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Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat

•Mice can be characterized as susceptible or resilient after social defeat.•Paradoxically, resilient mice display enhanced fear expression and poor extinction.•These effects are not due to increased anxiety or poor behavioral flexibility.•Mechanisms of resilience may leave animals vulnerable to mala...

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Published in:Behavioural brain research 2013-11, Vol.256, p.580-590
Main Authors: Meduri, Jeremy D., Farnbauch, Laure A., Jasnow, Aaron M.
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description •Mice can be characterized as susceptible or resilient after social defeat.•Paradoxically, resilient mice display enhanced fear expression and poor extinction.•These effects are not due to increased anxiety or poor behavioral flexibility.•Mechanisms of resilience may leave animals vulnerable to maladaptive fear behavior. The exposure to stress has been associated with increased depressive and anxiety symptoms, yet not all individuals respond negatively to the experience of stress. Recent rodent social defeat models demonstrate similar individual differences in response to social stress. In particular, mice subjected to chronic social defeat have been characterized as being either “susceptible” or “resilient” by the level of social interaction following social defeat. Susceptibility is associated with lasting social avoidance as well as increased anxiety-like behavior, and depressive-like symptoms. Resilient animals, however, do not show social avoidance or increased depressive-like symptoms, but retain increased anxiety-like behavior. Thus, it is unclear what “resilience” as measured by social interaction represents in terms of an overall behavioral and physiological phenotype. Here, we use an acute social defeat procedure, which produces distinct behavioral phenotypes in social interaction with no apparent changes in anxiety-like behavior. Susceptible mice display lasting social avoidance, whereas resilient mice display normal social interaction. Susceptible mice also displayed deficits in fear extinction retention but had normal within-session extinction. Paradoxically, resilience was associated with enhanced fear expression, and severe deficits in fear extinction and extinction retention beyond that observed in susceptible mice. These effects in resilient mice were only apparent after the experience of social stress and were not due to impaired behavioral flexibility. These data suggest that mechanisms controlling resilience to acute social defeat as characterized by social interaction leave animals vulnerable to maladaptive fear behavior.
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The exposure to stress has been associated with increased depressive and anxiety symptoms, yet not all individuals respond negatively to the experience of stress. Recent rodent social defeat models demonstrate similar individual differences in response to social stress. In particular, mice subjected to chronic social defeat have been characterized as being either “susceptible” or “resilient” by the level of social interaction following social defeat. Susceptibility is associated with lasting social avoidance as well as increased anxiety-like behavior, and depressive-like symptoms. Resilient animals, however, do not show social avoidance or increased depressive-like symptoms, but retain increased anxiety-like behavior. Thus, it is unclear what “resilience” as measured by social interaction represents in terms of an overall behavioral and physiological phenotype. Here, we use an acute social defeat procedure, which produces distinct behavioral phenotypes in social interaction with no apparent changes in anxiety-like behavior. Susceptible mice display lasting social avoidance, whereas resilient mice display normal social interaction. Susceptible mice also displayed deficits in fear extinction retention but had normal within-session extinction. Paradoxically, resilience was associated with enhanced fear expression, and severe deficits in fear extinction and extinction retention beyond that observed in susceptible mice. These effects in resilient mice were only apparent after the experience of social stress and were not due to impaired behavioral flexibility. 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Psychophysiology</topic><topic>Resilience</topic><topic>Resilience, Psychological</topic><topic>Social avoidance</topic><topic>Social Behavior</topic><topic>Social Dominance</topic><topic>Stress, Psychological - physiopathology</topic><topic>Susceptibility</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Meduri, Jeremy D.</creatorcontrib><creatorcontrib>Farnbauch, Laure A.</creatorcontrib><creatorcontrib>Jasnow, Aaron M.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Animal Behavior Abstracts</collection><collection>Neurosciences Abstracts</collection><jtitle>Behavioural brain research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meduri, Jeremy D.</au><au>Farnbauch, Laure A.</au><au>Jasnow, Aaron M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat</atitle><jtitle>Behavioural brain research</jtitle><addtitle>Behav Brain Res</addtitle><date>2013-11-01</date><risdate>2013</risdate><volume>256</volume><spage>580</spage><epage>590</epage><pages>580-590</pages><issn>0166-4328</issn><eissn>1872-7549</eissn><coden>BBREDI</coden><abstract>•Mice can be characterized as susceptible or resilient after social defeat.•Paradoxically, resilient mice display enhanced fear expression and poor extinction.•These effects are not due to increased anxiety or poor behavioral flexibility.•Mechanisms of resilience may leave animals vulnerable to maladaptive fear behavior. 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subjects Animals
Behavior, Animal - physiology
Behavioral flexibility
Behavioral psychophysiology
Biological and medical sciences
Extinction, Psychological - physiology
Fear - physiology
Fear learning
Fundamental and applied biological sciences. Psychology
Male
Mice
Mice, Inbred C57BL
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Resilience
Resilience, Psychological
Social avoidance
Social Behavior
Social Dominance
Stress, Psychological - physiopathology
Susceptibility
Vertebrates: nervous system and sense organs
title Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat
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