Neural variability determines coding strategies for natural self-motion in macaque monkeys

Author:

Mackrous Isabelle1,Carriot Jérome1,Cullen Kathleen E2345ORCID,Chacron Maurice J1ORCID

Affiliation:

1. Department of Physiology, McGill University, Montreal, Canada

2. The Department of Otolaryngology- Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, United States

3. The Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, United States

4. The Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States

5. Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, United States

Abstract

We have previously reported that central neurons mediating vestibulo-spinal reflexes and self-motion perception optimally encode natural self-motion (Mitchell et al., 2018). Importantly however, the vestibular nuclei also comprise other neuronal classes that mediate essential functions such as the vestibulo-ocular reflex (VOR) and its adaptation. Here we show that heterogeneities in resting discharge variability mediate a trade-off between faithful encoding and optimal coding via temporal whitening. Specifically, neurons displaying lower variability did not whiten naturalistic self-motion but instead faithfully represented the stimulus’ detailed time course, while neurons displaying higher variability displayed temporal whitening. Using a well-established model of VOR pathways, we demonstrate that faithful stimulus encoding is necessary to generate the compensatory eye movements found experimentally during naturalistic self-motion. Our findings suggest a novel functional role for variability toward establishing different coding strategies: (1) faithful stimulus encoding for generating the VOR; (2) optimized coding via temporal whitening for other vestibular functions.

Funder

Canadian Institutes of Health Research

National Institutes of Health

Publisher

eLife Sciences Publications, Ltd

Subject

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

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