Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses
A more complete understanding of how fear extinction alters neuronal activity and connectivity within fear circuits may aid in the development of strategies to treat human fear disorders. Using a c-fos-based transgenic mouse, we found that contextual fear extinction silenced basal amygdala (BA) exci...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2013-11, Vol.80 (4), p.1054-1065 |
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| creator | Trouche, Stéphanie Sasaki, Jennifer M. Tu, Tiffany Reijmers, Leon G. |
| description | A more complete understanding of how fear extinction alters neuronal activity and connectivity within fear circuits may aid in the development of strategies to treat human fear disorders. Using a c-fos-based transgenic mouse, we found that contextual fear extinction silenced basal amygdala (BA) excitatory neurons that had been previously activated during fear conditioning. We hypothesized that the silencing of BA fear neurons was caused by an action of extinction on BA inhibitory synapses. In support of this hypothesis, we found extinction-induced target-specific remodeling of BA perisomatic inhibitory synapses originating from parvalbumin and cholecystokinin-positive interneurons. Interestingly, the predicted changes in the balance of perisomatic inhibition matched the silent and active states of the target BA fear neurons. These observations suggest that target-specific changes in perisomatic inhibitory synapses represent a mechanism through which experience can sculpt the activation patterns within a neural circuit.
•Contextual fear extinction silences basal amygdala fear neurons•Perisomatic parvalbumin around silent fear neurons is increased after extinction•Perisomatic CB1 receptors around active fear neurons are increased after extinction•Behavior can cause target-specific remodeling of perisomatic inhibitory synapses
Fear extinction silences fear neurons in the basal amygdala. Trouche et al. show that contextual fear extinction causes changes in perisomatic inhibitory synapses around basal amygdala fear neurons and that these changes match the activation state of the fear neurons. |
| doi_str_mv | 10.1016/j.neuron.2013.07.047 |
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•Contextual fear extinction silences basal amygdala fear neurons•Perisomatic parvalbumin around silent fear neurons is increased after extinction•Perisomatic CB1 receptors around active fear neurons are increased after extinction•Behavior can cause target-specific remodeling of perisomatic inhibitory synapses
Fear extinction silences fear neurons in the basal amygdala. Trouche et al. show that contextual fear extinction causes changes in perisomatic inhibitory synapses around basal amygdala fear neurons and that these changes match the activation state of the fear neurons.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2013.07.047</identifier><identifier>PMID: 24183705</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Amygdala - physiology ; Animals ; Behavior ; Behavior, Animal - physiology ; Cholecystokinin - metabolism ; Electroshock ; Extinction, Psychological - physiology ; Fear - psychology ; Image Processing, Computer-Assisted ; Immunohistochemistry ; Interneurons - physiology ; Learning - physiology ; Limbic System - physiology ; Memory ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Microscopy, Confocal ; Neural Pathways - physiology ; Neurobiology ; Neurons ; Neurons - physiology ; Neurosciences ; Parvalbumins - metabolism ; Proto-Oncogene Proteins c-fos - physiology ; Receptor, Cannabinoid, CB1 - metabolism ; Studies ; Synapses - physiology</subject><ispartof>Neuron (Cambridge, Mass.), 2013-11, Vol.80 (4), p.1054-1065</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Nov 20, 2013</rights><rights>2013 Elsevier Inc. All rights reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c590t-ec0665ebd6ecba10fdf38b0b0f19fe47b40b4624781d1328b351d7abb1a228fb3</citedby><cites>FETCH-LOGICAL-c590t-ec0665ebd6ecba10fdf38b0b0f19fe47b40b4624781d1328b351d7abb1a228fb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2013.07.047$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24183705$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Trouche, Stéphanie</creatorcontrib><creatorcontrib>Sasaki, Jennifer M.</creatorcontrib><creatorcontrib>Tu, Tiffany</creatorcontrib><creatorcontrib>Reijmers, Leon G.</creatorcontrib><title>Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>A more complete understanding of how fear extinction alters neuronal activity and connectivity within fear circuits may aid in the development of strategies to treat human fear disorders. Using a c-fos-based transgenic mouse, we found that contextual fear extinction silenced basal amygdala (BA) excitatory neurons that had been previously activated during fear conditioning. We hypothesized that the silencing of BA fear neurons was caused by an action of extinction on BA inhibitory synapses. In support of this hypothesis, we found extinction-induced target-specific remodeling of BA perisomatic inhibitory synapses originating from parvalbumin and cholecystokinin-positive interneurons. Interestingly, the predicted changes in the balance of perisomatic inhibition matched the silent and active states of the target BA fear neurons. These observations suggest that target-specific changes in perisomatic inhibitory synapses represent a mechanism through which experience can sculpt the activation patterns within a neural circuit.
