Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality

Author:

Kim Brian12,Haney Seth3,Milan Ana P4,Joshi Shruti3,Aldworth Zane1ORCID,Rulkov Nikolai5,Kim Alexander T1,Bazhenov Maxim3ORCID,Stopfer Mark A1ORCID

Affiliation:

1. Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH)

2. Brown University - National Institutes of Health Graduate Partnership Program

3. Department of Medicine, University of California, San Diego

4. Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam

5. Biocircuits Institute, University of California, San Diego

Abstract

Odorants binding to olfactory receptor neurons (ORNs) trigger bursts of action potentials, providing the brain with its only experience of the olfactory environment. Our recordings made in vivo from locust ORNs showed that odor-elicited firing patterns comprise four distinct response motifs, each defined by a reliable temporal profile. Different odorants could elicit different response motifs from a given ORN, a property we term motif switching. Further, each motif undergoes its own form of sensory adaptation when activated by repeated plume-like odor pulses. A computational model constrained by our recordings revealed that organizing responses into multiple motifs provides substantial benefits for classifying odors and processing complex odor plumes: each motif contributes uniquely to encode the plume’s composition and structure. Multiple motifs and motif switching further improve odor classification by expanding coding dimensionality. Our model demonstrated that these response features could provide benefits for olfactory navigation, including determining the distance to an odor source.

Funder

Office of Naval Research

National Institutes of Health

National Science Foundation

Obra Social La Caixa

Eunice Kennedy Shriver National Institute of Child Health and Human Development

Intel Corp

NIH

NSF

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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