Shared neural coding for social hierarchy and reward value in primate amygdala

The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Nature neuroscience 2018-03, Vol.21 (3), p.415-423
Hauptverfasser: Munuera, Jérôme, Rigotti, Mattia, Salzman, C. Daniel
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 423
container_issue 3
container_start_page 415
container_title Nature neuroscience
container_volume 21
creator Munuera, Jérôme
Rigotti, Mattia
Salzman, C. Daniel
description The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. New data reveal that the amygdala—a brain area specialized for emotion—also signals the hierarchical rank of peers in a social group. These neural signals likely mediate appropriate social and emotional behavior in many social settings.
doi_str_mv 10.1038/s41593-018-0082-8
format Article
fullrecord <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6092962</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A574731626</galeid><sourcerecordid>A574731626</sourcerecordid><originalsourceid>FETCH-LOGICAL-c637t-566b187ea0a7a0da9612dc84fc5710fdfe4559a2c0186a7c589d66a82e49a04f3</originalsourceid><addsrcrecordid>eNp1kk1v1DAQhiMEoqXwA7igSFzKIcV2_BFfkKqqQKUKJApna2pPsq4Su9hJYf99vWwpXQTywdbMM69nXk1VvaTkiJK2e5s5FbptCO0aQjrWdI-qfSq4bKhi8nF5E60ayYTcq57lfEUIUaLTT6s9prnQSvL96tPFChK6OuCSYKxtdD4MdR9TnaP1JbLymCDZ1bqG4OqEPyC5-gbGBWsf6uvkJ5ixhmk9OBjhefWkhzHji7v7oPr2_vTrycfm_POHs5Pj88bKVs2NkPKSdgqBgALiQEvKnO14b4WipHc9ciE0MFtGk6Bs6dpJCR1DroHwvj2o3m11r5fLCZ3FMJf2za920tpE8GY3E_zKDPHGSKKZlqwIHN4JpPh9wTybyWeL4wgB45INK15RyhUTBX39F3oVlxTKeIWinOtOyQfUACMaH_pY_rUbUXMsFFctlUwW6ugfVDkOJ29jwN6X-E7Bm52Cwsz4cx5gydmcXXzZZemWtSnmnLC_94MSs1kYs10YU1w1m4UxXal59dDI-4rfG1IAtgVySYUB05_p_696C-0syTg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2014498765</pqid></control><display><type>article</type><title>Shared neural coding for social hierarchy and reward value in primate amygdala</title><source>MEDLINE</source><source>Springer Nature - Complete Springer Journals</source><source>Nature Journals Online</source><creator>Munuera, Jérôme ; Rigotti, Mattia ; Salzman, C. Daniel</creator><creatorcontrib>Munuera, Jérôme ; Rigotti, Mattia ; Salzman, C. Daniel</creatorcontrib><description>The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. New data reveal that the amygdala—a brain area specialized for emotion—also signals the hierarchical rank of peers in a social group. These neural signals likely mediate appropriate social and emotional behavior in many social settings.</description><identifier>ISSN: 1097-6256</identifier><identifier>EISSN: 1546-1726</identifier><identifier>DOI: 10.1038/s41593-018-0082-8</identifier><identifier>PMID: 29459764</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/378/1788 ; 631/378/2645 ; 631/378/2649 ; Amygdala ; Amygdala (Brain) ; Amygdala - physiology ; Analysis ; Animal behavior ; Animal Genetics and Genomics ; Animals ; Behavioral Sciences ; Biological Techniques ; Biomedical and Life Sciences ; Biomedicine ; Brain ; Complex variables ; Conditioning, Operant - physiology ; Fractals ; Hierarchy, Social ; Hypotheses ; Information processing ; Information systems ; Macaca mulatta ; Male ; Neural coding ; Neurobiology ; Neurons ; Neurons - physiology ; Neurophysiology ; Neurosciences ; Photic Stimulation ; Physiological aspects ; Primates ; Reinforcement ; Representations ; Reward ; Social factors ; Social hierarchy ; Stimuli ; Substrates</subject><ispartof>Nature neuroscience, 2018-03, Vol.21 (3), p.415-423</ispartof><rights>The Author(s) 2018</rights><rights>COPYRIGHT 2018 Nature Publishing Group</rights><rights>2018. This work is published under https://creativecommons.org/licenses/by/4.0 (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c637t-566b187ea0a7a0da9612dc84fc5710fdfe4559a2c0186a7c589d66a82e49a04f3</citedby><cites>FETCH-LOGICAL-c637t-566b187ea0a7a0da9612dc84fc5710fdfe4559a2c0186a7c589d66a82e49a04f3</cites><orcidid>0000-0001-6466-2810 ; 0000-0001-9532-8735 ; 