Serotonergic innervation of the human amygdala and evolutionary implications
Objectives The serotonergic system is involved in the regulation of socio‐emotional behavior and heavily innervates the amygdala, a key structure of social brain circuitry. We quantified serotonergic axon density of the four major nuclei of the amygdala in humans, and examined our results in light o...
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Veröffentlicht in: | American journal of physical anthropology 2019-11, Vol.170 (3), p.351-360 |
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creator | Lew, Caroline H. Hanson, Kari L. Groeniger, Kimberly M. Greiner, Demi Cuevas, Deion Hrvoj‐Mihic, Branka Schumann, Cynthia M. Semendeferi, Katerina |
description | Objectives
The serotonergic system is involved in the regulation of socio‐emotional behavior and heavily innervates the amygdala, a key structure of social brain circuitry. We quantified serotonergic axon density of the four major nuclei of the amygdala in humans, and examined our results in light of previously published data sets in chimpanzees and bonobos.
Materials and methods
Formalin‐fixed postmortem tissue sections of the amygdala from six humans were stained for serotonin transporter (SERT) utilizing immunohistochemistry. SERT‐immunoreactive (ir) axon fiber density in the lateral, basal, accessory basal, and central nuclei of the amygdala was quantified using unbiased stereology. Nonparametric statistical analyses were employed to examine differences in SERT‐ir axon density between amygdaloid nuclei within humans, as well as differences between humans and previously published data in chimpanzees and bonobos.
Results
Humans displayed a unique pattern of serotonergic innervation of the amygdala, and SERT‐ir axon density was significantly greater in the central nucleus compared to the lateral nucleus. SERT‐ir axon density was significantly greater in humans compared to chimpanzees in the basal, accessory basal, and central nuclei. SERT‐ir axon density was greater in humans compared to bonobos in the accessory basal and central nuclei.
Conclusions
The human pattern of SERT‐ir axon distribution in the amygdala complements the redistribution of neurons in the amygdala in human evolution. The present findings suggest that differential serotonergic modulation of cognitive and autonomic pathways in the amygdala in humans, bonobos, and chimpanzees may contribute to species‐level differences in social behavior. |
doi_str_mv | 10.1002/ajpa.23896 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7875516</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2250621965</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4486-47fe8d3eb43e057bee7fafd389335bb94281baab46c84f7c5a0daced08e45ba33</originalsourceid><addsrcrecordid>eNp9kVuLFDEQhYMo7rj64g-QBl-WhV5z63T6RRgW1wsDCupzqE5Xz2ToTsake2T-vZmZdVEfhIJUqK8OpziEvGT0hlHK38B2Bzdc6EY9IgtGG1VqJeVjsqB5WjZSiwvyLKVt_qpcT8mFYDx3DV-Q1VeMYQoe49rZwvnc7GFywRehL6YNFpt5BF_AeFh3MEABvitwH4b5yEA8FG7cDc6eVtJz8qSHIeGL-_eSfL979-32Q7n6_P7j7XJVWim1KmXdo-4EtlIgreoWse6h7_IBQlRt20iuWQvQSmW17GtbAe3AYkc1yqoFIS7J27Pubm5H7Cz6KcJgdtGN2ZIJ4MzfE-82Zh32ptZ1VTGVBa7uBWL4MWOazOiSxWEAj2FOhvOKKs4aVWX09T_oNszR5_MMF1RkSp-o6zNlY0gpYv9ghlFzDMkcQzKnkDL86k_7D-jvVDLAzsBPN-DhP1Jm-enL8iz6CxvOnxI</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2303621865</pqid></control><display><type>article</type><title>Serotonergic innervation of the human amygdala and evolutionary implications</title><source>MEDLINE</source><source>Access via Wiley Online Library</source><creator>Lew, Caroline H. ; Hanson, Kari L. ; Groeniger, Kimberly M. ; Greiner, Demi ; Cuevas, Deion ; Hrvoj‐Mihic, Branka ; Schumann, Cynthia M. ; Semendeferi, Katerina</creator><creatorcontrib>Lew, Caroline H. ; Hanson, Kari L. ; Groeniger, Kimberly M. ; Greiner, Demi ; Cuevas, Deion ; Hrvoj‐Mihic, Branka ; Schumann, Cynthia M. ; Semendeferi, Katerina</creatorcontrib><description>Objectives
The serotonergic system is involved in the regulation of socio‐emotional behavior and heavily innervates the amygdala, a key structure of social brain circuitry. We quantified serotonergic axon density of the four major nuclei of the amygdala in humans, and examined our results in light of previously published data sets in chimpanzees and bonobos.
