Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

The Olfactory Bulb: A Simple System in the Mammalian Brain

Gordon M. Shepherd

10.1002/cphy.cp010125

Source: Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons

Originally published: 1977

Published online: January 2011

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 128
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. 64
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 142
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 128
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 122
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 127
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. 108
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 122
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. 92. From Shepherd 126
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. 10B). Polarity of recording pipette indicated by (+) and (−). Voltage calibration, 1 mV.

From Rall & Shepherd 107
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 131
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 131
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. 10B, 11 and 12.

From Rall & Shepherd 107
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 107
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 107
Figure 17. Figure 17.

Two types of pathway for recurrent inhibition. A: classic Renshaw pathway 29 — excitation (E) of interneuron through axon collateral; inhibition (l) through axon of interneuron. B: dendrodendritic pathway 107,108 — 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 126
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 128
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 24. From Yamamoto et al. 150
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 128


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. 64


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 142


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 128


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 122


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 127


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. 108


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 122


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. 92. From Shepherd 126


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. 10B). Polarity of recording pipette indicated by (+) and (−). Voltage calibration, 1 mV.

From Rall & Shepherd 107


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 131


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 131


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. 10B, 11 and 12.

From Rall & Shepherd 107


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 107


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 107


Figure 17.

Two types of pathway for recurrent inhibition. A: classic Renshaw pathway 29 — excitation (E) of interneuron through axon collateral; inhibition (l) through axon of interneuron. B: dendrodendritic pathway 107,108 — 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 126


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 128


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 24. From Yamamoto et al. 150


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.

