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Peripheral Neural Processing of Auditory Information

Nelson Y. S. Kiang

10.1002/cphy.cp010315

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Anatomy of Primary Auditory Neurons
1.1 General Features of Primary Neurons
1.2 Nerve Endings in Cochlea
1.3 Nerve Fibers in Cochlea
1.4 Neuronal Cell Bodies in Spiral Ganglion
1.5 Auditory Nerve Fibers in Internal Auditory Meatus
1.6 Primary Innervation of Cochlear Nucleus
2 Physiological Data on Auditory Nerve
2.1 Conceptual Stages of Peripheral Auditory System
2.2 Methodology in Stimulus‐Response Relationships of Auditory Nerve Units
2.3 Stimulus‐Response Relationships For Auditory Nerve Units
2.4 Relationship Between Gross Neural Potentials and Unit Activity
2.5 Effects of Stimulating Efferent Fibers to Cochlea
2.6 Responses in Abnormal Ears
2.7 Electric Stimulation of Auditory Nerve Fibers
3 Implications of Data on Auditory Nerve
3.1 Peripheral Mechanisms Generating Auditory Nerve Activity
3.2 Central Processing of Auditory Information
3.3 Addendum
Figure 1. Figure 1.

Drawing of organ of Corti in basal turn of typical mammalian cochlea. There are differences among species, but basic plan is similar for all mammals. Foreground represents more basal part of cochlea. Here one hair cell is removed from middle row of outer hair cells so that 3‐dimensional aspects of relationship between supporting cells and hair cells can be seen. Diameter of an outer hair cell is approximately 7 μm. The most basal components are drawn so that some intracellular detail can be seen. Breaks in nerve fibers indicate that a portion has been displaced so that spiral ganglion cell bodies, which are normally located farther away, could be shown. Empty spaces at bases of outer hair cells are occupied by efferent endings that have been omitted from drawing. I, Basilar membrane; 2, Hensen cells; 3, outer phalangeal cells of Deiters; 4, nerve endings; 5, outer hair cells; 6, outer spiral fibers; 7, outer pillar cells; 8, inner tunnel; 9, inner pillar cells; 10, inner phalangeal cells; 11, border cell; 12, tectorial membrane; 13, type I spiral ganglion cell; 14, type II spiral ganglion cell; 15, bony spiral lamina; 16, spiral blood vessel; 17, spindle cells; 18, axons of spiral ganglion cells (auditory nerve fibers); 19, radial fiber.
Figure 2. Figure 2.

Schematic drawing of primary neurons. Drawing is approximately to scale except that small collateral branches and endings in cochlear nucleus are drawn thicker in order to be seen. One type of neuron (right), thought to be type I neurons in spiral ganglion, has peripheral extensions that innervate the base(s) of one or two inner hair cells. A second type (left), probably type II neurons, has peripheral extensions that cross tunnel of Corti to run longitudinally toward base for approximately 0.5 mm before innervating many outer hair cells. Peripheral and central extensions of type I neurons are myelinated; those of type II neurons are most likely not myelinated. Central extensions of type I neurons terminate with a variety of endings on cells of cochlear nucleus. Main axon bifurcates to form an ascending branch that innervates anteroventral cochlear nucleus (AVCN) and a descending branch that innervates posteroventral cochlear nucleus (PVCN) and dorsal cochlear nucleus (DCN). Central extensions of type II neurons proceed into the internal auditory meatus but are otherwise undescribed.
Figure 3. Figure 3.

Drawing of cross section through cat's auditory nerve. Top two‐thirds of section is peripheral to Schwann cell‐neuroglial junction; bottom one‐third is central to junction. Small area of cross section is enlarged at right, along with drawing of microelectrode to same scale. In enlargement, clear ovals surrounded by dark rings represent axons covered by myelin sheaths.
Figure 4. Figure 4.

Discharge pattern of single unit in auditory nerve during spoken utterance “shoo cat.” Top trace shows voltage input to earphone, which closely resembles wave form of acoustic stimulus. Stimulus level was −57 dB in terms of 200 V peak to peak into earphone. Middle trace shows sample recording from fiber; large vertical deflections are spike discharges. Bottom graph is PST histogram computed from responses to 64 presentations of speech stimulus. Histogram plots number of spike discharges in each bin as function of time after onset of stimulus. Bin width is 1 ms. All 3 displays have same time base. Unit is most sensitive to tone frequency of approximately 1 kHz. More examples of unitary responses to this speech stimulus can be found in refs. 104,108, and 109.
Figure 5. Figure 5.

