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Prior experience with behavioral control over stress facilitates social dominance

Philip T. Coleman, Gabriel W. Costanza-Chavez, Heather N. Martin, Jose Amat, Matthew G. Frank, Rory J. Sanchez, Garrett J. Potter, Simone M. Mellert, Rene K. Carter, Gianni N. Bonnici, Steven F. Maier, View ORCID ProfileMichael V. Baratta
doi: https://doi.org/10.1101/2023.06.06.543982
Philip T. Coleman
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Gabriel W. Costanza-Chavez
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Heather N. Martin
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Jose Amat
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Matthew G. Frank
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Rory J. Sanchez
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Garrett J. Potter
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Simone M. Mellert
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Rene K. Carter
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Gianni N. Bonnici
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Steven F. Maier
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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Michael V. Baratta
Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, Colorado, 80301, USA
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  • ORCID record for Michael V. Baratta
  • For correspondence: michael.baratta@colorado.edu
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Abstract

Dominance status has extensive effects on physical and mental health, and an individual’s relative position can be shaped by experiential factors. A variety of considerations suggest that the experience of behavioral control over stressors should produce winning in dominance tests and that winning should blunt the impact of later stressors, as does prior control. To investigate the interplay between competitive success and stressor control, we first examined the impact of stressor controllability on subsequent performance in a warm spot competition test modified for rats. Prior experience of controllable, but not physically identical uncontrollable, stress increased later effortful behavior and occupation of the warm spot. Controllable stress subjects consistently ranked higher than did uncontrollable stress subjects. Pharmacological inactivation of the prelimbic (PL) cortex during behavioral control prevented later facilitation of dominance. Next, we explored whether repeated winning experiences produced later resistance against the typical sequelae of uncontrollable stress. To establish dominance status, triads of rats were given five sessions of warm spot competition. Reversible inactivation of the PL or NMDA receptor blockade in the dorsomedial striatum led to a long-term reduction in social rank. Stable dominance blunted the later stress-induced increase in dorsal raphe nucleus serotonergic activity, as well as prevented stress-induced social avoidance. In contrast, endocrine and neuroimmune responses to uncontrollable stress were unaffected, indicating a selective impact of prior dominance. Together, these data demonstrate that instrumental control over stress promotes later dominance, but also reveal that winning experiences buffer against the neural and behavioral outcomes of future adversity.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 07, 2023.
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Prior experience with behavioral control over stress facilitates social dominance
Philip T. Coleman, Gabriel W. Costanza-Chavez, Heather N. Martin, Jose Amat, Matthew G. Frank, Rory J. Sanchez, Garrett J. Potter, Simone M. Mellert, Rene K. Carter, Gianni N. Bonnici, Steven F. Maier, Michael V. Baratta
bioRxiv 2023.06.06.543982; doi: https://doi.org/10.1101/2023.06.06.543982
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Prior experience with behavioral control over stress facilitates social dominance
Philip T. Coleman, Gabriel W. Costanza-Chavez, Heather N. Martin, Jose Amat, Matthew G. Frank, Rory J. Sanchez, Garrett J. Potter, Simone M. Mellert, Rene K. Carter, Gianni N. Bonnici, Steven F. Maier, Michael V. Baratta
bioRxiv 2023.06.06.543982; doi: https://doi.org/10.1101/2023.06.06.543982

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