Divergent projections of the prelimbic cortex bidirectionally regulate active avoidance

  1. Maria M Diehl  Is a corresponding author
  2. Jorge M Iravedra-Garcia
  3. Jonathan Morán-Sierra
  4. Gabriel Rojas-Bowe
  5. Fabiola N Gonzalez-Diaz
  6. Viviana P Valentín-Valentín
  7. Gregory J Quirk
  1. Kansas State University, United States
  2. University of Puerto Rico School of Medicine, Puerto Rico

Abstract

The prefrontal cortex (PFC) integrates incoming information to guide our actions. When motivation for food-seeking competes with avoidance, the PFC likely plays a role in selecting the optimal choice. In platform-mediated active avoidance, rats avoid a tone-signaled footshock by stepping onto a nearby platform, delaying access to sucrose pellets. This avoidance requires prelimbic (PL) prefrontal cortex, basolateral amygdala (BLA), and ventral striatum (VS). We previously showed that inhibitory tone responses of PL neurons correlate with avoidability of shock (Diehl et al., 2018). Here, we optogenetically modulated PL terminals in VS and BLA to identify PL outputs regulating avoidance. Photoactivating PL-VS projections reduced avoidance, whereas photoactivating PL-BLA projections increased avoidance. Moreover, photosilencing PL-BLA or BLA-VS projections reduced avoidance, suggesting that VS receives opposing inputs from PL and BLA. Bidirectional modulation of avoidance by PL projections to VS and BLA enables the animal to make appropriate decisions when faced with competing drives.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Maria M Diehl

    Psychological Sciences, Kansas State University, Manhattan, United States
    For correspondence
    maria.m.diehl@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7370-6106
  2. Jorge M Iravedra-Garcia

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
  3. Jonathan Morán-Sierra

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
  4. Gabriel Rojas-Bowe

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7042-930X
  5. Fabiola N Gonzalez-Diaz

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
  6. Viviana P Valentín-Valentín

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
  7. Gregory J Quirk

    Psychiatry and Neurobiology & Anatomy, University of Puerto Rico School of Medicine, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7534-2764

Funding

National Institute of Mental Health (F32-MH105185)

  • Maria M Diehl

National Institute of Mental Health (R37-MH058883)

  • Gregory J Quirk

National Institute of Mental Health (P50-MH106435)

  • Gregory J Quirk

University of Puerto Rico President's Office

  • Gregory J Quirk

National Institute of General Medical Sciences (R25-GM097635)

  • Jorge M Iravedra-Garcia
  • Viviana P Valentín-Valentín

National Institute of General Medical Sciences (R25-GM061151)

  • Fabiola N Gonzalez-Diaz

National Institute of General Medical Sciences (T34-GM007821)

  • Gabriel Rojas-Bowe

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

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, 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 (#A3340107) of the University of Puerto Rico. The protocol was approved by the Committee on the Ethics of Animal Experiments of the University of Puerto Rico. All surgery was performed under isofluorane anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: May 28, 2020
  2. Accepted: October 14, 2020
  3. Accepted Manuscript published: October 15, 2020 (version 1)
  4. Version of Record published: October 26, 2020 (version 2)

Copyright

© 2020, Diehl 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. Maria M Diehl
  2. Jorge M Iravedra-Garcia
  3. Jonathan Morán-Sierra
  4. Gabriel Rojas-Bowe
  5. Fabiola N Gonzalez-Diaz
  6. Viviana P Valentín-Valentín
  7. Gregory J Quirk
(2020)
Divergent projections of the prelimbic cortex bidirectionally regulate active avoidance
eLife 9:e59281.
https://doi.org/10.7554/eLife.59281

Share this article

https://doi.org/10.7554/eLife.59281

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