Neural control of affiliative touch in prosocial interaction
The ability to help and care for others fosters social cohesiveness and is vital to the physical and emotional well-being of social species, including humans 1 – 3 . Affiliative social touch, such as allogrooming (grooming behaviour directed towards another individual), is a major type of prosocial...
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creator | Wu, Ye Emily Dang, James Kingsbury, Lyle Zhang, Mingmin Sun, Fangmiao Hu, Rongfeng K. Hong, Weizhe |
description | The ability to help and care for others fosters social cohesiveness and is vital to the physical and emotional well-being of social species, including humans
1
–
3
. Affiliative social touch, such as allogrooming (grooming behaviour directed towards another individual), is a major type of prosocial behaviour that provides comfort to others
1
–
6
. Affiliative touch serves to establish and strengthen social bonds between animals and can help to console distressed conspecifics. However, the neural circuits that promote prosocial affiliative touch have remained unclear. Here we show that mice exhibit affiliative allogrooming behaviour towards distressed partners, providing a consoling effect. The increase in allogrooming occurs in response to different types of stressors and can be elicited by olfactory cues from distressed individuals. Using microendoscopic calcium imaging, we find that neural activity in the medial amygdala (MeA) responds differentially to naive and distressed conspecifics and encodes allogrooming behaviour. Through intersectional functional manipulations, we establish a direct causal role of the MeA in controlling affiliative allogrooming and identify a select, tachykinin-expressing subpopulation of MeA GABAergic (γ-aminobutyric-acid-expressing) neurons that promote this behaviour through their projections to the medial preoptic area. Together, our study demonstrates that mice display prosocial comforting behaviour and reveals a neural circuit mechanism that underlies the encoding and control of affiliative touch during prosocial interactions.
Neurons in the medial amygdala regulate prosocial comforting behaviour towards distressed social partners in mice. |
doi_str_mv | 10.1038/s41586-021-03962-w |
format | Article |
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1
–
3
. Affiliative social touch, such as allogrooming (grooming behaviour directed towards another individual), is a major type of prosocial behaviour that provides comfort to others
1
–
6
. Affiliative touch serves to establish and strengthen social bonds between animals and can help to console distressed conspecifics. However, the neural circuits that promote prosocial affiliative touch have remained unclear. Here we show that mice exhibit affiliative allogrooming behaviour towards distressed partners, providing a consoling effect. The increase in allogrooming occurs in response to different types of stressors and can be elicited by olfactory cues from distressed individuals. Using microendoscopic calcium imaging, we find that neural activity in the medial amygdala (MeA) responds differentially to naive and distressed conspecifics and encodes allogrooming behaviour. Through intersectional functional manipulations, we establish a direct causal role of the MeA in controlling affiliative allogrooming and identify a select, tachykinin-expressing subpopulation of MeA GABAergic (γ-aminobutyric-acid-expressing) neurons that promote this behaviour through their projections to the medial preoptic area. Together, our study demonstrates that mice display prosocial comforting behaviour and reveals a neural circuit mechanism that underlies the encoding and control of affiliative touch during prosocial interactions.