References
 1. Adey, W. R. Higher olfactory centres. In: Ciba Foundation Symposium on Taste and Smell in Vertebrates, edited by G. E. W. Wolstenholme and J. Knight. London: Churchill, 1970, p. 357–376.
 2. Adrian, E. D. Sensory messages and sensation: the response of the olfactory organ to different smells. Acta Physiol. Scand., 29: 5–14, 1953.
 3. Agduhr, E. Vergleich der Neuritenanzahl in den Wurzeln der Spinal nerven bie Kröte, Maus, Hund und Mensch. Z. Anat. Entwicklungsgeschichte, 102: 194–210, 1934.
 4. Akert, K., and U. Steiger. Über Glomeruli im Zentralnervensystem von Vertebraten und Invertebraten. Schweiz. Arch. Neurol. Neurochir. Psychiat., 100: 321–337, 1967.
 5. Allison, A. C. The morphology of the olfactory system in the vertebrates. Biol. Rev., 28: 195–244, 1953.
 6. Andres, K. H. Der Feinbau des Bulbus Olfactorius der Ratte unter besonderer Berücksichtigung der synaptischen Verbindungen. Z. Zellforsch. Mikroskop. Anat., 65: 530–561, 1965.
 7. Andres, K. H. Anatomy and ultrastructure of the olfactory bulb in fish, amphibia, reptiles, birds and mammals. In: Ciba Foundation Symposium on Taste and Smell in Vertebrates, edited by G. E. W. Wolstenholme, and J. Knight. London: Churchill, 1970, p. 177–194.
 8. Baylor, D. A., and J. G. Nicholls. After‐effects of nerve impulses on signalling in the central nervous system of the leech. J. Physiol. London, 203: 571–589, 1969.
 9. Best, J. B., and J. Noel. Complex synaptic configurations in Planarian brain. Science, 164: 1070–1071, 1969.
 10. Bishop, G. H. Natural history of the nerve impulse. Physiol. Rev., 36: 376–399, 1956.
 11. Bloom, F. E., E. Costa, and G. C. Salmoiraghi. Analysis of individual rabbit olfactory bulb neuron responses to the microelectrophoresis of acetylcholine, norepinephrine and serotonin synergists and antagonists. J. Pharmacol. Exptl. Therap., 146: 16–23, 1964.
 12. Bruesch, S. R., and L. B. Arey. The number of myelinated and unmyelinated fibers in the optic nerve of vertebrates. J. Comp. Neurol., 77: 631–665, 1942.
 13. Bullock, T. H. Neuron doctrine and electrophysiology. Science, 129: 997–1002, 1959.
 14. Ramon y Cajal, S. Histologie du Système Nerveux de l'Homme et des Vertébrés. Paris: Maloine, 1911.
 15. Callens, M. Peripheral and Central Regulatory Mechanisms of the Excitability in the Olfactory System. Brussels: Arscia Uitgaven, 1965.
 16. Calvin, W. H. Dendritic spikes revisited. Science, 166: 637–638, 1969.
 17. Carreras, M., D. Mancia, and M. Mancia. Centrifugal control of the olfactory bulb as revealed by induced DC potential changes. Brain Res., 6: 548–560, 1967.
 18. le Gros Clark, W. E. Inquiries into the anatomical basis of olfactory discrimination. Proc. Roy. Soc. London Ser. B, 146: 299–319, 1957.
 19. Colquhoun, D., R. Henderson, and J. M. Ritchie. The binding of labelled tetrodotoxin to non‐myelinated nerve fibres. J. Physiol. London, 227: 95–126, 1972.
 20. Coombs, J. S., D. R. Curtis, and J. C. Eccles. The interpretation of spike potentials of motoneurones. J. Physiol. London, 139: 198–231, 1957.
 21. Dahlstrom, A., K. Fuxe, L. Olson, and U. Ungerstedt. On the distribution and possible function of monoamine nerve terminals in the olfactory bulb of the rabbit. Life Sci., 4: 2071–2074, 1965.
 22. De Lorenzo, A. J. Electron microscopic observations of the olfactory mucosa and olfactory nerve. J. Biophys. Biochem. Cytol., 3: 839–848, 1957.
 23. De Lorenzo, A. J. D. The chemical senses: taste and olfaction. In: Medical Physiology, edited by V. B. Mountcastle. St. Louis: Mosby, 1968, p. 1626–1642.
 24. Dennis, B. J., and D. I. B. Kerr. An evoked potential study of centripetal and centrifugal connections of the olfactory bulb in the cat. Brain Res., 11: 373–396, 1968.
