐659, 1985.
 425. Mershon DH , Bowers JN . Absolute and relative cues for the auditory perception of egocentric distance. Perception 8: 311‐322, 1979. DOI: 10.1068/p080311.
 426. Michelet P , Kovacic D , Joris PX . Ongoing temporal coding of a stochastic stimulus as a function of intensity: time‐intensity trading. J Neurosci 32: 9517‐9527, 2012. DOI: 10.1523/JNEUROSCI.0103‐12.2012.
 427. Mickey BJ , Middlebrooks JC . Responses of auditory cortical neurons to pairs of sounds: correlates of fusion and localization. J Neurophysiol 86: 1333‐1350, 2001.
 428. Mickey BJ , Middlebrooks JC . Sensitivity of auditory cortical neurons to the locations of leading and lagging sounds. J Neurophysiol 94: 979‐989, 2005. DOI: 10.1152/jn.00580.2004.
 429. Middlebrooks JC , Knudsen EI . A neural code for auditory space in the cat's superior colliculus. J Neurosci 4: 2621‐2634, 1984.
 430. Middlebrooks JC , Knudsen EI . Changes in external ear position modify the spatial tuning of auditory units in the cat's superior colliculus. J Neurophysiol 57: 672‐687, 1987.
 431. Mills AW . On the minimum audible angle. J Acoust Soc Am 30: 237‐246, 1958.
 432. Mlynarski W , Jost J . Statistics of natural binaural sounds. PLoS One 9: e108968, 2014. DOI: 10.1371/journal.pone.0108968.
 433. Mogdans J , Knudsen EI . Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl's auditory system. Hear Res 74: 148‐164, 1994.
 434. Moller AR . Dynamic properties of the responses of single neurones in the cochlear nucleus of the rat. J Physiol 259: 63‐82, 1976.
 435. Moore BC . The role of temporal fine structure processing in pitch perception, masking, and speech perception for normal‐hearing and hearing‐impaired people. J Assoc Res Otolaryngol 9: 399‐406, 2008. DOI: 10.1007/s10162‐008‐0143‐x.
 436. Moore BCJ . An Introduction to the Psychology of Hearing. London: Academic Press, 1982, p. 293.
 437. Moore DR . Auditory brainstem of the ferret: sources of projections to the inferior colliculus. J Comp Neurol 269: 342‐354, 1988. DOI: 10.1002/cne.902690303.
 438. Moore DR , Russell FA , Cathcart NC . Lateral superior olive projections to the inferior colliculus in normal and unilaterally deafened ferrets. J Comp Neurol 357: 204‐216, 1995. DOI: 10.1002/cne.903570203.
 439. Moore JK . Organization of the human superior olivary complex. Microsc Res Tech 51: 403‐412, 2000. DOI: 10.1002/1097‐0029(20001115)51:4<403::AID‐JEMT8>3.0.CO;2‐Q.
 440. Moore JK , Moore RY . A comparative study of the superior olivary complex in the primate brain. Folia Primatol (Basel) 16: 35‐51, 1971. DOI: 10.1159/000155390.
 441. Moore MJ , Caspary DM . Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3: 237‐242, 1983.
 442. Morest DK . The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo‐cochlear bundle. Brain Res 9: 288‐311, 1968.
 443. Morest DK . The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z Anat Entwicklungsgesch 127: 201‐220, 1968.
 444. Morrison D , Schindler RA , Wersall J . A quantitative analysis of the afferent innervation of the organ of corti in guinea pig. Acta Otolaryngol 79: 11‐23, 1975.
 445. Mossop JE , Culling JF . Lateralization of large interaural delays. J Acoust Soc Am 104: 1574‐1579, 1998.
 446. Mugnaini E , Osen KK , Dahl AL , Friedrich VL Jr , Korte G . Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. J Neurocytol 9: 537‐570, 1980.
 447. Mugnaini E , Warr WB , Osen KK . Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J Comp Neurol 191: 581‐606, 1980. DOI: 10.1002/cne.901910406.
 448. Muniak MA , Ryugo DK . Tonotopic organization of vertical cells in the dorsal cochlear nucleus of the CBA/J mouse. J Comp Neurol 522: 937‐949, 2014. DOI: 10.1002/cne.23454.
 449. Musicant AD , Chan JC , Hind JE . Direction‐dependent spectral properties of cat external ear: new data and cross‐species comparisons. J Acoust Soc Am 87: 757‐781, 1990.
 450. Myoga MH , Lehnert S , Leibold C , Felmy F , Grothe B . Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat Commun 5: 3790, 2014. DOI: 10.1038/ncomms4790.
 451. Narayan SS , Temchin AN , Recio A , Ruggero MA . Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae. Science 282: 1882‐1884, 1998.
 452. Nayagam BA , Muniak MA , Ryugo DK . The spiral ganglion: connecting the peripheral and central auditory systems. Hear Res 278: 2‐20, 2011. DOI: 10.1016/j.heares.2011.04.003.
 453. Needham K , Paolini AG . Fast inhibition underlies the transmission of auditory information between cochlear nuclei. J Neurosci 23: 6357‐6361, 2003.
 454. Needham K , Paolini AG . Neural timing, inhibition and the nature of stellate cell interaction in the ventral cochlear nucleus. Hear Res 216‐217: 31‐42, 2006. DOI: 10.1016/j.heares.2006.01.016.
 455. Neher E . Some subtle lessons from the calyx of Held synapse. Biophys J 112: 215‐223, 2017. DOI: 10.1016/j.bpj.2016.12.017.
 456. Nelken I , Young ED . Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli. J Neurophysiol 71: 2446‐2462, 1994.
 457. Newlands SD , Perachio AA . Central projections of the vestibular nerve: a review and single fiber study in the Mongolian gerbil. Brain Res Bull 60: 475‐495, 2003.
 458. Nicol MJ , Walmsley B . Ultrastructural basis of synaptic transmission between endbulbs of Held and bushy cells in the rat cochlear nucleus. J Physiol 539: 713‐723, 2002.
 459. Nordeen KW , Killackey HP , Kitzes LM . Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus . J Comp Neurol 214: 131‐143, 1983. DOI: 10.1002/cne.902140203.
 460. Nothwang HG . Evolution of mammalian sound localization circuits: a developmental perspective. Prog Neurobiol 141: 1‐24, 2016. DOI: 10.1016/j.pneurobio.2016.02.003.
 461. Nothwang HG , Ebbers L , Schluter T , Willaredt MA . The emerging framework of mammalian auditory hindbrain development. Cell Tissue Res 361: 33‐48, 2015. DOI: 10.1007/s00441‐014‐2110‐7.
 462. Nouvian R , Eybalin M , Puel JL . Cochlear efferents in developing adult and pathological conditions. Cell Tissue Res 361: 301‐309, 2015. DOI: 10.1007/s00441‐015‐2158‐z.
 463. Oertel D . Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043‐2053, 1983.
 464. Oertel D , Bal R , Gardner SM , Smith PH , Joris PX . Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc Natl Acad Sci U S A 97: 11773‐11779, 2000. DOI: 10.1073/pnas.97.22.11773.
 465. Oertel D , Wright S , Cao XJ , Ferragamo M , Bal R . The multiple functions of T stellate/multipolar/chopper cells in the ventral cochlear nucleus. Hear Res 276: 61‐69, 2011. DOI: 10.1016/j.heares.2010.10.018.
 466. Oertel D , Wu SH . Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J Comp Neurol 283: 228‐247, 1989. DOI: 10.1002/cne.902830206.
 467. Oertel D , Wu SH , Garb MW , Dizack C . Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurol 295: 136‐154, 1990. DOI: 10.1002/cne.902950112.
 468. Oertel D , Young ED . What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27: 104‐110, 2004. DOI: 10.1016/j.tins.2003.12.001.
 469. Ohlrogge M , Doucet JR , Ryugo DK . Projections of the pontine nuclei to the cochlear nucleus in rats. J Comp Neurol 436: 290‐303, 2001.
 470. Oldfield SR , Parker SP . Acuity of sound localisation: a topography of auditory space. I. Normal hearing conditions. Perception 13: 581‐600, 1984. DOI: 10.1068/p130581.
 471. Oldfield SR , Parker SP . Acuity of sound localisation: a topography of auditory space. II. Pinna cues absent. Perception 13: 601‐617, 1984. DOI: 10.1068/p130601.
 472. Oliver DL . Dorsal cochlear nucleus projections to the inferior colliculus in the cat: a light and electron microscopic study. J Comp Neurol 224: 155‐172, 1984.
 473. Oliver DL . Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction. J Comp Neurol 264: 24‐46, 1987. DOI: 10.1002/cne.902640104.
 474. Oliver DL . Ascending efferent projections of the superior olivary complex. Microsc Res Tech 51: 355‐363, 2000. DOI: 10.1002/1097‐0029(20001115)51:4<355::AID‐JEMT5>3.0.CO;2‐J.
 475. Oliver DL , Beckius GE , Bishop DC , Loftus WC , Batra R . Topography of interaural temporal disparity coding in projections of medial superior olive to inferior colliculus. J Neurosci 23: 7438‐7449, 2003.
 476. Oliver DL , Beckius GE , Shneiderman A . Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography. J Comp Neurol 360: 17‐32, 1995. DOI: 10.1002/cne.903600103.
 477. Ollo C , Schwartz IR . The superior olivary complex in C57BL/6 mice. Am J Anat 155: 349‐373, 1979. DOI: 10.1002/aja.1001550306.
 478. Osen KK . Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136: 453‐484, 1969. DOI: 10.1002/cne.901360407.
 479. Osen KK . The intrinsic organization of the cochlear nuclei. Acta Otolaryngol 67: 352‐359, 1969.
 480. Osen KK . Course and termination of the primary afferents in the cochlear nuclei of the cat. An experimental anatomical study. Arch Ital Biol 108: 21‐51, 1970.
 481. Osen KK , Lopez DE , Slyngstad TA , Ottersen OP , Storm‐Mathisen J . GABA‐like and glycine‐like immunoreactivities of the cochlear root nucleus in rat. J Neurocytol 20: 17‐25, 1991.
 482. Osen KK , Mugnaini E , Dahl AL , Christiansen AH . Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch Ital Biol 122: 169‐212, 1984.
 483. Ostapoff EM , Benson CG , Saint Marie RL . GABA‐ and glycine‐immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381: 500‐512, 1997.
 484. Ostapoff EM , Morest DK . Synaptic organization of globular bushy cells in the ventral cochlear nucleus of the cat: a quantitative study. J Comp Neurol 314: 598‐613, 1991. DOI: 10.1002/cne.903140314.
 485. Palmer AR . Encoding of rapid amplitude fluctuations by Cochlear‐nerve fibres in the guinea‐pig. Arch Otorhinolaryngol 236: 197‐202, 1982.
 486. Palmer AR , Jiang D , Marshall DH . Responses of ventral cochlear nucleus onset and chopper units as a function of signal bandwidth. J Neurophysiol 75: 780‐794, 1996.
 487. Palmer AR , Jiang D , McAlpine D . Neural responses in the inferior colliculus to binaural masking level differences created by inverting the noise in one ear. J Neurophysiol 84: 844‐852, 2000.
 488. Palmer AR , King AJ . The representation of auditory space in the mammalian superior colliculus. Nature 299: 248‐249, 1982.
 489. Palmer AR , Russell IJ . Phase‐locking in the cochlear nerve of the guinea‐pig and its relation to the receptor potential of inner hair‐cells. Hear Res 24: 1‐15, 1986.
 490. Paolini AG , Clarey JC , Needham K , Clark GM . Fast inhibition alters first spike timing in auditory brainstem neurons. J Neurophysiol 92: 2615‐2621, 2004. DOI: 10.1152/jn.00327.2004.
 491. Paolini AG , FitzGerald JV , Burkitt AN , Clark GM . Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear Res 159: 101‐116, 2001.
