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Punishment insensitivity emerges from impaired contingency detection, not aversion insensitivity or reward dominance

Research Article
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Cite this article as: eLife 2019;8:e52765 doi: 10.7554/eLife.52765

Abstract

Our behaviour is shaped by its consequences – we seek rewards and avoid harm. It has been reported that individuals vary markedly in their avoidance of detrimental consequences, i.e. in their sensitivity to punishment. The underpinnings of this variability are poorly understood; they may be driven by differences in aversion sensitivity, motivation for reward, and/or instrumental control. We examined these hypotheses by applying several analysis strategies to the behaviour of rats (n = 48; 18 female) trained in a conditioned punishment task that permitted concurrent assessment of punishment, reward-seeking, and Pavlovian fear. We show that punishment insensitivity is a unique phenotype, unrelated to differences in reward-seeking and Pavlovian fear, and due to a failure of instrumental control. Subjects insensitive to punishment are afraid of aversive events, they are simply unable to change their behaviour to avoid them.

Data availability

All data generated or analysed during this study are included in the manuscript in Figure 1. Source data files, for all figures, have been provided.

Article and author information

Author details

  1. Philip Jean-Richard-dit-Bressel

    School of Psychology, University of New South Wales, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0898-8987
  2. Cassandra Ma

    School of Psychology, University of New South Wales, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Laura A Bradfield

    School of Psychology, University of New South Wales, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3921-0745
  4. Simon Killcross

    School of Psychology, University of New South Wales, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Gavan P McNally

    School of Psychology, University of New South Wales, Sydney, Australia
    For correspondence
    g.mcnally@unsw.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9061-6463

Funding

Australian Research Council (DP190100482)

  • Gavan P McNally

Australian Research Council (DP170100075)

  • Gavan P McNally

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 procedures were approved by the UNSW Animal Ethics Committee (AEC) (ACEC16/160B) and in accordance with the code set out by the National Health and Medical Research Council (NHMRC) for the treatment of animals in research.

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, United States

Publication history

  1. Received: October 16, 2019
  2. Accepted: November 21, 2019
  3. Accepted Manuscript published: November 26, 2019 (version 1)
  4. Version of Record published: December 3, 2019 (version 2)

Copyright

© 2019, Jean-Richard-dit-Bressel 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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