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Common principles for odour coding across vertebrates and invertebrates

Abstract

The olfactory system is an ideal and tractable system for exploring how the brain transforms sensory inputs into behaviour. The basic tasks of any olfactory system include odour detection, discrimination and categorization. The challenge for the olfactory system is to transform the high-dimensional space of olfactory stimuli into the much smaller space of perceived objects and valence that endows odours with meaning. Our current understanding of how neural circuits address this challenge has come primarily from observations of the mechanisms of the brain for processing other sensory modalities, such as vision and hearing, in which optimized deep hierarchical circuits are used to extract sensory features that vary along continuous physical dimensions. The olfactory system, by contrast, contends with an ill-defined, high-dimensional stimulus space and discrete stimuli using a circuit architecture that is shallow and parallelized. Here, we present recent observations in vertebrate and invertebrate systems that relate the statistical structure and state-dependent modulation of olfactory codes to mechanisms of perception and odour-guided behaviour.

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Fig. 1: Anatomical characterization of fly and mouse olfactory systems.
Fig. 2: Local interneurons and principal cells in the antennal lobe and olfactory bulb.
Fig. 3: Local connectivity of early olfactory regions in the mouse and fly.
Fig. 4: Effect of neuromodulation on olfactory circuits.

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Acknowledgements

K.V. acknowledges support from the Deutsche Forschungsgemeinschaft (German Research Foundation) under Germany’s Excellence Strategy EXC 2117-422037984 and FOR5424 (466488864). S.R.D. is supported by NIH grants R011DC016222 and U19 NS112953 and by grants from the Simons Collaboration on the Global Brain, the Brain Research Foundation and the Tan Yang Center at Harvard Medical School.

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Glossary

Connectome

A comprehensive map of the synaptic connections between neurons across the brain.

Critical period

A window of time during development when neurons exhibit greater activity-dependent synaptic plasticity and structural remodelling or refinement.

Ensemble

A set of neurons encoding specific information, such as odour identity.

Gain control

The transformation that serves to reduce the firing rate of a population of neurons. Gain control may be dependent on input strength (divisive) or not (subtractive).

Habituation

Reduced response sensitivity to repeated exposure to an odorant.

Hebbian plasticity

A mechanism for activity-dependent learning that occurs through the strengthening of ensembles or associative connections by repeated co-activation of neurons.

Lateral inhibition

A mechanism for contrast enhancement in which an activated neuron inhibits the activity of neighbouring neurons.

Memory extinction

A paradigm in which a learned association with a given odour is erased by repeated exposure to the odour in the absence of paired reinforcement.

Neuromodulation

The effect on neural activity of neurons that release neuromodulators, such as acetylcholine, noradrenaline or dopamine. Neuromodulation often outlasts the effect of neurotransmitter release.

Odour space

A high-dimensional representation of odours based on their chemical and perceptual qualities.

Pattern separation

The transformation of similar population-level odour representations into more distinct activity patterns.

Pheromone

An odour molecule excreted by the body that can generally trigger a social response.

Recurrent circuitry

A form of circuitry in which the output of a neuron influences its own input through excitatory or inhibitory feedback.

Topographic map

A stereotyped spatial map in which olfactory receptor neurons or olfactory sensory neurons converge in discrete glomerular channels in specific areas of the antennal lobe or olfactory bulb.

Valence

The hedonic value of an odour, described as appetitive, aversive or neutral, that can be either learned or innate.

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Fulton, K.A., Zimmerman, D., Samuel, A. et al. Common principles for odour coding across vertebrates and invertebrates. Nat. Rev. Neurosci. 25, 453–472 (2024). https://doi.org/10.1038/s41583-024-00822-0

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