 25. Dowling, J. E. Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates. Proc. Roy. Soc. London Ser. B., 170: 205–228, 1968.
 26. Dowling, J. E. Organization of vertebrate retinas. Invest. Ophthalmol., 9: 655–680, 1970.
 27. Easton, D. M. Garfish olfactory nerve: easily accessible source of numerous long, homogeneous, nonmyelinated axons. Science, 172: 952–955, 1971.
 28. Eccles, J. C. The Physiology of Synapses. Berlin: Springer, 1964.
 29. Eccles, J. C., P. Fatt, and K. Koketsu. Cholinergic and inhibitory synapses in a pathway from motor‐axon collaterals to motoneurones. J. Physiol. London, 216: 524–562, 1955.
 30. Eccles, J. C., M. Ito, and J. Szentagothai. The Cerebellum As a Neuronal Machine. Berlin: Springer, 1967.
 31. Famiglietti, E. V., Jr., and A. Peters. The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J. Comp. Neurol., 144: 285–334, 1972.
 32. Felix, D., and H. MacLennan. The effect of bicuculline on the inhibition of mitral cells of the olfactory bulb. Brain Res., 25: 661–664, 1971.
 33. Freeman, W. J. Spatial divergence and temporal dispersion in primary olfactory nerve of cat. J. Neurophysiol., 35: 733–744, 1972.
 34. Freeman, W. J. Measurement of open‐loop responses to electrical stimulation in olfactory bulb of cat. J. Neurophysiol., 35: 745–761, 1972.
 35. Freeman, W. J. Measurement of oscillatory responses to electrical stimulation in olfactory bulb of cat. J. Neurophysiol., 35: 745–761, 1972.
 36. Freeman, W. J. Depth recording of average evoked potential of olfactory bulb. J. Neurophysiol., 35: 780–796, 1973.
 37. Freygang, W. H., and K. Frank. Extracellular potentials from single spinal motoneurons. J. Gen. Physiol., 42: 749–760, 1959.
 38. Fuortes, M. G. F., K. Frank, and M. C. Becker. Steps in the production of motoneuron spikes. J. Gen. Physiol., 40: 749–760, 1957.
 39. Gasser, H. S. Olfactory nerve fibers. J. Gen. Physiol., 39: 473–496, 1956.
 40. Getchell, J. V., and G. M. Shepherd. Short‐axon cells in the olfactory bulb: dendrodendritic synaptic interactions. J. Physiol. London, 251: 523–548, 1975.
 41. Granit, R. Receptors and Sensory Perception. New Haven: Yale Univ. Press, 1955.
 42. Granit, R., and C. G. Phillips. Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J. Physiol. London, 133: 520–547, 1956.
 43. Gray, E. G. Axo‐somatic and axo‐dendritic synapses of the cerebral cortex: an electron‐microscope study. J. Anat., 93: 420–433, 1959.
 44. Gray, E. G. The fine structure of the vertical lobe of Octopus brain. Phil. Trans. Roy. Soc. London Ser. B, 281: 379–394, 1970.
 45. Green, J. D., M. Mancia, and R. von Baumgarten. Recurrent inhibition in the olfactory bulb. I. Effects of antidromic stimulation of the lateral olfactory tract. J. Neurophysiol., 25: 467–488, 1962.
 46. Greengaard, P., J. F. Kuo, and E. Miyamoto. Studies on the mechanism of action of cyclic AMP in nervous and other tissues. In: Advances in Enzyme Regulations, edited by G. Weber. Oxford: Pergamon, 1971, p. 113–125.
 47. Harding, B. N. Dendro‐dendritic synapses, including reciprocal synapses, in the ventrolateral nucleus of the monkey thalamus. Brain Res., 34: 181–185, 1971.
 48. Harding, B. N. An ultrastructural study of the centre median and ventrolateral thalamic nuclei of the monkey. Brain Res., 54: 335–340, 1973.
 49. Hellerstein, D. Cable theory and gross potential analysis. Science, 166: 638–639, 1969.
 50. Hess, A., and P. Zapata. Innervation of the cat carotid body: normal and experimental studies. Federation Proc., 31: 1365–1382, 1972.
 51. Hinds, J. W. Ultrastructure of an anaxonic neuron: the internal granule cell of the olfactory bulb. Anat. Record 163: 199, 1969.
 52. Hinds, J. W. Reciprocal and serial dendrodendritic synapses in the glomerular layer of the rat olfactory bulb. Brain Res., 17: 530–534, 1970.