 492. Parham K , Bonaiuto G , Carlson S , Turner JG , D'Angelo WR , Bross LS , Fox A , Willott JF , Kim DO . Purkinje cell degeneration and control mice: responses of single units in the dorsal cochlear nucleus and the acoustic startle response. Hear Res 148: 137‐152, 2000.
 493. Parham K , Kim DO . Spontaneous and sound‐evoked discharge characteristics of complex‐spiking neurons in the dorsal cochlear nucleus of the unanesthetized decerebrate cat. J Neurophysiol 73: 550‐561, 1995.
 494. Parham K , Zhao HB , Kim DO . Responses of auditory nerve fibers of the unanesthetized decerebrate cat to click pairs as simulated echoes. J Neurophysiol 76: 17‐29, 1996.
 495. Parham K , Zhao HB , Ye Y , Kim DO . Responses of anteroventral cochlear nucleus neurons of the unanesthetized decerebrate cat to click pairs as simulated echoes. Hear Res 125: 131‐146, 1998.
 496. Park TJ . IID sensitivity differs between two principal centers in the interaural intensity difference pathway: the LSO and the IC. J Neurophysiol 79: 2416‐2431, 1998.
 497. Park TJ , Grothe B , Pollak GD , Schuller G , Koch U . Neural delays shape selectivity to interaural intensity differences in the lateral superior olive. J Neurosci 16: 6554‐6566, 1996.
 498. Park TJ , Monsivais P , Pollak GD . Processing of interaural intensity differences in the LSO: role of interaural threshold differences. J Neurophysiol 77: 2863‐2878, 1997.
 499. Park TJ , Pollak GD . GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location. J Neurosci 13: 2050‐2067, 1993.
 500. Pecka M , Brand A , Behrend O , Grothe B . Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J Neurosci 28: 6914‐6925, 2008. DOI: 10.1523/JNEUROSCI.1660‐08.2008.
 501. Pecka M , Zahn TP , Saunier‐Rebori B , Siveke I , Felmy F , Wiegrebe L , Klug A , Pollak GD , Grothe B . Inhibiting the inhibition: a neuronal network for sound localization in reverberant environments. J Neurosci 27: 1782‐1790, 2007. DOI: 10.1523/JNEUROSCI.5335‐06.2007.
 502. Pfeiffer RR . Anteroventral cochlear nucleus: wave forms of extracellularly recorded spike potentials. Science 154: 667‐668, 1966.
 503. Pfeiffer RR . Classification of response patterns of spike discharges for units in the cochlear nucleus: tone‐burst stimulation. Exp Brain Res 1: 220‐235, 1966.
 504. Plauska A , Borst JG , van der Heijden M . Predicting binaural responses from monaural responses in the gerbil medial superior olive. J Neurophysiol 115: 2950‐2963, 2016. DOI: 10.1152/jn.01146.2015.
 505. Plauska A , van der Heijden M , Borst JGG . A test of the stereausis hypothesis for sound localization in mammals. J Neurosci 37: 7278‐7289, 2017. DOI: 10.1523/JNEUROSCI.0233‐17.2017.
 506. Pollak GD . Time is traded for intensity in the bat's auditory system. Hear Res 36: 107‐124, 1988.
 507. Pollak GD . Circuits for processing dynamic interaural intensity disparities in the inferior colliculus. Hear Res 288: 47‐57, 2012. DOI: 10.1016/j.heares.2012.01.011.
 508. Populin LC , Yin TC . Behavioral studies of sound localization in the cat. J Neurosci 18: 2147‐2160, 1998.
 509. Populin LC , Yin TC . Pinna movements of the cat during sound localization. J Neurosci 18: 4233‐4243, 1998.
 510. Portfors CV , Roberts PD . Temporal and frequency characteristics of cartwheel cells in the dorsal cochlear nucleus of the awake mouse. J Neurophysiol 98: 744‐756, 2007. DOI: 10.1152/jn.01356.2006.
 511. Priebe NJ . Mechanisms of orientation selectivity in the primary visual cortex. Annu Rev Vis Sci 2: 85‐107, 2016. DOI: 10.1146/annurev‐vision‐111815‐114456.
 512. Radtke‐Schuller S , Seeler S , Grothe B . Restricted loss of olivocochlear but not vestibular efferent neurons in the senescent gerbil (Meriones unguiculatus). Front Aging Neurosci 7: 4, 2015. DOI: 10.3389/fnagi.2015.00004.
 513. Rajan R . Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization. Brain Res 506: 192‐204, 1990.
 514. Ramachandran R , Davis KA , May BJ . Single‐unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82: 152‐163, 1999.
 515. Ramachandran R , May BJ . Functional segregation of ITD sensitivity in the inferior colliculus of decerebrate cats. J Neurophysiol 88: 2251‐2261, 2002. DOI: 10.1152/jn.00356.2002.
 516. Ramon y Cajal S . Histologie du Systeme Nerveux de l'Homme et des Vertebres. Paris, France: Maloine, 1909.
 517. Rasmussen AT . Studies of the VIIIth cranial nerve of man. Laryngoscope 50: 67‐83, 1940.
 518. Rautenberg PL , Grothe B , Felmy F . Quantification of the three‐dimensional morphology of coincidence detector neurons in the medial superior olive of gerbils during late postnatal development. J Comp Neurol 517: 385‐396, 2009. DOI: 10.1002/cne.22166.
 519. Reale RA , Brugge JF . Auditory cortical neurons are sensitive to static and continuously changing interaural phase cues. J Neurophysiol 64: 1247‐1260, 1990. DOI: 10.1152/jn.1990.64.4.1247.
 520. Reale RA , Brugge JF . Directional sensitivity of neurons in the primary auditory (AI) cortex of the cat to successive sounds ordered in time and space. J Neurophysiol 84: 435‐450, 2000. DOI: 10.1152/jn.2000.84.1.435.
 521. Recio‐Spinoso A . Enhancement and distortion in the temporal representation of sounds in the ventral cochlear nucleus of chinchillas and cats. PLoS One 7: e44286, 2012. DOI: 10.1371/journal.pone.0044286.
 522. Recio‐Spinoso A , Temchin AN , van Dijk P , Fan YH , Ruggero MA . Wiener‐kernel analysis of responses to noise of chinchilla auditory‐nerve fibers. J Neurophysiol 93: 3615‐3634, 2005. DOI: 10.1152/jn.00882.2004.
 523. Reiss LA , Young ED . Spectral edge sensitivity in neural circuits of the dorsal cochlear nucleus. J Neurosci 25: 3680‐3691, 2005. DOI: 10.1523/JNEUROSCI.4963‐04.2005.
 524. Remme MW , Donato R , Mikiel‐Hunter J , Ballestero JA , Foster S , Rinzel J , McAlpine D . Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues. Proc Natl Acad Sci U S A 111: E2339‐E2348, 2014. DOI: 10.1073/pnas.1316216111.
 525. Requarth T , Sawtell NB . Neural mechanisms for filtering self‐generated sensory signals in cerebellum‐like circuits. Curr Opin Neurobiol 21: 602‐608, 2011. DOI: 10.1016/j.conb.2011.05.031.
 526. Rhode WS . Vertical cell responses to sound in cat dorsal cochlear nucleus. J Neurophysiol 82: 1019‐1032, 1999.
 527. Rhode WS , Smith PH . Characteristics of tone‐pip response patterns in relationship to spontaneous rate in cat auditory nerve fibers. Hear Res 18: 159‐168, 1985.
 528. Rhode WS , Smith PH . Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56: 261‐286, 1986.
 529. Rhode WS , Smith PH , Oertel D . Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J Comp Neurol 213: 426‐447, 1983. DOI: 10.1002/cne.902130407.
 530. Rice JJ , May BJ , Spirou GA , Young ED . Pinna‐based spectral cues for sound localization in cat. Hear Res 58: 132‐152, 1992.
 531. Rietzel HJ , Friauf E . Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390: 20‐40, 1998.
 532. Roberts MT , Seeman SC , Golding NL . A mechanistic understanding of the role of feedforward inhibition in the mammalian sound localization circuitry. Neuron 78: 923‐935, 2013. DOI: 10.1016/j.neuron.2013.04.022.
 533. Roberts MT , Seeman SC , Golding NL . The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings. Front Neural Circuits 8: 49, 2014. DOI: 10.3389/fncir.2014.00049.
 534. Roberts PD , Portfors CV . Design principles of sensory processing in cerebellum‐like structures. Early stage processing of electrosensory and auditory objects. Biol Cybern 98: 491‐507, 2008. DOI: 10.1007/s00422‐008‐0217‐1.
 535. Roberts PD , Portfors CV . Responses to social vocalizations in the dorsal cochlear nucleus of mice. Front Syst Neurosci 9: 172, 2015. DOI: 10.3389/fnsys.2015.00172.
 536. Robertson D . Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion. Hear Res 15: 113‐121, 1984.
 537. Robertson D . Physiology and morphology of cells in the ventral nucleus of the trapezoid body and rostral periolivary regions of the rat superior olivary complex studied in slices. Audit Neurosci 2: 12‐31, 1996.
 538. Rodrigues AR , Oertel D . Hyperpolarization‐activated currents regulate excitability in stellate cells of the mammalian ventral cochlear nucleus. J Neurophysiol 95: 76‐87, 2006. DOI: 10.1152/jn.00624.2005.
 539. Romand MR , Romand R . The ultrastructure of spiral ganglion cells in the mouse. Acta Otolaryngol 104: 29‐39, 1987.
 540. Rose JE , Brugge JF , Anderson DJ , Hind JE . Phase‐locked response to low‐frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30: 769‐793, 1967. DOI: 10.1152/jn.1967.30.4.769.
 541. Rose JE , Gross NB , Geisler CD , Hind JE . Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source. J Neurophysiol 29: 288‐314, 1966.
 542. Roth GL , Aitkin LM , Andersen RA , Merzenich MM . Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182: 661‐680, 1978. DOI: 10.1002/cne.901820407.
 543. Roth GL , Kochhar RK , Hind JE . Interaural time differences: implications regarding the neurophysiology of sound localization. J Acoust Soc Am 68: 1643‐1651, 1980.
 544. Rothman JS , Young ED . Enhancement of neural synchronization in computational models of ventral cochlear nucleus bushy cells. Audit Neurosci 2: 47‐62, 1996.
 545. Rothman JS , Young ED , Manis PB . Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J Neurophysiol 70: 2562‐2583, 1993.
 546. Rubio ME , Gudsnuk KA , Smith Y , Ryugo DK . Revealing the molecular layer of the primate dorsal cochlear nucleus. Neuroscience 154: 99‐113, 2008. DOI: 10.1016/j.neuroscience.2007.12.016.
 547. Ruggero MA . Response to noise of auditory nerve fibers in the squirrel monkey. J Neurophysiol 36: 569‐587, 1973. DOI: 10.1152/jn.1973.36.4.569.
 548. Ryugo DK . Projections of low spontaneous rate, high threshold auditory nerve fibers to the small cell cap of the cochlear nucleus in cats. Neuroscience 154: 114‐126, 2008. DOI: 10.1016/j.neuroscience.2007.10.052.
 549. Ryugo DK , Sento S . Synaptic connections of the auditory nerve in cats: relationship between endbulbs of held and spherical bushy cells. J Comp Neurol 305: 35‐48, 1991. DOI: 10.1002/cne.903050105.
 550. Sachs MB , Abbas PJ . Rate versus level functions for auditory‐nerve fibers in cats: tone‐burst stimuli. J Acoust Soc Am 56: 1835‐1847, 1974.
 551. Saint Marie RL , Ostapoff EM , Morest DK , Wenthold RJ . Glycine‐immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J Comp Neurol 279: 382‐396, 1989. DOI: 10.1002/cne.902790305.
 552. Saldana E , Aparicio MA , Fuentes‐Santamaria V , Berrebi AS . Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus. Neuroscience 163: 372‐387, 2009. DOI: 10.1016/j.neuroscience.2009.06.030.
 553. Saldana E , Berrebi AS . Anisotropic organization of the rat superior paraolivary nucleus. Anat Embryol (Berl) 202: 265‐279, 2000. DOI: 10.1007/s004290002020265.429.
