A neural circuit for flexible control of persistent behavioral states

Abstract

To adapt to their environments, animals must generate behaviors that are closely aligned to a rapidly changing sensory world. However, behavioral states such as foraging or courtship typically persist over long time scales to ensure proper execution. It remains unclear how neural circuits generate persistent behavioral states while maintaining the flexibility to select among alternative states when the sensory context changes. Here, we elucidate the functional architecture of a neural circuit controlling the choice between roaming and dwelling states, which underlie exploration and exploitation during foraging in C. elegans. By imaging ensemble-level neural activity in freely-moving animals, we identify stereotyped changes in circuit activity corresponding to each behavioral state. Combining circuit-wide imaging with genetic analysis, we find that mutual inhibition between two antagonistic neuromodulatory systems underlies the persistence and mutual exclusivity of the neural activity patterns observed in each state. Through machine learning analysis and circuit perturbations, we identify a sensory processing neuron that can transmit information about food odors to both the roaming and dwelling circuits and bias the animal towards different states in different sensory contexts, giving rise to context-appropriate state transitions. Our findings reveal a potentially general circuit architecture that enables flexible, sensory-driven control of persistent behavioral states.

Data availability

Code has been made available on Github. Data has been made available on Dryad.

The following data sets were generated

Article and author information

Author details

  1. Ni Ji

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7870-0678
  2. Gurrein K Madan

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Guadalupe I Fabre

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alyssa Dayan

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Casey M Baker

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Talya S Kramer

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ijeoma Nwabudike

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Steven W Flavell

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    flavell@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9464-1877

Funding

National Institute of Neurological Disorders and Stroke (R01NS104892)

  • Steven W Flavell

National Science Foundation (IOS 1845663)

  • Steven W Flavell

National Science Foundation (DUE 1734870)

  • Steven W Flavell

JPB Foundation (PIIF)

  • Steven W Flavell

JPB Foundation (PNDRF)

  • Steven W Flavell

Brain and Behavior Research Foundation (NARSAD Young Investigator Award)

  • Steven W Flavell

McKnight Foundation (McKnight Scholars Award)

  • Steven W Flavell

JPB Foundation (Picower Fellowship)

  • Ni Ji

Alfred P. Sloan Foundation (Sloan Research Fellowship)

  • Steven W Flavell

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

Reviewing Editor

  1. Manuel Zimmer, University of Vienna, Austria

Version history

  1. Preprint posted: February 5, 2020 (view preprint)
  2. Received: September 7, 2020
  3. Accepted: November 17, 2021
  4. Accepted Manuscript published: November 18, 2021 (version 1)
  5. Version of Record published: December 9, 2021 (version 2)

Copyright

© 2021, Ji 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. Ni Ji
  2. Gurrein K Madan
  3. Guadalupe I Fabre
  4. Alyssa Dayan
  5. Casey M Baker
  6. Talya S Kramer
  7. Ijeoma Nwabudike
  8. Steven W Flavell
(2021)
A neural circuit for flexible control of persistent behavioral states
eLife 10:e62889.
https://doi.org/10.7554/eLife.62889

Share this article

https://doi.org/10.7554/eLife.62889

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