 53. Hirata, Y. Some observations on the fine structure of the synapses in the olfactory bulb of the mouse, with particular reference to the atypical synaptic configuration. Arch. Histol. Japan., 24: 293–302, 1964.
 54. Hopsu, V. K., and A. U. Arstila. An apparent somatosomatic synaptic structure in the pineal gland of the rat. Exptl. Cell Res., 37: 484–487, 1965.
 55. Hosoya, Y. Electron microscopic observations of the granule cells (Calleja's island) in the olfactory tubercle of rats. Brain Res., 54: 330–334, 1973.
 56. Jansen, J. K. S., and J. G. Nicholls. Conductance changes, an electrogenic pump and the hyperpolarization of leech neurones following impulses. J. Physiol. London, 229: 635–655, 1973.
 57. Jones, E. G., and T. P. S. Powell. Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc. Roy. Soc. London Ser. B, 172: 153–171, 1969.
 58. Kandel, E. R., and W. A. Spencer. Electrophysiology of hippocampal neurons. II. After‐potentials and repetitive firing. J. Neurophysiol., 24: 243–259, 1961.
 59. Katz, B., and R. Miledi. A study of synaptic transmission in the absence of nerve impulses. J. Physiol. London, 192: 407–436, 1967.
 60. Katz, B., and R. Miledi. The release of acetylcholine from nerve endings by graded electric pulses. Proc. Roy. Soc. London Ser. B, 167: 23–38, 1967.
 61. Kerr, D. I. B. Properties of the olfactory efferent system. Australian J. Exptl. Biol. Med. Sci., 38: 29–36, 1960.
 62. Kerr, D. I. B., and K. E. Hagbarth. An investigation of olfactory centrifugal fiber system. J. Neurophysiol., 18: 362–374, 1955.
 63. Land, L. J. Localized projection of olfactory nerves to rabbit olfactory bulb. Brain Res., 63: 153–166, 1973.
 64. Land, L. J., R. P. Eager, and G. M. Shepherd. Olfactory nerve projections to the olfactory bulb in rabbit: demonstration by means of a simple ammoniacal silver degeneration method. Brain Res., 23: 250–254, 1970.
 65. Land, L. J., and G. M. Shepherd. Autoradiographic analysis of olfactory receptor projections in the rabbit. Brain Res., 70: 506–510, 1974.
 66. LeVay, S. Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. J. Comp. Neurol., 150: 53–86, 1973.
 67. Leveteau, J., and P. MacLeod. Olfactory discrimination in the rabbit olfactory glomerulus. Science, 153: 175–176, 1966.
 68. Lichtensteiger, W. Uptake of norepinephrine in periglomerular cells of the olfactory bulb of the mouse. Nature, 210: 955–956, 1966.
 69. Lieberman, A. R. Neurons with presynaptic perikarya and presynaptic dendrites in the rat geniculate nucleus. Brain Res., 59: 35–59, 1973.
 70. Llinas, R., and C. Nicholson. Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J. Neurophysiol., 34: 532–551, 1971.
 71. Lohman, A. H. M., and J. J. Lammers. On the structure and fibre connections of the olfactory centres in mammals. Progr. Brain Res., 23: 65–82, 1967.
 72. Lorente de Nó, R. La corteza cerebral del ration. Trabajos Lab. Invest. Biol. Madrid, 20: 41–78, 1922.
 73. Lund, R. D. Synaptic patterns of the superficial layers of the superior colliculus of the rat. J. Comp. Neurol., 135: 179–208, 1969.
 74. MacLean, P. D., B. S. Rosner, and F. Robinson. Pyriform responses to electrical stimulation of olfactory fila, bulb and tract. Am. J. Physiol., 189: 395–400, 1957.
 75. MacLennan, H. The pharmacology of inhibition of mitral cells in the olfactory bulb. Brain Res., 29: 177–184, 1971.
 76. Mancia, M., J. D. Green, and R. von Baumgarten. Reticular control of single neurons in the olfactory bulb. Arch. Ital. Biol., 100: 463–475, 1962.
 77. Matthews, M. R., and G. Raisman. The ultrastructure and somatic efferent synapses of small granule‐containing cells in the superior cervical ganglion. J. Anat. London, 105: 255–282, 1969.