 554. Samson FK , Barone P , Irons WA , Clarey JC , Poirier P , Imig TJ . Directionality derived from differential sensitivity to monaural and binaural cues in the cat's medial geniculate body. J Neurophysiol 84: 1330‐1345, 2000.
 555. Sandel TT , Teas DC , Feddersen WE , Jeffress LA . Localization of sound from single and paired sources. J Acoust Soc Am 27: 842‐852, 1955.
 556. Sanes DH . An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive. J Neurosci 10: 3494‐3506, 1990.
 557. Sanes DH . The development of synaptic function and integration in the central auditory system. J Neurosci 13: 2627‐2637, 1993.
 558. Sanes DH , Geary WA , Wooten GF , Rubel EW . Quantitative distribution of the glycine receptor in the auditory brain stem of the gerbil. J Neurosci 7: 3793‐3802, 1987.
 559. Sayles M , Smith PH , Joris JX . Inter‐aural time sensitivity of superior‐olivary‐complex neurons is shaped by systematic cochlear disparities. Assoc Res Otolaryngol Abs 39: 273, 2016.
 560. Scheibel ME , Scheibel AB . Neuropil organization in the superior olive of the cat. Exp Neurol 43: 339‐348, 1974.
 561. Schnupp JW , King AJ . Coding for auditory space in the nucleus of the brachium of the inferior colliculus in the ferret. J Neurophysiol 78: 2717‐2731, 1997.
 562. Schofield BR . Superior paraolivary nucleus in the pigmented guinea pig: separate classes of neurons project to the inferior colliculus and the cochlear nucleus. J Comp Neurol 312: 68‐76, 1991. DOI: 10.1002/cne.903120106.
 563. Schofield BR . Projections to the cochlear nuclei from principal cells in the medial nucleus of the trapezoid body in guinea pigs. J Comp Neurol 344: 83‐100, 1994. DOI: 10.1002/cne.903440107.
 564. Schofield BR . Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. J Comp Neurol 360: 135‐149, 1995. DOI: 10.1002/cne.903600110.
 565. Schofield BR , Cant NB . Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology. J Comp Neurol 314: 645‐670, 1991. DOI: 10.1002/cne.903140403.
 566. Schofield BR , Cant NB . Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus. J Comp Neurol 317: 438‐455, 1992. DOI: 10.1002/cne.903170409.
 567. Schofield BR , Motts SD , Mellott JG , Foster NL . Projections from the dorsal and ventral cochlear nuclei to the medial geniculate body. Front Neuroanat 8: 10, 2014. DOI: 10.3389/fnana.2014.00010.
 568. Schroeder MR . New viewpoints in binaural interactions. In: Evans EF , Wilson JP , editors. Psychophysics and Physiology of Hearing. New York: Academic Press, 1977, p. 455‐467.
 569. Schwartz IR . Dendritic arrangements in the cat medial superior olive. Neuroscience 2: 81‐101, 1977.
 570. Schwartz IR , Ryan AF . Amino acid labeling patterns in the efferent innervation of the cochlea: an electron microscopic autoradiographic study. J Comp Neurol 246: 500‐512, 1986. DOI: 10.1002/cne.902460407.
 571. Scott LL , Hage TA , Golding NL . Weak action potential backpropagation is associated with high‐frequency axonal firing capability in principal neurons of the gerbil medial superior olive. J Physiol 583: 647‐661, 2007. DOI: 10.1113/jphysiol.2007.136366.
 572. Scott LL , Mathews PJ , Golding NL . Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J Neurosci 25: 7887‐7895, 2005. DOI: 10.1523/JNEUROSCI.1016‐05.2005.
 573. Sedlacek M , Brenowitz SD . Cell‐type specific short‐term plasticity at auditory nerve synapses controls feed‐forward inhibition in the dorsal cochlear nucleus. Front Neural Circuits 8: 78, 2014. DOI: 10.3389/fncir.2014.00078.
 574. Sedlacek M , Tipton PW , Brenowitz SD . Sustained firing of cartwheel cells in the dorsal cochlear nucleus evokes endocannabinoid release and retrograde suppression of parallel fiber synapses. J Neurosci 31: 15807‐15817, 2011. DOI: 10.1523/JNEUROSCI.4088‐11.2011.
 575. Semple MN , Kitzes LM . Binaural processing of sound pressure level in the inferior colliculus. J Neurophysiol 57: 1130‐1147, 1987.
 576. Semple MN , Kitzes LM . Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences. J Neurophysiol 69: 449‐461, 1993. DOI: 10.1152/jn.1993.69.2.449.
 577. Semple MN , Kitzes LM . Focal selectivity for binaural sound pressure level in cat primary auditory cortex: two‐way intensity network tuning. J Neurophysiol 69: 462‐473, 1993. DOI: 10.1152/jn.1993.69.2.462.
 578. Sento S , Ryugo DK . Endbulbs of held and spherical bushy cells in cats: morphological correlates with physiological properties. J Comp Neurol 280: 553‐562, 1989. DOI: 10.1002/cne.902800406.
 579. Series P , Latham PE , Pouget A . Tuning curve sharpening for orientation selectivity: coding efficiency and the impact of correlations. Nat Neurosci 7: 1129‐1135, 2004. DOI: 10.1038/nn1321.
 580. Seshagiri CV , Delgutte B . Response properties of neighboring neurons in the auditory midbrain for pure‐tone stimulation: a tetrode study. J Neurophysiol 98: 2058‐2073, 2007. DOI: 10.1152/jn.01317.2006.
 581. Shackleton TM , Arnott RH , Palmer AR . Sensitivity to interaural correlation of single neurons in the inferior colliculus of guinea pigs. J Assoc Res Otolaryngol 6: 244‐259, 2005. DOI: 10.1007/s10162‐005‐0005‐8.
 582. Shamma S . On the role of space and time in auditory processing. Trends Cogn Sci 5: 340‐348, 2001.
 583. Shamma SA , Shen NM , Gopalaswamy P . Stereausis: binaural processing without neural delays. J Acoust Soc Am 86: 989‐1006, 1989.
 584. Shannon RV , Zeng FG , Kamath V , Wygonski J , Ekelid M . Speech recognition with primarily temporal cues. Science 270: 303‐304, 1995.
 585. Shera CA , Bergevin C , Kalluri R , Laughlin MM , Michelet P , van der Heijden M , Joris PX . Otoacoustic estimates of cochlear tuning: testing predictions in macaque. AIP Conf Proc 1403: 286‐292, 2011. DOI: 10.1063/1.3658099.
 586. Sherriff FE , Henderson Z . Cholinergic neurons in the ventral trapezoid nucleus project to the cochlear nuclei in the rat. Neuroscience 58: 627‐633, 1994.
 587. Shneiderman A , Oliver DL , Henkel CK . Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276: 188‐208, 1988. DOI: 10.1002/cne.902760204.
 588. Shneiderman A , Stanforth DA , Henkel CK , Saint Marie RL . Input‐output relationships of the dorsal nucleus of the lateral lemniscus: possible substrate for the processing of dynamic spatial cues. J Comp Neurol 410: 265‐276, 1999.
 589. Shore SE , Godfrey DA , Helfert RH , Altschuler RA , Bledsoe SC Jr . Connections between the cochlear nuclei in guinea pig. Hear Res 62: 16‐26, 1992.
 590. Shore SE , Helfert RH , Bledsoe SC Jr , Altschuler RA , Godfrey DA . Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig. Hear Res 52: 255‐268, 1991.
 591. Shore SE , Sumner CJ , Bledsoe SC , Lu J . Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons. Exp Brain Res 153: 427‐435, 2003. DOI: 10.1007/s00221‐003‐1610‐6.
 592. Shore SE , Vass Z , Wys NL , Altschuler RA . Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419: 271‐285, 2000.
 593. Shore SE , Zhou J . Somatosensory influence on the cochlear nucleus and beyond. Hear Res 216‐217: 90‐99, 2006. DOI: 10.1016/j.heares.2006.01.006.
 594. Sinclair JL , Barnes‐Davies M , Kopp‐Scheinpflug C , Forsythe ID . Strain‐specific differences in the development of neuronal excitability in the mouse ventral nucleus of the trapezoid body. Hear Res 354: 28‐37, 2017. DOI: 10.1016/j.heares.2017.08.004.
 595. Sinex DG , Lopez DE , Warr WB . Electrophysiological responses of cochlear root neurons. Hear Res 158: 28‐38, 2001.
 596. Singla S , Dempsey C , Warren R , Enikolopov AG , Sawtell NB . A cerebellum‐like circuit in the auditory system cancels responses to self‐generated sounds. Nat Neurosci 20: 943‐950, 2017. DOI: 10.1038/nn.4567.
 597. Skaliora I , Doubell TP , Holmes NP , Nodal FR , King AJ . Functional topography of converging visual and auditory inputs to neurons in the rat superior colliculus. J Neurophysiol 92: 2933‐2946, 2004. DOI: 10.1152/jn.00450.2004.
 598. Slee SJ , Young ED . Information conveyed by inferior colliculus neurons about stimuli with aligned and misaligned sound localization cues. J Neurophysiol 106: 974‐985, 2011. DOI: 10.1152/jn.00384.2011.
 599. Slee SJ , Young ED . Linear processing of interaural level difference underlies spatial tuning in the nucleus of the brachium of the inferior colliculus. J Neurosci 33: 3891‐3904, 2013. DOI: 10.1523/JNEUROSCI.3437‐12.2013.
 600. Slee SJ , Young ED . Alignment of sound localization cues in the nucleus of the brachium of the inferior colliculus. J Neurophysiol 111: 2624‐2633, 2014. DOI: 10.1152/jn.00885.2013.
 601. Smith AJ , Owens S , Forsythe ID . Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J Physiol 529 (Pt 3): 681‐698, 2000.
 602. Smith AL , Parsons CH , Lanyon RG , Bizley JK , Akerman CJ , Baker GE , Dempster AC , Thompson ID , King AJ . An investigation of the role of auditory cortex in sound localization using muscimol‐releasing Elvax. Eur J Neurosci 19: 3059‐3072, 2004. DOI: 10.1111/j.0953‐816X.2004.03379.x.
 603. Smith PH . Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J Neurophysiol 73: 1653‐1667, 1995.
 604. Smith PH , Joris PX , Carney LH , Yin TC . Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304: 387‐407, 1991. DOI: 10.1002/cne.903040305.
 605. Smith PH , Joris PX , Yin TC . Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331: 245‐260, 1993. DOI: 10.1002/cne.903310208.
 606. Smith PH , Joris PX , Yin TC . Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J Neurophysiol 79: 3127‐3142, 1998.
 607. Smith PH , Massie A , Joris PX . Acoustic stria: anatomy of physiologically characterized cells and their axonal projection patterns. J Comp Neurol 482: 349‐371, 2005. DOI: 10.1002/cne.20407.
 608. Smith PH , Rhode WS . Electron microscopic features of physiologically characterized, HRP‐labeled fusiform cells in the cat dorsal cochlear nucleus. J Comp Neurol 237: 127‐143, 1985. DOI: 10.1002/cne.902370110.
 609. Smith PH , Rhode WS . Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282: 595‐616, 1989. DOI: 10.1002/cne.902820410.
 610. Smith RL , Brachman ML . Response modulation of auditory‐nerve fibers by AM stimuli: effects of average intensity. Hear Res 2: 123‐133, 1980.
 611. Smith RL , Brachman ML , Frisina RD . Sensitivity of auditory‐nerve fibers to changes in intensity: a dichotomy between decrements and increments. J Acoust Soc Am 78: 1310‐1316, 1985.
 612. Sommer I , Lingenhohl K , Friauf E . Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Exp Brain Res 95: 223‐239, 1993.
 613. Song P , Wang N , Wang H , Xie Y , Jia J , Li H . Pentobarbital anesthesia alters neural responses in the precedence effect. Neurosci Lett 498: 72‐77, 2011. DOI: 10.1016/j.neulet.2011.04.066.
 614. Spangler KM , Cant NB , Henkel CK , Farley GR , Warr WB . Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J Comp Neurol 259: 452‐465, 1987. DOI: 10.1002/cne.902590311.