Response of auditory nerve fiber to single tone burst. Graph at top displays spike rate before, during, and after 5‐min, 53‐dB sound pressure level tone burst at frequency to which unit is most sensitive (0.26 kHz). Each point represents spike rate over a 0.5‐s sample of spike activity. Total of points, nearly 1,700, covering 850 s. Average spontaneous discharge rate is approximately 85 spikes/s. Bottom: interspike interval histograms before (A), during (B), and after (C) tone burst. Each histogram is computed for approximately 5 min of data.
Figure 6. Figure 6.

Schematic plot of spike rate vs. tone intensity and frequency for auditory nerve unit. Large plot shows a surface in 3 dimensions. Intersections of families of parallel planes with this surface will define contour lines. Three families of contour lines made by planes orthogonal to axes have been studied and are shown in smaller 2‐dimensional plots. Point of lowest intensity on each isorate contour line is frequency of maximal sensitivity, the value of which approaches characteristic frequency for low isorates. Highest point on each isointensity contour line is frequency of maximal responsiveness, the value of which also approaches characteristic frequency as stimulus intensity decreases. Because this figure is intended only to illustrate the definition of contour lines, no numbers are given for scales.
Figure 7. Figure 7.

Map relating characteristic frequency of auditory nerve fibers to longitudinal location along basilar membrane. Map is based on data from cochleas of cats subjected to acoustic trauma. Correspondence between characteristic frequency (CF) and cochlear location was made by associating regions along basilar membrane where outer hair cells were missing with CF ranges over which units could not be found 121. A formula relating percentage distance from base (d) to CF is d = 71 − 37 log (CF). At top of figure, basilar membrane is drawn to scale as if it were uncoiled and viewed from below. For different cats the absolute length may vary by a few millimeters. For cat from which these data were taken, length of basilar membrane from surface preparations was 24.5 mm, which is very close to average value of 24.4 mm for 12 adult cats. Average value obtained by Cabezudo 19, using reconstructions from sectioned cochleas, is 23.66 mm, which is closer to value of 23.5 mm given by Retzius 172. Below drawing of entire basilar membrane, three 0.25‐mm segments are shown enlarged. Locations of tops of hair cells are depicted. The 3 rows of outer hair cells (OHC) and 1 row of inner hair cells (IHC) are seen to be perched at 1 edge of the membrane, rather than near middle. Because of slant of hair cells (see Fig. 1), bottoms of inner hair cells in base of cochlea sit over bone. Tops of outer and inner hair cells are separated by top of inner pillar cell, width of which is systematically greater for more apical locations.
Figure 8. Figure 8.

Tuning curves of 10 units from 1 cat auditory nerve. Tuning curves were obtained by using an automated procedure 111. Numbers within plot identify units. Each curve in plot is an average of 4 tuning curves obtained for that unit, except for unit 14 (an average of 12 tuning curves), and unit 59 (an average of 3 tuning curves). When 2 curves intersect, the curve for unit with lower characteristic frequency is broken. Each tuning curve consists of 256 possible points, with 32 points distributed linearly within each octave. Intensity resolution is 2/3 dB/step. The criterion for positive response is that number of spikes occurring during 50‐ms interval when tone is on exceeds number of spikes for 50‐ms interval when tone is off. Tone bursts (10/s) have a rise time of 2.5 ms to reduce effects related to spread of spectral energy whenever tones are turned on or off. With these stimulus parameters, tuning curves for most units are very close to those taken manually with continuous tones or tone bursts, as described in ref. 113. All these units have high spontaneous discharge rates (>18 spikes/s).
Figure 9. Figure 9.

Tuning curves of 3 units with nearly the same characteristic frequency (CF) but widely different rates of spontaneous activity; taken from 4‐mo‐old cat born and raised in a soundproof chamber in an attempt to minimize possible effects of high‐level environmental noise. Pertinent data for unit 124: CF, 3.8 kHz; threshold, 28 dB sound pressure level (SPL); spontaneous activity, 0.27 spikes/s. Unit 179: CF, 3.9 kHz; threshold, 6 dB SPL; spontaneous activity, 5.60 spikes/s. Unit 250: CF, 3.8 kHz; threshold, 0.5 dB SPL; spontaneous activity, 52.40 spikes/s.
Figure 10. Figure 10.

Discharge rate (histograms) and response times (dot displays) of 6 auditory nerve fibers for tones swept in level. Histogram given for each unit shows spike rate (expressed as a percentage of 200 spikes/s), as level of tone is increased over 120‐dB range. Tone is on during interval indicated by bar at top of each histogram and off for first 10 and last 10 bins of each histogram. An individual histogram consists of 200 bins, each bin corresponding to an increment of approximately 3/4 dB. Except for the one on the top left (5 sweeps), each histogram represents 10 intensity sweeps, individual sweeps lasting 10 s. Intensity function changes little with sweep rate over a range of 1–1000 s for these stimulus parameters. Dot displays beneath histograms have as ordinates the time after a positive zero crossing for every other cycle of the tone. Abscissas are the same as for histograms. Each dot represents time of occurrence of a spike. Thus phase of responses as a function of stimulus level can be derived from dot displays. Zero dB is approximately 120 dB sound pressure level for these experiments. In each case characteristic frequency (CF) and frequency of stimulating tone (TF) are given at top and bottom of the figure.
Figure 11. Figure 11.