 78. McDonald, D. M., and R. A. Mitchell. A quantitative analysis of synaptic connections in the rat carotid body. In: The Peripheral Arterial Chemoreceptors, edited by M. J. Purves. Cambridge: Cambridge Univ. Press, 1974.
 79. Morest, D. K. Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z. Anat. Entwicklungsgeschichte, 133: 216–246, 1971.
 80. Nicholson, C., and R. Llinas. Field potentials in the alligator cerebellum and theory of their relationship to Purkinje cell spikes. J. Neurophysiol., 34: 509–531, 1971.
 81. Nicoll, R. A. Inhibitory mechanisms in the rabbit olfactory bulb: dendrodendritic mechanisms. Brain Res., 14: 157–172, 1969.
 82. Nicoll, R. A. Recurrent excitatory pathways of anterior commissure and mitral cell axons in the olfactory bulb. Brain Res., 19: 491–493, 1970.
 83. Nicoll, R. A. Identification of tufted cells in the olfactory bulb. Nature, 227: 623–625, 1970.
 84. Nicoll, R. A. Recurrent excitation of secondary olfactory neurons: a possible mechanism for signal amplification. Science, 171: 824–825, 1971.
 85. Nicoll, R. A. Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res., 35: 137–149, 1971.
 86. Nicoll, R. A. The olfactory nerves and their excitatory action in the olfactory bulb. Exptl. Brain Res., 14: 185–197, 1972.
 87. Ochi, J. Olfactory bulb response to antidromic olfactory tract stimulation in the rabbit. Japan J. Physiol., 13: 113–128, 1963.
 88. Pasik, P., T. Pasik, J. Hamori, and J. Szentagothai. Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Exptl. Brain Res., 17: 18–34, 1973.
 89. Peters, A., and S. L. Palay. The morphology of laminae A and A1 of the dorsal nucleus of the lateral geniculate body of the cat. J. Anat., 100: 451–486, 1966.
 90. Peute, J. Somato‐dendritic synapses in the paraventricular organ of two anuran species. Z. Zellforsch. Mikroskop. Anat., 112: 31–41, 1971.
 91. Phillips, C. G. Actions of antidromic pyramidal volleys on single Betz cells in the cat. Quart. J. Exptl. Physiol., 44: 1–25, 1959.
 92. Phillips, C. G., T. P. S. Powell, and G. M. Shepherd. Responses of mitral cells to stimulation of the lateral olfactory tract in the rabbit. J. Physiol. London, 168: 65–88, 1963.
 93. Pinching, A. J. Myelinated dendritic segments in the monkey olfactory bulb. Brain Res., 29: 133–138, 1971.
 94. Pinching, A. J., and T. P. A. Powell. The neuron types of the glomerular layer of the olfactory bulb. J. Cell Sci., 9: 305–345, 1971.
 95. Pinching, A. J., and T. P. S. Powell. The neuropil of the glomeruli of the olfactory bulb. J. Cell Sci., 9: 347–377, 1971.
 96. Pinching, A. J., and T. P. S. Powell. The neuropil of the periglomerular region of the olfactory bulb. J. Cell Sci., 9: 379–409, 1971.
 97. Price, J. L., and T. P. S. Powell. The morphology of the granule cells of the olfactory bulb. J. Cell Sci., 7: 91–123, 1970.
 98. Price, J. L., and T. P. S. Powell. The synaptology of the granule cells of the olfactory bulb. J. Cell Sci., 7: 125–155, 1970.
 99. Price, J. L., and T. P. S. Powell. The mitral and short axon cells of the olfactory bulb. J. Cell Sci., 7: 631–651, 1970.
 100. Price, J. L., and T. P. S. Powell. An experimental study of the site of origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J. Anat., 107: 215–237, 1970.
 101. Rakić, P., and R. L. Sidman. Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice. J. Comp. Neurol., 152: 133–162, 1973.
 102. Rall, W. Branching dendritic trees and motoneuron membrane resistivity. Exptl. Neurol., 1: 491–527, 1959.
 103. Rall, W. Theoretical significance of dendritic trees for neuronal input‐output relations. In: Neural Theory and Modeling, edited by R. F. Reiss. Stanford: Stanford Univ. Press, 1964, p. 73–97.
 104. Rall, W. Distinguishing theoretical synaptic potentials computed for different soma‐dendritic distributions of synaptic input. J. Neurophysiol., 30: 1138–1168, 1967.