 615. Spangler KM , Warr WB , Henkel CK . The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J Comp Neurol 238: 249‐262, 1985. DOI: 10.1002/cne.902380302.
 616. Spirou GA , Berrebi AS . Organization of ventrolateral periolivary cells of the cat superior olive as revealed by PEP‐19 immunocytochemistry and Nissl stain. J Comp Neurol 368: 100‐120, 1996. DOI: 10.1002/(SICI)1096‐9861(19960422)368:1<100::AID‐CNE7>3.0.CO;2‐7.
 617. Spirou GA , Berrebi AS . Glycine immunoreactivity in the lateral nucleus of the trapezoid body of the cat. J Comp Neurol 383: 473‐488, 1997.
 618. Spirou GA , Brownell WE , Zidanic M . Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63: 1169‐1190, 1990.
 619. Spirou GA , Davis KA , Nelken I , Young ED . Spectral integration by type II interneurons in dorsal cochlear nucleus. J Neurophysiol 82: 648‐663, 1999. DOI: 10.1152/jn.1999.82.2.648.
 620. Spirou GA , May BJ , Wright DD , Ryugo DK . Frequency organization of the dorsal cochlear nucleus in cats. J Comp Neurol 329: 36‐52, 1993. DOI: 10.1002/cne.903290104.
 621. Spirou GA , Rager J , Manis PB . Convergence of auditory‐nerve fiber projections onto globular bushy cells. Neuroscience 136: 843‐863, 2005. DOI: 10.1016/j.neuroscience.2005.08.068.
 622. Spirou GA , Young ED . Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. J Neurophysiol 66: 1750‐1768, 1991.
 623. Spitzer MW , Semple MN . Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J Neurophysiol 73: 1668‐1690, 1995.
 624. Spoendlin H . Innervation patterns in the organ of corti of the cat. Acta Otolaryngol 67: 239‐254, 1969.
 625. Spoendlin H , Schrott A . Analysis of the human auditory nerve. Hear Res 43: 25‐38, 1989.
 626. Stange A , Myoga MH , Lingner A , Ford MC , Alexandrova O , Felmy F , Pecka M , Siveke I , Grothe B . Adaptation in sound localization: from GABA(B) receptor‐mediated synaptic modulation to perception. Nat Neurosci 16: 1840‐1847, 2013. DOI: 10.1038/nn.3548.
 627. Stecker GC , Middlebrooks JC . Distributed coding of sound locations in the auditory cortex. Biol Cybern 89: 341‐349, 2003. DOI: 10.1007/s00422‐003‐0439‐1.
 628. Sterenborg JC , Pilati N , Sheridan CJ , Uchitel OD , Forsythe ID , Barnes‐Davies M . Lateral olivocochlear (LOC) neurons of the mouse LSO receive excitatory and inhibitory synaptic inputs with slower kinetics than LSO principal neurons. Hear Res 270: 119‐126, 2010. DOI: 10.1016/j.heares.2010.08.013.
 629. Stern RM , Zeiberg AS , Trahiotis C . Lateralization of complex binaural stimuli: a weighted‐image model. J Acoust Soc Am 84: 156‐165, 1988.
 630. Stevens SS , Newman EB . The localization of pure tones. Proc Natl Acad Sci U S A 20: 593‐596, 1934.
 631. Stevens SS , Newman EB . The localization of actual sources of sound. Am J Psychol 48: 297‐306, 1936.
 632. Stotler WA . An experimental study of the cells and connections of the superior olivary complex of the cat. J Comp Neurol 98: 401‐431, 1953.
 633. Strutt JW (3rd Baron Rayleigh). On our perception of sound direction. Philos Mag Ser 6 13: 214‐232, 1907.
 634. Sutherland DP , Glendenning KK , Masterton RB . Role of acoustic striae in hearing: discrimination of sound‐source elevation. Hear Res 120: 86‐108, 1998.
 635. Sutherland DP , Masterton RB , Glendenning KK . Role of acoustic striae in hearing: reflexive responses to elevated sound‐sources. Behav Brain Res 97: 1‐12, 1998.
 636. Svirskis G , Kotak V , Sanes DH , Rinzel J . Enhancement of signal‐to‐noise ratio and phase locking for small inputs by a low‐threshold outward current in auditory neurons. J Neurosci 22: 11019‐11025, 2002.
 637. Taberner AM , Liberman MC . Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93: 557‐569, 2005. DOI: 10.1152/jn.00574.2004.
 638. Tang ZQ , Trussell LO . Serotonergic regulation of excitability of principal cells of the dorsal cochlear nucleus. J Neurosci 35: 4540‐4551, 2015. DOI: 10.1523/JNEUROSCI.4825‐14.2015.
 639. Temchin AN , Recio‐Spinoso A , van Dijk P , Ruggero MA . Wiener kernels of chinchilla auditory‐nerve fibers: verification using responses to tones, clicks, and noise and comparison with basilar‐membrane vibrations. J Neurophysiol 93: 3635‐3648, 2005. DOI: 10.1152/jn.00885.2004.
 640. Thompson AM , Thompson GC . Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303: 267‐285, 1991. DOI: 10.1002/cne.903030209.
 641. Thompson AM , Thompson GC . Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335: 402‐412, 1993. DOI: 10.1002/cne.903350309.
 642. Thompson GC , Masterton RB . Brain stem auditory pathways involved in reflexive head orientation to sound. J Neurophysiol 41: 1183‐1202, 1978.
 643. Thompson SP . On the function of the two ears in the perception of space. Philos Mag 13: 406‐416, 1882.
 644. Tollin DJ , Dent ML , Yin TCT . Psychophysical and physiological studies of the precedence effect and echo threshold in the behaving cat. In: Pressnitzer D , Cheveigne AD , McAdams S , Collet L , editors. Auditory Signal Processing: Physiology, Psychoacoustics and Models. Berlin: Springer‐Verlag, 2004, p. 429‐435.
 645. Tollin DJ , Henning GB . Some aspects of the lateralization of echoed sound in man. I. The classical interaural‐delay based precedence effect. J Acoust Soc Am 104: 3030‐3038, 1998.
 646. Tollin DJ , Henning GB . Some aspects of the lateralization of echoed sound in man. II. The role of the stimulus spectrum. J Acoust Soc Am 105: 838‐849, 1999.
 647. Tollin DJ , Populin LC , Moore JM , Ruhland JL , Yin TC . Sound‐localization performance in the cat: the effect of restraining the head. J Neurophysiol 93: 1223‐1234, 2005. DOI: 10.1152/jn.00747.2004.
 648. Tollin DJ , Populin LC , Yin TC . Neural correlates of the precedence effect in the inferior colliculus of behaving cats. J Neurophysiol 92: 3286‐3297, 2004. DOI: 10.1152/jn.00606.2004.
 649. Tollin DJ , Ruhland JL , Yin TC . The vestibulo‐auricular reflex. J Neurophysiol 101: 1258‐1266, 2009. DOI: 10.1152/jn.90977.2008.
 650. Tollin DJ , Ruhland JL , Yin TC . The role of spectral composition of sounds on the localization of sound sources by cats. J Neurophysiol 109: 1658‐1668, 2013. DOI: 10.1152/jn.00358.2012.
 651. Tollin DJ , Yin TC . The coding of spatial location by single units in the lateral superior olive of the cat. I. Spatial receptive fields in azimuth. J Neurosci 22: 1454‐1467, 2002.
 652. Tollin DJ , Yin TC . The coding of spatial location by single units in the lateral superior olive of the cat. II. The determinants of spatial receptive fields in azimuth. J Neurosci 22: 1468‐1479, 2002.
 653. Tollin DJ , Yin TC . Psychophysical investigation of an auditory spatial illusion in cats: the precedence effect. J Neurophysiol 90: 2149‐2162, 2003. DOI: 10.1152/jn.00381.2003.
 654. Tollin DJ , Yin TC . Spectral cues explain illusory elevation effects with stereo sounds in cats. J Neurophysiol 90: 525‐530, 2003. DOI: 10.1152/jn.00107.2003.
 655. Tollin DJ , Yin TC . Interaural phase and level difference sensitivity in low‐frequency neurons in the lateral superior olive. J Neurosci 25: 10648‐10657, 2005. DOI: 10.1523/JNEUROSCI.1609‐05.2005.
 656. Tolnai S , Litovsky RY , King AJ . The precedence effect and its buildup and breakdown in ferrets and humans. J Acoust Soc Am 135: 1406‐1418, 2014. DOI: 10.1121/1.4864486.
 657. Tsuchitani C . Functional organization of lateral cell groups of cat superior olivary complex. J Neurophysiol 40: 296‐318, 1977.
 658. Tsuchitani C . Discharge patterns of cat lateral superior olivary units to ipsilateral tone‐burst stimuli. J Neurophysiol 47: 479‐500, 1982.
 659. Tsuchitani C , Boudreau JC . Single unit analysis of cat superior olive S segment with tonal stimuli. J Neurophysiol 29: 684‐697, 1966.
 660. Tsuchitani C , Boudreau JC . Stimulus level of dichotically presented tones and cat superior olive S‐segment cell dcharge. J Acoust Soc Am 46: 979‐988, 1969.
 661. Tsuji J , Liberman MC . Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381: 188‐202, 1997.
 662. Tzounopoulos T , Kim Y , Oertel D , Trussell LO . Cell‐specific, spike timing‐dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: 719‐725, 2004. DOI: 10.1038/nn1272.
 663. van Adel BA , Kelly JB . Kainic acid lesions of the superior olivary complex: effects on sound localization by the albino rat. Behav Neurosci 112: 432‐446, 1998.
 664. van der Heijden M , Lorteije JA , Plauska A , Roberts MT , Golding NL , Borst JG . Directional hearing by linear summation of binaural inputs at the medial superior olive. Neuron 78: 936‐948, 2013. DOI: 10.1016/j.neuron.2013.04.028.
 665. van der Heijden M , Louage DH , Joris PX . Responses of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise: implications for the sensitivity to interaural delays. J Assoc Res Otolaryngol 12: 485‐502, 2011. DOI: 10.1007/s10162‐011‐0268‐1.
 666. van der Heijden M , Trahiotis C . Masking with interaurally delayed stimuli: the use of “internal” delays in binaural detection. J Acoust Soc Am 105: 388‐399, 1999.
 667. Vater M , Feng AS . Functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats. J Comp Neurol 292: 373‐395, 1990. DOI: 10.1002/cne.902920305.
 668. Vetter DE , Mugnaini E . Distribution and dendritic features of three groups of rat olivocochlear neurons. A study with two retrograde cholera toxin tracers. Anat Embryol (Berl) 185: 1‐16, 1992.
 669. Vetter DE , Saldana E , Mugnaini E . Input from the inferior colliculus to medial olivocochlear neurons in the rat: a double label study with PHA‐L and cholera toxin. Hear Res 70: 173‐186, 1993.
 670. Vliegen J , Van Opstal AJ . The influence of duration and level on human sound localization. J Acoust Soc Am 115: 1705‐1713, 2004.
 671. Voigt HF , Young ED . Evidence of inhibitory interactions between neurons in dorsal cochlear nucleus. J Neurophysiol 44: 76‐96, 1980.
 672. Voigt HF , Young ED . Cross‐correlation analysis of inhibitory interactions in dorsal cochlear nucleus. J Neurophysiol 64: 1590‐1610, 1990.
 673. von Bekesy G . Experiments in Hearing. New York: McGraw‐Hill, 1989, p. 745.
 674. Wallach H . The role of head movements and vestibular and visual cues in sound localization. J Exp Psychol 27: 339‐368, 1940.
 675. Wallach H , Newman EB , Rosenzweig MR . The precedence effect in sound localization. Am J Psychol 62: 315‐336, 1949.
 676. Wang L , Devore S , Delgutte B , Colburn HS . Dual sensitivity of inferior colliculus neurons to ITD in the envelopes of high‐frequency sounds: experimental and modeling study. J Neurophysiol 111: 164‐181, 2014. DOI: 10.1152/jn.00450.2013.
 677. Warr WB . Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat. Exp Neurol 23: 140‐155, 1969.
