Abstract

Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that - in addition to jumping, and rearing - is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing - all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveal a fear conditioned cue to orchestrate a temporally organized suite of behaviors.

Data availability

Raw images and observer judgments are freely available: https://doi.org/10.7910/DVN/HKMUUN

The following data sets were generated

Article and author information

Author details

  1. Amanda Chu

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    For correspondence
    amanda.chu@bc.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Nicholas T Gordon

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Aleah M DuBois

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Christa B Michel

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Katherine E Hanrahan

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. David C Williams

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Stefano Anzellotti

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael A McDannald

    Department of Psychology and Neuroscience, Boston College, Chestnut Hill, United States
    For correspondence
    michael.mcdannald@bc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8525-1260

Funding

National Institutes of Health (MH117791)

  • Michael A McDannald

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

Reviewing Editor

  1. Matthew N Hill, University of Calgary, Canada

Ethics

Animal experimentation: All protocols were approved by the Boston College Animal Care and Use Committee and all experiments were carried out in accordance with the NIH guidelines regarding the care and use of rats for experimental procedures. The Boston College experimental protocol supporting these procedures is 2024-001.

Version history

  1. Received: August 6, 2022
  2. Accepted: May 16, 2024
  3. Accepted Manuscript published: May 21, 2024 (version 1)

Copyright

© 2024, Chu 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. Amanda Chu
  2. Nicholas T Gordon
  3. Aleah M DuBois
  4. Christa B Michel
  5. Katherine E Hanrahan
  6. David C Williams
  7. Stefano Anzellotti
  8. Michael A McDannald
(2024)
A fear conditioned cue orchestrates a suite of behaviors in rats
eLife 13:e82497.
https://doi.org/10.7554/eLife.82497

Share this article

https://doi.org/10.7554/eLife.82497

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