Instantaneous discharge rates for single auditory nerve fiber responding to continuous tones (CT). Discharge patterns over 2 cycles of a tone (bottom) are shown in 200‐bin PST histograms based on 15‐s samples of data. Each row contains data for same stimulus level; each column contains data for same tone frequency. Zero time corresponds to positive zero crossing of electrical input to 1‐in condenser earphone. Vertical axis of each histogram is instantaneous spike discharge rate with full‐scale value being either 500 spikes/s or 1,000 spikes/s. Histogram at top, labeled SPONT, is based on a sample of spontaneous activity processed as if there were a tone at characteristic frequency. For this figure the sound pressure level at −10 dB is approximately 106 dB in terms of 0.0002 dyn/cm2 for all frequencies.
Figure 12. Figure 12.

Phase of responses to tones as function of frequency for 2 units of low characteristic frequency. Each half of figure shows tuning curve and plot of response phase vs. frequency for 1 auditory nerve unit. Ordinate on left of each plot is associated with tuning curve; ordinate on right is related to phase curve. Abscissa is tone frequency on linear scale. For each curve there are 32 points linearly distributed within each octave. Lowest frequency used is 160 Hz. Phase curves plot phase of fundamental component of PST histograms where zero time corresponds to positive zero crossing of electric input to the 1‐in. condenser earphone.
Figure 13. Figure 13.

Response patterns of 3 auditory nerve fibers to tone bursts at characteristic frequencies. Wave form of electric input to condenser earphone is shown under each PST histogram. There is a 0.07‐ms travel time for acoustic signal to arrive at tympanic membrane. PST histograms on left show response patterns to entire tone burst; histograms on right show response pattern to tone burst onset on expanded time scale. Each histogram represents an average of >3,000 tone‐burst presentations. The 50‐ms tone bursts had rise‐fall times of 2.5 ms and were delivered at a rate of 10 bursts/s. At this stimulus repetition rate, the spontaneous activity does not recover to its full value before next tone burst arrives. Spontaneous discharge rates of the 3 units, from top to bottom, were 85, 95, and 62 spikes/s, respectively. Vertical axis in PST histograms is expressed most directly as spikes per bin but can be converted into instantaneous spike rate by using the formula: spike rate = number of spikes per bin, divided by the binwidth times the number of stimulus presentations. This procedure can yield instantaneous spike rates as high as thousands of spikes per second. These values may at first be disconcerting to some neurophysiologists, but they follow directly from the definition of instantaneous rate. Perfectly time‐locked responses would have arbitrarily high instantaneous rates.
Figure 14. Figure 14.

Effect of background tone on tuning curve. Isorate curve A (dotted line) was obtained by using stimulus paradigm A (single tone bursts swept in frequency). Isorate curve B (solid line) was obtained by using stimulus paradigm B (one tone burst fixed in frequency and a second swept in frequency). In both cases response rate was defined to be difference between spike rates during periods a and c (at left). Tone I was test tone that was swept in frequency. Parameters of fixed tone 2 are indicated by open circle in plots on right (7 kHz and 65 dB). Unit characteristic frequency was 5.4 kHz and spontaneous rate of discharge was 18 spikes/s. Arrow points to a peak of sensitivity at a frequency of 8.4 kHz.
Figure 15. Figure 15.

Response of auditory nerve unit to 2 simultaneously presented tone bursts. Left column shows 4 stimulus situations; right column plots rate of response under conditions described on left. Each box on left shows unit's tuning curve with dot showing frequency and level of fixed tone burst. Horizontal line with arrow pointing to left indicates frequency range and intensity level of tone bursts swept in frequency. Stimulus paradigms are shown in Fig. 14. Characteristic frequency (CF) of unit was 5.4 kHz at 14.5 dB sound pressure level. On right are frequency‐response curves with normalized driven rate defined as (spike rate ‐ spontaneous discharge rate)/(maximum spike rate ‐ spontaneous discharge rate). Spontaneous discharge rate of this unit was 18 spikes/s. Maximum spike rate is estimated by measuring spike rate for 80‐dB tone bursts at CF. Dashed lines across bottom 3 boxes on right indicate, in each instance, spike rate for fixed tone burst alone, based on 20 tone burst presentations, 10 before and 10 after swept tones were presented. Frequency‐response curves on right have frequency resolution that is one‐fourth that of tuning curves. Each point is based on 10 repetitions of a pair of tone bursts (or of single tone bursts for box at top. For top row there are no fixed tone bursts, so the frequency‐response curve is simply a plot of driven rate vs. frequency of tone burst. Second row shows frequency‐response curve for same swept tones but with fixed tone burst at CF presented simultaneously. Third row repeats experiment except that fixed tone bursts are at a frequency far removed from CF. For fixed tone bursts to generate responses, level of fixed tone bursts had to be increased above that of swept tones. Bottom row shows results for stimulus conditions similar to that for third row except that intensity level of swept tone bursts is increased to be almost equal with that of fixed tone bursts. (Some areas are stippled for easy reference.)
Figure 16. Figure 16.