Materials and methods
Formalin‐fixed postmortem tissue sections of the amygdala from six humans were stained for serotonin transporter (SERT) utilizing immunohistochemistry. SERT‐immunoreactive (ir) axon fiber density in the lateral, basal, accessory basal, and central nuclei of the amygdala was quantified using unbiased stereology. Nonparametric statistical analyses were employed to examine differences in SERT‐ir axon density between amygdaloid nuclei within humans, as well as differences between humans and previously published data in chimpanzees and bonobos.
Results
Humans displayed a unique pattern of serotonergic innervation of the amygdala, and SERT‐ir axon density was significantly greater in the central nucleus compared to the lateral nucleus. SERT‐ir axon density was significantly greater in humans compared to chimpanzees in the basal, accessory basal, and central nuclei. SERT‐ir axon density was greater in humans compared to bonobos in the accessory basal and central nuclei.
Conclusions
The human pattern of SERT‐ir axon distribution in the amygdala complements the redistribution of neurons in the amygdala in human evolution. The present findings suggest that differential serotonergic modulation of cognitive and autonomic pathways in the amygdala in humans, bonobos, and chimpanzees may contribute to species‐level differences in social behavior.</description><identifier>ISSN: 0002-9483</identifier><identifier>ISSN: 1096-8644</identifier><identifier>EISSN: 1096-8644</identifier><identifier>EISSN: 2692-7691</identifier><identifier>DOI: 10.1002/ajpa.23896</identifier><identifier>PMID: 31260092</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adult ; Aged ; amygdala ; Amygdala - chemistry ; Amygdala - cytology ; Anthropology, Physical ; Biological Evolution ; Brain ; brain evolution ; Density ; Emotional regulation ; Female ; Human evolution ; Humans ; Immunohistochemistry ; Male ; Neurons ; Neurons - chemistry ; Neurons - cytology ; Primates ; Redistribution ; Serotonin ; Serotonin Plasma Membrane Transport Proteins - analysis ; Serotonin Plasma Membrane Transport Proteins - chemistry ; Social Behavior ; Statistical analysis ; Young Adult</subject><ispartof>American journal of physical anthropology, 2019-11, Vol.170 (3), p.351-360</ispartof><rights>2019 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4486-47fe8d3eb43e057bee7fafd389335bb94281baab46c84f7c5a0daced08e45ba33</citedby><cites>FETCH-LOGICAL-c4486-47fe8d3eb43e057bee7fafd389335bb94281baab46c84f7c5a0daced08e45ba33</cites><orcidid>0000-0002-4734-3153</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fajpa.23896$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fajpa.23896$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31260092$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lew, Caroline H.</creatorcontrib><creatorcontrib>Hanson, Kari L.</creatorcontrib><creatorcontrib>Groeniger, Kimberly M.</creatorcontrib><creatorcontrib>Greiner, Demi</creatorcontrib><creatorcontrib>Cuevas, Deion</creatorcontrib><creatorcontrib>Hrvoj‐Mihic, Branka</creatorcontrib><creatorcontrib>Schumann, Cynthia M.</creatorcontrib><creatorcontrib>Semendeferi, Katerina</creatorcontrib><title>Serotonergic innervation of the human amygdala and evolutionary implications</title><title>American journal of physical anthropology</title><addtitle>Am J Phys Anthropol</addtitle><description>Objectives
The serotonergic system is involved in the regulation of socio‐emotional behavior and heavily innervates the amygdala, a key structure of social brain circuitry. We quantified serotonergic axon density of the four major nuclei of the amygdala in humans, and examined our results in light of previously published data sets in chimpanzees and bonobos.
Materials and methods
Formalin‐fixed postmortem tissue sections of the amygdala from six humans were stained for serotonin transporter (SERT) utilizing immunohistochemistry. SERT‐immunoreactive (ir) axon fiber density in the lateral, basal, accessory basal, and central nuclei of the amygdala was quantified using unbiased stereology. Nonparametric statistical analyses were employed to examine differences in SERT‐ir axon density between amygdaloid nuclei within humans, as well as differences between humans and previously published data in chimpanzees and bonobos.
