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The olfactory glomerulus: A cortical module with specific functions

  • Published:
Journal of Neurocytology

Abstract

The axons of many olfactory receptor cells converge on an individual glomerulus in the olfactory bulb, where they make contacts with the distal dendrites of mitral and tufted cells. Each glomerulus is targeted by olfactory receptor neurons expressing a single type of olfactory receptor protein. The glomerulus provides a unique model in which the function of a cortical module can be unambiguously established. Here we review the increasing evidence that a key functional operation of the glomerulus is to act as a signal-to-noise enhancing device in the processing of sensory input and that this function is critical across vertebrate and invertebrate species for the ability to detect specific odor stimuli within “noisy” odor environments and to carry out discriminations between odor molecules that are structurally closely related.

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References

  • ADRIAN, E. D. (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalography and Clinical Neurophysiology 2, 377–388.

    Article  PubMed  CAS  Google Scholar 

  • ALLISON, A. C. (1952) The morphology of the olfactory system in the vertebrates. Biological Reviews 28, 195–244.

    Google Scholar 

  • ARONIADOU-ANDERJASKA, V., ZHOU, F. M., PRIEST, C. A., ENNIS, M. & SHIPLEY, M. T. (2000) Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. Journal of Neurophysiology 84, 1194–1203.

    PubMed  CAS  Google Scholar 

  • AUNGST, L. L., HEYWARD, P. M., PUCHE, A. C., KARNUP, S. V., HAYAR, A., SZABO, G. & SHIPLEY, M. T. (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426, 623–629.

    Article  PubMed  CAS  Google Scholar 

  • BERKOWICZ, D. A., TROMBLEY, P. Q. & SHEPHERD, G. M. (1994) Evidence for glutamate as the olfactory receptor cell neurotransmitter. Journal of Neurophysiology 71, 2557–2561.

    PubMed  CAS  Google Scholar 

  • BOECKH, J., BOECKH, V. & KUHN, A. (1977) Further data on the topography and physiology of central olfactory neurons in insects. In: Olfaction and Taste VI (edited by Le Magnen, J. & Mac Leod, P.), pp.315–321. London: IRL.

    Google Scholar 

  • CAJAL, S. & RAMON, Y. (1911) Histologie du Systéme Nerveux de l’Homme et des Vertébrés. Paris: Maloine.

    Google Scholar 

  • CAPADAY, C. & STEIN, R. B. (1987) A method for simulating the reflex output of a motoneuron pool. Journal of Neuroscience Methods 21, 91–104.

    Article  PubMed  CAS  Google Scholar 

  • CARLSON, G. C., SHIPLEY, M. T. & KELLER, A. (2000) Long-lasting depolarizations in mitral cells of the rat olfactory bulb. Journal of Neuroscience 20, 2011–2021.

    PubMed  CAS  Google Scholar 

  • CHAMBILLE, I., MASSON, C. & ROSPARS, J. P. (1980) The deutocerebrum of the cockroach Blaberus craniifer Burm. Spatial organization of the sensory glomeruli. Journal of Neurobiology 11, 135–157.

    Article  PubMed  CAS  Google Scholar 

  • CHEN, W. R., MIDTGAARD, J. & SHEPHERD, G. M. (1997) Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. Science 278, 463–467.

    Article  PubMed  CAS  Google Scholar 

  • CHRISTIE, J. M., BARK, C., HORMUZDI, S. G., HELBIG, I., MONYER, H. & WESTBROOK, G. L. (2005) Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46, 761–772.

    Article  PubMed  CAS  Google Scholar 

  • ENNIS, M., ZIMMER, L. A. & SHIPLEY, M. T. (1996) Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. NeuroReport 7, 989–992.

    Article  PubMed  CAS  Google Scholar 

  • ENNIS, M., ZHOU, F. M., CIOMBOR, K. J., ARONIADOU-ANDERJASKA, V., HAYAR, A., BORRELLI, E., ZIMMER, L. A., MARGOLIS, F. L. & SHIPLEY, M. T. (2001) Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. Journal of Neurophysiology 86, 2986–2997.

    PubMed  CAS  Google Scholar 

  • GETCHELL, T. V. & SHEPHERD, G. M. (1975a) Short-axon cells in the olfactory bulb: Dendrodendritic synaptic interactions. Journal of Physiology (London) 251, 523–548.

    CAS  Google Scholar 

  • GETCHELL, T. V. & SHEPHERD, G. M. (1975b) Synaptic actions on mitral and tufted cells elicited by olfactory nerve volleys in the rabbit. Journal of Physiology (London) 251, 497–522.

    CAS  Google Scholar 

  • GOLDMAN, P. S. & NAUTA, W. J. (1977) An intricately patterned prefronto-caudate projection in the rhesus monkey. The Journal of Comparative Neurology 72, 369–386.

