Comprehensive Physiology Wiley Online Library

The Olfactory Bulb: A Simple System in the Mammalian Brain

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Cell Types and Laminae
1.1 Input Fibers
1.2 Principal Neuron
1.3 Intrinsic Neurons
1.4 Periglomerular Cells
1.5 Granule Cells
1.6 Lamination
2 Organization of Olfactory Glomeruli
2.1 Olfactory Nerves
2.2 Synaptic Connections
2.3 Physiological Properties
2.4 Comparative Aspects of Glomerular Organization
3 Organization of External Plexiform Layer
3.1 Synaptic Connections
3.2 Mitral Cell Excitation and Inhibition
3.3 Analysis of Summed Extracellular Potentials
3.4 Reconstruction of Mitral Cell Potentials
3.5 Reconstruction of Granule Cell Potentials
3.6 Dendrodendritic Recurrent Inhibition
4 Organization of Granule Cells
5 Transmitter Substances
6 General Discussion
Figure 1. Figure 1.

A: olfactory structures of rabbit. B: main types of neuron in mammalian olfactory bulb. ON: olfactory nerves; PGb: periglomerular cell with biglomerular dendrites; PGm: periglomerular cell with monoglomerular dendrites; SAe: short‐axon cell with extraglomerular dendrites; M: mitral cell; M/Td: displaced mitral or deep tufted cell; Tm: middle tufted cell; Ts: superficial tufted cell; Gm: granule cell with cell body in mitral body layer; Gd: granule cell with cell body in deep layers; SAc: short‐axon cell of Cajal; SAg: short‐axon cell of Golgi; C: centrifugal fibers; AON: fibers from anterior olfactory nucleus; AC: fibers from anterior commissure; LOT: lateral olfactory tract. Histological layers are indicated at left. ONL: olfactory nerve layer; GL: glomerular layer; EPL: external plexiform layer; MBL: mitral body layer; IPL: internal plexiform layer; GRL: granule layer.

Adapted from Shepherd
Figure 2. Figure 2.

Photomicrograph of degenerated bundle of olfactory nerve fibers (thick arrow) that terminates in 2 olfactory glomeruli; degeneration was subsequent to a small lesion in the nasal cavity. Normal glomeruli (NG) and parts of the affected glomeruli (thin arrows) are without degeneration. Fink‐Heimer method. × 250.

From Land et al.
Figure 3. Figure 3.

Electron micrographs of olfactory glomerulus. 1: serial synapses from receptor cell axon (A) to mitral cell dendrite (M) to periglomerular cell dendrite (P). Balb/c mouse. × 44,000.2 and 3: reciprocal synapses between mitral and periglomerular cell dendrite. Sections are from a serial reconstruction. × 49,000.

From White
Figure 4. Figure 4.

Synaptic organization of glomerular layer. Note separation into intra‐ and interglomerular fields. Unshaded profiles indicate presumed excitatory synaptic actions; shaded profiles indicate presumed inhibitory actions. pg, periglomerular cell; on, olfactory nerve.

From Shepherd
Figure 5. Figure 5.

Unit responses in glomerular layer to paired volleys in olfactory nerve. A: single conditioning volley (shock artifact indicated by •) at just‐subthreshold strength has little effect on repetitive response to single test volley • (control for • to the right.). B: conditioning volley ○ at same strength as test volley • causes complete suppression of all but the initial test spike. Extracellular recordings; 10 sweeps superimposed in each record to show stability of responses.

From Shepherd
Figure 6. Figure 6.

Summary of responses of a glomerular layer unit to paired volleys at threshold. A: control responses to conditioning (unshaded) and test (shaded) volleys alone. B: responses to test volley when preceding conditioning volley did not elicit a spike response in this unit. C: responses to test volley when previous conditioning volley elicited a spike. Asterisks indicate occurrence of a second spike discharge in 3 trials. Stimulus interval: 10 ms.

From Shepherd
Figure 7. Figure 7.

Glomerular organization. ON: olfactory nerve; OT: olfactory terminal; MD: mitral dendrite; PGD: periglomerular cell dendrite; AFF: specific sensory afferent; AT: afferent terminal; PD: principal cell dendrite; IND: intrinsic cell dendrite; MF: mossy fiber; MT: mossy fiber terminal; GRD: granule cell dendrite; GoD: Golgi cell dendrite; G: granule cell; P: pyramidal cell; PG: periglomerular cell.