Times of unit responses to clicks compared with potentials recorded near round window. Trace at top is 30‐s average of round window responses to condensation clicks (10 clicks/s, 88 dB sound pressure level) produced by delivering 100‐μs pulses to 1‐in. condenser earphone. Upward deflection indicates negativity at gross electrode referred to head holder. Cochlear microphonic potential, CM; first negative deflection representing neural activity, N1. Plot at bottom shows times at which the instantaneous discharge rates of units are >666 spikes/s as displayed in PST histograms of unit responses to clicks. Times of unit responses were all displaced by 0.2 ms in an attempt to compensate roughly for conduction time from point of spike initiation to recording micropipette. Data from 54 units.
Figure 17. Figure 17.

N0 calculations for 2 units recorded simultaneously with separate micropipettes in auditory nerve. A 0.3‐s sample of spontaneous spikes is shown for each unit, along with simultaneously recorded round window (RW) potential (top trace) recorded with gross silver ball electrode. N0 is an estimate of voltage contribution of a spike to potential recorded at gross electrode. Two N0 wave forms at bottom were obtained by cross‐correlating round window recording with times of spike discharges for 2 units. Zero time is time of half‐amplitude point on rising part of spike waveforms. Peak of N0 occurs before zero time because it takes time for spike to travel from point of spike initiation to recording electrode. For unit 11A (characteristic frequency = 0.53 kHz) 27,572 spikes were used to compute average, while only 6,090 spikes were used for unit 11B (characteristic frequency = 0.5 kHz).
Figure 18. Figure 18.

Comparison of synthesized and recorded compound action potential (CAP) for auditory nerve of I cat. Unit recordings were made with micropipette in internal auditory meatus; gross‐potential recordings were taken with wire loop on ipsilateral round window. Both were recorded simultaneously for 65‐dB sound pressure level rarefaction clicks presented at a rate of 10/s; recordings were also made in the absence of acoustic stimulation. Synthesized CAP was constructed as follows: 1) The total range of characteristic frequencies (CFs) between 0.2 and 40 kHz was divided into 128 CF groups of equal intervals on a log CF scale. Each CF group was further separated into 3 divisions based on spontaneous discharge rate: high (>18 spikes/s), medium (0.5–18 spikes/s), and low (<0.5 spikes/s). Data were collected for 181 units selected to cover as broad a range of groups and divisions as possible. Contributions of low‐spontaneous units are negligible, so these units were not represented in synthesizing CAPs. 2) PST histograms of responses to clicks were computed for 30‐s samples of data. When no unit data were available for a bin, an interpolation procedure was used based on neighboring bins. When data from more than 1 unit were available for a bin, they were averaged. A CF‐dependent latency shift (up to 0.18 ms) was incorporated, based on N0 data that show shortest (0.04 ms) latencies for units with CF around 3–6 kHz and longest (0.22 ms) latencies for units with high CF. Finally a weighting factor for unit density as a function of CF was introduced, based on Schuknecht's 197 data on primary neuron distribution and a total estimated 50,000 fibers 54. 3) A compound PST histogram was then calculated that gave time distribution of activity over the whole nerve. 4) Data obtained under no‐click condition were used in computing N0s (see Fig. 16) for 6 units from this cat. These N0s had a wave form that was close to that of an idealized N0 based on an average of 232 N0 calculations taken from many animals. Although wave form of idealized N0 was used in later calculations, amplitude of idealized N0 was made to equal mean amplitude of 6 N0s from this cat. The compound PST histogram was convolved with idealized N0 to give synthesized CAP (dotted trace). Upward deflection is considered to be negative at round window referred to head holder. The 30‐s samples of round window responses to clicks recorded simultaneously with unit recordings used in obtaining PST histograms were averaged and displayed as recorded CAP (solid line). Trace showing recorded CAP contains some cochlear microphonic components as well as later neural components.
Figure 19. Figure 19.