    Article  PubMed  CAS  Google Scholar 

  • GOLDMAN-RAKIC, P. S. (1982) Cytoarchitectonic hete-rogeneity of the primate neostriatum—Subdivision into island and matrix cellular compartments. The Journal of Comparative Neurology 205, 398–413.

    Article  PubMed  CAS  Google Scholar 

  • HANSTRÖM, B. (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Berlin: Springer.

    Google Scholar 

  • HILDEBRAND, J. G. & SHEPHERD, G. M. (1997) Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annual Review of Neuroscience 20, 595–631.

    Article  PubMed  CAS  Google Scholar 

  • HOPPE, R., BREER, H. & STROTMANN, J. (2003) Organization and evolutionary relatedness of OR37 olfactory receptor genes in mouse and human. Genomics 82, 355–364.

    Article  PubMed  CAS  Google Scholar 

  • HORTON, J. C. & ADAMS, D. L. (2005) The cortical column: A structure without a function. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 837–862.

    Article  Google Scholar 

  • HUBEL, D. H. & WIESEL, T. N. (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. Journal of Physiology (London) 160, 106–154.

    CAS  Google Scholar 

  • IGARASHI, K. M. & MORI, K. (2005) Spatial representation of hydrocarbon odorants in the ventrolateral zones of the rat olfactory bulb. Journal of Neurophysiology 93, 1007–1019.

    Article  PubMed  CAS  Google Scholar 

  • KOSAKA, K. & KOSAKA, T. (2005) Synaptic organization of the glomerulus in the main olfactory bulb: Compartments of the glomerulus and heterogeneity of the periglomerular cells. Anatomical Science International 80, 80–90.

    Article  PubMed  Google Scholar 

  • KOSAKA, T., DEANS, M. R., PAUL, D. L. & KOSAKA, K. (2005) Neuronal gap junctions in the mouse main olfactory bulb: Morphological analyses on transgenic mice. Neuroscience 134,757–769.

    Article  PubMed  CAS  Google Scholar 

  • Le GROS CLARK, W. E. (1957) Inquiries into the anatomical basis of olfactory discrimination. Proceedings of the Royal Society B (London) 146, 299–319.

    Google Scholar 

  • LEISE, E. M. (1990) Modular construction of nervous systems: A basic principle of design for invertebrates and vertebrates. Brain Research Brain Research Reviews 15, 1–23.

    Article  PubMed  CAS  Google Scholar 

  • LEVETEAU, J. & MACLEOD, P. (1966) Olfactory discrimination in the rabbit olfactory glomerulus. Science 175, 170–178.

    Google Scholar 

  • MASSON, C. & MUSTAPARTA, H. (1990) Chemical information processing in the olfactory system of insects. Physiological Reviews 70, 199–245.

    CAS  Google Scholar 

  • MATSUMOTO, S. G. & HILDEBRAND, J. G. (1981) Olfactory mechanisms in the moth Manduca sexta: Response characteristics and morphology of central neurons in the antennal lobes. Proceedings of the Royal Society B (London) 213, 249–277.

    Article  CAS  Google Scholar 

  • MEISAMI, E. (1991) Chemoreception. In: Neural and Integrative Animal Physiology Comparative Animal Physiology, 4th Edition (edited by Prosser, C. L.), pp.335–434. New York: Wiley-Liss.

    Google Scholar 

  • MIGLIORE, M., HINES, M. L. & SHEPHERD, G. M. (2005) The role of distal dendritic gap junctions in synchronization of mitral cell axonal output. Journal of Computational Neuroscience 18, 151–161.

    Article  PubMed  CAS  Google Scholar 

  • MOMBAERTS, P. (2004) Genes and ligand for odorant, vomeronasal and taste receptors. Nature Reviews Neuroscience 5, 263–278.

    Article  PubMed  CAS  Google Scholar 

  • MOUNTCASTLE, V. B. (1957) Modality and topographic properties of single neurons in cat’s somatic sensory cortex. Journal of Neurophysiology 20,408–434.

    PubMed  CAS  Google Scholar 

  • NOWYCKY, M. C., MORI, K. & SHEPHERD, G. M. (1981) Blockade of synaptic inhibition reveals long-lasting synaptic excitation in isolated turtle olfactory bulb. Journal of Neurophysiology 46, 649–658.

    PubMed  CAS  Google Scholar 

  • PINCHING, A. J. & POWELL, T. P. S. (1971) The neuropil of the glomeruli of the olfactory bulb. Journal of Cell Science 9, 347–377.

    PubMed  CAS  Google Scholar 

  • POWELL, T. P. S. & MOUNTCASTLE, V. B. (1959) Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. Bulletin of The Johns Hopkins Hospital 105, 201–232.