 678. Warr WB . Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res 40: 247‐270, 1972.
 679. Warr WB . Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 161: 159‐181, 1975. DOI: 10.1002/cne.901610203.
 680. Warr WB . Efferent components of the auditory system. Ann Otol Rhinol Laryngol Suppl 89: 114‐120, 1980.
 681. Warren EH 3rd , Liberman MC . Effects of contralateral sound on auditory‐nerve responses. I. Contributions of cochlear efferents. Hear Res 37: 89‐104, 1989.
 682. Watkins PV , Barbour DL . Specialized neuronal adaptation for preserving input sensitivity. Nat Neurosci 11: 1259‐1261, 2008. DOI: 10.1038/nn.2201.
 683. Weedman DL , Ryugo DK . Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. J Comp Neurol 371: 311‐324, 1996. DOI: 10.1002/(SICI)1096‐9861(19960722)371:2<311::AID‐CNE10>3.0.CO;2‐V.
 684. Wei L , Karino S , Verschooten E , Joris PX . Enhancement of phase‐locking in rodents. I. An axonal recording study in gerbil. J Neurophysiol 118: 2009‐2023, 2017. DOI: 10.1152/jn.00194.2016.
 685. Weiss TF , Rose C . A comparison of synchronization filters in different auditory receptor organs. Hear Res 33: 175‐179, 1988.
 686. Wen B , Wang GI , Dean I , Delgutte B . Dynamic range adaptation to sound level statistics in the auditory nerve. J Neurosci 29: 13797‐13808, 2009. DOI: 10.1523/JNEUROSCI.5610‐08.2009.
 687. Wen B , Wang GI , Dean I , Delgutte B . Time course of dynamic range adaptation in the auditory nerve. J Neurophysiol 108: 69‐82, 2012. DOI: 10.1152/jn.00055.2012.
 688. Wenstrup JJ , Ross LS , Pollak GD . Binaural response organization within a frequency‐band representation of the inferior colliculus: implications for sound localization. J Neurosci 6: 962‐973, 1986.
 689. Wenthold RJ , Huie D , Altschuler RA , Reeks KA . Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22: 897‐912, 1987.
 690. Wenzel EM , Arruda M , Kistler DJ , Wightman FL . Localization using nonindividualized head‐related transfer functions. J Acoust Soc Am 94: 111‐123, 1993.
 691. White JS , Warr WB . The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219: 203‐214, 1983. DOI: 10.1002/cne.902190206.
 692. Wigderson E , Nelken I , Yarom Y . Early multisensory integration of self and source motion in the auditory system. Proc Natl Acad Sci U S A 113: 8308‐8313, 2016. DOI: 10.1073/pnas.1522615113.
 693. Wightman FL , Kistler DJ . Headphone simulation of free‐field listening. I: stimulus synthesis. J Acoust Soc Am 85: 858‐867, 1989.
 694. Wightman FL , Kistler DJ . Headphone simulation of free‐field listening. II: psychophysical validation. J Acoust Soc Am 85: 868‐878, 1989.
 695. Wightman FL , Kistler DJ . Resolution of front‐back ambiguity in spatial hearing by listener and source movement. J Acoust Soc Am 105: 2841‐2853, 1999.
 696. Winter IM , Palmer AR . Responses of single units in the anteroventral cochlear nucleus of the guinea pig. Hear Res 44: 161‐178, 1990.
 697. Winter IM , Palmer AR . Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. J Neurophysiol 73: 141‐159, 1995.
 698. Winter IM , Robertson D , Cole KS . Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig. J Comp Neurol 280: 143‐157, 1989. DOI: 10.1002/cne.902800110.
 699. Wise LZ , Irvine DR . Auditory response properties of neurons in deep layers of cat superior colliculus. J Neurophysiol 49: 674‐685, 1983.
 700. Wise LZ , Irvine DR . Interaural intensity difference sensitivity based on facilitatory binaural interaction in cat superior colliculus. Hear Res 16: 181‐187, 1984.
 701. Wise LZ , Irvine DR . Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation. J Neurophysiol 54: 185‐211, 1985.
 702. Wright D , Hebrank JH , Wilson B . Pinna reflections as cues for localization. J Acoust Soc Am 56: 957‐962, 1974.
 703. Wright DD , Ryugo DK . Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 365: 159‐172, 1996. DOI: 10.1002/(SICI)1096‐9861(19960129)365:1<159::AID‐CNE12>3.0.CO;2‐L.
 704. Wu C , Stefanescu RA , Martel DT , Shore SE . Listening to another sense: somatosensory integration in the auditory system. Cell Tissue Res 361: 233‐250, 2015. DOI: 10.1007/s00441‐014‐2074‐7.
 705. Wu SH , Kelly JB . Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J Neurophysiol 65: 230‐246, 1991.
 706. Wu SH , Kelly JB . Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. J Neurophysiol 68: 1151‐1159, 1992.
 707. Wu SH , Kelly JB . Physiological evidence for ipsilateral inhibition in the lateral superior olive: synaptic responses in mouse brain slice. Hear Res 73: 57‐64, 1994.
 708. Wu SH , Oertel D . Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J Neurosci 4: 1577‐1588, 1984.
 709. Wu SH , Oertel D . Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J Neurosci 6: 2691‐2706, 1986.
 710. Wullimann MF , Mueller T , Distel M , Babaryka A , Grothe B , Koster RW . The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat 5: 27, 2011. DOI: 10.3389/fnana.2011.00027.
 711. Wyttenbach RA , Hoy RR . Demonstration of the precedence effect in an insect. J Acoust Soc Am 94: 777‐784, 1993.
 712. Xia J , Brughera A , Colburn HS , Shinn‐Cunningham B . Physiological and psychophysical modeling of the precedence effect. J Assoc Res Otolaryngol 11: 495‐513, 2010. DOI: 10.1007/s10162‐010‐0212‐9.
 713. Xia J , Shinn‐Cunningham B . Isolating mechanisms that influence measures of the precedence effect: theoretical predictions and behavioral tests. J Acoust Soc Am 130: 866‐882, 2011. DOI: 10.1121/1.3605549.
 714. Xu‐Friedman MA , Regehr WG . Dynamic‐clamp analysis of the effects of convergence on spike timing. I. Many synaptic inputs. J Neurophysiol 94: 2512‐2525, 2005. DOI: 10.1152/jn.01307.2004.
 715. Yang L , Pollak G . Binaural inhibitioin in the dorsal nucleus of the lateral lemniscus of the mustache bat affects responses for multiple sounds. Aud Neurosci 1: 1‐17, 1994.
 716. Yang L , Pollak GD . The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat. J Neurophysiol 71: 1999‐2013, 1994.
 717. Yassin L , Radtke‐Schuller S , Asraf H , Grothe B , Hershfinkel M , Forsythe ID , Kopp‐Scheinpflug C . Nitric oxide signaling modulates synaptic inhibition in the superior paraolivary nucleus (SPN) via cGMP‐dependent suppression of KCC2. Front Neural Circuits 8: 65, 2014. DOI: 10.3389/fncir.2014.00065.
 718. Yates GK . Dynamic effects in the input/output relationship of auditory nerve. Hear Res 27: 221‐230, 1987.
 719. Yeomans JS , Frankland PW . The acoustic startle reflex: neurons and connections. Brain Res Brain Res Rev 21: 301‐314, 1995.
 720. Yin TC . Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat. J Neurosci 14: 5170‐5186, 1994.
 721. Yin TC . Neural mechanisms of encoding binaural localization cues in the auditory brainstem. In: Oertel D , Popper AN , Fay RR , editors. Integrative Functions in the Mammalian Auditory Pathway. Berlin: Springer‐Verlag, 2002, p. 99‐159.
 722. Yin TC , Chan JC . Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64: 465‐488, 1990.
 723. Yin TC , Chan JC , Carney LH . Effects of interaural time delays of noise stimuli on low‐frequency cells in the cat's inferior colliculus. III. Evidence for cross‐correlation. J Neurophysiol 58: 562‐583, 1987.
 724. Yin TC , Chan JC , Irvine DR . Effects of interaural time delays of noise stimuli on low‐frequency cells in the cat's inferior colliculus. I. Responses to wideband noise. J Neurophysiol 55: 280‐300, 1986.
 725. Yin TC , Hirsch JA , Chan JC . Responses of neurons in the cat's superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity. J Neurophysiol 53: 746‐758, 1985.
 726. Yin TC , Kuwada S . Binaural interaction in low‐frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. J Neurophysiol 50: 1000‐1019, 1983.
 727. Yin TC , Kuwada S . Binaural interaction in low‐frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. J Neurophysiol 50: 1020‐1042, 1983.
 728. Yin TC , Kuwada S . Binaural localization cues. In: Palmer AR , Rees A , editors. The Auditory Brain Vol 2 Oxford Handbook of Auditory Science. Oxford: Oxford University Press, 2010, p. 269‐300.
 729. Yost WA . Lateral position of sinusoids presented with interaural intensive and temporal differences. J Acoust Soc Am 70: 397‐409, 1981.
 730. Young ED , Brownell WE . Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39: 282‐300, 1976.
 731. Young ED , Davis KA . Circuitry and function of the dorsal cochlear nucleus. In: Oertel D , Fay RR , Popper AN , editors. Integrative Functions in the Mammalian Auditory Pathway. New York: Springer‐Verlag, 2002, p. 160‐206.
 732. Young ED , Nelken I , Conley RA . Somatosensory effects on neurons in dorsal cochlear nucleus. J Neurophysiol 73: 743‐765, 1995.
 733. Young ED , Rice JJ , Spirou GA , Nelken I , Conley RA . Head‐related transfer functions in cat: neural representation and the effects of pinna movement. In: Gilkey RH , Anderson TR , editors. Binaural and Spatial Hearing in Real and Virtual Environments. Mahwah, NJ: Lawrence Erlbaum Associates, Inc., 1997, p. 475‐498.
 734. Young ED , Rice JJ , Tong SC . Effects of pinna position on head‐related transfer functions in the cat. J Acoust Soc Am 99: 3064‐3076, 1996.
 735. Young ED , Spirou GA , Rice JJ , Voigt HF . Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. Philos Trans R Soc Lond Ser B Biol Sci 336: 407‐413, 1992. DOI: 10.1098/rstb.1992.0076.
 736. Zahorik P , Brungart D , Bronkhorst AW . Auditory distance perception in humans: a summary of past and present research. Acta Acustica 91: 409‐420, 2005.
 737. Zarbin MA , Wamsley JK , Kuhar MJ . Glycine receptor: light microscopic autoradiographic localization with [3H]strychnine. J Neurosci 1: 532‐547, 1981.
 738. Zhang S , Oertel D . Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69: 1384‐1397, 1993. DOI: 10.1152/jn.1993.69.5.1384.
 739. Zhang S , Oertel D . Giant cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69: 1398‐1408, 1993.
 740. Zhang S , Oertel D . Tuberculoventral cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69: 1409‐1421, 1993.
 741. Zhang S , Oertel D . Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J Neurophysiol 71: 914‐930, 1994.
 742. Zhou Y , Carney LH , Colburn HS . A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology. J Neurosci 25: 3046‐3058, 2005. DOI: 10.1523/JNEUROSCI.3064‐04.2005.
 743. Zilany MS , Carney LH . Power‐law dynamics in an auditory‐nerve model can account for neural adaptation to sound‐level statistics. J Neurosci 30: 10380‐10390, 2010. DOI: 10.1523/JNEUROSCI.0647‐10.2010.
 744. Zurek PM . The precedence effect and its possible role in the avoidance of interaural ambiguities. J Acoust Soc Am 67: 953‐964, 1980.
 745. Zwislocki J , Feldman RS . Just noticeable differences in dichotic phase. J Acoust Soc Am 28: 860‐864, 1956.