Effect of crossed divocochlear bundle (COCB) stimulation on auditory nerve responses. A: N1 click‐intensity functions with and without electric stimulation of COCB at midline on floor of fourth ventricle. Inset is PST histogram of discharge rate of auditory nerve unit for 20 s of exposure to continuous 10‐dB tone at characteristic frequency (CF) of 0.6 kHz, during which bursts of shocks (400/s) were delivered to the COCB. (Bar above histogram shows duration of burst of shocks.) Histogram represents an average over 20 bursts of shocks. B: same as A except that COCB is now cut laterally to facial genu on side where recordings are made. Inset is PST histogram for another unit (CF = 2 kHz). Except for frequency, stimulus parameters were same as for other unit.


Figure 1.

Drawing of organ of Corti in basal turn of typical mammalian cochlea. There are differences among species, but basic plan is similar for all mammals. Foreground represents more basal part of cochlea. Here one hair cell is removed from middle row of outer hair cells so that 3‐dimensional aspects of relationship between supporting cells and hair cells can be seen. Diameter of an outer hair cell is approximately 7 μm. The most basal components are drawn so that some intracellular detail can be seen. Breaks in nerve fibers indicate that a portion has been displaced so that spiral ganglion cell bodies, which are normally located farther away, could be shown. Empty spaces at bases of outer hair cells are occupied by efferent endings that have been omitted from drawing. I, Basilar membrane; 2, Hensen cells; 3, outer phalangeal cells of Deiters; 4, nerve endings; 5, outer hair cells; 6, outer spiral fibers; 7, outer pillar cells; 8, inner tunnel; 9, inner pillar cells; 10, inner phalangeal cells; 11, border cell; 12, tectorial membrane; 13, type I spiral ganglion cell; 14, type II spiral ganglion cell; 15, bony spiral lamina; 16, spiral blood vessel; 17, spindle cells; 18, axons of spiral ganglion cells (auditory nerve fibers); 19, radial fiber.



Figure 2.

Schematic drawing of primary neurons. Drawing is approximately to scale except that small collateral branches and endings in cochlear nucleus are drawn thicker in order to be seen. One type of neuron (right), thought to be type I neurons in spiral ganglion, has peripheral extensions that innervate the base(s) of one or two inner hair cells. A second type (left), probably type II neurons, has peripheral extensions that cross tunnel of Corti to run longitudinally toward base for approximately 0.5 mm before innervating many outer hair cells. Peripheral and central extensions of type I neurons are myelinated; those of type II neurons are most likely not myelinated. Central extensions of type I neurons terminate with a variety of endings on cells of cochlear nucleus. Main axon bifurcates to form an ascending branch that innervates anteroventral cochlear nucleus (AVCN) and a descending branch that innervates posteroventral cochlear nucleus (PVCN) and dorsal cochlear nucleus (DCN). Central extensions of type II neurons proceed into the internal auditory meatus but are otherwise undescribed.



Figure 3.

Drawing of cross section through cat's auditory nerve. Top two‐thirds of section is peripheral to Schwann cell‐neuroglial junction; bottom one‐third is central to junction. Small area of cross section is enlarged at right, along with drawing of microelectrode to same scale. In enlargement, clear ovals surrounded by dark rings represent axons covered by myelin sheaths.



Figure 4.

Discharge pattern of single unit in auditory nerve during spoken utterance “shoo cat.” Top trace shows voltage input to earphone, which closely resembles wave form of acoustic stimulus. Stimulus level was −57 dB in terms of 200 V peak to peak into earphone. Middle trace shows sample recording from fiber; large vertical deflections are spike discharges. Bottom graph is PST histogram computed from responses to 64 presentations of speech stimulus. Histogram plots number of spike discharges in each bin as function of time after onset of stimulus. Bin width is 1 ms. All 3 displays have same time base. Unit is most sensitive to tone frequency of approximately 1 kHz. More examples of unitary responses to this speech stimulus can be found in refs. 104,108, and 109.



Figure 5.

Response of auditory nerve fiber to single tone burst. Graph at top displays spike rate before, during, and after 5‐min, 53‐dB sound pressure level tone burst at frequency to which unit is most sensitive (0.26 kHz). Each point represents spike rate over a 0.5‐s sample of spike activity. Total of points, nearly 1,700, covering 850 s. Average spontaneous discharge rate is approximately 85 spikes/s. Bottom: interspike interval histograms before (A), during (B), and after (C) tone burst. Each histogram is computed for approximately 5 min of data.



Figure 6.