•Contextual fear extinction silences basal amygdala fear neurons•Perisomatic parvalbumin around silent fear neurons is increased after extinction•Perisomatic CB1 receptors around active fear neurons are increased after extinction•Behavior can cause target-specific remodeling of perisomatic inhibitory synapses
Fear extinction silences fear neurons in the basal amygdala. Trouche et al. show that contextual fear extinction causes changes in perisomatic inhibitory synapses around basal amygdala fear neurons and that these changes match the activation state of the fear neurons.</description><subject>Amygdala - physiology</subject><subject>Animals</subject><subject>Behavior</subject><subject>Behavior, Animal - physiology</subject><subject>Cholecystokinin - metabolism</subject><subject>Electroshock</subject><subject>Extinction, Psychological - physiology</subject><subject>Fear - psychology</subject><subject>Image Processing, Computer-Assisted</subject><subject>Immunohistochemistry</subject><subject>Interneurons - physiology</subject><subject>Learning - physiology</subject><subject>Limbic System - physiology</subject><subject>Memory</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Microscopy, Confocal</subject><subject>Neural Pathways - physiology</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Neurosciences</subject><subject>Parvalbumins - metabolism</subject><subject>Proto-Oncogene Proteins c-fos - physiology</subject><subject>Receptor, Cannabinoid, CB1 - metabolism</subject><subject>Studies</subject><subject>Synapses - physiology</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUFv1DAQhS0EokvhHyAUiQuXhHHi2PEFCa1aqFQJRJezZTuTrVeJvdhJxf57XG1bCgc4-TDfe-N5j5DXFCoKlL_fVR6XGHxVA20qEBUw8YSsKEhRMirlU7KCTvKS16I5IS9S2gFQ1kr6nJzUjHaNgHZFNueoY3H2c3bezi74Yq2XhKnY6LjFubzao3WDs8U3nEKPo_PbIgzFV4wuhUnPeXLhr51xc4iH4urg9T6rX5Jngx4Tvrp7T8n387PN-nN5-eXTxfrjZWlbCXOJFjhv0fQcrdEUhn5oOgMGBioHZMIwMIzXTHS0p03dmaalvdDGUF3X3WCaU_Lh6LtfzIS9RT9HPap9dJOOBxW0U39OvLtW23Cjmo4BCJ4N3t0ZxPBjwTSrySWL46g9hiUp2lIuGDAu_48yTjshM5nRt3-hu7BEn5PIhgxk17TQZoodKRtDShGHh39TULcNq506NqxuG1YgVG44y948vvlBdF_p71AwJ3_jMKpkHXqLvYtoZ9UH9-8NvwDRmLqY</recordid><startdate>20131120</startdate><enddate>20131120</enddate><creator>Trouche, Stéphanie</creator><creator>Sasaki, Jennifer M.</creator><creator>Tu, Tiffany</creator><creator>Reijmers, Leon G.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20131120</creationdate><title>Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses</title><author>Trouche, Stéphanie ; Sasaki, Jennifer M. ; Tu, Tiffany ; Reijmers, Leon G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c590t-ec0665ebd6ecba10fdf38b0b0f19fe47b40b4624781d1328b351d7abb1a228fb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amygdala - physiology</topic><topic>Animals</topic><topic>Behavior</topic><topic>Behavior, Animal - physiology</topic><topic>Cholecystokinin - metabolism</topic><topic>Electroshock</topic><topic>Extinction, Psychological - physiology</topic><topic>Fear - psychology</topic><topic>Image Processing, Computer-Assisted</topic><topic>Immunohistochemistry</topic><topic>Interneurons - physiology</topic><topic>Learning - physiology</topic><topic>Limbic System - physiology</topic><topic>Memory</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Microscopy, Confocal</topic><topic>Neural Pathways - physiology</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Neurosciences</topic><topic>Parvalbumins - metabolism</topic><topic>Proto-Oncogene Proteins c-fos - physiology</topic><topic>Receptor, Cannabinoid, CB1 - metabolism</topic><topic>Studies</topic><topic>Synapses - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Trouche, Stéphanie</creatorcontrib><creatorcontrib>Sasaki, Jennifer M.