Figure 8. Figure 8.

Electron micrograph of reciprocal synapses between mitral cell dendrite (m) and granule cell dendrite (g). Note postsynaptic fuzz (f). × 71,000.

From Rall et al.
Figure 9. Figure 9.

Histogram of latencies and depths of 228 units recorded from olfactory bulb that were driven antidromically from the LOT. Recordings were of giant extracellular spikes. Filled bars: 20–73‐mV peak‐to‐peak amplitude; shaded bars: 5–20 mV; unshaded bars: 1–5 mV. Latencies in ms. Depths in terms of histological layers at left. ON‐Glom: olfactory nerve‐glomerulus; Supfl Plex: superficial plexiform; Gran: granule.

From Shepherd
Figure 10. Figure 10.

A: giant extracellular spike recorded from mitral cell; antidromic invasion from LOT. Superimposed sweeps show full spike at longer intervals, small spike (possibly in initial segment) at shorter intervals. Time in ms; voltage calibration, 50 mV upper sweep, 3 mV lower sweep. B: a, intracellular recording from mitral cell, showing long‐lasting hyperpolarization following LOT volley; b, extracellular summed potential, same gain; c, extracellular summed potential, higher gain. Numerals I, II, and III and vertical lines indicate time periods of field potential responses. Time in 2‐ms divisions; voltage calibration: a and b, 5 mV; c, 1 mV.

From Phillips et al. . From Shepherd
Figure 11. Figure 11.

Summed extracellular potentials recorded from olfactory bulb, evoked by single volley in LOT. Depths and histological layers shown at left. Note division of responses into successive time periods I, II, and III (cf. Fig. B). Polarity of recording pipette indicated by (+) and (−). Voltage calibration, 1 mV.

From Rall & Shepherd
Figure 12. Figure 12.

Comparison of summed extracellular potentials in different layers of active and inactive regions of olfactory bulb. Voltage calibration, 1 mV.

From Shepherd & Haberly
Figure 13. Figure 13.

Pathways for summed extracellular current flows caused by activation of limited granule cell population in olfactory bulb. Five elements representing granule cells are shown; shading indicates site of EPSP. Directions of extracellular current flows indicated by arrows; polarities of potentials when microelectrode is inserted in active and inactive regions are indicated by (+) and (−).

From Shepherd & Haberly
Figure 14. Figure 14.

Compartmental model of mitral cell is represented at left. Computed intra‐ and extracellular transients for simulated antidromic impulse invasion from the LOT are shown for soma , mid‐dendrites , and terminal dendrites . Time periods I and II are comparable to time periods in Figs. B, and .

From Rall & Shepherd
Figure 15. Figure 15.

Compartmental model of granule cell is represented at left. Computed intra‐ and extracellular transients for simulated synaptic depolarization of dendritic tree in EPL (•) are shown at right. Time course of depolarizing conductance change is indicated at bottom by bars. Time scale is time (t) over membrane time constant (τ).

From Rall & Shepherd
Figure 16. Figure 16.

Mechanism of dendrodendritic synapses in EPL during time periods I, II, and III following an LOT volley. ℰ: excitatory synapse; ��: inhibitory synapse; D: depolarization; H: hyperpolarization; AD: antidromic; OD: orthodromic.

From Rall & Shepherd
Figure 17. Figure 17.

Two types of pathway for recurrent inhibition. A: classic Renshaw pathway — excitation (E) of interneuron through axon collateral; inhibition (l) through axon of interneuron. B: dendrodendritic pathway — excitation of interneuronal dendrite through presynaptic dendrite; inhibition through reciprocal synapse and through spread of synaptic potential through interneuronal dendritic tree to other dendritic synaptic output sites. Site of impulse generation at axon hillock of mitral cell is indicated by shading.

From Shepherd
Figure 18. Figure 18.

Synaptic organization of granule cell. Extrinsic inputs are at right, intrinsic inputs at left. Presumed excitatory and inhibitory actions are indicated by unshaded and shaded profiles, respectively. Collats, collaterals.

From Shepherd
Figure 19. Figure 19.

Left: comparison between summed extracellular potentials in granule layer evoked by single and repetitive volleys in lateral olfactory tract (LOT) and anterior commissure (AC). Positivity is downward in these recordings. Right: intracellular recordings of mitral cell responses to conditioning train of 4 volleys in AC and test volley in LOT (dot).