Schematic plot of spike rate vs. tone intensity and frequency for auditory nerve unit. Large plot shows a surface in 3 dimensions. Intersections of families of parallel planes with this surface will define contour lines. Three families of contour lines made by planes orthogonal to axes have been studied and are shown in smaller 2‐dimensional plots. Point of lowest intensity on each isorate contour line is frequency of maximal sensitivity, the value of which approaches characteristic frequency for low isorates. Highest point on each isointensity contour line is frequency of maximal responsiveness, the value of which also approaches characteristic frequency as stimulus intensity decreases. Because this figure is intended only to illustrate the definition of contour lines, no numbers are given for scales.



Figure 7.

Map relating characteristic frequency of auditory nerve fibers to longitudinal location along basilar membrane. Map is based on data from cochleas of cats subjected to acoustic trauma. Correspondence between characteristic frequency (CF) and cochlear location was made by associating regions along basilar membrane where outer hair cells were missing with CF ranges over which units could not be found 121. A formula relating percentage distance from base (d) to CF is d = 71 − 37 log (CF). At top of figure, basilar membrane is drawn to scale as if it were uncoiled and viewed from below. For different cats the absolute length may vary by a few millimeters. For cat from which these data were taken, length of basilar membrane from surface preparations was 24.5 mm, which is very close to average value of 24.4 mm for 12 adult cats. Average value obtained by Cabezudo 19, using reconstructions from sectioned cochleas, is 23.66 mm, which is closer to value of 23.5 mm given by Retzius 172. Below drawing of entire basilar membrane, three 0.25‐mm segments are shown enlarged. Locations of tops of hair cells are depicted. The 3 rows of outer hair cells (OHC) and 1 row of inner hair cells (IHC) are seen to be perched at 1 edge of the membrane, rather than near middle. Because of slant of hair cells (see Fig. 1), bottoms of inner hair cells in base of cochlea sit over bone. Tops of outer and inner hair cells are separated by top of inner pillar cell, width of which is systematically greater for more apical locations.



Figure 8.

Tuning curves of 10 units from 1 cat auditory nerve. Tuning curves were obtained by using an automated procedure 111. Numbers within plot identify units. Each curve in plot is an average of 4 tuning curves obtained for that unit, except for unit 14 (an average of 12 tuning curves), and unit 59 (an average of 3 tuning curves). When 2 curves intersect, the curve for unit with lower characteristic frequency is broken. Each tuning curve consists of 256 possible points, with 32 points distributed linearly within each octave. Intensity resolution is 2/3 dB/step. The criterion for positive response is that number of spikes occurring during 50‐ms interval when tone is on exceeds number of spikes for 50‐ms interval when tone is off. Tone bursts (10/s) have a rise time of 2.5 ms to reduce effects related to spread of spectral energy whenever tones are turned on or off. With these stimulus parameters, tuning curves for most units are very close to those taken manually with continuous tones or tone bursts, as described in ref. 113. All these units have high spontaneous discharge rates (>18 spikes/s).



Figure 9.

Tuning curves of 3 units with nearly the same characteristic frequency (CF) but widely different rates of spontaneous activity; taken from 4‐mo‐old cat born and raised in a soundproof chamber in an attempt to minimize possible effects of high‐level environmental noise. Pertinent data for unit 124: CF, 3.8 kHz; threshold, 28 dB sound pressure level (SPL); spontaneous activity, 0.27 spikes/s. Unit 179: CF, 3.9 kHz; threshold, 6 dB SPL; spontaneous activity, 5.60 spikes/s. Unit 250: CF, 3.8 kHz; threshold, 0.5 dB SPL; spontaneous activity, 52.40 spikes/s.



Figure 10.

Discharge rate (histograms) and response times (dot displays) of 6 auditory nerve fibers for tones swept in level. Histogram given for each unit shows spike rate (expressed as a percentage of 200 spikes/s), as level of tone is increased over 120‐dB range. Tone is on during interval indicated by bar at top of each histogram and off for first 10 and last 10 bins of each histogram. An individual histogram consists of 200 bins, each bin corresponding to an increment of approximately 3/4 dB. Except for the one on the top left (5 sweeps), each histogram represents 10 intensity sweeps, individual sweeps lasting 10 s. Intensity function changes little with sweep rate over a range of 1–1000 s for these stimulus parameters. Dot displays beneath histograms have as ordinates the time after a positive zero crossing for every other cycle of the tone. Abscissas are the same as for histograms. Each dot represents time of occurrence of a spike. Thus phase of responses as a function of stimulus level can be derived from dot displays. Zero dB is approximately 120 dB sound pressure level for these experiments. In each case characteristic frequency (CF) and frequency of stimulating tone (TF) are given at top and bottom of the figure.



Figure 11.