 

Teaching Material

T. C. T. Yin, P. H. Smith, P. X. Joris. Neural Mechanisms of Binaural Processing in the Auditory Brainstem. Compr Physiol 9: 2019, 1503-1575.

Didactic Synopsis

Major Teaching Points:

  • To localize the spatial location of sounds, the brain must compute tiny differences in the sound to the two ears as well as the fine spectral properties of the sounds.
  • Three primary cues are used: differences in the time and intensity of sounds to the two ears are used to determine the horizontal component, while the spectral properties are used to code the vertical dimension.
  • Neurons in the cochlear nucleus show great diversity in the way in which they transform their inputs from the auditory nerve and convey that information to the auditory brainstem nuclei.
  • Neurons in the auditory brainstem appear to have evolved specialized anatomical and physiological properties that are not found anywhere else in the nervous system.
  • Circuits in the superior olivary complex use highly sensitive coincidence detectors to encode interaural time differences and inhibitory mechanisms to encode interaural level differences.
  • Despite considerable progress in recent years in studying these neural mechanisms, many questions still remain unresolved.

Didactic Legends

The following legends to the figures that appear throughout the article are written to be useful for teaching.

Figure 1 Teaching points. (A) The uniform spectral properties of ANFs: they have a narrow V-shaped filter, regardless of the CF of the fiber. (B) The temporal responses of ANFs depend on whether they are low or high CF. The low CF fiber on the left phase-locks to the tone, while the high CF fibers to the right do not. Also, there is some difference that depends on the spontaneous rate: fibers with high spontaneous rate have a higher initial response and adapt quickly, while those with low spontaneous rate have a lower initial response and adapt slower.

Figure 2 Teaching points. (A) Intracellular recordings from IHCs reveal that at low frequencies where the ANFs phase-lock, there is a prominent AC component to the IHC response with a cyclic response corresponding to each cycle of the input tone. This cyclic response disappears at the higher frequencies where phase-locking is no longer present. (B) When the responses to tones are plotted as period histograms, the phase-locking is revealed by the peaks in the histogram. The phase at which the peak occurs varies with frequency in a manner consistent with cochlear mechanics.

Figure 3 Teaching points. The top row of histograms (A-D) shows all-order interspike interval histograms. The easiest way to look at these is as follows: if the neuron fires a spike now (= 0 ms), when are the next spikes occurring? For a certain duration (equal to the refractory period), no other spike will be fired. Besides this gap, the histograms in (B-D) are featureless. However, the histogram of the low-frequency nerve fiber (A) has an oscillatory pattern. The dots indicate the periodicity associated with the cochlear place innervated by this fiber (1/550 Hz = 1.8 ms). Indeed, when this fiber fires, it has a somewhat higher probability to fire again at 1.8 ms and at 2 × 1.8 ms. Annoying in this analysis is that the refractory period obscures what happens at shorter timescales. The middle row shows shuffled autocorrelograms. Here, the stimulus is presented multiple times, and we ask the question: if the cell fires a spike at a certain time during a presentation of the stimulus (again we call this time 0 ms), how many spikes are then fired at the same timepoint of the stimulus, or later, when we repeat the stimulus? For this comparison across responses to a given stimulus, the refractory period is irrelevant. The histograms reveal a clear oscillatory pattern for fibers tuned to low frequencies (E-G), reflecting phase-locking to fast cochlear vibrations, and a broader peak for the high-frequency fiber (H), reflecting slower envelope fluctuations. The bottom row shows these shuffled autocorrelograms mirrored around 0 and as function rather than a histogram. Note the similarity in the shape of these functions with the ITD functions shown later in response to noise (Figure 16B). The shuffled autocorrelograms are a straightforward way to compare monaural spike trains with the output of coincidence detectors like MSO neurons. Indeed, the process of computing intervals between spikes in two spike trains is identical to the process of detecting coincidences between these spike trains when shifted in time w.r.t. each other.

Figure 4 Teaching points. The rate-level curves of a sample of ANFs varying in CF from low to high (rows) and with different spontaneous rates (columns) are shown. There is a tendency for high spontaneous rate fibers to have lower thresholds and saturating rate-level curves than those with low spontaneous rate, but the sample shows that there are exceptions to these tendencies.

Figure 5 Teaching points. A schematic diagram of the different cell types in the two divisions of the cochlear nucleus, the dorsal (DCN) and ventral cochlear nucleus (VCN), with their inputs from the auditory nerve fibers (ANF), interconnections between cell types, and their axonal projections to the trapezoid body (TB) or dorsal (DAS) or ventral acoustic stria (VAS). The three major classes of neurotransmitters, glutamate (excitatory), glycine (inhibitory), or GABAergic (inhibitory), are shown by different-colored axonal terminals. Note that the cells in the VCN, especially the two flavors of bushy cells, receive strong input from the ANF and relatively little input from other cells, whereas the cells in the DCN receive much more local connections from other cells in the cochlear nucleus.

Figure 6 Teaching points. Illustration of the differences in the physiological response properties of five of the major cell types in the cochlear nucleus as compared to their auditory nerve fiber input (extreme left). The poststimulus time histogram to pure tones at CF and their frequency tuning curve are shown. As expected, the bushy cells in the VCN that get strong input from the ANF and relatively weak inhibition have PSTH and tuning curves that resemble their ANF input, while the other cell types transform the input substantially.

