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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 |
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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. These data suggest that mechanisms controlling resilience to acute social defeat as characterized by social interaction leave animals vulnerable to maladaptive fear behavior.</description><identifier>ISSN: 0166-4328</identifier><identifier>EISSN: 1872-7549</identifier><identifier>DOI: 10.1016/j.bbr.2013.09.009</identifier><identifier>PMID: 24029700</identifier><identifier>CODEN: BBREDI</identifier><language>eng</language><publisher>Shannon: Elsevier B.V</publisher><subject>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</subject><ispartof>Behavioural brain research, 2013-11, Vol.256, p.580-590</ispartof><rights>2013 Elsevier B.V.</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2013 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c459t-bd3cb3d6ccbac6e2aa1c53afc43ec228a67b1a3e3c5d59af935ae1be4eae39473</citedby><cites>FETCH-LOGICAL-c459t-bd3cb3d6ccbac6e2aa1c53afc43ec228a67b1a3e3c5d59af935ae1be4eae39473</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28262990$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24029700$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Meduri, Jeremy D.</creatorcontrib><creatorcontrib>Farnbauch, Laure A.</creatorcontrib><creatorcontrib>Jasnow, Aaron M.</creatorcontrib><title>Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat</title><title>Behavioural brain research</title><addtitle>Behav Brain Res</addtitle><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.</description><subject>Animals</subject><subject>Behavior, Animal - physiology</subject><subject>Behavioral flexibility</subject><subject>Behavioral psychophysiology</subject><subject>Biological and medical sciences</subject><subject>Extinction, Psychological - physiology</subject><subject>Fear - physiology</subject><subject>Fear learning</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Psychology. Psychoanalysis. Psychiatry</subject><subject>Psychology. Psychophysiology</subject><subject>Resilience</subject><subject>Resilience, Psychological</subject><subject>Social avoidance</subject><subject>Social Behavior</subject><subject>Social Dominance</subject><subject>Stress, Psychological - physiopathology</subject><subject>Susceptibility</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0166-4328</issn><issn>1872-7549</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFkUuLFDEUhYM4OO3oD3Aj2QhuqiavegRXMviCAWeh63Dr5hamqUebpGXm30-KbnWnq3DhO4fwHcZeSVFLIdvrfT0MsVZC6lrYWgj7hO1k36mqa4x9ynaFaSujVX_Jnqe0F0IY0chn7FIZoWwnxI7RHUTw631AmDgtP2BBmmnJfB35SBA53R8ipRTWhcPiy5nDgnk7PY0BQ048LHwOSLxwYQpbOK88rRhKZYEI8gt2McKU6OX5vWLfP374dvO5uv366cvN-9sKTWNzNXiNg_Yt4gDYkgKQ2GgY0WhCpXpou0GCJo2NbyyMVjdAciBDQNqaTl-xt6feQ1x_HillN4eENE2w0HpMTrZdqxthOvV_1JheCVvsFVSeUIxrSpFGd4hhhvjgpHDbEG7vyhBuG8IJ68oQJfP6XH8cZvJ_Er_NF-DNGYBU3I-xmA_pL9erVlm7ce9OHBVvvwJFl7A4RvIhEmbn1_CPbzwCH-anwA</recordid><startdate>20131101</startdate><enddate>20131101</enddate><creator>Meduri, Jeremy D.</creator><creator>Farnbauch, Laure A.</creator><creator>Jasnow, Aaron M.</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7QG</scope><scope>7TK</scope></search><sort><creationdate>20131101</creationdate><title>Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat</title><author>Meduri, Jeremy D. ; Farnbauch, Laure A. ; Jasnow, Aaron M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c459t-bd3cb3d6ccbac6e2aa1c53afc43ec228a67b1a3e3c5d59af935ae1be4eae39473</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Behavior, Animal - physiology</topic><topic>Behavioral flexibility</topic><topic>Behavioral psychophysiology</topic><topic>Biological and medical sciences</topic><topic>Extinction, Psychological - physiology</topic><topic>Fear - physiology</topic><topic>Fear learning</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Psychology. Psychoanalysis. Psychiatry</topic><topic>Psychology. 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.
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.</abstract><cop>Shannon</cop><pub>Elsevier B.V</pub><pmid>24029700</pmid><doi>10.1016/j.bbr.2013.09.009</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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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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