From Dennis & Kerr . From Yamamoto et al.
Figure 20. Figure 20.

Evidence regarding possible transmitter substances at different synaptic sites in olfactory bulb. GABA: χ‐aminobutyric acid; DLH: DL‐homocysteate; DOPA: dihydroxyphenylalanine.

Figure 21. Figure 21.

Functional units in olfactory bulb. Dashed lines enclose morphological substrates for specific input‐output functions. ON, olfactory nerve; PG, periglomerular cell; M, mitral cell; GR, granule cell; AON, anterior olfactory nucleus.



Figure 1.

A: olfactory structures of rabbit. B: main types of neuron in mammalian olfactory bulb. ON: olfactory nerves; PGb: periglomerular cell with biglomerular dendrites; PGm: periglomerular cell with monoglomerular dendrites; SAe: short‐axon cell with extraglomerular dendrites; M: mitral cell; M/Td: displaced mitral or deep tufted cell; Tm: middle tufted cell; Ts: superficial tufted cell; Gm: granule cell with cell body in mitral body layer; Gd: granule cell with cell body in deep layers; SAc: short‐axon cell of Cajal; SAg: short‐axon cell of Golgi; C: centrifugal fibers; AON: fibers from anterior olfactory nucleus; AC: fibers from anterior commissure; LOT: lateral olfactory tract. Histological layers are indicated at left. ONL: olfactory nerve layer; GL: glomerular layer; EPL: external plexiform layer; MBL: mitral body layer; IPL: internal plexiform layer; GRL: granule layer.

Adapted from Shepherd


Figure 2.

Photomicrograph of degenerated bundle of olfactory nerve fibers (thick arrow) that terminates in 2 olfactory glomeruli; degeneration was subsequent to a small lesion in the nasal cavity. Normal glomeruli (NG) and parts of the affected glomeruli (thin arrows) are without degeneration. Fink‐Heimer method. × 250.

From Land et al.


Figure 3.

Electron micrographs of olfactory glomerulus. 1: serial synapses from receptor cell axon (A) to mitral cell dendrite (M) to periglomerular cell dendrite (P). Balb/c mouse. × 44,000.2 and 3: reciprocal synapses between mitral and periglomerular cell dendrite. Sections are from a serial reconstruction. × 49,000.

From White


Figure 4.

Synaptic organization of glomerular layer. Note separation into intra‐ and interglomerular fields. Unshaded profiles indicate presumed excitatory synaptic actions; shaded profiles indicate presumed inhibitory actions. pg, periglomerular cell; on, olfactory nerve.

From Shepherd


Figure 5.

Unit responses in glomerular layer to paired volleys in olfactory nerve. A: single conditioning volley (shock artifact indicated by •) at just‐subthreshold strength has little effect on repetitive response to single test volley • (control for • to the right.). B: conditioning volley ○ at same strength as test volley • causes complete suppression of all but the initial test spike. Extracellular recordings; 10 sweeps superimposed in each record to show stability of responses.

From Shepherd


Figure 6.

Summary of responses of a glomerular layer unit to paired volleys at threshold. A: control responses to conditioning (unshaded) and test (shaded) volleys alone. B: responses to test volley when preceding conditioning volley did not elicit a spike response in this unit. C: responses to test volley when previous conditioning volley elicited a spike. Asterisks indicate occurrence of a second spike discharge in 3 trials. Stimulus interval: 10 ms.

From Shepherd


Figure 7.

Glomerular organization. ON: olfactory nerve; OT: olfactory terminal; MD: mitral dendrite; PGD: periglomerular cell dendrite; AFF: specific sensory afferent; AT: afferent terminal; PD: principal cell dendrite; IND: intrinsic cell dendrite; MF: mossy fiber; MT: mossy fiber terminal; GRD: granule cell dendrite; GoD: Golgi cell dendrite; G: granule cell; P: pyramidal cell; PG: periglomerular cell.



Figure 8.

Electron micrograph of reciprocal synapses between mitral cell dendrite (m) and granule cell dendrite (g). Note postsynaptic fuzz (f). × 71,000.

From Rall et al.


Figure 9.

Histogram of latencies and depths of 228 units recorded from olfactory bulb that were driven antidromically from the LOT. Recordings were of giant extracellular spikes. Filled bars: 20–73‐mV peak‐to‐peak amplitude; shaded bars: 5–20 mV; unshaded bars: 1–5 mV. Latencies in ms. Depths in terms of histological layers at left. ON‐Glom: olfactory nerve‐glomerulus; Supfl Plex: superficial plexiform; Gran: granule.

