Olfaction

Abstract

Olfaction, the ability to recognise and discriminate myriad airborne molecules with great accuracy and sensitivity, is one of the most remarkable, but least understood senses. It permits continuous monitoring of the surroundings for small volatile molecules, including chemical signals that identify territories, food, predators and mates; thus, olfaction plays a key role in survival and adaptation in the animal world. Recent work suggests that in mammals, odour perception begins through volatile molecules binding to a subset of several hundred G‐protein‐coupled receptors on the olfactory sensory neurons in the nose. The identity of the odorant is encoded by a spatiotemporal pattern of activity within the first central relay, the olfactory bulb. The olfactory cortex then functions as a combinatorial array that allows recognition of those odorant‐specific patterns and forms synthetic odour percepts. This pattern recognition process is experience‐dependent, and thus odour discrimination and perception can be affected by a variety of memory and cognitive disorders.

Key Concepts

  • Odorous stimuli are transduced by olfactory sensory neurons through a large family of G‐protein‐coupled receptors, with individual sensory neurons expressing a single type of receptor.
  • Olfactory sensory neurons project axons directly into the mammalian forebrain targeting the olfactory bulb and are continually replaced throughout life.
  • Odorant identity is initially encoded by odour‐specific spatiotemporal patterns of activity in the olfactory bulb which emerges due to highly specific sensory neuron axonal projections.
  • In contrast to other sensory systems, the direct projection to the primary olfactory cortex does not pass through the thalamus, although there is an olfactory thalamocortical pathway.
  • Encoding of odour quality in the piriform cortex is performed by populations of highly distributed neurons, with no known odour‐specific spatial topography.
  • Information about internal state, emotion, expectation and past experience can influence odour processing as early as the first central synapse, and odour learning can influence processing through the entire olfactory pathway.
  • Given that most natural odours are mixtures of many volatile components, odour perception is based on an experience‐dependent combinatorial process resulting in the perception of synthetic odour objects.
  • Odour habituation is a central phenomenon involving changes in the strength of connections between specific neurons within the olfactory bulb and cortex.
  • Through extensive interaction with other sensory systems, olfaction plays a critical role in the perception of flavour and food perception.
  • Impairment in olfactory perception is a prevalent problem which is associated with a wide variety of neurological disorders.

Keywords: odorants; olfactory epithelium; olfactory receptors; expression pattern; olfactory sensory neurons; olfactory bulb; piriform cortex; odour coding; odour perception; odour habituation

Figure 1. Schematic representation of the cAMP pathway for odorant signalling in olfactory sensory neurons. Upon binding of appropriate odorous ligands, distinct receptor types in the ciliary membrane act through specific G‐proteins (Golf) to stimulate adenylyl cyclase (type III) generating cAMP. The resulting elevated second messenger levels elicit the activation of cation channels, allowing the influx of sodium and especially calcium ions. Calcium ions, in turn, activate Ca2+‐dependent chloride channels. Owing to the characteristic equilibrium potential for chloride in olfactory neurons, the induced Cl current is depolarising, thus resulting in a significant amplification of the primary odour‐induced current.
Figure 2. Topographic projection of olfactory sensory neurons (OSNs) expressing distinct receptor types (colours) to distinct glomeruli (GLOM) in the olfactory bulb. The chemospecific responsiveness of olfactory sensory cells, as well as the targeting of their axons in the olfactory bulb, is determined by the receptor type they express. However, different odorants (A and B) that share a defined structural feature (epitope) may well interact with cells expressing a distinct receptor type and thus leading to an activation of the same glomerulus. Complex odorous compounds comprising multiple epitopes may interact with various receptor types eliciting the activation of several glomeruli. In this way, each odorant would be represented spatially in the bulb by a unique ensemble of active glomeruli. Local interneurons within the olfactory bulb (juxtaglomerular (JG) and granule cells (GC)) help enhance contrast and control excitability of output neurons, mitral and tufted (M/T) cells. Individual neurons within the primary olfactory (piriform) cortex can receive convergent input via the lateral olfactory tract (LOT) from multiple mitral/tufted cells each conveying information from different receptors. This convergence allows synthesis of odour objects from the features extracted at the receptor sheet and refined in the olfactory bulb. The olfactory cortex also sends feedback to the olfactory bulb.
Figure 3. Different odour stimulation conditions evoke different perceptions. Orthonasal olfaction, which occurs during normal breathing when an odorant is in the external environment, activates the olfactory receptor sheet, olfactory bulb (OB), olfactory cortex (OC), amygdala (AM) and orbitofrontal cortex (OFC) which together allow perception and identification of the odour, along with emotional and memorial responses. Food in the mouth, however, is also an odour source which activates receptors in the nose during exhalation, a process known as retronasal olfaction. The combination of the odour along with taste, sight of the food and feel of the food in the mouth create our perception of flavour.
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Further Reading

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Wilson DA and Stevenson RJ (2006) Learning to Smell: Olfactory Perception from Neurobiology to Behavior. Johns Hopkins University Press: Baltimore.

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East, Brett S, and Wilson, Donald A(Feb 2020) Olfaction. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000077.pub3]