Amygdala growth from youth to adulthood in the macaque monkey

Cynthia Schumann, Julia A. Scott, Aaron Lee, Melissa D Bauman, David G Amaral

Research output: Contribution to journalArticle

Abstract

Emerging evidence suggests that the human amygdala undergoes extensive growth through adolescence, coinciding with the acquisition of complex socioemotional learning. Our objective was to longitudinally map volumetric growth of the nonhuman primate amygdala in a controlled, naturalistic social environment from birth to adulthood. Magnetic resonance images were collected at five time-points in 24 male and female rhesus macaques from 6 months to adulthood at 5 years. We then compared amygdala growth to other brain regions, including newly collected isocortical gray and white matter volumes, and previously published data on the same cohort. We found that amygdala volume increases by nearly 50% from age 6 months to 5 years. This dramatic growth is in contrast to overall brain and hippocampal volume, which peak near 3 years, white matter, which slows from 3 to 5 years, and isocortical gray, which has a net decrease. Similar to isocortical gray and hippocampal volumes, amygdala volume is ~8% larger in males than females. Rate of growth does not differ by sex. Although the underlying neurobiological substrate for protracted amygdala growth into adulthood is unclear, we propose it may be due in part to the unique cellular development of immature neurons in paralaminar nucleus that mature in size and connectivity with age. Prolonged amygdala maturation raises the possibility that environmental and genetic perturbations that disrupt this trajectory may contribute to the emergence of psychiatric disorders, such as anxiety, depression, schizophrenia, and autism; all in which the amygdala is strongly implicated.

Original languageEnglish (US)
JournalJournal of Comparative Neurology
DOIs
StatePublished - Jan 1 2019

Fingerprint

Macaca
Amygdala
Haplorhini
Growth
Social Environment
Brain
Autistic Disorder
Macaca mulatta
Primates
Psychiatry
Schizophrenia
Magnetic Resonance Spectroscopy
Anxiety
Learning
Parturition
Depression
Neurons

Keywords

  • amygdaloid complex
  • animal model
  • anxiety RRID:SCR_005988
  • autism
  • development
  • magnetic resonance imaging
  • MRI
  • neuroanatomy
  • nonhuman primate
  • rhesus
  • RRID:SCR_004757
  • schizophrenia
  • trajectory
  • volume

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Amygdala growth from youth to adulthood in the macaque monkey. / Schumann, Cynthia; Scott, Julia A.; Lee, Aaron; Bauman, Melissa D; Amaral, David G.

In: Journal of Comparative Neurology, 01.01.2019.

Research output: Contribution to journalArticle

@article{4f9b5f5ae0744b9dbdbd17e389488a98,
title = "Amygdala growth from youth to adulthood in the macaque monkey",
abstract = "Emerging evidence suggests that the human amygdala undergoes extensive growth through adolescence, coinciding with the acquisition of complex socioemotional learning. Our objective was to longitudinally map volumetric growth of the nonhuman primate amygdala in a controlled, naturalistic social environment from birth to adulthood. Magnetic resonance images were collected at five time-points in 24 male and female rhesus macaques from 6 months to adulthood at 5 years. We then compared amygdala growth to other brain regions, including newly collected isocortical gray and white matter volumes, and previously published data on the same cohort. We found that amygdala volume increases by nearly 50{\%} from age 6 months to 5 years. This dramatic growth is in contrast to overall brain and hippocampal volume, which peak near 3 years, white matter, which slows from 3 to 5 years, and isocortical gray, which has a net decrease. Similar to isocortical gray and hippocampal volumes, amygdala volume is ~8{\%} larger in males than females. Rate of growth does not differ by sex. Although the underlying neurobiological substrate for protracted amygdala growth into adulthood is unclear, we propose it may be due in part to the unique cellular development of immature neurons in paralaminar nucleus that mature in size and connectivity with age. Prolonged amygdala maturation raises the possibility that environmental and genetic perturbations that disrupt this trajectory may contribute to the emergence of psychiatric disorders, such as anxiety, depression, schizophrenia, and autism; all in which the amygdala is strongly implicated.",
keywords = "amygdaloid complex, animal model, anxiety RRID:SCR_005988, autism, development, magnetic resonance imaging, MRI, neuroanatomy, nonhuman primate, rhesus, RRID:SCR_004757, schizophrenia, trajectory, volume",
author = "Cynthia Schumann and Scott, {Julia A.} and Aaron Lee and Bauman, {Melissa D} and Amaral, {David G}",
year = "2019",
month = "1",
day = "1",
doi = "10.1002/cne.24728",
language = "English (US)",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley-Liss Inc.",

