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
Hauptverfasser: Lew, Caroline H., Hanson, Kari L., Groeniger, Kimberly M., Greiner, Demi, Cuevas, Deion, Hrvoj‐Mihic, Branka, Schumann, Cynthia M., Semendeferi, Katerina
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container_end_page 360
container_issue 3
container_start_page 351
container_title American journal of physical anthropology
container_volume 170
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
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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 &amp; 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 &amp; 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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 &amp; 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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