Evidence that emotion mediates social attention in rhesus macaques
Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual's e...
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description | Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual's emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.
We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.
The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.
These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing. |
doi_str_mv | 10.1371/journal.pone.0044387 |
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We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.
The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.
These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0044387</identifier><identifier>PMID: 22952968</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aggression - physiology ; Animal behavior ; Animals ; Anxiety ; Arousal ; Attention - physiology ; Bias ; Biology ; Cues ; Emotions - physiology ; Enrichment ; Face ; Fixation, Ocular - physiology ; Genotypes ; Health ; Human behavior ; Humans ; Laboratory animals ; Macaca mulatta ; Macaca mulatta - physiology ; Male ; Primates ; Psychological factors ; Science Policy ; Social and Behavioral Sciences ; Social Behavior ; Social interactions ; Studies ; Time Factors ; Veterinary medicine ; Veterinary Science ; Vigilance</subject><ispartof>PloS one, 2012-08, Vol.7 (8), p.e44387</ispartof><rights>Bethell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2012 Bethell et al 2012 Bethell et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-b6f153e07d79a1cafe6fad89008c27f3002b25c819a8e31d96ab2607ef152f7c3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3431396/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3431396/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22952968$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Vitzthum, Virginia J.</contributor><creatorcontrib>Bethell, Emily J</creatorcontrib><creatorcontrib>Holmes, Amanda</creatorcontrib><creatorcontrib>Maclarnon, Ann</creatorcontrib><creatorcontrib>Semple, Stuart</creatorcontrib><title>Evidence that emotion mediates social attention in rhesus macaques</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual's emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.
We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.
The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.
These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.</description><subject>Aggression - physiology</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Anxiety</subject><subject>Arousal</subject><subject>Attention - physiology</subject><subject>Bias</subject><subject>Biology</subject><subject>Cues</subject><subject>Emotions - physiology</subject><subject>Enrichment</subject><subject>Face</subject><subject>Fixation, Ocular - physiology</subject><subject>Genotypes</subject><subject>Health</subject><subject>Human behavior</subject><subject>Humans</subject><subject>Laboratory animals</subject><subject>Macaca mulatta</subject><subject>Macaca mulatta - physiology</subject><subject>Male</subject><subject>Primates</subject><subject>Psychological factors</subject><subject>Science Policy</subject><subject>Social and Behavioral Sciences</subject><subject>Social Behavior</subject><subject>Social interactions</subject><subject>Studies</subject><subject>Time Factors</subject><subject>Veterinary medicine</subject><subject>Veterinary Science</subject><subject>Vigilance</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNp1UUtP3DAQtioQUOAfVBCp5138iB37gkQRLUhIvZSzNbEnrFfZeLG9SPz7ZtmA4MDJI8_3mJmPkB-Mzplo2MUybtIA_XwdB5xTWtdCN9_IETOCzxSnYu9DfUi-57ykVAqt1AE55NxIbpQ-Ir9unoPHwWFVFlAqXMUS4lCt0AcomKscXYC-glJweO2EoUoLzJtcrcDB0wbzCdnvoM94Or3H5OH3zb_r29n93z9311f3Mye5KrNWdUwKpI1vDDAHHaoOvDaUasebTlDKWy6dZgY0CuaNgpYr2uBI413jxDE53-mu-5jttH62THAlGZdGjIi7HcJHWNp1CitILzZCsK8fMT1aSCW4Hi0bPb1krHG1q5VptTLeuRap5Nor7Uety8lt047XcOP6CfpPop87Q1jYx_hsRS2YMGoU-DkJpLg9U_li5HqHcinmnLB7d2DUbnN-Y9ltznbKeaSdfZzunfQWrPgPixWnEQ</recordid><startdate>20120830</startdate><enddate>20120830</enddate><creator>Bethell, Emily J</creator><creator>Holmes, Amanda</creator><creator>Maclarnon, Ann</creator><creator>Semple, Stuart</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</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>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</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>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>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120830</creationdate><title>Evidence that emotion mediates social attention in rhesus macaques</title><author>Bethell, Emily J ; Holmes, Amanda ; Maclarnon, Ann ; Semple, Stuart</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-b6f153e07d79a1cafe6fad89008c27f3002b25c819a8e31d96ab2607ef152f7c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Aggression - 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Studies of humans indicate that an individual's emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.
We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.
The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.
These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22952968</pmid><doi>10.1371/journal.pone.0044387</doi><oa>free_for_read</oa></addata></record> |
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subjects | Aggression - physiology Animal behavior Animals Anxiety Arousal Attention - physiology Bias Biology Cues Emotions - physiology Enrichment Face Fixation, Ocular - physiology Genotypes Health Human behavior Humans Laboratory animals Macaca mulatta Macaca mulatta - physiology Male Primates Psychological factors Science Policy Social and Behavioral Sciences Social Behavior Social interactions Studies Time Factors Veterinary medicine Veterinary Science Vigilance |
title | Evidence that emotion mediates social attention in rhesus macaques |
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