Neural correlates of conceptual-level fear generalization in posttraumatic stress disorder
Posttraumatic stress disorder (PTSD) may develop when mechanisms for making accurate distinctions about threat relevance have gone awry. Generalization across conceptually related objects has been hypothesized based on clinical observation in PTSD, but the neural mechanisms remain unexplored. Recent...
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| Veröffentlicht in: | Neuropsychopharmacology (New York, N.Y.) N.Y.), 2020-07, Vol.45 (8), p.1380-1389 |
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| creator | Morey, Rajendra A Haswell, Courtney C Stjepanović, Daniel Dunsmoor, Joseph E LaBar, Kevin S |
| description | Posttraumatic stress disorder (PTSD) may develop when mechanisms for making accurate distinctions about threat relevance have gone awry. Generalization across conceptually related objects has been hypothesized based on clinical observation in PTSD, but the neural mechanisms remain unexplored. Recent trauma-exposed military veterans (n = 46) were grouped into PTSD (n = 23) and non-PTSD (n = 23). Participants learned to generalize fear across conceptual categories (animals or tools) of semantically related items that were partially reinforced by shock during functional magnetic resonance imaging. Conditioned fear learning was quantified by shock expectancy and skin conductance response (SCR). Relative to veteran controls, PTSD subjects exhibited a stronger neural response associated with fear generalization to the reinforced object category in the striatum, anterior cingulate cortex, amygdala, occipitotemporal cortex, and insula (Z > 2.3; p |
| doi_str_mv | 10.1038/s41386-020-0661-8 |
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Generalization across conceptually related objects has been hypothesized based on clinical observation in PTSD, but the neural mechanisms remain unexplored. Recent trauma-exposed military veterans (n = 46) were grouped into PTSD (n = 23) and non-PTSD (n = 23). Participants learned to generalize fear across conceptual categories (animals or tools) of semantically related items that were partially reinforced by shock during functional magnetic resonance imaging. Conditioned fear learning was quantified by shock expectancy and skin conductance response (SCR). Relative to veteran controls, PTSD subjects exhibited a stronger neural response associated with fear generalization to the reinforced object category in the striatum, anterior cingulate cortex, amygdala, occipitotemporal cortex, and insula (Z > 2.3; p < 0.05; whole-brain corrected). Based on SCR, both groups generalized the shock contingency to the reinforced conceptual category, but learning was not significantly different between groups. We found that PTSD was associated with an enhanced neural response in fronto-limbic, midline, and occipitotemporal regions to a learned representation of threat that is based on previously established conceptual knowledge of the relationship between basic-level exemplars within a semantic category. Behaviorally, veterans with PTSD were somewhat slower to differentiate threat and safety categories as compared with trauma-exposed veteran controls owing in part to an initial overgeneralized behavioral response to the safe category. 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Generalization across conceptually related objects has been hypothesized based on clinical observation in PTSD, but the neural mechanisms remain unexplored. Recent trauma-exposed military veterans (n = 46) were grouped into PTSD (n = 23) and non-PTSD (n = 23). Participants learned to generalize fear across conceptual categories (animals or tools) of semantically related items that were partially reinforced by shock during functional magnetic resonance imaging. Conditioned fear learning was quantified by shock expectancy and skin conductance response (SCR). Relative to veteran controls, PTSD subjects exhibited a stronger neural response associated with fear generalization to the reinforced object category in the striatum, anterior cingulate cortex, amygdala, occipitotemporal cortex, and insula (Z > 2.3; p < 0.05; whole-brain corrected). Based on SCR, both groups generalized the shock contingency to the reinforced conceptual category, but learning was not significantly different between groups. We found that PTSD was associated with an enhanced neural response in fronto-limbic, midline, and occipitotemporal regions to a learned representation of threat that is based on previously established conceptual knowledge of the relationship between basic-level exemplars within a semantic category. Behaviorally, veterans with PTSD were somewhat slower to differentiate threat and safety categories as compared with trauma-exposed veteran controls owing in part to an initial overgeneralized behavioral response to the safe category. These results have implications for understanding how fear spreads across semantically related concepts in PTSD.