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

  1. Jakob Voigts  Is a corresponding author
  2. Christopher A Deister
  3. Christopher I Moore  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
  2. Brown University, United States

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

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5174-7214
  2. 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.
  3. 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.
    ORCID icon "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

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

Publication history

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

Copyright

© 2020, Voigts et al.

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.

Metrics

  • 2,125
    Page views
  • 306
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jakob Voigts
  2. Christopher A Deister
  3. Christopher I Moore
(2020)
Layer 6 ensembles can selectively regulate the behavioral impact and layer-specific representation of sensory deviants
eLife 9:e48957.
https://doi.org/10.7554/eLife.48957

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Sabrina A Jones, Jacob H Barfield ... Woodrow L Shew
    Research Article

    Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.

    1. Neuroscience
    Barna Zajzon, David Dahmen ... Renato Duarte
    Research Article

    Information from the sensory periphery is conveyed to the cortex via structured projection pathways that spatially segregate stimulus features, providing a robust and efficient encoding strategy. Beyond sensory encoding, this prominent anatomical feature extends throughout the neocortex. However, the extent to which it influences cortical processing is unclear. In this study, we combine cortical circuit modeling with network theory to demonstrate that the sharpness of topographic projections acts as a bifurcation parameter, controlling the macroscopic dynamics and representational precision across a modular network. By shifting the balance of excitation and inhibition, topographic modularity gradually increases task performance and improves the signal-to-noise ratio across the system. We demonstrate that in biologically constrained networks, such a denoising behavior is contingent on recurrent inhibition. We show that this is a robust and generic structural feature that enables a broad range of behaviorally-relevant operating regimes, and provide an in-depth theoretical analysis unravelling the dynamical principles underlying the mechanism.