</creatorcontrib><creatorcontrib>Tu, Tiffany</creatorcontrib><creatorcontrib>Reijmers, Leon G.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Trouche, Stéphanie</au><au>Sasaki, Jennifer M.</au><au>Tu, Tiffany</au><au>Reijmers, Leon G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2013-11-20</date><risdate>2013</risdate><volume>80</volume><issue>4</issue><spage>1054</spage><epage>1065</epage><pages>1054-1065</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>A more complete understanding of how fear extinction alters neuronal activity and connectivity within fear circuits may aid in the development of strategies to treat human fear disorders. Using a c-fos-based transgenic mouse, we found that contextual fear extinction silenced basal amygdala (BA) excitatory neurons that had been previously activated during fear conditioning. We hypothesized that the silencing of BA fear neurons was caused by an action of extinction on BA inhibitory synapses. In support of this hypothesis, we found extinction-induced target-specific remodeling of BA perisomatic inhibitory synapses originating from parvalbumin and cholecystokinin-positive interneurons. Interestingly, the predicted changes in the balance of perisomatic inhibition matched the silent and active states of the target BA fear neurons. These observations suggest that target-specific changes in perisomatic inhibitory synapses represent a mechanism through which experience can sculpt the activation patterns within a neural circuit.
•Contextual fear extinction silences basal amygdala fear neurons•Perisomatic parvalbumin around silent fear neurons is increased after extinction•Perisomatic CB1 receptors around active fear neurons are increased after extinction•Behavior can cause target-specific remodeling of perisomatic inhibitory synapses
Fear extinction silences fear neurons in the basal amygdala. Trouche et al. show that contextual fear extinction causes changes in perisomatic inhibitory synapses around basal amygdala fear neurons and that these changes match the activation state of the fear neurons.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>24183705</pmid><doi>10.1016/j.neuron.2013.07.047</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; Access via ScienceDirect (Elsevier); EZB-FREE-00999 freely available EZB journals |
| subjects | Amygdala - physiology Animals Behavior Behavior, Animal - physiology Cholecystokinin - metabolism Electroshock Extinction, Psychological - physiology Fear - psychology Image Processing, Computer-Assisted Immunohistochemistry Interneurons - physiology Learning - physiology Limbic System - physiology Memory Mice Mice, Inbred C57BL Mice, Transgenic Microscopy, Confocal Neural Pathways - physiology Neurobiology Neurons Neurons - physiology Neurosciences Parvalbumins - metabolism Proto-Oncogene Proteins c-fos - physiology Receptor, Cannabinoid, CB1 - metabolism Studies Synapses - physiology |
| title | Fear Extinction Causes Target-Specific Remodeling of Perisomatic Inhibitory Synapses |
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