Cue-inhibited ventrolateral periaqueductal gray neurons signal fear output and threat probability in male rats

Abstract

The ventrolateral periaqueductal gray (vlPAG) is proposed to mediate fear responses to imminent danger. Previously we reported that vlPAG neurons showing short-latency increases in firing to danger cues - the presumed neural substrate for fear output - signal threat probability in male rats (Wright et al., 2019). Here, we scrutinize the activity of cue-inhibited vlPAG neurons that show decreases in firing to danger cues. One cue-inhibited population flipped danger activity from early inhibition to late excitation: a poor neural substrate for fear output, but a better substrate for threat timing. A second population showed differential firing with greatest inhibition to danger, less to uncertainty and no inhibition to safety. Differential firing by this second population reflected the pattern of fear output, and was observed throughout cue presentation. The results reveal an expected vlPAG signal for fear output in an unexpected, cue-inhibited population.

Data availability

Data have been deposited at: http://crcns.org/data-sets/bst/pag-1

The following previously published data sets were used

Article and author information

Author details

  1. Kristina M Wright

    Department of Psychology, Boston College, Chestnut Hill, United States
    For correspondence
    wrightko@bc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1446-3009
  2. Thomas C Jhou

    Department of Psychology, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8811-0156
  3. Daniel Pimpinelli

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

    Department of Psychology, 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 (R01MH117791)

  • Michael A McDannald

National Institutes of Health (R00DA034010)

  • Michael A McDannald

National Science Foundation (5106201)

  • Kristina M Wright

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

Reviewing Editor

  1. Thorsten Kahnt, Northwestern University Feinberg School of Medicine, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#2018-002) of Boston College. The protocol was approved by the Institutional Animal Care and Use Committee of Boston College. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: July 10, 2019
  2. Accepted: September 28, 2019
  3. Accepted Manuscript published: September 30, 2019 (version 1)
  4. Version of Record published: October 30, 2019 (version 2)

Copyright

© 2019, Wright 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. Kristina M Wright
  2. Thomas C Jhou
  3. Daniel Pimpinelli
  4. Michael A McDannald
(2019)
Cue-inhibited ventrolateral periaqueductal gray neurons signal fear output and threat probability in male rats
eLife 8:e50054.
https://doi.org/10.7554/eLife.50054

Share this article

https://doi.org/10.7554/eLife.50054

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