Olfaction: Central Processing

Olfactory receptor neurons in the nasal epithelium detect a huge variety of airborne chemicals (termed ‘odorants’) and encode information about these stimuli in the form of action potentials. This code is then transmitted to the brain, where patterns of neural activity represent the identity, concentration and temporal dynamics of the odorants. Neural processing of olfactory information at multiple levels in the brain mediates odour recognition, synthetic olfactory perceptions and provides feedback control to the initial stages of the olfactory pathway. This article presents some of the challenges in olfactory information processing and then reviews our current knowledge of the mechanisms by which the olfactory bulb and olfactory cortex represent odours and analyse olfactory information.

Keywords: odour coding; sensory coding; olfactory bulb; olfactory cortex; smell; piriform cortex

Figure 1. Principal structures of the mammalian olfactory system. Axons of olfactory receptor neurons in the olfactory epithelium sort themselves as they project to the olfactory bulb so that all of the neurons expressing a given olfactory receptor project to the same glomerulus (dashed circle), where they make synapses on to mitral cells. The mitral cells project broadly to a variety of cortical and subcortical structures. Ant. Cort. amygdala stands for the anterior cortical nucleus of the amygdala. The olfactory peduncle includes the anterior olfactory nucleus, the indusium griseum, the anterior hippocampal continuation and the ventral tenia tecta (see Cleland and Linster, 2003).
Figure 2. Odorant-specific patterns of glomerular activation in the mouse olfactory bulb. The baseline fluorescence of the olfactory bulbs of a mouse that expresses synaptopHluorin, a fluorescent indicator of transmitter release, in its olfactory nerve terminals. Bar, 1 mm (left). Image is from an anaesthetized mouse imaging through thinned bone. See Bozza et al., 2004, In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42: 9–21 for details. Pseudocolour maps showing the fluorescence increase (indicating transmitter release from olfactory receptor axons) evoked by the presentation of each of the named odorants. Increases in fluorescence in individual glomeruli are clearly visible, and the pattern of fluorescence increases is unique to each odorant (right three panels).
Figure 3. Temporal mechanisms of odour coding. (a) Pseudocolour maps showing patterns of receptor input to olfactory bulb imaged in response to the odorant ethyl butyrate during one respiratory cycle of an anaesthetized mouse. These spatial patterns (and thus the glomerular representation of the odorant) change through the time course of a single sniff. The outline of the dorsal bulb is shown in white. (b) The sequence of response times for input to different glomeruli changes with the identity of the odorant. Vertical lines indicate response times for five different glomeruli imaged during one respiratory cycle. Because the sequence is different for different odorants, the timing of inputs to different glomeruli may contribute to coding information about odorant identity. (c) Action potentials of mitral/tufted cells (middle trace) are phase-locked to the local field potential (bottom trace) during odour stimulation. Upper trace shows the time course of inhalation of the odorant enanthic acid. (d) Simultaneous recordings of action potentials from two mitral/tufted cells (trace 2 and 3) show that both cells respond to odour stimulation with a burst of spikes. Trace 1 shows the respiration cycle (dark bar indicates presentation of the odorant caproic acid). Bracket indicates spikes used in (c). (e) Action potentials from bracketed part of d shown at higher temporal resolution. The spikes of these neurons tend to synchronize (arrows) during odorant inhalation. Parts 3(c)–(e) adapted from Kashiwadani et al. 1999. Reproduced by permission of the American Physiological Society.
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 References
    Aungst JL, Heyward PM, Puche AC et al. (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426: 623–629.
    book Cleland TA and Linster C (2003) "Central olfactory structures". In: Doty RL (ed.) Handbook of Olfaction and Gustation, 2nd edn, pp. 165–180. New York: Marcel Dekker.
    Kadohisa M and Wilson DA (2006) Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proceedings of the National Academy of Sciences of the USA 103: 15206–15211.
    Kashiwadani H, Sasaki YF, Uchida N and Mori K (1999) Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. Journal of Neurophysics 82: 1786–1792.
    McGann JP, Pirez N, Gainey MA et al. (2005) Odorant representations are modulated by intra- but not inter-glomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48: 1039–1053.
    book Shepherd GM, Chen WR and Greer CA (2004) "Olfactory bulb". In: Shepherd GM (ed.) The Synaptic Organization of the Brain, pp. 165–216. New York: Oxford University Press.
    Spors H, Wachowiak M, Cohen LB and Friedrich RW (2006) Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. Journal of Neuroscience 26: 1247–1259.
    Suzuki N and Bekkers JM (2006) Neural coding by two classes of principal cells in the mouse piriform cortex. Journal of Neuroscience 26: 11938–11947.
    Wehr M and Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162–166.
    Yokoi M, Mori K and Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proceedings of the National Academy of Sciences of the USA 92: 3371–3375.
 Further Reading
    Adrian ED (1942) Olfactory reactions in the brain of the hedgehog. Journal of Physiology 100: 459–473.
    Buck LB (1996) Information coding in the vertebrate olfactory system. Annual Review of Neuroscience 19: 517–544.
    Buck L and Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65: 175–187.
    book Doty RL (2003) Handbook of Olfaction and Gustation. New York: Marcel Dekker.
    Laurent G (1999) A systems perspective on early olfactory coding. Science 286: 723–728.
    Malnic B, Hirono J, Sato T and Buck LB (1999) Combinatorial receptor codes for odors. Cell 96: 713–723.
    book Serby MJ and Chobor KL (1992) Science of Olfaction. New York: Springer.
    Wachowiak M and Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Seminars in Cell and Developmental Biology 17: 411–423.
    book Wilson DA and Stevenson RJ (2006) Learning to Smell. Baltimore, MD: Johns Hopkins University Press.
    Wilson RI and Mainen ZF (2006) Early events in olfactory processing. Annual Review of Neuroscience 29: 163–201.
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McGann, John P, and Wachowiak, Matt(Sep 2007) Olfaction: Central Processing. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020290]