Prior experience with behavioral control over stress facilitates social dominance.

Coping Dominance Dorsal raphe nucleus Medial prefrontal cortex Resilience

Journal

Neurobiology of stress
ISSN: 2352-2895
Titre abrégé: Neurobiol Stress
Pays: United States
ID NLM: 101643409

Informations de publication

Date de publication:
Jan 2024
Historique:
received: 13 06 2023
revised: 13 11 2023
accepted: 01 12 2023
medline: 12 1 2024
pubmed: 12 1 2024
entrez: 12 1 2024
Statut: epublish

Résumé

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. The development of stable dominance was prevented by reversible inactivation of the PL or NMDA receptor blockade in the dorsomedial striatum. Stable winning blunted the later stress-induced increase in dorsal raphe nucleus serotonergic activity, as well as prevented uncontrollable 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.

Identifiants

pubmed: 38213318
doi: 10.1016/j.ynstr.2023.100597
pii: S2352-2895(23)00085-1
pmc: PMC10783635
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100597

Informations de copyright

© 2023 The Authors.

Déclaration de conflit d'intérêts

None

Auteurs

Philip T Coleman (PT)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Gabriel W Costanza-Chavez (GW)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Heather N Martin (HN)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Jose Amat (J)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Matthew G Frank (MG)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Rory J Sanchez (RJ)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Garrett J Potter (GJ)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Simone M Mellert (SM)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Rene K Carter (RK)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Gianni N Bonnici (GN)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Steven F Maier (SF)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Michael V Baratta (MV)

Department of Psychology and Neuroscience, Center for Neuroscience, University of Colorado Boulder, Boulder, CO, 80301, USA.

Classifications MeSH