Scale-free behavioral dynamics directly linked with scale-free cortical dynamics

  1. Sabrina A Jones
  2. Jacob H Barfield
  3. V Kindler Norman
  4. Woodrow L Shew  Is a corresponding author
  1. University of Arkansas at Fayetteville, United States

Abstract

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.

Data availability

The data analyzed here were first published in Stringer et al. (2019) and are publicly available on Figshare at Stringer, Carsen; Pachitariu, Marius; Reddy, Charu; Carandini, Matteo; Harris, Kenneth D. (2018): Recordings of ten thousand neurons in visual cortex during spontaneous behaviors. Janelia Research Campus. Dataset. https://doi.org/10.25378/janelia.6163622.v6. Analysis and simulation codes are publicly available on Figshare https://doi.org/10.6084/m9.figshare.21954389.v1

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Sabrina A Jones

    Department of Physics, University of Arkansas at Fayetteville, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jacob H Barfield

    Department of Physics, University of Arkansas at Fayetteville, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. V Kindler Norman

    Department of Physics, University of Arkansas at Fayetteville, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Woodrow L Shew

    Department of Physics, University of Arkansas at Fayetteville, Fayetteville, United States
    For correspondence
    shew@uark.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0679-1766

Funding

National Institutes of Health (NIHR15NS116742)

  • Woodrow L Shew

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 conducted according to the UK Animals Scientific Procedures Act (1986). Experiments were performed at University College London under personal and project licenses released by the Home Office following appropriate ethics review.

Reviewing Editor

  1. Gordon J Berman, Emory University, United States

Publication history

  1. Preprint posted: May 13, 2021 (view preprint)
  2. Received: May 3, 2022
  3. Accepted: January 6, 2023
  4. Accepted Manuscript published: January 27, 2023 (version 1)
  5. Version of Record published: February 15, 2023 (version 2)

Copyright

© 2023, Jones 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. Sabrina A Jones
  2. Jacob H Barfield
  3. V Kindler Norman
  4. Woodrow L Shew
(2023)
Scale-free behavioral dynamics directly linked with scale-free cortical dynamics
eLife 12:e79950.
https://doi.org/10.7554/eLife.79950

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