How many neurons are sufficient for perception of cortical activity?

  1. Henry William Peter Dalgleish
  2. Lloyd E Russell
  3. Adam Max Packer
  4. Arnd Roth
  5. Oliver M Gauld
  6. Francesca Greenstreet
  7. Emmett J Thompson
  8. Michael Häusser  Is a corresponding author
  1. University College London, United Kingdom
  2. University of Oxford, United Kingdom

Abstract

Many theories of brain function assume that information is encoded and behaviour is controlled through sparse, distributed patterns of activity. It is therefore crucial to place a lower bound on the amount of neural activity that can drive behaviour and to understand how neuronal networks operate within these constraints. We use an all-optical approach to test this lower limit by driving behaviour with targeted two-photon optogenetic activation of small ensembles of L2/3 pyramidal neurons in mouse barrel cortex while using two-photon calcium imaging to record the impact on the local network. By precisely titrating the number of neurons in activated ensembles we demonstrate that the lower bound for detection of cortical activity is ~14 pyramidal neurons. We show that there is a very steep sigmoidal relationship between the number of activated neurons and behavioural output, saturating at only ~37 neurons, and that this relationship can shift with learning. By simultaneously measuring activity in the local network, we show that the activation of stimulated ensembles is balanced by the suppression of neighbouring neurons. This surprising behavioural sensitivity in the face of potent network suppression supports the sparse coding hypothesis and suggests that perception of cortical activity balances a trade-off between minimizing the impact of noise while efficiently detecting relevant signals.

Data availability

Import, processing, analysis and figure code is available on Github (Dalgleish, 2020; https://github.com/alloptical/Dalgleish-eLife-2020) for use with analysed data (https://doi.org/10.6084/m9.figshare.13135505) and/or unprocessed behavioural session data (https://doi.org/10.6084/m9.figshare.13128950). Raw calcium imaging movies are ~1TB in size and are thus available upon reasonable request.

The following data sets were generated

Article and author information

Author details

  1. Henry William Peter Dalgleish

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Lloyd E Russell

    Wolfson Institute for Biomedical Research, Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6332-756X
  3. Adam Max Packer

    Department of Physiology, Anatomy, and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5884-794X
  4. Arnd Roth

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0325-4287
  5. Oliver M Gauld

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Francesca Greenstreet

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Emmett J Thompson

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Häusser

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    For correspondence
    m.hausser@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2673-8957

Funding

ERC (695709)

  • Michael Häusser

Wellcome Trust (201225)

  • Michael Häusser

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 experimental procedures were carried out under Project Licence 70/14018 (PCC4A4ECE) issued by the UK Home Office in accordance with the UK Animals (Scientific Procedures) Act (1986) and were also subject to local ethical review. All surgical procedures were carried out under isoflurane anaesthesia (5% for induction, 1.5% for maintenance), and every effort was made to minimize suffering.

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Publication history

  1. Received: May 13, 2020
  2. Accepted: October 17, 2020
  3. Accepted Manuscript published: October 26, 2020 (version 1)
  4. Version of Record published: November 27, 2020 (version 2)

Copyright

© 2020, Dalgleish 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. Henry William Peter Dalgleish
  2. Lloyd E Russell
  3. Adam Max Packer
  4. Arnd Roth
  5. Oliver M Gauld
  6. Francesca Greenstreet
  7. Emmett J Thompson
  8. Michael Häusser
(2020)
How many neurons are sufficient for perception of cortical activity?
eLife 9:e58889.
https://doi.org/10.7554/eLife.58889

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