Neurons in the medial amygdala regulate prosocial comforting behaviour towards distressed social partners in mice.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-021-03962-w</identifier><identifier>PMID: 34646019</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378/3919 ; 631/378/3920 ; 64/60 ; Amygdala ; Amygdala (Brain) ; Amygdala - cytology ; Amygdala - physiology ; Animals ; Behavior ; Bonding strength ; Calcium imaging ; Circuits ; Conspecifics ; Cooperative Behavior ; Emotions ; Female ; Grooming ; Helping behavior ; Humanities and Social Sciences ; Male ; Mice ; multidisciplinary ; Neural networks ; Neural Pathways ; Neurological research ; Neurons ; Neurons - physiology ; Olfactory pathways ; Olfactory stimuli ; Physiological aspects ; Preoptic area ; Preoptic area (medial) ; Preoptic Area - cytology ; Preoptic Area - physiology ; Science ; Science (multidisciplinary) ; Social Behavior ; Social bonds ; Stress ; Stress, Psychological - prevention & control ; Stress, Psychological - psychology ; Tachykinin ; Tachykinin receptors ; Tactile stimuli ; Touch - physiology ; Well being ; γ-Aminobutyric acid</subject><ispartof>Nature (London), 2021-11, Vol.599 (7884), p.262-267</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2021</rights><rights>2021. The Author(s), under exclusive licence to Springer Nature Limited.</rights><rights>COPYRIGHT 2021 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Nov 11, 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c706t-88a3dbe5c7208df858630f8e0fe1db0a31ebb30258b4f863ca863f637b6e15e83</citedby><cites>FETCH-LOGICAL-c706t-88a3dbe5c7208df858630f8e0fe1db0a31ebb30258b4f863ca863f637b6e15e83</cites><orcidid>0000-0003-1523-8575 ; 0000-0001-8052-1073</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-021-03962-w$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-021-03962-w$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,778,782,883,27911,27912,41475,42544,51306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34646019$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Ye Emily</creatorcontrib><creatorcontrib>Dang, James</creatorcontrib><creatorcontrib>Kingsbury, Lyle</creatorcontrib><creatorcontrib>Zhang, Mingmin</creatorcontrib><creatorcontrib>Sun, Fangmiao</creatorcontrib><creatorcontrib>Hu, Rongfeng K.</creatorcontrib><creatorcontrib>Hong, Weizhe</creatorcontrib><title>Neural control of affiliative touch in prosocial interaction</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>The ability to help and care for others fosters social cohesiveness and is vital to the physical and emotional well-being of social species, including humans
1
–
3
. Affiliative social touch, such as allogrooming (grooming behaviour directed towards another individual), is a major type of prosocial behaviour that provides comfort to others
1
–
6
. Affiliative touch serves to establish and strengthen social bonds between animals and can help to console distressed conspecifics. However, the neural circuits that promote prosocial affiliative touch have remained unclear. Here we show that mice exhibit affiliative allogrooming behaviour towards distressed partners, providing a consoling effect. The increase in allogrooming occurs in response to different types of stressors and can be elicited by olfactory cues from distressed individuals. Using microendoscopic calcium imaging, we find that neural activity in the medial amygdala (MeA) responds differentially to naive and distressed conspecifics and encodes allogrooming behaviour. Through intersectional functional manipulations, we establish a direct causal role of the MeA in controlling affiliative allogrooming and identify a select, tachykinin-expressing subpopulation of MeA GABAergic (γ-aminobutyric-acid-expressing) neurons that promote this behaviour through their projections to the medial preoptic area. Together, our study demonstrates that mice display prosocial comforting behaviour and reveals a neural circuit mechanism that underlies the encoding and control of affiliative touch during prosocial interactions.