Figure 7 Teaching points. The two circuits in the superior olivary complex that are critical for encoding the interaural cues of ITD and ILD. The EE circuit involves the MSO which receives excitatory input from both sides and computes ITDs. The IE circuit of the LSO receives inhibition from the contralateral side via the MNTB, and excitation from the ipsilateral side computes ILDs.

Figure 8 Teaching points. Drawings of Golgi-stained axons projecting to the superior olivary nuclei in (A) show the large calyces of Held endings in the MNTB and the axonal input to the two sides of MSO cells from the AVCN of both sides. Panel (B) shows the cellular architecture of the LSO, while panel (C) shows the MSO.

Figure 9 Teaching points. Graphs showing the changes in the acoustic input to the two ears as the position of a sound source is varied along the horizontal (A) or vertical (B) dimension. The signals are obtained from a microphone placed near the eardrum of the left (blue) and right (red) ears. The horizontal angle for five different positions is shown by the drawing in the center. For each of the five positions, the upper traces are the recordings from the microphone as a function of time for a click stimulus, while the lower traces are the frequency spectra for the same signals. The difference in the arrival times of the click response in the upper traces reflects the ITD, while the amplitude of the spectral traces reflects the ILD as a function of frequency. Note that when the sound originates directly opposite the left ear (-90°), the left ear signal arrives earlier and is larger in amplitude than the right ear signal. For signals varying in the vertical dimension (B) along the median plane, the left and right ear signals are essentially identical, but the position of a prominent notch in the frequency spectrum designated by the * varies in frequency and is thought to play a crucial role in encoding the vertical component of the sound. The filters for the left and right ears for each position in space are referred to as the head-related transfer function (HRTF).

Figure 10 Teaching points. A simplified drawing of the Jeffress model. Inputs from the ipsilateral and contralateral sides arrive to the MSO cell array by way of a lattice-like pattern so that, for example inputs from the contralateral side arrive at cell 1 before they arrive at cell 2 and subsequent higher numbered cells by virtue of a longer delay line (?t). If the MSO cells are coincident detectors, then only the cell for which the delay lines on the two sides compensate for the acoustic delay resulting from the sound in space will fire. See supplementary information for a video illustration of this model.

Figure 11 Teaching points. Illustration of the enhancement in phase-locking from the auditory nerve (A,B) to the bushy cells in the AVCN (C,D) for a pure tone stimulus of about 350 Hz. Each dot in the rasters in (A) and (C) represents the time of the occurrence of the discharge with respect to the onset of the stimulus at 0 ms. Each row of dots is one trial of the 200 identical presentations. The vertical alignment of dots reflects the propensity of the cell to respond at a particular phase angle of the input, i.e. phase-locking. The enhancement in phase-locking is seen by the improved alignment of dots in (C) as compared to (A). The period histograms in (B) and (D) are computed by graphing the occurrence of each spike with respect to 0 phase. Again the enhancement in the bushy cell is apparent in the narrowness of the period histogram in (D) as compared to (E). The enhancement is quantified by the synchronization index plotted as a function of CF. The range of synchronization indices in the auditory nerve is shown by the two lines, while the responses of bushy cells are indicated by the different symbols. Most bushy cells with CF < 1 kHz have synchronization indices above 0.9, which exceeds that ever seen in ANFs.

Figure 12 Teaching points. Illustration of coincidence detection in an MSO cell for tones at CF of 1000 Hz. Binaural response as a function of ITD is shown in (A), while monaural responses to stimulation of the contralateral ear (B) and ipsilateral ear (C) are shown as period histograms. The period histograms show phase-locked responses to stimulation of both ears, with the contralateral ear responding with a mean phase angle indicated by the downward arrow of 0.02, while the ipsilateral response leads the contralateral response with a mean phase angle of -0.13. For coincidence to occur when stimulated binaurally, the ipsilateral stimulus should then be delayed by 0.15 ms. The binaural response in (A) shows that the MSO cell responds maximally when the ipsilateral stimulus is delayed by 0.10 ms.

Figure 13 Teaching points. Illustration of the theoretical basis for the characteristic delay analysis. The three examples show responses that have a common peak (A), trough (B), and relative amplitude (C). For illustrative purposes, the cyclic ITD curves are simulated as triangular-shaped curves, and ITD responses are shown at six different frequencies. (A) For a cell that peaks at the same ITD (300 ?s) regardless of frequency, the plot of the interaural phase as a function of frequency to the right is linear with a slope of 300 ?s and a phase intercept or characteristic phase of 0.0. (B) For a cell that has a common trough at -100 ?s, the interaural phase versus frequency plot has a slope of -100 ?s and a CP of 0.5. (C) For a cell in which the response reaches a common relative amplitude at 200 ?s, the interaural phase versus frequency plot has a slope of 200 ?s and a CP of 0.2.

Figure 14 Teaching points. Examples of three cells in the IC with CD characteristics corresponding to those in Figure 13. Each of the ITD curves is normalized to the peak, and responses at different frequencies are plotted on the same ITD axis for a cell with a common peak (A), trough (B), and relative amplitude (C). As shown in these examples, cells with a common peak or trough are relatively easy to identify, but many cells have responses like those shown in (C) where it is not clear if and where a common amplitude exists. This is where the CD analysis is useful. The interaural phase versus frequency plots on the right are linear, which identifies cells as CD, with corresponding CPs near 0 for common peak and near 0.5 for common trough and intermediate CPs. Most, but not all, cells in the IC have linear phase-frequency plots, but there is a wide range of CPs. On the other hand, CD cells in MSO tend to have CPs near 0, while those in the LSO have CPs near 0.5, reflecting their EE and IE binaural interaction, respectively.

Figure 15 Teaching points. Using binaural beats to study interaural phase sensitivity. The binaural beat stimulus is illustrated in (A); it provides a continuously changing interaural phase through each period of the beat frequency. So, for example a 1-Hz beat frequency will repeat the same interaural phase sequence every 1000 ms. If the stimuli are turned on in phase, then the ear (contralateral in this drawing) receiving the higher frequency signal initially leads until the stimuli are out of phase (p = 0.5), and then the other ear stimulus leads until the stimuli are back in phase. The perceived movement inside the head is drawn in (B) with the sound initially in the middle of the head, then moving toward the contralateral ear, suddenly jumping to the ipsilateral ear as the tones are out of phase, and returning to the midline. In this case, the perceived movement is from the ipsilateral toward the contralateral ear. The direction of movement can be changed by using a negative beat frequency, and the speed of movement is determined by the magnitude of the beat frequency. Panel (C) shows the poststimulus time histogram of a response to the binaural beat for a cell in the IC. In this case, the stimulus duration is 3 s long with a beat frequency of 1 Hz, resulting in three bursts at the preferred interaural phase. Panel (D) shows the ITD curve for the same cell. As expected, it responds at a preferred interaural phase with four repetitions over the ±2 cycles of ITD tested. Panel (E) compares the interaural phase sensitivity obtained using binaural beats in (C) (histogram) and ITDs in (D) (solid line). The value of the binaural beat stimulus is the efficiency with which all possible interaural phases can be probed as compared with static ITD measurements, and the similarity between the two measures of interaural phase sensitivity (E) demonstrates its utility.

Figure 16 Teaching points. Figure depicting that the sensitivity to ITDs of a broad band noise signal can be approximated by summing the ITD curves of individual frequencies within the noise band. Panel (A) shows superimposed ITD curves over eight different frequencies between 500 and 1.7 kHz plotted on a common ITD axis. Individual ITD curves are as number of spikes, not normalized to the peak. Panel (B) compares the summed responses to the eight different frequencies in (A) (curve labeled “Tones”) with the response to ITDs of a wide band noise (Noise). The two responses are very similar. The interaural phase versus frequency plot for this cell in panel (C) shows that it demonstrates CD and has a common peak.

Figure 17 Teaching points. Plots like Figure 16B for nine different cells in the IC illustrate how similar the noise and tone delay curves are for a population of cells.

Figure 18 Teaching points. The computation of ITD to noise in the IC is similar to the process of cross-correlation. This was tested by creating pairs of noises that had different amount of correlation, from perfectly correlated (correlation coefficient r = 1.0) to completely uncorrelated (r = 0.0) and several values in between. When tested with these pairs of noises, the IC cells invariably responded best to the correlated pair with systematically decreasing modulation as the interaural correlation of the stimuli decreased toward 0. Responses to uncorrelated noises were unmodulated by ITD.

Figure 19 Teaching points. This schematic contrasts the distributions of optimal delays (ODs) expected for the Jeffress model with the distribution experimentally observed. The OD is the ITD to which a coincidence detector neuron is most active (red dot in top and bottom ITD curves): it reflects the internal delay, which is the difference in delay for the signals from the two ears to influence the binaural neuron. In (A), the distribution is rectangular. Each circle represents one neuron. Here, there is a range of internal delays that is independent of the best frequency to which the coincidence detector is tuned. The ITD curves illustrate the effect of a large internal delay (0.4 ms) on a fiber tuned to a low (bottom) and high (top) frequency. What is seen physiologically (B) is a pattern of ODs with a small range at high and a large range at low frequencies. The largest ODs approximate half a period of the frequency to which the neuron is tuned.

Figure 20 Teaching points. These intracellular recordings from an MSO neuron show the coincidence process. The top traces show 45 ms from a response to a monaural tone played either ipsilaterally (200 Hz) or contralaterally (201 Hz). The membrane potential shows postsynaptic potentials: brief depolarizations that are phase-locked to the stimulus and that remain subthreshold. When the stimuli are combined and produce a binaural beat, the cell shows spiking when the stimuli are in-phase (lower left) but not when they are in antiphase (right). For the in-phase part of the stimulus, the postsynaptic potentials from the two sides are now aligned and generate fast and phase-locked upswings in membrane potential, which in two cases set off an action potential. For the antiphase part, the potentials are interspersed and do not line up, so that they remain subthreshold.

Figure 21 Teaching points. Illustration of the sensitivity to ILD of LSO cells. Panels (A-D), a dot raster and PSTH of the responses to stimulation of the ipsilateral ear at 30 dB SPL, while the contralateral level was varied from 5 (A) to 45 (D) dB SPL. The inhibition provided by the contralateral side is evident in the systematic decrease in response as the contralateral level is increased. The ILD function is plotted in (E). The inset in (A) shows the first 40 ms of the response, which reveals the chopper pattern typical of LSO nonprincipal cells. Again, this clearly shows that increasing the contralateral stimulus level decreases the response.