Results
Humans displayed a unique pattern of serotonergic innervation of the amygdala, and SERT‐ir axon density was significantly greater in the central nucleus compared to the lateral nucleus. SERT‐ir axon density was significantly greater in humans compared to chimpanzees in the basal, accessory basal, and central nuclei. SERT‐ir axon density was greater in humans compared to bonobos in the accessory basal and central nuclei.
Conclusions
The human pattern of SERT‐ir axon distribution in the amygdala complements the redistribution of neurons in the amygdala in human evolution. The present findings suggest that differential serotonergic modulation of cognitive and autonomic pathways in the amygdala in humans, bonobos, and chimpanzees may contribute to species‐level differences in social behavior.</description><subject>Adult</subject><subject>Aged</subject><subject>amygdala</subject><subject>Amygdala - chemistry</subject><subject>Amygdala - cytology</subject><subject>Anthropology, Physical</subject><subject>Biological Evolution</subject><subject>Brain</subject><subject>brain evolution</subject><subject>Density</subject><subject>Emotional regulation</subject><subject>Female</subject><subject>Human evolution</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>Male</subject><subject>Neurons</subject><subject>Neurons - chemistry</subject><subject>Neurons - cytology</subject><subject>Primates</subject><subject>Redistribution</subject><subject>Serotonin</subject><subject>Serotonin Plasma Membrane Transport Proteins - analysis</subject><subject>Serotonin Plasma Membrane Transport Proteins - chemistry</subject><subject>Social Behavior</subject><subject>Statistical analysis</subject><subject>Young Adult</subject><issn>0002-9483</issn><issn>1096-8644</issn><issn>1096-8644</issn><issn>2692-7691</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kVuLFDEQhYMo7rj64g-QBl-WhV5z63T6RRgW1wsDCupzqE5Xz2ToTsake2T-vZmZdVEfhIJUqK8OpziEvGT0hlHK38B2Bzdc6EY9IgtGG1VqJeVjsqB5WjZSiwvyLKVt_qpcT8mFYDx3DV-Q1VeMYQoe49rZwvnc7GFywRehL6YNFpt5BF_AeFh3MEABvitwH4b5yEA8FG7cDc6eVtJz8qSHIeGL-_eSfL979-32Q7n6_P7j7XJVWim1KmXdo-4EtlIgreoWse6h7_IBQlRt20iuWQvQSmW17GtbAe3AYkc1yqoFIS7J27Pubm5H7Cz6KcJgdtGN2ZIJ4MzfE-82Zh32ptZ1VTGVBa7uBWL4MWOazOiSxWEAj2FOhvOKKs4aVWX09T_oNszR5_MMF1RkSp-o6zNlY0gpYv9ghlFzDMkcQzKnkDL86k_7D-jvVDLAzsBPN-DhP1Jm-enL8iz6CxvOnxI</recordid><startdate>201911</startdate><enddate>201911</enddate><creator>Lew, Caroline H.</creator><creator>Hanson, Kari L.</creator><creator>Groeniger, Kimberly M.</creator><creator>Greiner, Demi</creator><creator>Cuevas, Deion</creator><creator>Hrvoj‐Mihic, Branka</creator><creator>Schumann, Cynthia M.</creator><creator>Semendeferi, Katerina</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</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>8BJ</scope><scope>FQK</scope><scope>JBE</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4734-3153</orcidid></search><sort><creationdate>201911</creationdate><title>Serotonergic innervation of the human amygdala and evolutionary implications</title><author>Lew, Caroline H. ; Hanson, Kari L. ; Groeniger, Kimberly M. ; Greiner, Demi ; Cuevas, Deion ; Hrvoj‐Mihic, Branka ; Schumann, Cynthia M. ; Semendeferi, Katerina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4486-47fe8d3eb43e057bee7fafd389335bb94281baab46c84f7c5a0daced08e45ba33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Aged</topic><topic>amygdala</topic><topic>Amygdala - chemistry</topic><topic>Amygdala - cytology</topic><topic>Anthropology, Physical</topic><topic>Biological Evolution</topic><topic>Brain</topic><topic>brain evolution</topic><topic>Density</topic><topic>Emotional regulation</topic><topic>Female</topic><topic>Human evolution</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>Male</topic><topic>Neurons</topic><topic>Neurons - chemistry</topic><topic>Neurons - cytology</topic><topic>Primates</topic><topic>Redistribution</topic><topic>Serotonin</topic><topic>Serotonin Plasma Membrane Transport Proteins - analysis</topic><topic>Serotonin Plasma Membrane Transport Proteins - chemistry</topic><topic>Social Behavior</topic><topic>Statistical analysis</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lew, Caroline H.