Neurons in the medial amygdala regulate prosocial comforting behaviour towards distressed social partners in mice.</description><subject>631/378/3919</subject><subject>631/378/3920</subject><subject>64/60</subject><subject>Amygdala</subject><subject>Amygdala (Brain)</subject><subject>Amygdala - cytology</subject><subject>Amygdala - physiology</subject><subject>Animals</subject><subject>Behavior</subject><subject>Bonding strength</subject><subject>Calcium imaging</subject><subject>Circuits</subject><subject>Conspecifics</subject><subject>Cooperative Behavior</subject><subject>Emotions</subject><subject>Female</subject><subject>Grooming</subject><subject>Helping behavior</subject><subject>Humanities and Social Sciences</subject><subject>Male</subject><subject>Mice</subject><subject>multidisciplinary</subject><subject>Neural networks</subject><subject>Neural Pathways</subject><subject>Neurological research</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Olfactory pathways</subject><subject>Olfactory stimuli</subject><subject>Physiological aspects</subject><subject>Preoptic area</subject><subject>Preoptic area (medial)</subject><subject>Preoptic Area - cytology</subject><subject>Preoptic Area - physiology</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Social Behavior</subject><subject>Social bonds</subject><subject>Stress</subject><subject>Stress, Psychological - prevention & control</subject><subject>Stress, Psychological - psychology</subject><subject>Tachykinin</subject><subject>Tachykinin receptors</subject><subject>Tactile stimuli</subject><subject>Touch - physiology</subject><subject>Well being</subject><subject>γ-Aminobutyric acid</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9kk1r3DAQhkVpabZp_0APxbSX9uBkZNmSDKEQQj8CoYF-nIUsjxwFr7SR7KT999V20yRbliKQDvPMO6OZl5CXFA4oMHmYatpIXkJFS2Atr8qbR2RBa8HLmkvxmCwAKlmCZHyPPEvpEgAaKuqnZI_VvOZA2wU5-oJz1GNhgp9iGItgC22tG52e3DUWU5jNReF8sYohBeMy6fyEUZvJBf-cPLF6TPji9t0nPz5--H7yuTw7_3R6cnxWGgF8KqXUrO-wMaIC2VuZm2ZgJYJF2negGcWuY1A1sqttjhmdL8uZ6DjSBiXbJ-83uqu5W2JvMPeqR7WKbqnjLxW0U9sR7y7UEK6V5NDwqs4Cb28FYriaMU1q6ZLBcdQew5xULl1RkIJDRt_8g16GOfr8vUy1oqmY4OKeGvSIynkbcl2zFlXHXNK2lSDbTJU7qAF9HuAYPOY54zb_egdvVu5KPYQOdkD59Lh0Zqfqu62E9arx5zToOSV1-u3rNlttWJP3nSLauyFTUGvTqY3pVDad-mM6dZOTXj1cz13KX5dlgG2AlEN-wHg_0__I_gZ-pt-e</recordid><startdate>20211111</startdate><enddate>20211111</enddate><creator>Wu, Ye Emily</creator><creator>Dang, James</creator><creator>Kingsbury, Lyle</creator><creator>Zhang, Mingmin</creator><creator>Sun, Fangmiao</creator><creator>Hu, Rongfeng K.</creator><creator>Hong, Weizhe</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PCBAR</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>Q9U</scope><scope>R05</scope><scope>RC3</scope><scope>S0X</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1523-8575</orcidid><orcidid>https://orcid.org/0000-0001-8052-1073</orcidid></search><sort><creationdate>20211111</creationdate><title>Neural control of affiliative touch in prosocial interaction</title><author>Wu, Ye Emily ; Dang, James ; Kingsbury, Lyle ; Zhang, Mingmin ; Sun, Fangmiao ; Hu, Rongfeng K. ; Hong, Weizhe</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c706t-88a3dbe5c7208df858630f8e0fe1db0a31ebb30258b4f863ca863f637b6e15e83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>631/378/3919</topic><topic>631/378/3920</topic><topic>64/60</topic><topic>Amygdala</topic><topic>Amygdala (Brain)</topic><topic>Amygdala - cytology</topic><topic>Amygdala - physiology</topic><topic>Animals</topic><topic>Behavior</topic><topic>Bonding strength</topic><topic>Calcium imaging</topic><topic>Circuits</topic><topic>Conspecifics</topic><topic>Cooperative Behavior</topic><topic>Emotions</topic><topic>Female</topic><topic>Grooming</topic><topic>Helping behavior</topic><topic>Humanities and Social Sciences</topic><topic>Male</topic><topic>Mice</topic><topic>multidisciplinary</topic><topic>Neural networks</topic><topic>Neural Pathways</topic><topic>Neurological research</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Olfactory pathways</topic><topic>Olfactory stimuli</topic><topic>Physiological aspects</topic><topic>Preoptic area</topic><topic>Preoptic area (medial)</topic><topic>Preoptic Area - cytology</topic><topic>Preoptic Area - physiology</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Social Behavior</topic><topic>Social bonds</topic><topic>Stress</topic><topic>Stress, Psychological - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Ye Emily</au><au>Dang, James</au><au>Kingsbury, Lyle</au><au>Zhang, Mingmin</au><au>Sun, Fangmiao</au><au>Hu, Rongfeng K.