0000-0002-7501-5480</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/s41593-018-0082-8$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41593-018-0082-8$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29459764$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Munuera, Jérôme</creatorcontrib><creatorcontrib>Rigotti, Mattia</creatorcontrib><creatorcontrib>Salzman, C. Daniel</creatorcontrib><title>Shared neural coding for social hierarchy and reward value in primate amygdala</title><title>Nature neuroscience</title><addtitle>Nat Neurosci</addtitle><addtitle>Nat Neurosci</addtitle><description>The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. New data reveal that the amygdala—a brain area specialized for emotion—also signals the hierarchical rank of peers in a social group. These neural signals likely mediate appropriate social and emotional behavior in many social settings.</description><subject>631/378/1788</subject><subject>631/378/2645</subject><subject>631/378/2649</subject><subject>Amygdala</subject><subject>Amygdala (Brain)</subject><subject>Amygdala - physiology</subject><subject>Analysis</subject><subject>Animal behavior</subject><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Behavioral Sciences</subject><subject>Biological Techniques</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Complex variables</subject><subject>Conditioning, Operant - physiology</subject><subject>Fractals</subject><subject>Hierarchy, Social</subject><subject>Hypotheses</subject><subject>Information processing</subject><subject>Information systems</subject><subject>Macaca mulatta</subject><subject>Male</subject><subject>Neural coding</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Neurophysiology</subject><subject>Neurosciences</subject><subject>Photic Stimulation</subject><subject>Physiological aspects</subject><subject>Primates</subject><subject>Reinforcement</subject><subject>Representations</subject><subject>Reward</subject><subject>Social factors</subject><subject>Social hierarchy</subject><subject>Stimuli</subject><subject>Substrates</subject><issn>1097-6256</issn><issn>1546-1726</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kk1v1DAQhiMEoqXwA7igSFzKIcV2_BFfkKqqQKUKJApna2pPsq4Su9hJYf99vWwpXQTywdbMM69nXk1VvaTkiJK2e5s5FbptCO0aQjrWdI-qfSq4bKhi8nF5E60ayYTcq57lfEUIUaLTT6s9prnQSvL96tPFChK6OuCSYKxtdD4MdR9TnaP1JbLymCDZ1bqG4OqEPyC5-gbGBWsf6uvkJ5ixhmk9OBjhefWkhzHji7v7oPr2_vTrycfm_POHs5Pj88bKVs2NkPKSdgqBgALiQEvKnO14b4WipHc9ciE0MFtGk6Bs6dpJCR1DroHwvj2o3m11r5fLCZ3FMJf2za920tpE8GY3E_zKDPHGSKKZlqwIHN4JpPh9wTybyWeL4wgB45INK15RyhUTBX39F3oVlxTKeIWinOtOyQfUACMaH_pY_rUbUXMsFFctlUwW6ugfVDkOJ29jwN6X-E7Bm52Cwsz4cx5gydmcXXzZZemWtSnmnLC_94MSs1kYs10YU1w1m4UxXal59dDI-4rfG1IAtgVySYUB05_p_696C-0syTg</recordid><startdate>20180301</startdate><enddate>20180301</enddate><creator>Munuera, Jérôme</creator><creator>Rigotti, Mattia</creator><creator>Salzman, C. Daniel</creator><general>Nature Publishing Group US</general><general>Nature Publishing Group</general><scope>C6C</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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</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>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6466-2810</orcidid><orcidid>https://orcid.org/0000-0001-9532-8735</orcidid><orcidid>https://orcid.org/0000-0002-7501-5480</orcidid></search><sort><creationdate>20180301</creationdate><title>Shared neural coding for social hierarchy and reward value in primate amygdala</title><author>Munuera, Jérôme ; Rigotti, Mattia ; Salzman, C. Daniel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c637t-566b187ea0a7a0da9612dc84fc5710fdfe4559a2c0186a7c589d66a82e49a04f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>631/378/1788</topic><topic>631/378/2645</topic><topic>631/378/2649</topic><topic>Amygdala</topic><topic>Amygdala (Brain)</topic><topic>Amygdala - physiology</topic><topic>Analysis</topic><topic>Animal behavior</topic><topic>Animal Genetics and