 105. Rall, W. Dendritic neuron theory and dendrodendritic synapses in a simple cortical system. In: The Neurosciences: Second Study Program, edited by F. O. Schmitt. New York: Rockefeller, 1970, p. 552–565.
 106. Rall, W. Cable properties of dendrites and effects of synaptic location. In: Excitatory Synaptic Mechanisms, edited by P. Andersen, and J. K. S. Jansen. Oslo: Universitetsforlag, 1970, p. 175–187.
 107. Rall, W., and G. M. Shepherd. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol., 31: 884–915, 1968.
 108. Rall, W., G. M. Shepherd, T. S. Reese, and M. W. Brightman. Dendro‐dendritic synaptic pathway for inhibition in the olfactory bulb. Exptl. Neurol., 14: 44–56, 1966.
 109. Ralston, H. J. III. The fine structure of neurons in the dorsal horn of the cat spinal cord. J. Comp. Neurol., 132: 275–302, 1968.
 110. Ralston, H. J. III. Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature, 230: 585–587, 1971.
 111. Ralston, H. J. III. The synaptic organization in the dorsal horn of the spinal cord and in the ventrobasal thalamus of the cat. In: Oral‐Facial Sensory and Motor Mechanisms, edited by R. Dubner, and Y. Kawamura. New York: Appleton, 1971, p. 229–250.
 112. Ralston, H. J. III, and M. M. Herman. The fine structure of neurons and synapses in the ventrobasal thalamus of the cat. Brain Res., 14: 77–98, 1969.
 113. Ramon‐Moliner, E. The morphology of dendrites. In: Structure and Function of Nervous Tissue, edited by G. H. Bourne. New York: Academic, 1968, vol. 1, p. 205–267.
 114. Reese, T. S., and M. W. Brightman. Electron microscopic studies on the rat olfactory bulb. Anat. Record 151: 492, 1965.
 115. Reese, T. S., and M. W. Brightman. Olfactory surface and central olfactory connections in some vertebrates. In: Ciba Foundation Symposium on Taste and Smell in Vertebrates, edited by G. E. W. Wolstenholme, and J. Knight. London: Churchill, 1970, p. 115–149.
 116. Reese, T. S., and G. M. Shepherd. Dendro‐dendritic synapses in the central nervous system. In: Structure and Function of Synapses, edited by G. D. Pappas, and D. P. Purpura. New York: Raven, 1972, p. 121–136.
 117. Ritchie, J. M. Electrogenic ion pumping in nervous tissue. Current Topics Bioenergeties, 4: 327–356, 1971.
 118. Salmoiraghi, G. C., F. E. Bloom, and E. Costa. Adrenergic mechanisms in rabbit olfactory bulb. Am. J. Physiol., 207: 1417–1424, 1964.
 119. Schiebel, M. E., T. L. Davies, and A. B. Schiebel. An unusual axonless cell in the thalamus of the adult cat. Exptl. Neurol., 36: 512–518, 1972.
 120. Sétáló, G., and G. Székely. The presence of membrane specializations indicative of somato‐dendritic synaptic junctions in the optic tectum of the frog. Exptl. Brain Res., 4: 237–242, 1967.
 121. Shanthaveerappa, T. R., and G. H. Bourne. Histochemical studies on the olfactory glomeruli of squirrel monkey. Histochemie, 5: 125–129, 1965.
 122. Shepherd, G. M. Transmission in the Olfactory Pathway. (Ph.D. thesis). Oxford: Oxford Univ. Press, 1962.
 123. Shepherd, G. M. Responses of mitral cells to olfactory nerve volleys in the rabbit. J. Physiol. London, 168: 89–100, 1963.
 124. Shepherd, G. M. Neuronal systems controlling mitral cell excitability. J. Physiol. London, 168: 101–117, 1963.
 125. Shepherd, G. M. Dendrodendritic synaptic interactions in olfactory bulb. J. Physiol. London, 204: 132–133 P, 1969.
 126. Shepherd, G. M. The olfactory bulb as a simple cortical system: experimental analysis and functional implications. In: The Neurosciences: Second Study Program, edited by F. O. Schmitt. New York: Rockefeller, 1970, p. 539–552.
 127. Shepherd, G. M. Physiological evidence for dendrodendritic synaptic interactions in the rabbit's olfactory glomerulus. Brain Res., 32: 212–217, 1971.