</creatorcontrib><creatorcontrib>Hanson, Kari L.</creatorcontrib><creatorcontrib>Groeniger, Kimberly M.</creatorcontrib><creatorcontrib>Greiner, Demi</creatorcontrib><creatorcontrib>Cuevas, Deion</creatorcontrib><creatorcontrib>Hrvoj‐Mihic, Branka</creatorcontrib><creatorcontrib>Schumann, Cynthia M.</creatorcontrib><creatorcontrib>Semendeferi, Katerina</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>International Bibliography of the Social Sciences (IBSS)</collection><collection>International Bibliography of the Social Sciences</collection><collection>International Bibliography of the Social Sciences</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>American journal of physical anthropology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lew, Caroline H.</au><au>Hanson, Kari L.</au><au>Groeniger, Kimberly M.</au><au>Greiner, Demi</au><au>Cuevas, Deion</au><au>Hrvoj‐Mihic, Branka</au><au>Schumann, Cynthia M.</au><au>Semendeferi, Katerina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Serotonergic innervation of the human amygdala and evolutionary implications</atitle><jtitle>American journal of physical anthropology</jtitle><addtitle>Am J Phys Anthropol</addtitle><date>2019-11</date><risdate>2019</risdate><volume>170</volume><issue>3</issue><spage>351</spage><epage>360</epage><pages>351-360</pages><issn>0002-9483</issn><issn>1096-8644</issn><eissn>1096-8644</eissn><eissn>2692-7691</eissn><abstract>Objectives
The serotonergic system is involved in the regulation of socio‐emotional behavior and heavily innervates the amygdala, a key structure of social brain circuitry. We quantified serotonergic axon density of the four major nuclei of the amygdala in humans, and examined our results in light of previously published data sets in chimpanzees and bonobos.
Materials and methods
Formalin‐fixed postmortem tissue sections of the amygdala from six humans were stained for serotonin transporter (SERT) utilizing immunohistochemistry. SERT‐immunoreactive (ir) axon fiber density in the lateral, basal, accessory basal, and central nuclei of the amygdala was quantified using unbiased stereology. Nonparametric statistical analyses were employed to examine differences in SERT‐ir axon density between amygdaloid nuclei within humans, as well as differences between humans and previously published data in chimpanzees and bonobos.
Results
Humans displayed a unique pattern of serotonergic innervation of the amygdala, and SERT‐ir axon density was significantly greater in the central nucleus compared to the lateral nucleus. SERT‐ir axon density was significantly greater in humans compared to chimpanzees in the basal, accessory basal, and central nuclei. SERT‐ir axon density was greater in humans compared to bonobos in the accessory basal and central nuclei.
Conclusions
The human pattern of SERT‐ir axon distribution in the amygdala complements the redistribution of neurons in the amygdala in human evolution. The present findings suggest that differential serotonergic modulation of cognitive and autonomic pathways in the amygdala in humans, bonobos, and chimpanzees may contribute to species‐level differences in social behavior.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>31260092</pmid><doi>10.1002/ajpa.23896</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-4734-3153</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Aged amygdala Amygdala - chemistry Amygdala - cytology Anthropology, Physical Biological Evolution Brain brain evolution Density Emotional regulation Female Human evolution Humans Immunohistochemistry Male Neurons Neurons - chemistry Neurons - cytology Primates Redistribution Serotonin Serotonin Plasma Membrane Transport Proteins - analysis Serotonin Plasma Membrane Transport Proteins - chemistry Social Behavior Statistical analysis Young Adult |
title | Serotonergic innervation of the human amygdala and evolutionary implications |
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