From Shepherd


Figure 10.

A: giant extracellular spike recorded from mitral cell; antidromic invasion from LOT. Superimposed sweeps show full spike at longer intervals, small spike (possibly in initial segment) at shorter intervals. Time in ms; voltage calibration, 50 mV upper sweep, 3 mV lower sweep. B: a, intracellular recording from mitral cell, showing long‐lasting hyperpolarization following LOT volley; b, extracellular summed potential, same gain; c, extracellular summed potential, higher gain. Numerals I, II, and III and vertical lines indicate time periods of field potential responses. Time in 2‐ms divisions; voltage calibration: a and b, 5 mV; c, 1 mV.

From Phillips et al. . From Shepherd


Figure 11.

Summed extracellular potentials recorded from olfactory bulb, evoked by single volley in LOT. Depths and histological layers shown at left. Note division of responses into successive time periods I, II, and III (cf. Fig. B). Polarity of recording pipette indicated by (+) and (−). Voltage calibration, 1 mV.

From Rall & Shepherd


Figure 12.

Comparison of summed extracellular potentials in different layers of active and inactive regions of olfactory bulb. Voltage calibration, 1 mV.

From Shepherd & Haberly


Figure 13.

Pathways for summed extracellular current flows caused by activation of limited granule cell population in olfactory bulb. Five elements representing granule cells are shown; shading indicates site of EPSP. Directions of extracellular current flows indicated by arrows; polarities of potentials when microelectrode is inserted in active and inactive regions are indicated by (+) and (−).

From Shepherd & Haberly


Figure 14.

Compartmental model of mitral cell is represented at left. Computed intra‐ and extracellular transients for simulated antidromic impulse invasion from the LOT are shown for soma , mid‐dendrites , and terminal dendrites . Time periods I and II are comparable to time periods in Figs. B, and .

From Rall & Shepherd


Figure 15.

Compartmental model of granule cell is represented at left. Computed intra‐ and extracellular transients for simulated synaptic depolarization of dendritic tree in EPL (•) are shown at right. Time course of depolarizing conductance change is indicated at bottom by bars. Time scale is time (t) over membrane time constant (τ).

From Rall & Shepherd


Figure 16.

Mechanism of dendrodendritic synapses in EPL during time periods I, II, and III following an LOT volley. ℰ: excitatory synapse; ��: inhibitory synapse; D: depolarization; H: hyperpolarization; AD: antidromic; OD: orthodromic.

From Rall & Shepherd


Figure 17.

Two types of pathway for recurrent inhibition. A: classic Renshaw pathway — excitation (E) of interneuron through axon collateral; inhibition (l) through axon of interneuron. B: dendrodendritic pathway — excitation of interneuronal dendrite through presynaptic dendrite; inhibition through reciprocal synapse and through spread of synaptic potential through interneuronal dendritic tree to other dendritic synaptic output sites. Site of impulse generation at axon hillock of mitral cell is indicated by shading.

From Shepherd


Figure 18.

Synaptic organization of granule cell. Extrinsic inputs are at right, intrinsic inputs at left. Presumed excitatory and inhibitory actions are indicated by unshaded and shaded profiles, respectively. Collats, collaterals.

From Shepherd


Figure 19.

Left: comparison between summed extracellular potentials in granule layer evoked by single and repetitive volleys in lateral olfactory tract (LOT) and anterior commissure (AC). Positivity is downward in these recordings. Right: intracellular recordings of mitral cell responses to conditioning train of 4 volleys in AC and test volley in LOT (dot).

From Dennis & Kerr . From Yamamoto et al.


Figure 20.

Evidence regarding possible transmitter substances at different synaptic sites in olfactory bulb. GABA: χ‐aminobutyric acid; DLH: DL‐homocysteate; DOPA: dihydroxyphenylalanine.



Figure 21.

Functional units in olfactory bulb. Dashed lines enclose morphological substrates for specific input‐output functions. ON, olfactory nerve; PG, periglomerular cell; M, mitral cell; GR, granule cell; AON, anterior olfactory nucleus.

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Gordon M. Shepherd. The Olfactory Bulb: A Simple System in the Mammalian Brain. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 945-968. First published in print 1977. doi: 10.1002/cphy.cp010125