 128. Shepherd, G. M. Synaptic organization of the mammalian olfactory bulb. Physiol. Rev., 52: 864–917, 1972.
 129. Shepherd, G. M. The neuron doctrine: a revision of functional concepts. Yale J. Biol. Med., 45: 584–599, 1972.
 130. Shepherd, G. M. The Synaptic Organization of the Brain. New York: Oxford, 1974.
 131. Shepherd, G. M., and L. B. Haberly. Partial activation of olfactory bulb: analysis of field potentials and topographic relation between bulb and lateral olfactory tract. J. Neurophysiol., 33: 643–653, 1970.
 132. Sloper, J. J. Dendro‐dendritic synapses in the primate motor cortex. Brain Res., 34: 186–192, 1972.
 133. Stell, W. K. The morphological organization of the vertebrate retina. In: Handbook of Sensory Physiology. Physiology of Photoreceptor Organs, edited by M. G. F. Fuortes. Berlin: Springer, 1972, vol. VII/1B, p. 111–214.
 134. Sterling, P. Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Res. Suppl., 3: 309–328, 1971.
 135. Szentagothai, J. Glomerular synapses, complex synaptic arrangements, and their operational significance. In: The Neurosciences: Second Study Program, edited by F. O. Schmitt. New York: Rockefeller, 1970, p. 427–443.
 136. Uchizono, K. Synaptic organization of the Purkinje cells in the cerebellum of the cat. Explt. Brain Res., 4: 97–113, 1967.
 137. Walsh, R. R. Olfactory bulb potentials evoked by electrical stimulation of the contralateral bulb. Am. J. Physiol., 196: 327–329, 1959.
 138. Weiss, P., and Y. Holland. Neuronal dynamics and axonal flow. II. The olfactory nerve as model test object. Proc. Natl. Acad. Sci. US, 57: 258–264, 1965.
 139. Westecker, M. E. The time course of facilitation and inhibition in the olfactory bulb, investigated with double pulse stimulation of the lateral olfactory tract. Brain Res., 16: 527–529, 1969.
 140. Westecker, M. E. Alternation characteristics of the evoked potential in the olfactory bulb in response to repetitive stimulation of the lateral olfactory tract. Brain Res., 17: 142–144, 1970.
 141. Westecker, M. E. Excitatory and inhibitory interactions in the olfactory bulb involving dendrodendritic synapses between mitral and granular cells. Pfluegers Arch. European J. Physiol., 317: 173–186, 1970.
 142. White, E. L. Synaptic organization in the olfactory glomerulus of the mouse. Brain Res., 37: 69–80, 1972.
 143. White, E. L. Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation. Brain Res., 60: 299–313, 1973.
 144. Whitfield, I. C. The Auditory Pathway. London: Arnold, 1967.
 145. Willey, T. J. The ultrastructure of the cat olfactory bulb. Comp. Neurol., 152: 211–232, 1973.
 146. Williams, T. H., and S. L. Palay. Ultrastructure of the small neurons in the superior cervical ganglion. Brain Res., 15: 17–34, 1969.
 147. Wong, M. T. T. Somato‐dendritic and dendro‐dendritic synapses in the squirrel monkey lateral geniculate nucleus. Brain Res., 20: 135–139, 1970.
 148. Woolsey, T. A., and H. Van Der Loos. The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res., 17: 205–242, 1970.
 149. Yamamoto, C., and K. Iwama. Intracellular potential recording from olfactory bulb neurones of the rabbit. Japan J. Physiol., 38: 63–67, 1962.
 150. Yamamoto, C., T. Yamamoto, and K. Iwama. The inhibitory system in the olfactory bulb studied by intracellular recording. J. Neurophysiol., 26: 403–415, 1963.
 151. Young, J. Z. The organization of a cephalopod ganglion. Phil. Trans. Roy. Soc. London Ser. B, 263: 409–429, 1972.
 152. Zucker, R. S. Field potentials generated by dendritic spikes and synaptic potentials. Science, 165: 409–413, 1969.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: The Olfactory Bulb: A Simple System in the Mammalian Brain
 

How to Cite

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