Olfaction: Central Processing

Abstract

Olfactory receptor neurons in the nasal epithelium detect a huge variety of airborne chemicals (termed ‘odourants’) and encode information about these stimuli in the form of action potentials. This code is then transmitted to the brain, where spatiotemporal patterns of neural activity represent the identity, concentration and temporal dynamics of the odourants. 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.

Key Concepts:

  • The chemical identity of an odourant is represented by the set of ORNs it stimulates and determines the odour's perceived quality.

  • The concentration of an odourant is represented jointly by the amplitude of the ORN response and the recruitment of ORNs expressing lower affinity receptors; this determines the odour's perceived intensity.

  • Each olfactory bulb glomerulus receives axonal projections from a set of ORNs expressing the same odour receptor.

  • An odour stimulates a subset of ORNs (based on their odour receptor expression) and thus drives activity in a corresponding subset of olfactory bulb glomeruli – this odour‐to‐glomerulus mapping is one of the most accessible codes in the nervous system.

  • Activity in olfactory bulb glomeruli is determined by a complex set of interactions among ORN sensory inputs, interneurons within and between glomeruli and modulatory inputs from other brain regions.

  • The set of mitral cells responding during odour presentation represents the chemical identity of the odour, whereas their firing frequency and timing provides additional information about the odour concentration.

  • Activity in mitral cells is shaped by complex interactions with inhibitory granule cells that interconnect mitral cells receiving disparate sensory input.

  • Neurons in piriform cortex respond to specific combinations of input from mitral cells in the olfactory bulb, thus selectively responding to certain odours or combinations of odours.

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

Figure 1.

Principal structures of the mammalian olfactory system. Axons of ORNs 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 onto 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, ).

Figure 2.

Odourant‐specific patterns of glomerular activation in the mouse olfactory bulb. (Left) The baseline fluorescence of the olfactory bulbs of a mouse that expresses synaptopHluorin, a fluorescent indicator of transmitter release, in its olfactory nerve terminals. The scale bar indicates 1 mm. Image is from an anesthetised mouse imaging through thinned bone. See Bozza et al. () for details. (Right 3 images) Pseudocolour maps showing the fluorescence increase (indicating transmitter release from olfactory receptor axons) evoked by the presentation of each of the named odourants. Increases in fluorescence in individual glomeruli are clearly visible, and the pattern of fluorescence increases is unique to each odourant.

Figure 3.

Temporal mechanisms of odour coding. (a) Pseudocolour maps showing patterns of receptor input to olfactory bulb imaged in response to the odourant ethyl butyrate during one respiratory cycle of an anesthetised mouse. These spatial patterns (and thus the glomerular representation of the odourant) 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 odourant. Vertical lines indicate response times for five different glomeruli imaged during one respiratory cycle. Because the sequence is different for different odourants, the timing of inputs to different glomeruli may contribute to coding information about odourant 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 odourant 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 odourant 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 synchronise (arrows) during odourant inhalation. Parts (c–e) are adapted from Kashiwadani et al. (). Reproduced by permission of the American Physiological Society. © American Physiological Society.

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McGann, John P(Nov 2013) Olfaction: Central Processing. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020290.pub2]