Instantaneous discharge rates for single auditory nerve fiber responding to continuous tones (CT). Discharge patterns over 2 cycles of a tone (bottom) are shown in 200‐bin PST histograms based on 15‐s samples of data. Each row contains data for same stimulus level; each column contains data for same tone frequency. Zero time corresponds to positive zero crossing of electrical input to 1‐in condenser earphone. Vertical axis of each histogram is instantaneous spike discharge rate with full‐scale value being either 500 spikes/s or 1,000 spikes/s. Histogram at top, labeled SPONT, is based on a sample of spontaneous activity processed as if there were a tone at characteristic frequency. For this figure the sound pressure level at −10 dB is approximately 106 dB in terms of 0.0002 dyn/cm2 for all frequencies.



Figure 12.

Phase of responses to tones as function of frequency for 2 units of low characteristic frequency. Each half of figure shows tuning curve and plot of response phase vs. frequency for 1 auditory nerve unit. Ordinate on left of each plot is associated with tuning curve; ordinate on right is related to phase curve. Abscissa is tone frequency on linear scale. For each curve there are 32 points linearly distributed within each octave. Lowest frequency used is 160 Hz. Phase curves plot phase of fundamental component of PST histograms where zero time corresponds to positive zero crossing of electric input to the 1‐in. condenser earphone.



Figure 13.

Response patterns of 3 auditory nerve fibers to tone bursts at characteristic frequencies. Wave form of electric input to condenser earphone is shown under each PST histogram. There is a 0.07‐ms travel time for acoustic signal to arrive at tympanic membrane. PST histograms on left show response patterns to entire tone burst; histograms on right show response pattern to tone burst onset on expanded time scale. Each histogram represents an average of >3,000 tone‐burst presentations. The 50‐ms tone bursts had rise‐fall times of 2.5 ms and were delivered at a rate of 10 bursts/s. At this stimulus repetition rate, the spontaneous activity does not recover to its full value before next tone burst arrives. Spontaneous discharge rates of the 3 units, from top to bottom, were 85, 95, and 62 spikes/s, respectively. Vertical axis in PST histograms is expressed most directly as spikes per bin but can be converted into instantaneous spike rate by using the formula: spike rate = number of spikes per bin, divided by the binwidth times the number of stimulus presentations. This procedure can yield instantaneous spike rates as high as thousands of spikes per second. These values may at first be disconcerting to some neurophysiologists, but they follow directly from the definition of instantaneous rate. Perfectly time‐locked responses would have arbitrarily high instantaneous rates.



Figure 14.

Effect of background tone on tuning curve. Isorate curve A (dotted line) was obtained by using stimulus paradigm A (single tone bursts swept in frequency). Isorate curve B (solid line) was obtained by using stimulus paradigm B (one tone burst fixed in frequency and a second swept in frequency). In both cases response rate was defined to be difference between spike rates during periods a and c (at left). Tone I was test tone that was swept in frequency. Parameters of fixed tone 2 are indicated by open circle in plots on right (7 kHz and 65 dB). Unit characteristic frequency was 5.4 kHz and spontaneous rate of discharge was 18 spikes/s. Arrow points to a peak of sensitivity at a frequency of 8.4 kHz.



Figure 15.

Response of auditory nerve unit to 2 simultaneously presented tone bursts. Left column shows 4 stimulus situations; right column plots rate of response under conditions described on left. Each box on left shows unit's tuning curve with dot showing frequency and level of fixed tone burst. Horizontal line with arrow pointing to left indicates frequency range and intensity level of tone bursts swept in frequency. Stimulus paradigms are shown in Fig. 14. Characteristic frequency (CF) of unit was 5.4 kHz at 14.5 dB sound pressure level. On right are frequency‐response curves with normalized driven rate defined as (spike rate ‐ spontaneous discharge rate)/(maximum spike rate ‐ spontaneous discharge rate). Spontaneous discharge rate of this unit was 18 spikes/s. Maximum spike rate is estimated by measuring spike rate for 80‐dB tone bursts at CF. Dashed lines across bottom 3 boxes on right indicate, in each instance, spike rate for fixed tone burst alone, based on 20 tone burst presentations, 10 before and 10 after swept tones were presented. Frequency‐response curves on right have frequency resolution that is one‐fourth that of tuning curves. Each point is based on 10 repetitions of a pair of tone bursts (or of single tone bursts for box at top. For top row there are no fixed tone bursts, so the frequency‐response curve is simply a plot of driven rate vs. frequency of tone burst. Second row shows frequency‐response curve for same swept tones but with fixed tone burst at CF presented simultaneously. Third row repeats experiment except that fixed tone bursts are at a frequency far removed from CF. For fixed tone bursts to generate responses, level of fixed tone bursts had to be increased above that of swept tones. Bottom row shows results for stimulus conditions similar to that for third row except that intensity level of swept tone bursts is increased to be almost equal with that of fixed tone bursts. (Some areas are stippled for easy reference.)



Figure 16.