Genomics</topic><topic>Animals</topic><topic>Behavioral Sciences</topic><topic>Biological Techniques</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Brain</topic><topic>Complex variables</topic><topic>Conditioning, Operant - physiology</topic><topic>Fractals</topic><topic>Hierarchy, Social</topic><topic>Hypotheses</topic><topic>Information processing</topic><topic>Information systems</topic><topic>Macaca mulatta</topic><topic>Male</topic><topic>Neural coding</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Neurophysiology</topic><topic>Neurosciences</topic><topic>Photic Stimulation</topic><topic>Physiological aspects</topic><topic>Primates</topic><topic>Reinforcement</topic><topic>Representations</topic><topic>Reward</topic><topic>Social factors</topic><topic>Social hierarchy</topic><topic>Stimuli</topic><topic>Substrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Munuera, Jérôme</creatorcontrib><creatorcontrib>Rigotti, Mattia</creatorcontrib><creatorcontrib>Salzman, C. Daniel</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health &amp; 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>Technology Research Database</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>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Psychology</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Munuera, Jérôme</au><au>Rigotti, Mattia</au><au>Salzman, C. Daniel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Shared neural coding for social hierarchy and reward value in primate amygdala</atitle><jtitle>Nature neuroscience</jtitle><stitle>Nat Neurosci</stitle><addtitle>Nat Neurosci</addtitle><date>2018-03-01</date><risdate>2018</risdate><volume>21</volume><issue>3</issue><spage>415</spage><epage>423</epage><pages>415-423</pages><issn>1097-6256</issn><eissn>1546-1726</eissn><abstract>The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. New data reveal that the amygdala—a brain area specialized for emotion—also signals the hierarchical rank of peers in a social group. These neural signals likely mediate appropriate social and emotional behavior in many social settings.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>29459764</pmid><doi>10.1038/s41593-018-0082-8</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-6466-2810</orcidid><orcidid>https://orcid.org/0000-0001-9532-8735</orcidid><orcidid>https://orcid.org/0000-0002-7501-5480</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1097-6256
ispartof Nature neuroscience, 2018-03, Vol.21 (3), p.415-423
issn 1097-6256
1546-1726
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6092962
source MEDLINE; Springer Nature - Complete Springer Journals; Nature Journals Online
subjects 631/378/1788
631/378/2645
631/378/2649
Amygdala
Amygdala (Brain)
Amygdala - physiology
Analysis
Animal behavior
Animal Genetics and Genomics
Animals
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain
Complex variables
Conditioning, Operant - physiology
Fractals
Hierarchy, Social
Hypotheses
Information processing
Information systems
Macaca mulatta
Male
Neural coding
Neurobiology
Neurons
Neurons - physiology
Neurophysiology
Neurosciences
Photic Stimulation
Physiological aspects
Primates
Reinforcement
Representations
Reward
Social factors
Social hierarchy
Stimuli
Substrates
title Shared neural coding for social hierarchy and reward value in primate amygdala
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-20T02%3A19%3A32IST&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=Shared%20neural%20coding%20for%20social%20hierarchy%20and%20reward%20value%20in%20primate%20amygdala&rft.jtitle=Nature%20neuroscience&rft.au=Munuera,%20J%C3%A9r%C3%B4me&rft.date=2018-03-01&rft.volume=21&rft.issue=3&rft.spage=415&rft.epage=423&rft.pages=415-423&rft.issn=1097-6256&rft.eissn=1546-1726&rft_id=info:doi/10.1038/s41593-018-0082-8&rft_dat=%3Cgale_pubme%3EA574731626%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=2014498765&rft_id=info:pmid/29459764&rft_galeid=A574731626&rfr_iscdi=true