</description><subject>Amygdala</subject><subject>Brain mapping</subject><subject>Conductance</subject><subject>Cortex (cingulate)</subject><subject>Expectancy</subject><subject>Fear conditioning</subject><subject>Functional magnetic resonance imaging</subject><subject>Neostriatum</subject><subject>Neuroimaging</subject><subject>Post traumatic stress disorder</subject><subject>Skin conductance response</subject><subject>Trauma</subject><issn>0893-133X</issn><issn>1740-634X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNqFkU1PGzEQhi3UCtLAD-CCVuqFi1t7_X2pVEXQVoraCwfExXLsWVjkrIO9G6n99TgKIOgFz8Gy55lXM_MidErJF0qY_lo4ZVpi0hJMpKRYH6AZVZxgyfj1BzQj2jBMGbs-Qp9KuSeECiX1ITpibT2qFTN08xum7GLjU84Q3QilSV19DR424-QijrCF2HTgcnMLA1S2_-fGPg1NPzSbVMYxu2ldf3xTxgylNKEvKQfIx-hj52KBk6d7jq4uL64WP_Hyz49fi-9L7LkQI-bANSdK0I4YB5StOhqMExCcCp3ycgWK1fBCtNAZIYJixgUVDGe-boHN0be97GZarSF4GGpH0W5yv3b5r02ut28zQ39nb9PWqtYoRU0VOH8SyOlhgjLadV88xOgGSFOxLdOcm7o4VdHP_6H3acpDnc62XEnFmRTvUJQprSXfUXRP-ZxKydC9tEyJ3dlr9_baaq_d2Wt1rTl7PetLxbOf7BHlqKIo</recordid><startdate>20200701</startdate><enddate>20200701</enddate><creator>Morey, Rajendra A</creator><creator>Haswell, Courtney C</creator><creator>Stjepanović, Daniel</creator><creator>Dunsmoor, Joseph E</creator><creator>LaBar, Kevin S</creator><general>Nature Publishing Group</general><general>Springer International Publishing</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5448-6873</orcidid></search><sort><creationdate>20200701</creationdate><title>Neural correlates of conceptual-level fear generalization in posttraumatic stress disorder</title><author>Morey, Rajendra A ; Haswell, Courtney C ; Stjepanović, Daniel ; Dunsmoor, Joseph E ; LaBar, Kevin S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-4e4840751f09ae13bf1d9a5eda7df7c6be73737c552ef955d739ad7d943c1033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amygdala</topic><topic>Brain mapping</topic><topic>Conductance</topic><topic>Cortex (cingulate)</topic><topic>Expectancy</topic><topic>Fear conditioning</topic><topic>Functional magnetic resonance imaging</topic><topic>Neostriatum</topic><topic>Neuroimaging</topic><topic>Post traumatic stress disorder</topic><topic>Skin conductance response</topic><topic>Trauma</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Morey, Rajendra A</creatorcontrib><creatorcontrib>Haswell, Courtney C</creatorcontrib><creatorcontrib>Stjepanović, Daniel</creatorcontrib><creatorcontrib>Dunsmoor, Joseph E</creatorcontrib><creatorcontrib>LaBar, Kevin S</creatorcontrib><creatorcontrib>Mid-Atlantic MIRECC Workgroup</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Psychology</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Morey, Rajendra A</au><au>Haswell, Courtney C</au><au>Stjepanović, Daniel</au><au>Dunsmoor, Joseph E</au><au>LaBar, Kevin S</au><aucorp>Mid-Atlantic MIRECC Workgroup</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural correlates of conceptual-level fear generalization in posttraumatic stress disorder</atitle><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle><addtitle>Neuropsychopharmacology</addtitle><date>2020-07-01</date><risdate>2020</risdate><volume>45</volume><issue>8</issue><spage>1380</spage><epage>1389</epage><pages>1380-1389</pages><issn>0893-133X</issn><eissn>1740-634X</eissn><abstract>Posttraumatic stress disorder (PTSD) may develop when mechanisms for making accurate distinctions about threat relevance have gone awry. Generalization across conceptually related objects has been hypothesized based on clinical observation in PTSD, but the neural mechanisms remain unexplored. Recent trauma-exposed military veterans (n = 46) were grouped into PTSD (n = 23) and non-PTSD (n = 23). Participants learned to generalize fear across conceptual categories (animals or tools) of semantically related items that were partially reinforced by shock during functional magnetic resonance imaging. Conditioned fear learning was quantified by shock expectancy and skin conductance response (SCR). Relative to veteran controls, PTSD subjects exhibited a stronger neural response associated with fear generalization to the reinforced object category in the striatum, anterior cingulate cortex, amygdala, occipitotemporal cortex, and insula (Z > 2.3; p < 0.05; whole-brain corrected). Based on SCR, both groups generalized the shock contingency to the reinforced conceptual category, but learning was not significantly different between groups. We found that PTSD was associated with an enhanced neural response in fronto-limbic, midline, and occipitotemporal regions to a learned representation of threat that is based on previously established conceptual knowledge of the relationship between basic-level exemplars within a semantic category. Behaviorally, veterans with PTSD were somewhat slower to differentiate threat and safety categories as compared with trauma-exposed veteran controls owing in part to an initial overgeneralized behavioral response to the safe category. These results have implications for understanding how fear spreads across semantically related concepts in PTSD.</abstract><cop>England</cop><pub>Nature Publishing Group</pub><pmid>32222725</pmid><doi>10.1038/s41386-020-0661-8</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-5448-6873</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 0893-133X |
| ispartof | Neuropsychopharmacology (New York, N.Y.), 2020-07, Vol.45 (8), p.1380-1389 |
| issn | 0893-133X 1740-634X |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7297719 |
| source | EZB-FREE-00999 freely available EZB journals; PubMed Central; SpringerLink Journals - AutoHoldings |
| subjects | Amygdala Brain mapping Conductance Cortex (cingulate) Expectancy Fear conditioning Functional magnetic resonance imaging Neostriatum Neuroimaging Post traumatic stress disorder Skin conductance response Trauma |
| title | Neural correlates of conceptual-level fear generalization in posttraumatic stress disorder |
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