Synthesis of a comprehensive population code for contextual features in the awake sensory cortex

  1. Evan H Lyall
  2. Daniel P Mossing
  3. Scott R Pluta
  4. Yun Wen Chu
  5. Amir Dudai
  6. Hillel Adesnik  Is a corresponding author
  1. UC Berkeley, United States
  2. Purdue University, United States
  3. The Hebrew University of Jerusalem, Israel
  4. University of California, Berkeley, United States

Abstract

How cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a population that forms a comprehensive code for these global stimulus properties. Although the logic for how single neurons summate over their spatial inputs has been well-explored in anesthetized animals, how large groups of neurons compose a flexible population code of higher order features in awake animals is not known. To address this question, we probed the integration and population coding of higher order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We developed a novel tactile stimulator that allowed the precise measurement of spatial summation even in actively whisking mice. Using this system, we found a sparse but comprehensive population code for higher order tactile features that depends on a heterogeneous and neuron-specific logic of spatial summation beyond the receptive field. Different somatosensory cortical neurons summed specific combinations of sensory inputs supra-linearly, but integrated other inputs sub-linearly, leading to selective responses to higher order features. Visual cortical populations employed a nearly identical scheme to generate a comprehensive population code for contextual stimuli. These results suggest that a heterogeneous logic of input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of sparse higher order feature codes in neural populations. This may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli.

Data availability

All source data and analysis software is uploaded to Dryad.

The following data sets were generated

Article and author information

Author details

  1. Evan H Lyall

    Molecular and Cell Biolgoy, UC Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6946-7333
  2. Daniel P Mossing

    Molecular and Cell Biology, UC Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Scott R Pluta

    Biology, Purdue University, West Lafayette, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3057-8095
  4. Yun Wen Chu

    Biology, Purdue University, West Lafayette, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Amir Dudai

    The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Hillel Adesnik

    Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    hadesnik@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3796-8643

Funding

NIH Office of the Director (DP2NS087725)

  • Hillel Adesnik

National Eye Institute (R01EY023756)

  • Hillel Adesnik

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

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (ACUC) protocols AUP-2014-10-6832-2 of the University of California, Berkeley. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: September 1, 2020
  2. Accepted: October 25, 2021
  3. Accepted Manuscript published: November 1, 2021 (version 1)
  4. Version of Record published: November 17, 2021 (version 2)

Copyright

© 2021, Lyall 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.

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  1. Evan H Lyall
  2. Daniel P Mossing
  3. Scott R Pluta
  4. Yun Wen Chu
  5. Amir Dudai
  6. Hillel Adesnik
(2021)
Synthesis of a comprehensive population code for contextual features in the awake sensory cortex
eLife 10:e62687.
https://doi.org/10.7554/eLife.62687

Share this article

https://doi.org/10.7554/eLife.62687

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