    PubMed  Google Scholar 

  • REESE, T. S. & BRIGHTMAN, M. W. (1970) Olfactory surface and central olfactory connections in some vertebrates. In: Taste and Smell in Vertebrates (edited by Wolstenholme, G. E. W. & Knight, J.), pp 115–149. London: J & A Churchill.

    Google Scholar 

  • RESSLER, K. J., SULLIVAN, S. L. & BUCK, L. B. (1994) Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79,1245–1255.

    Article  PubMed  CAS  Google Scholar 

  • RIECKE, F., WARLAND, D., DE RUYTER VAN STEVENINCK, R. & BIALEK, W. (1997) Spikes. Exploring the Neural Code. Cambridge, MA: A Bradford Book. MIT Press.

    Google Scholar 

  • ROSPARS, J. P. & CHAMBILLE, I. (1989) Identified glomeruli in the antennal lobes of insects: Invariance, sexual variation and postembryonic development. In: Neurobiology of Sensory Systems (edited by Singh, R. N. & Strausfeld, N. J.), pp. 355–375. New York: Plenum.

    Google Scholar 

  • SCHOPPA, N. E. & WESTBROOK, G. L. (2001) Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31, 639–651.

    Article  PubMed  CAS  Google Scholar 

  • SHARP, F. R., KAUER. J. S. & SHEPHERD, G. M. (1975) Local sites of activity-related glucose metabolism in rat olfactory bulb during olfactory stimulation. Brain Research 98, 596–600.

    Article  PubMed  CAS  Google Scholar 

  • SHEN, G. Y., CHEN, W. R., MIDTGAARD, J., SHEPHERD, G. M., & HINES, M. L. (1999) Computational analysis of action potential initiation in mitral cell soma and dendrites based on dual patch recordings. Journal of Neurophysiology 82, 3006–3020.

    PubMed  CAS  Google Scholar 

  • SHEPHERD, G. M. (1963) Responses of mitral cells to olfactory nerve volleys in the rabbit. Journal of Physiology (London) 168, 89–100.

    CAS  Google Scholar 

  • SHEPHERD, G. M. (1971) Physiological evidence for dendrodendritic synaptic interactions in the rabbit’s olfactory glomerulus. Brain Research 32, 212–217.

    Article  PubMed  CAS  Google Scholar 

  • SHEPHERD, G. M. (1972) Synaptic organization of the mammalian olfactory bulb. Physiological Reviews 52, 864–917.

    PubMed  CAS  Google Scholar 

  • SHEPHERD, G. M. (1979) The Synaptic Organization of the Brain. Second Edition. New York: Oxford University Press.

    Google Scholar 

  • SHEPHERD, G. M. (1981) The olfactory glomerulus: Its significance for sensory processing. In: Brain Mechanisms of Sensation (edited by Katsuki, Y., Norgren, R. & SATO, M.), pp. 209–223. New York: Wiley.

    Google Scholar 

  • SHIPLEY, M. T. & ENNIS, M. (1996) Functional organization of the olfactory system. Journal of Neurobiology 30, 123–176.

    Article  PubMed  CAS  Google Scholar 

  • STEWART, W. B., KAUER, J. S. & SHEPHERD, G. M. (1979) Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. The Journal of Comparative Neurology 185, 715–734.

    Article  PubMed  CAS  Google Scholar 

  • TAKAHASHI, Y. K., KUROSAKI, M., HIRONO, S. & MORI, K.(2004) Topographic representation of odorant molecular features in the rat olfactory bulb. Journal of Neurophysiology 92, 2413–2427.

    Article  PubMed  CAS  Google Scholar 

  • URBAN, N. N. & SAKMANN, B. (2002) Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. Journal of Physiology (London) 542, 355–367.

    Article  CAS  Google Scholar 

  • VAN DRONGELEN W. A. H. & DøVING, K. B. (1978) Convergence in the olfactory system: Quantitative aspects of odour sensitivity. Journal of Theoretical Biology 71, 39–48.

    Article  PubMed  Google Scholar 

  • VASSAR, R., NGAI, J. & AXEL, R. (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309–318.

    Article  PubMed  CAS  Google Scholar 

  • WHITE, E. L. (1972) Synaptic organization in the olfactory glomerulus of the mouse. Brain Research 37, 69–80.

    Article  PubMed  CAS  Google Scholar 

  • WOOLSEY, T. A. & VAN DER LOOS, H. (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Research 17, 205–242.

    Article  PubMed  CAS  Google Scholar 

  • XU, F., GREER, C. A. & SHEPHERD, G. M. (2000) Odor maps in the olfactory bulb. The Journal of Comparative Neurology 422, 489–495.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Gordon M. Shepherd.

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Chen, W.R., Shepherd, G.M. The olfactory glomerulus: A cortical module with specific functions. J Neurocytol 34, 353–360 (2005). https://doi.org/10.1007/s11068-005-8362-0

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