}

TY - JOUR

T1 - Amygdala growth from youth to adulthood in the macaque monkey

AU - Schumann, Cynthia

AU - Scott, Julia A.

AU - Lee, Aaron

AU - Bauman, Melissa D

AU - Amaral, David G

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Emerging evidence suggests that the human amygdala undergoes extensive growth through adolescence, coinciding with the acquisition of complex socioemotional learning. Our objective was to longitudinally map volumetric growth of the nonhuman primate amygdala in a controlled, naturalistic social environment from birth to adulthood. Magnetic resonance images were collected at five time-points in 24 male and female rhesus macaques from 6 months to adulthood at 5 years. We then compared amygdala growth to other brain regions, including newly collected isocortical gray and white matter volumes, and previously published data on the same cohort. We found that amygdala volume increases by nearly 50% from age 6 months to 5 years. This dramatic growth is in contrast to overall brain and hippocampal volume, which peak near 3 years, white matter, which slows from 3 to 5 years, and isocortical gray, which has a net decrease. Similar to isocortical gray and hippocampal volumes, amygdala volume is ~8% larger in males than females. Rate of growth does not differ by sex. Although the underlying neurobiological substrate for protracted amygdala growth into adulthood is unclear, we propose it may be due in part to the unique cellular development of immature neurons in paralaminar nucleus that mature in size and connectivity with age. Prolonged amygdala maturation raises the possibility that environmental and genetic perturbations that disrupt this trajectory may contribute to the emergence of psychiatric disorders, such as anxiety, depression, schizophrenia, and autism; all in which the amygdala is strongly implicated.

AB - Emerging evidence suggests that the human amygdala undergoes extensive growth through adolescence, coinciding with the acquisition of complex socioemotional learning. Our objective was to longitudinally map volumetric growth of the nonhuman primate amygdala in a controlled, naturalistic social environment from birth to adulthood. Magnetic resonance images were collected at five time-points in 24 male and female rhesus macaques from 6 months to adulthood at 5 years. We then compared amygdala growth to other brain regions, including newly collected isocortical gray and white matter volumes, and previously published data on the same cohort. We found that amygdala volume increases by nearly 50% from age 6 months to 5 years. This dramatic growth is in contrast to overall brain and hippocampal volume, which peak near 3 years, white matter, which slows from 3 to 5 years, and isocortical gray, which has a net decrease. Similar to isocortical gray and hippocampal volumes, amygdala volume is ~8% larger in males than females. Rate of growth does not differ by sex. Although the underlying neurobiological substrate for protracted amygdala growth into adulthood is unclear, we propose it may be due in part to the unique cellular development of immature neurons in paralaminar nucleus that mature in size and connectivity with age. Prolonged amygdala maturation raises the possibility that environmental and genetic perturbations that disrupt this trajectory may contribute to the emergence of psychiatric disorders, such as anxiety, depression, schizophrenia, and autism; all in which the amygdala is strongly implicated.

KW - amygdaloid complex

KW - animal model

KW - anxiety RRID:SCR_005988

KW - autism

KW - development

KW - magnetic resonance imaging

KW - MRI

KW - neuroanatomy

KW - nonhuman primate

KW - rhesus

KW - RRID:SCR_004757

KW - schizophrenia

KW - trajectory

KW - volume

UR - http://www.scopus.com/inward/record.url?scp=85067428790&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85067428790&partnerID=8YFLogxK

U2 - 10.1002/cne.24728

DO - 10.1002/cne.24728

M3 - Article

C2 - 31173365

AN - SCOPUS:85067428790

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

ER -