Feedback optimizes neural coding and perception of natural stimuli

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Abstract

Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species.

Data availability

All data have been deposited on Figshare under the URL: https://figshare.com/s/b9e094a67a38e29212e8

The following data sets were generated

(2018) Figure source data for: Feedback optimizes neural coding and perception of natural stimuli
https://figshare.com/s/b9e094a67a38e29212e8.

https://figshare.com/s/b9e094a67a38e29212e8

Article and author information

Author details

Chengjie G Huang

Department of Physiology, McGill University, Montreal, Canada

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7491-6060
Michael G Metzen

Department of Physiology, McGill University, Montreal, Canada

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2365-4192
Maurice J Chacron

Department of Physiology, McGill University, Montreal, Canada

For correspondence
maurice.chacron@mcgill.ca

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3032-452X

Funding

Canadian Institutes of Health Research

Maurice J Chacron

Fonds de Recherche du Québec - Nature et Technologies

Maurice J Chacron

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures were approved by McGill University's animal care committee and were performed in accordance to the guidelines set out by the Canadian Council of Animal Care. Protocol 5285.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.