Figure 22 Teaching points. The spatial receptive field of the same LSO cell as in Figure 21 using virtual acoustic space techniques. The spatial location of the stimuli was simulated using the HRTFs (Figure 9). The responses to 21 spatial positions varying in azimuth along the frontal sound field are stacked and plotted as dot rasters in (A) and (B). The stimulus is turned on at 0 ms and turned off at 200 ms. In (A), both ears are stimulated and the cell responds for stimuli with negative azimuths (left frontal field) and inhibited for stimuli in the right frontal field. In (B), the stimuli to the contralateral ear are turned off so that only the excitatory ipsilateral is on. Without the contralateral input, the inhibition is eliminated. The spike counts during the duration of the stimulus are plotted in panel (C). The distance between the two curves represents the inhibition from the contralateral side.

Figure 23 Teaching points. The ITD sensitivity of an LSO cell to click stimuli. Since LSO cells show IE binaural interaction, the contralateral input inhibits the ipsilateral response but only for a short range of ITDs for a transient stimulus. In this experiment, the excitatory ipsilateral stimulus was held constant at 50 dB SPL, while the contralateral click varied from 30 to 70 dB SPL. When the contralateral click was at 30 or 35 dB, there is little effect. At 40 dB, the response is inhibited over a narrow range of ITDs, which broadens as the contralateral SPL is raised. The curves at the top show the putative EPSPs and IPSPs for three different ITDs. For ITD of -1500 ?s, the inhibition arrives too late to effect the EPSP, while at +1500 ?s ITD, the inhibition is over when the EPSP arrives.

Figure 24 Teaching points. A test of the latency hypothesis in the LSO of the rat. Panel (A) shows plots of the ipsilateral click alone (dotted curve and lower axis) and binaural response (solid curve, circles) in which the inhibitory contralateral level is held constant at 70 dB, while the ipsilateral varies from 50 to 100 dB. Panel (B) shows the ITD sensitivity in a manner similar to that shown in Figure 23. The question raised in this experiment is whether the ILD sensitivity is due to the ITD sensitivity coupled with the change in latency as the SPL is changed. Since the excitatory stimulus is varied to vary ILD, the latency changes can be measured from the rate-level curves. Two curves are obtained to compare with the natural ILD (here labeled IID) curve: (i) the equivalent ITD curve (ITDe) is calculated by incorporating the changes in latency with the ITD function of panel (B) with constant SPL of both ears, while (ii) the delay cancelled ILD (IIDdc) is generated by delivering the ILD but with latency changes from the rate-level curves nulled so that ITDs are not present. Panel (C) shows responses of a cell in which the natural ILD curve (ILD) is essentially the same as the ITDe curve, while the IIDdc curve is flat, so it would correspond to a cell that fits the latency hypothesis. On the other hand, panel (D) shows responses from a different cell in which the ILD curve matches the IIDdc curve, while the ITDe is flat, which corresponds to a cell where the ILD function is not affected by response latency.

Figure 25 Teaching points. A family of ILD functions showing the variability in form of ILD functions in the LSO of the awake bat. Note that the half-maximal ILD, which is defined as the inhibitory threshold, varies over about 40 dB. One can consider the ILD functions as a crude representation of the spatial receptive field of the cell, and the change in threshold ILD would be equivalent to changes in the border of the receptive field.

Figure 26 Teaching points. Plots of the inhibitory threshold as a function of depth of the penetration in the IC of the bat at four different locations. The numbers for all four penetrations have a systematic change as a function of depth, suggesting that ILDs are mapped in a systematic way in the IC.

Figure 27 Teaching points. The type IV cells (fusiform) have unusual response maps (C) that are thought to be established by the circuitry in the DCN shown in panel (A). The frequency tuning of the inputs to the type IV cell is shown in (B). The CFs of the inputs from the ANFs are depicted by the horizontal line at the bottom. The type IV cells receive strong excitatory ANF input and inhibitory input from type II cell that has a slightly lower CF and from the wide band inhibitor which receives ANF input from a broader range of frequencies. The response map in (C) shows responses of the type IV cell at nine different attenuation levels. At the highest attenuation, the cell only responds at CF, but as the attenuation is decreased, the small excitatory bump at CF is replaced by inhibition over a band around CF. This inhibition is created by type II input at frequencies lower than CF and by the WBI at higher frequencies.

Figure 28 Teaching points. Sensitivity of a type IV neuron to the frequency of spectral notches like those found in the HRTFs. Typical spectral notches at three different frequencies are plotted in panel (A). Panel (B) shows the response map of a type IV cell with the typical excitatory bump at low sound levels (high attenuation) near CF and inhibition at higher levels. Panels (C) and (D) show the response of the cell to five different noise stimuli with different spectral notches with the notch frequencies indicated by (a), (b), (c), (d), and (e) in panels (A) and (B). In this cell, as the level is raised with a spectral notch at CF (11.6 kHz), there is pronounced inhibition at higher levels. The inhibition is not present for the same levels when the notch frequencies are 0.7 or 1.4 kHz distant from CF. Thus, this cell is a good candidate for detecting a spectral notch at 11.6 kHz and not at nearby notch frequencies.

Figure 29 Teaching points. An example of testing an IC cell with intermediate CP for convergent input. Panel (A) shows the interaural phase versus frequency plot that the cell exhibits CD, but has an intermediate CP of 0.20. Individual ITD curves are shown in panel (B) for six different frequencies. To test for convergent input, a suppressor tone was delivered at the same time as binaural beats at other frequencies. So, in panel (C), the histogram shows the PSTH of responses to binaural beats at 250 Hz. The suppressor tone was chosen to be 100 Hz at an unfavorable phase. When the suppressor tone is added, the binaural beat response changes to the heavy black line. Panels (D-H) show similar results as in (C) at different frequencies and the same suppressor tone. Panel (I) plots the interaural phase versus frequency for both the original and responses with the suppressor (circles). Black dots show that at the frequencies near the suppressor the ITD curve is flat. At the four highest frequencies distant from the suppressor, the interaural phase versus frequency plot is linear and has a CP = 0.03, reflecting a common peak, as plotted in panel (J). These results suggest that the cell has an intermediate CP due to convergent input which at high frequencies has a common peak, reflecting the MSO input.

Figure 30 Teaching points. The precedence effect (PE) and demonstration that cats also experience the effect. Panel (A) shows a typical situation for testing the PE: a subject faces two speakers placed symmetrically in front. When identical sounds are delivered to the two speakers with no ISD, the subject perceives the sound to come from a phantom source at the midline. As the ISD is gradually increased, the perceived source location moves toward the leading speaker. This is the period of summing localization (B). At about ISD = 1 ms, the perceived source is entirely at the leading speaker and the lagging speaker is not perceived spatially: this is the period of the PE. The name comes from the situation of a sound that is delivered in an echoic environment but is localized to the speaker, despite the presence of later arriving echoes, i.e. the leading sound takes precedence for spatial localization. As the ISD is increased even further, the echo threshold is reached, and the subject hears both sounds at their respective locations. Panel (C) shows results of a behavioral localization experiment in which cats were trained to direct their gaze to the location of sound sources. When PE stimuli were used, the perceived location of the speaker followed the model results shown in (B), i.e. they looked between the speakers for ISDs in the summing localization range, and at the leading speaker for ISDs in the PE range. For large ISDs, the response was much more variable, presumably because the cat heard both sounds and was confused about which to look at. These results were obtained by delivering other non-PE stimuli at high probability and the PE at low probability, while rewarding the PE trials regardless of the response.

Figure 31 Teaching points. Correlates of the perceived PE in responses of cells in the IC of the cat when stimulated with PE stimuli. When pairs of clicks are delivered with variable ISD, the cell responds to the initial click and the response to the lagging click can be suppressed for periods that depend on the strength of the initial response. When the speaker (a) leads, the response to the lagging speaker (b) is suppressed for all ISDs out to around 100 ms, as seen in the top half of the dot rasters of panel (C) (positive ISDs). When speaker (b) leads, the suppression is weaker since the response to (b) is weaker, while that to (a) is stronger, as seen in the bottom half of the dot rasters of panel (C) (negative ISDs). For ISDs in the summing localization range (between -1 and +1 ms of panel B), the response maps that obtained from single clicks varying in spatial position from (b) to (a) (panel A). Thus, the cell responds in the summing localization range as if it is “perceiving” the stimulus spatially between speakers (b) and (a).

Figure 32 Teaching points. Illustration of the counterintuitive nature of the binaural masking level difference (BMLD). (A) Delivering noise and tone in one ear makes it difficult to hear the tone (frowning expression of subject). (B) Adding noise in phase to the other ear makes the tone more easily detectable (smiling). (C) Then adding a tone in phase to the second ear makes the tone less detectable. (D) Inverting the phase of the tone makes it more detectable. So, in some cases, adding noise makes the tone easier to hear, while adding a tone can make it more difficult to hear.

Figure 33 Teaching points. Examples of studies of BMLD in the IC of guinea pigs. Three different cells are shown in the three rows. In each row, the ITD curve to noise is on the left, the interaural period histograms of responses to a 500-Hz binaural beat are in the middle, and the masked rate-level function on the right. The masked rate-level function is obtained using signal detection to calculate the detectability index D as a function of tone level for a fixed noise level. Comparisons between the NoSo (solid circles) and NoS? (open circles) conditions are shown. The point at which the absolute value of D exceeds ±1 is considered detectable. The cell in panel (A) has a positive BMLD of 11 dB (NoS? condition has a lower threshold), and adding signal in phase increases the discharge, while adding signal out of phase causes a decrease. The cell in panel (B) also has a positive BMLD, but in this case adding the signal in or out of phase causes an increase response. Finally, the cell in panel (C) has a negative BMLD (NoS? condition has a higher threshold). As might be expected, IC cells show a variety of different responses to the BMLD stimuli, but on average they have positive BMLDs, and the hierarchy of the BMLDs is similar to that seen psychophysically.

Figure 34 Teaching points. The studies of spatial release from masking in the IC of cat using virtual acoustic space techniques. The stimulus configuration is shown by the cartoons in the top row. In panel (A), both the signal and noise were delivered at +90°, i.e. to the spatial position opposite the right ear. In panel (B), the noise is opposite the left ear, while the signal is opposite the right. In panel (C), the configuration is opposite to panel (B). In the dot rasters on the bottom row, the responses as the noise level is varied from 25 to 67 dB are shown. The signal is on from 0 to 200 ms, while the noise is continuous. This cell responded best for a sound on the right. The highest noise level at which the signal can still be detected is a measure of the spatial release from masking. In panel (A), the response to the periodic chirp signal can be seen in the dot rasters at between 43 and 49 dB noise level, while in panel (B), the periodic chirp response can be seen between 55 and 61 dB. Thus, the signal is more detectable when the noise is spatially separated. Note that in panel (B), there is no response to the noise, but it does suppress the response to the signal at the highest noise levels.

 


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Article Title: Neural Mechanisms of Binaural Processing in the Auditory Brainstem
 

How to Cite

Tom C.T. Yin, Phil H. Smith, Philip X. Joris. Neural Mechanisms of Binaural Processing in the Auditory Brainstem. Compr Physiol 2019, 9: 1503-1575. doi: 10.1002/cphy.c180036