Times of unit responses to clicks compared with potentials recorded near round window. Trace at top is 30‐s average of round window responses to condensation clicks (10 clicks/s, 88 dB sound pressure level) produced by delivering 100‐μs pulses to 1‐in. condenser earphone. Upward deflection indicates negativity at gross electrode referred to head holder. Cochlear microphonic potential, CM; first negative deflection representing neural activity, N1. Plot at bottom shows times at which the instantaneous discharge rates of units are >666 spikes/s as displayed in PST histograms of unit responses to clicks. Times of unit responses were all displaced by 0.2 ms in an attempt to compensate roughly for conduction time from point of spike initiation to recording micropipette. Data from 54 units.



Figure 17.

N0 calculations for 2 units recorded simultaneously with separate micropipettes in auditory nerve. A 0.3‐s sample of spontaneous spikes is shown for each unit, along with simultaneously recorded round window (RW) potential (top trace) recorded with gross silver ball electrode. N0 is an estimate of voltage contribution of a spike to potential recorded at gross electrode. Two N0 wave forms at bottom were obtained by cross‐correlating round window recording with times of spike discharges for 2 units. Zero time is time of half‐amplitude point on rising part of spike waveforms. Peak of N0 occurs before zero time because it takes time for spike to travel from point of spike initiation to recording electrode. For unit 11A (characteristic frequency = 0.53 kHz) 27,572 spikes were used to compute average, while only 6,090 spikes were used for unit 11B (characteristic frequency = 0.5 kHz).



Figure 18.

Comparison of synthesized and recorded compound action potential (CAP) for auditory nerve of I cat. Unit recordings were made with micropipette in internal auditory meatus; gross‐potential recordings were taken with wire loop on ipsilateral round window. Both were recorded simultaneously for 65‐dB sound pressure level rarefaction clicks presented at a rate of 10/s; recordings were also made in the absence of acoustic stimulation. Synthesized CAP was constructed as follows: 1) The total range of characteristic frequencies (CFs) between 0.2 and 40 kHz was divided into 128 CF groups of equal intervals on a log CF scale. Each CF group was further separated into 3 divisions based on spontaneous discharge rate: high (>18 spikes/s), medium (0.5–18 spikes/s), and low (<0.5 spikes/s). Data were collected for 181 units selected to cover as broad a range of groups and divisions as possible. Contributions of low‐spontaneous units are negligible, so these units were not represented in synthesizing CAPs. 2) PST histograms of responses to clicks were computed for 30‐s samples of data. When no unit data were available for a bin, an interpolation procedure was used based on neighboring bins. When data from more than 1 unit were available for a bin, they were averaged. A CF‐dependent latency shift (up to 0.18 ms) was incorporated, based on N0 data that show shortest (0.04 ms) latencies for units with CF around 3–6 kHz and longest (0.22 ms) latencies for units with high CF. Finally a weighting factor for unit density as a function of CF was introduced, based on Schuknecht's 197 data on primary neuron distribution and a total estimated 50,000 fibers 54. 3) A compound PST histogram was then calculated that gave time distribution of activity over the whole nerve. 4) Data obtained under no‐click condition were used in computing N0s (see Fig. 16) for 6 units from this cat. These N0s had a wave form that was close to that of an idealized N0 based on an average of 232 N0 calculations taken from many animals. Although wave form of idealized N0 was used in later calculations, amplitude of idealized N0 was made to equal mean amplitude of 6 N0s from this cat. The compound PST histogram was convolved with idealized N0 to give synthesized CAP (dotted trace). Upward deflection is considered to be negative at round window referred to head holder. The 30‐s samples of round window responses to clicks recorded simultaneously with unit recordings used in obtaining PST histograms were averaged and displayed as recorded CAP (solid line). Trace showing recorded CAP contains some cochlear microphonic components as well as later neural components.



Figure 19.

Effect of crossed divocochlear bundle (COCB) stimulation on auditory nerve responses. A: N1 click‐intensity functions with and without electric stimulation of COCB at midline on floor of fourth ventricle. Inset is PST histogram of discharge rate of auditory nerve unit for 20 s of exposure to continuous 10‐dB tone at characteristic frequency (CF) of 0.6 kHz, during which bursts of shocks (400/s) were delivered to the COCB. (Bar above histogram shows duration of burst of shocks.) Histogram represents an average over 20 bursts of shocks. B: same as A except that COCB is now cut laterally to facial genu on side where recordings are made. Inset is PST histogram for another unit (CF = 2 kHz). Except for frequency, stimulus parameters were same as for other unit.

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Article Title: Peripheral Neural Processing of Auditory Information
 

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Nelson Y. S. Kiang. Peripheral Neural Processing of Auditory Information. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 639-674. First published in print 1984. doi: 10.1002/cphy.cp010315