1. Neuroscience

A fear conditioned cue orchestrates a suite of behaviors in rats

  1. Amanda Chu  Is a corresponding author
  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  Is a corresponding author
  1. Boston College, United States
https://doi.org/10.7554/eLife.82497
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

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.

Metrics

  • 1,334
    views
  • 167
    downloads
  • 16
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Citations by DOI

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Ethograms predict visual fear conditioning status in rats

    David C Williams, Amanda Chu ... Michael A McDannald
    Research Advance Updated

    Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (eight total) in a conditioned suppression setting using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. These shock-paired visual cues further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.