A Subpopulation of Amygdala Neurons Mediates the Affective Component of Itch
Itch consists of both sensory and affective components. For chronic itch patients, the affective component of itch affects both quality of life (leading to psychological comorbidities) and disease prognosis (by promoting scratching of itchy skin). We found that acute itch stimuli, such as histamine,...
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Veröffentlicht in: | The Journal of neuroscience 2019-04, Vol.39 (17), p.3345-3356 |
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description | Itch consists of both sensory and affective components. For chronic itch patients, the affective component of itch affects both quality of life (leading to psychological comorbidities) and disease prognosis (by promoting scratching of itchy skin). We found that acute itch stimuli, such as histamine, induced anxiety-like behavior and increased activity (c-Fos expression) in the amygdala in adult male C57BL/6 mice. Itch stimuli also increased activity in projection areas to the amygdala, suggesting that these regions form a circuit for affective itch processing. Electrophysiological characterization of histamine-responsive amygdala neurons showed that this population was active on a behaviorally relevant timescale and partially overlapped with pain signaling. Selective optogenetic activation of histamine-responsive amygdala neurons in adult male and female Fos:CreER
;R26
mice using the Targeted Recombination in Active Populations system enhanced both scratching and anxiety-like behavior. These results highlight the importance of itch-responsive amygdala neurons in modulating itch-related affect and behavior.
The sensation of itch includes an affective component that leads to stress and anxiety in chronic itch patients. We investigated the neuronal basis of affective itch in mice, with a focus on the amygdala, the key brain region for the generation of anxiety. A subpopulation of amygdala neurons responded to itch stimuli such as histamine. Optogenetic activation of histamine-responsive amygdala neurons affected both scratching and anxiety-like behavior. Therefore, this population appears to be important for mediating the affective component of itch. |
doi_str_mv | 10.1523/JNEUROSCI.2759-18.2019 |
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;R26
mice using the Targeted Recombination in Active Populations system enhanced both scratching and anxiety-like behavior. These results highlight the importance of itch-responsive amygdala neurons in modulating itch-related affect and behavior.
The sensation of itch includes an affective component that leads to stress and anxiety in chronic itch patients. We investigated the neuronal basis of affective itch in mice, with a focus on the amygdala, the key brain region for the generation of anxiety. A subpopulation of amygdala neurons responded to itch stimuli such as histamine. Optogenetic activation of histamine-responsive amygdala neurons affected both scratching and anxiety-like behavior. Therefore, this population appears to be important for mediating the affective component of itch.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.2759-18.2019</identifier><identifier>PMID: 30819800</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Amygdala ; Amygdala - drug effects ; Amygdala - physiopathology ; Animals ; Anxiety ; Avoidance Learning - physiology ; c-Fos protein ; Chloroquine - pharmacology ; Female ; Histamine ; Histamine - pharmacology ; Male ; Mice ; Mice, Inbred C57BL ; Neurons ; Neurons - drug effects ; Neurons - physiology ; Optogenetics ; Pain ; Pruritus - physiopathology ; Quality of life ; Recombination ; Scratching ; Serotonin - pharmacology ; Stimuli</subject><ispartof>The Journal of neuroscience, 2019-04, Vol.39 (17), p.3345-3356</ispartof><rights>Copyright © 2019 the authors.</rights><rights>Copyright Society for Neuroscience Apr 24, 2019</rights><rights>Copyright © 2019 the authors 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c561t-144b2cd04131a29b9f9ee74bdb1002cd726a50687d37c278204f8a51e31d9ec63</citedby><cites>FETCH-LOGICAL-c561t-144b2cd04131a29b9f9ee74bdb1002cd726a50687d37c278204f8a51e31d9ec63</cites><orcidid>0000-0001-7155-4228 ; 0000-0001-6779-5598 ; 0000-0002-9326-427X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788830/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788830/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,724,777,781,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30819800$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sanders, Kristen M</creatorcontrib><creatorcontrib>Sakai, Kent</creatorcontrib><creatorcontrib>Henry, Tyler D</creatorcontrib><creatorcontrib>Hashimoto, Takashi</creatorcontrib><creatorcontrib>Akiyama, Tasuku</creatorcontrib><title>A Subpopulation of Amygdala Neurons Mediates the Affective Component of Itch</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Itch consists of both sensory and affective components. For chronic itch patients, the affective component of itch affects both quality of life (leading to psychological comorbidities) and disease prognosis (by promoting scratching of itchy skin). We found that acute itch stimuli, such as histamine, induced anxiety-like behavior and increased activity (c-Fos expression) in the amygdala in adult male C57BL/6 mice. Itch stimuli also increased activity in projection areas to the amygdala, suggesting that these regions form a circuit for affective itch processing. Electrophysiological characterization of histamine-responsive amygdala neurons showed that this population was active on a behaviorally relevant timescale and partially overlapped with pain signaling. Selective optogenetic activation of histamine-responsive amygdala neurons in adult male and female Fos:CreER
;R26
mice using the Targeted Recombination in Active Populations system enhanced both scratching and anxiety-like behavior. These results highlight the importance of itch-responsive amygdala neurons in modulating itch-related affect and behavior.
