Layer 6 ensembles can selectively regulate the behavioral impact and layer-specific representation of sensory deviants

Abstract

Predictive models can enhance the salience of unanticipated input. Here, we tested a key potential node in neocortical model formation in this process, layer (L) 6, using behavioral, electrophysiological and imaging methods in mouse primary somatosensory neocortex. We found that deviant stimuli enhanced tactile detection and were encoded in L2/3 neural tuning. To test the contribution of L6, we applied weak optogenetic drive that changed which L6 neurons were sensory responsive, without affecting overall firing rates in L6 or L2/3. This stimulation selectively suppressed behavioral sensitivity to deviant stimuli, without impacting baseline performance. This stimulation also eliminated deviance encoding in L2/3 but did not impair basic stimulus responses across layers. In contrast, stronger L6 drive inhibited firing and suppressed overall sensory function. These findings indicate that, despite their sparse activity, specific ensembles of stimulus driven L6 neurons are required to form neocortical predictions, and to realize their behavioral benefit.

Data availability

Underlying data for all main result figures is included in the supporting files.

Article and author information

Author details

Jakob Voigts

Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States

For correspondence
jvoigts@mit.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5174-7214
Christopher A Deister

Department of Neuroscience and Brown Institute for Brain Sciences, Brown University, Providence, United States

Competing interests
The authors declare that no competing interests exist.
Christopher I Moore

Department of Neuroscience, Brown University, Providence, United States

For correspondence
Christopher_Moore@brown.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4534-1602

Funding

National Institutes of Health (R01NS045130)

Christopher I Moore

National Institutes of Health (F32MH100749)

Christopher A Deister

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 and animal care protocols conformed to guidelines established by the National Institutes of Health, and approved by the Institutional Animal Care and Use Committee (IACUC) protocol (#1710000308) at Brown University (PHS Animal Welfare Assurance number D16-00183)

Reviewing Editor

John R Huguenard, Stanford University School of Medicine, United States

Publication history

Received: June 1, 2019
Accepted: December 1, 2020
Accepted Manuscript published: December 2, 2020 (version 1)
Version of Record published: January 20, 2021 (version 2)

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.