</au><au>Hong, Weizhe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural control of affiliative touch in prosocial interaction</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2021-11-11</date><risdate>2021</risdate><volume>599</volume><issue>7884</issue><spage>262</spage><epage>267</epage><pages>262-267</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>The ability to help and care for others fosters social cohesiveness and is vital to the physical and emotional well-being of social species, including humans
1
–
3
. Affiliative social touch, such as allogrooming (grooming behaviour directed towards another individual), is a major type of prosocial behaviour that provides comfort to others
1
–
6
. Affiliative touch serves to establish and strengthen social bonds between animals and can help to console distressed conspecifics. However, the neural circuits that promote prosocial affiliative touch have remained unclear. Here we show that mice exhibit affiliative allogrooming behaviour towards distressed partners, providing a consoling effect. The increase in allogrooming occurs in response to different types of stressors and can be elicited by olfactory cues from distressed individuals. Using microendoscopic calcium imaging, we find that neural activity in the medial amygdala (MeA) responds differentially to naive and distressed conspecifics and encodes allogrooming behaviour. Through intersectional functional manipulations, we establish a direct causal role of the MeA in controlling affiliative allogrooming and identify a select, tachykinin-expressing subpopulation of MeA GABAergic (γ-aminobutyric-acid-expressing) neurons that promote this behaviour through their projections to the medial preoptic area. Together, our study demonstrates that mice display prosocial comforting behaviour and reveals a neural circuit mechanism that underlies the encoding and control of affiliative touch during prosocial interactions.
Neurons in the medial amygdala regulate prosocial comforting behaviour towards distressed social partners in mice.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>34646019</pmid><doi>10.1038/s41586-021-03962-w</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0003-1523-8575</orcidid><orcidid>https://orcid.org/0000-0001-8052-1073</orcidid><oa>free_for_read</oa></addata></record> |
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ispartof | Nature (London), 2021-11, Vol.599 (7884), p.262-267 |
issn | 0028-0836 1476-4687 |
language | eng |
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source | MEDLINE; Nature; Springer Nature - Complete Springer Journals |
subjects | 631/378/3919 631/378/3920 64/60 Amygdala Amygdala (Brain) Amygdala - cytology Amygdala - physiology Animals Behavior Bonding strength Calcium imaging Circuits Conspecifics Cooperative Behavior Emotions Female Grooming Helping behavior Humanities and Social Sciences Male Mice multidisciplinary Neural networks Neural Pathways Neurological research Neurons Neurons - physiology Olfactory pathways Olfactory stimuli Physiological aspects Preoptic area Preoptic area (medial) Preoptic Area - cytology Preoptic Area - physiology Science Science (multidisciplinary) Social Behavior Social bonds Stress Stress, Psychological - prevention & control Stress, Psychological - psychology Tachykinin Tachykinin receptors Tactile stimuli Touch - physiology Well being γ-Aminobutyric acid |
title | Neural control of affiliative touch in prosocial interaction |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-15T21%3A37%3A14IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Neural%20control%20of%20affiliative%20touch%20in%20prosocial%20interaction&rft.jtitle=Nature%20(London)&rft.au=Wu,%20Ye%20Emily&rft.date=2021-11-11&rft.volume=599&rft.issue=7884&rft.spage=262&rft.epage=267&rft.pages=262-267&rft.issn=0028-0836&rft.eissn=1476-4687&rft_id=info:doi/10.1038/s41586-021-03962-w&rft_dat=%3Cgale_pubme%3EA681998089%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2597523767&rft_id=info:pmid/34646019&rft_galeid=A681998089&rfr_iscdi=true |