The sensation of itch includes an affective component that leads to stress and anxiety in chronic itch patients. We investigated the neuronal basis of affective itch in mice, with a focus on the amygdala, the key brain region for the generation of anxiety. A subpopulation of amygdala neurons responded to itch stimuli such as histamine. Optogenetic activation of histamine-responsive amygdala neurons affected both scratching and anxiety-like behavior. Therefore, this population appears to be important for mediating the affective component of itch.</description><subject>Amygdala</subject><subject>Amygdala - drug effects</subject><subject>Amygdala - physiopathology</subject><subject>Animals</subject><subject>Anxiety</subject><subject>Avoidance Learning - physiology</subject><subject>c-Fos protein</subject><subject>Chloroquine - pharmacology</subject><subject>Female</subject><subject>Histamine</subject><subject>Histamine - pharmacology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neurons</subject><subject>Neurons - drug effects</subject><subject>Neurons - physiology</subject><subject>Optogenetics</subject><subject>Pain</subject><subject>Pruritus - physiopathology</subject><subject>Quality of life</subject><subject>Recombination</subject><subject>Scratching</subject><subject>Serotonin - pharmacology</subject><subject>Stimuli</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1P3DAQhq2Kqmxp_wKKxIVLtjN2EtsXpNWKj60WkEo5W44zYYOSOMQJEv-eRNAV5TSH92Nm9DB2jLDElItfv2_O7__c3q03Sy5THaNackD9hS0mVcc8ATxgC-AS4iyRySH7HsIjAEhA-Y0dClCoFcCCbVfR3Zh3vhtrO1S-jXwZrZqXh8LWNrqhsfdtiK6pqOxAIRp2FK3KktxQPVO09k3nW2qHObQZ3O4H-1raOtDP93nE7i_O_66v4u3t5Wa92sYuzXCIMUly7gpIUKDlOtelJpJJXuQIMAmSZzaFTMlCSMel4pCUyqZIAgtNLhNH7Oyttxvzhgo3ndDb2nR91dj-xXhbmf-VttqZB_9sMqmUEjAVnL4X9P5ppDCYpgqO6tq25MdgOCqZCshw3nXyyfrox76d3jOcc-QCQePkyt5crvch9FTuj0EwMzCzB2ZmYAaVmYFNweOPr-xj_wiJV-eCkfA</recordid><startdate>20190424</startdate><enddate>20190424</enddate><creator>Sanders, Kristen M</creator><creator>Sakai, Kent</creator><creator>Henry, Tyler D</creator><creator>Hashimoto, Takashi</creator><creator>Akiyama, Tasuku</creator><general>Society for Neuroscience</general><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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7155-4228</orcidid><orcidid>https://orcid.org/0000-0001-6779-5598</orcidid><orcidid>https://orcid.org/0000-0002-9326-427X</orcidid></search><sort><creationdate>20190424</creationdate><title>A Subpopulation of Amygdala Neurons Mediates the Affective Component of Itch</title><author>Sanders, Kristen M ; Sakai, Kent ; Henry, Tyler D ; Hashimoto, Takashi ; Akiyama, Tasuku</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c561t-144b2cd04131a29b9f9ee74bdb1002cd726a50687d37c278204f8a51e31d9ec63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amygdala</topic><topic>Amygdala - drug effects</topic><topic>Amygdala - physiopathology</topic><topic>Animals</topic><topic>Anxiety</topic><topic>Avoidance Learning - physiology</topic><topic>c-Fos protein</topic><topic>Chloroquine - pharmacology</topic><topic>Female</topic><topic>Histamine</topic><topic>Histamine - pharmacology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neurons</topic><topic>Neurons - drug effects</topic><topic>Neurons - physiology</topic><topic>Optogenetics</topic><topic>Pain</topic><topic>Pruritus - physiopathology</topic><topic>Quality of life</topic><topic>Recombination</topic><topic>Scratching</topic><topic>Serotonin - pharmacology</topic><topic>Stimuli</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sanders, Kristen M</creatorcontrib><creatorcontrib>Sakai, Kent</creatorcontrib><creatorcontrib>Henry, Tyler D</creatorcontrib><creatorcontrib>Hashimoto, Takashi</creatorcontrib><creatorcontrib>Akiyama, Tasuku</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sanders, Kristen M</au><au>Sakai, Kent</au><au>Henry, Tyler D</au><au>Hashimoto, Takashi</au><au>Akiyama, Tasuku</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Subpopulation of Amygdala Neurons Mediates the Affective Component of Itch</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2019-04-24</date><risdate>2019</risdate><volume>39</volume><issue>17</issue><spage>3345</spage><epage>3356</epage><pages>3345-3356</pages><issn>0270-6474</issn><issn>1529-2401</issn><eissn>1529-2401</eissn><abstract>Itch consists of both sensory and affective components. For chronic itch patients, the affective component of itch affects both quality of life (leading to psychological comorbidities) and disease prognosis (by promoting scratching of itchy skin). We found that acute itch stimuli, such as histamine, induced anxiety-like behavior and increased activity (c-Fos expression) in the amygdala in adult male C57BL/6 mice. Itch stimuli also increased activity in projection areas to the amygdala, suggesting that these regions form a circuit for affective itch processing. Electrophysiological characterization of histamine-responsive amygdala neurons showed that this population was active on a behaviorally relevant timescale and partially overlapped with pain signaling. Selective optogenetic activation of histamine-responsive amygdala neurons in adult male and female Fos:CreER
;R26
mice using the Targeted Recombination in Active Populations system enhanced both scratching and anxiety-like behavior. These results highlight the importance of itch-responsive amygdala neurons in modulating itch-related affect and behavior.
The sensation of itch includes an affective component that leads to stress and anxiety in chronic itch patients. We investigated the neuronal basis of affective itch in mice, with a focus on the amygdala, the key brain region for the generation of anxiety. A subpopulation of amygdala neurons responded to itch stimuli such as histamine. Optogenetic activation of histamine-responsive amygdala neurons affected both scratching and anxiety-like behavior. Therefore, this population appears to be important for mediating the affective component of itch.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>30819800</pmid><doi>10.1523/JNEUROSCI.2759-18.2019</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7155-4228</orcidid><orcidid>https://orcid.org/0000-0001-6779-5598</orcidid><orcidid>https://orcid.org/0000-0002-9326-427X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amygdala Amygdala - drug effects Amygdala - physiopathology Animals Anxiety Avoidance Learning - physiology c-Fos protein Chloroquine - pharmacology Female Histamine Histamine - pharmacology Male Mice Mice, Inbred C57BL Neurons Neurons - drug effects Neurons - physiology Optogenetics Pain Pruritus - physiopathology Quality of life Recombination Scratching Serotonin - pharmacology Stimuli |
title | A Subpopulation of Amygdala Neurons Mediates the Affective Component of Itch |
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