Activity of striatal neurons reflects social action and own reward
Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent i...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2013-10, Vol.110 (41), p.16634-16639 |
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creator | Báez-Mendoza, Raymundo Harris, Christopher J. Schultz, Wolfram |
description | Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific’s reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions. |
doi_str_mv | 10.1073/pnas.1211342110 |
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A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific’s reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1211342110</identifier><identifier>PMID: 24062436</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences</publisher><subject>Acting ; Analysis of Variance ; Animals ; Behavioral neuroscience ; Biological and medical sciences ; Biological Sciences ; Brain ; computers ; Corpus Striatum - cytology ; Discounting ; Discrimination, Psychological - physiology ; Eye movements ; Eye Movements - physiology ; Fundamental and applied biological sciences. Psychology ; humans ; learning ; Linear Models ; Macaca mulatta ; Macaca mulatta - physiology ; Male ; Monkeys & apes ; Neurons ; Neurons - metabolism ; neurophysiology ; Neuropsychology ; Primates ; Reward ; ROC Curve ; Social Behavior ; Social interaction ; Social movements ; Vertebrates: nervous system and sense organs</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-10, Vol.110 (41), p.16634-16639</ispartof><rights>copyright © 1993–2008 National Academy of Sciences of the United States of America</rights><rights>2015 INIST-CNRS</rights><rights>Copyright National Academy of Sciences Oct 8, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c654t-8082ef5d3329eb49a14802c644b3ce791b5a9bcfeadafed654425a8a2e3331a13</citedby><cites>FETCH-LOGICAL-c654t-8082ef5d3329eb49a14802c644b3ce791b5a9bcfeadafed654425a8a2e3331a13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/41.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23749574$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23749574$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27805847$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24062436$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Báez-Mendoza, Raymundo</creatorcontrib><creatorcontrib>Harris, Christopher J.</creatorcontrib><creatorcontrib>Schultz, Wolfram</creatorcontrib><title>Activity of striatal neurons reflects social action and own reward</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific’s reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.</description><subject>Acting</subject><subject>Analysis of Variance</subject><subject>Animals</subject><subject>Behavioral neuroscience</subject><subject>Biological and medical sciences</subject><subject>Biological Sciences</subject><subject>Brain</subject><subject>computers</subject><subject>Corpus Striatum - cytology</subject><subject>Discounting</subject><subject>Discrimination, Psychological - physiology</subject><subject>Eye movements</subject><subject>Eye Movements - physiology</subject><subject>Fundamental and applied biological sciences. 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Psychology</topic><topic>humans</topic><topic>learning</topic><topic>Linear Models</topic><topic>Macaca mulatta</topic><topic>Macaca mulatta - physiology</topic><topic>Male</topic><topic>Monkeys & apes</topic><topic>Neurons</topic><topic>Neurons - metabolism</topic><topic>neurophysiology</topic><topic>Neuropsychology</topic><topic>Primates</topic><topic>Reward</topic><topic>ROC Curve</topic><topic>Social Behavior</topic><topic>Social interaction</topic><topic>Social movements</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Báez-Mendoza, Raymundo</creatorcontrib><creatorcontrib>Harris, Christopher J.</creatorcontrib><creatorcontrib>Schultz, Wolfram</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Báez-Mendoza, Raymundo</au><au>Harris, Christopher J.</au><au>Schultz, Wolfram</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Activity of striatal neurons reflects social action and own reward</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2013-10-08</date><risdate>2013</risdate><volume>110</volume><issue>41</issue><spage>16634</spage><epage>16639</epage><pages>16634-16639</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><coden>PNASA6</coden><abstract>Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific’s reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences</pub><pmid>24062436</pmid><doi>10.1073/pnas.1211342110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acting Analysis of Variance Animals Behavioral neuroscience Biological and medical sciences Biological Sciences Brain computers Corpus Striatum - cytology Discounting Discrimination, Psychological - physiology Eye movements Eye Movements - physiology Fundamental and applied biological sciences. Psychology humans learning Linear Models Macaca mulatta Macaca mulatta - physiology Male Monkeys & apes Neurons Neurons - metabolism neurophysiology Neuropsychology Primates Reward ROC Curve Social Behavior Social interaction Social movements Vertebrates: nervous system and sense organs |
title | Activity of striatal neurons reflects social action and own reward |
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