Serotonergic innervation of the human amygdala and evolutionary implications

Caroline H. Lew, Kari L. Hanson, Kimberly M. Groeniger, Demi Greiner, Deion Cuevas, Branka Hrvoj-Mihic, Cynthia Schumann, Katerina Semendeferi

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
JournalAmerican Journal of Physical Anthropology
DOIs
StatePublished - Jan 1 2019

Fingerprint

Amygdala
Serotonin Plasma Membrane Transport Proteins
Pan paniscus
Axons
social behavior
redistribution
Pan troglodytes
brain
regulation
Autonomic Pathways
Social Behavior
Formaldehyde
Immunohistochemistry
Neurons
Basolateral Nuclear Complex
Brain

Keywords

  • amygdala
  • brain evolution
  • serotonin
  • social behavior

ASJC Scopus subject areas

  • Anatomy
  • Anthropology

Cite this

Lew, C. H., Hanson, K. L., Groeniger, K. M., Greiner, D., Cuevas, D., Hrvoj-Mihic, B., ... Semendeferi, K. (2019). Serotonergic innervation of the human amygdala and evolutionary implications. American Journal of Physical Anthropology. https://doi.org/10.1002/ajpa.23896

Serotonergic innervation of the human amygdala and evolutionary implications. / Lew, Caroline H.; Hanson, Kari L.; Groeniger, Kimberly M.; Greiner, Demi; Cuevas, Deion; Hrvoj-Mihic, Branka; Schumann, Cynthia; Semendeferi, Katerina.

In: American Journal of Physical Anthropology, 01.01.2019.

Research output: Contribution to journalArticle

Lew, Caroline H. ; Hanson, Kari L. ; Groeniger, Kimberly M. ; Greiner, Demi ; Cuevas, Deion ; Hrvoj-Mihic, Branka ; Schumann, Cynthia ; Semendeferi, Katerina. / Serotonergic innervation of the human amygdala and evolutionary implications. In: American Journal of Physical Anthropology. 2019.
@article{8e9d4dd708524e789ce8908a3fa2da6b,
title = "Serotonergic innervation of the human amygdala and evolutionary implications",
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.",
keywords = "amygdala, brain evolution, serotonin, social behavior",
author = "Lew, {Caroline H.} and Hanson, {Kari L.} and Groeniger, {Kimberly M.} and Demi Greiner and Deion Cuevas and Branka Hrvoj-Mihic and Cynthia Schumann and Katerina Semendeferi",
year = "2019",
month = "1",
day = "1",
doi = "10.1002/ajpa.23896",
language = "English (US)",
journal = "American Journal of Physical Anthropology",
issn = "0002-9483",
publisher = "Wiley-Liss Inc.",

}

TY - JOUR

T1 - Serotonergic innervation of the human amygdala and evolutionary implications

AU - Lew, Caroline H.

AU - Hanson, Kari L.

AU - Groeniger, Kimberly M.

AU - Greiner, Demi

AU - Cuevas, Deion

AU - Hrvoj-Mihic, Branka

AU - Schumann, Cynthia

AU - Semendeferi, Katerina

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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.

KW - amygdala

KW - brain evolution

KW - serotonin

KW - social behavior

UR - http://www.scopus.com/inward/record.url?scp=85068473754&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85068473754&partnerID=8YFLogxK

U2 - 10.1002/ajpa.23896

DO - 10.1002/ajpa.23896

M3 - Article

JO - American Journal of Physical Anthropology

JF - American Journal of Physical Anthropology

SN - 0002-9483

ER -