Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys

Jessica Raper, Mark Wilson, Mar Sanchez, Christopher J. Machado, Jocelyne Bachevalier

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

The current study examined the long-term effects of neonatal amygdala lesions on emotional and hypothalamic-pituitary-adrenal (HPA) axis reactivity to an acute stressor in rhesus monkeys. Rhesus monkeys received either bilateral MRI-guided ibotenic acid amygdala (Neo-Aibo; n=. 6) or sham (Neo-C; n=. 7) lesions between 7 and 14 days of age. Emotional reactivity was assessed using the Human Intruder paradigm at 2 months, 4.5 months, and 6-8 years of age, whereas stress neuroendocrine response was only assessed in adulthood (6-8 years). The modulation of defensive and emotional behaviors based on the gaze direction of the intruder emerged between 2 and 4 months of age in surrogate-peer reared sham-operated infant monkeys, as already shown for mother-reared infants. Although neonatal amygdala lesions did not impair the ability to exhibit defensive and emotional behaviors, it altered the modulation of these responses based on the intruder's gaze direction. The changes in emotional reactivity after neonatal amygdala lesions emerged in infancy and persisted throughout adulthood when they were associated with a reduction of basal cortisol levels and a blunted cortisol response to the stressor. These changes are reminiscent of those found after adult-onset amygdala lesions, demonstrating little functional compensation following early amygdala damage.

Original languageEnglish (US)
Pages (from-to)1021-1035
Number of pages15
JournalPsychoneuroendocrinology
Volume38
Issue number7
DOIs
StatePublished - Jul 2013

Fingerprint

Amygdala
Macaca mulatta
Hydrocortisone
Ibotenic Acid
Aptitude
Haplorhini
Mothers

Keywords

  • Amygdala
  • Development
  • Emotion
  • HPA-axis

ASJC Scopus subject areas

  • Endocrinology
  • Endocrinology, Diabetes and Metabolism
  • Psychiatry and Mental health
  • Biological Psychiatry
  • Endocrine and Autonomic Systems

Cite this

Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys. / Raper, Jessica; Wilson, Mark; Sanchez, Mar; Machado, Christopher J.; Bachevalier, Jocelyne.

In: Psychoneuroendocrinology, Vol. 38, No. 7, 07.2013, p. 1021-1035.

Research output: Contribution to journalArticle

Raper, Jessica ; Wilson, Mark ; Sanchez, Mar ; Machado, Christopher J. ; Bachevalier, Jocelyne. / Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys. In: Psychoneuroendocrinology. 2013 ; Vol. 38, No. 7. pp. 1021-1035.
@article{85c7f645e00b45d38636a1f7f30c0f37,
title = "Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys",
abstract = "The current study examined the long-term effects of neonatal amygdala lesions on emotional and hypothalamic-pituitary-adrenal (HPA) axis reactivity to an acute stressor in rhesus monkeys. Rhesus monkeys received either bilateral MRI-guided ibotenic acid amygdala (Neo-Aibo; n=. 6) or sham (Neo-C; n=. 7) lesions between 7 and 14 days of age. Emotional reactivity was assessed using the Human Intruder paradigm at 2 months, 4.5 months, and 6-8 years of age, whereas stress neuroendocrine response was only assessed in adulthood (6-8 years). The modulation of defensive and emotional behaviors based on the gaze direction of the intruder emerged between 2 and 4 months of age in surrogate-peer reared sham-operated infant monkeys, as already shown for mother-reared infants. Although neonatal amygdala lesions did not impair the ability to exhibit defensive and emotional behaviors, it altered the modulation of these responses based on the intruder's gaze direction. The changes in emotional reactivity after neonatal amygdala lesions emerged in infancy and persisted throughout adulthood when they were associated with a reduction of basal cortisol levels and a blunted cortisol response to the stressor. These changes are reminiscent of those found after adult-onset amygdala lesions, demonstrating little functional compensation following early amygdala damage.",
keywords = "Amygdala, Development, Emotion, HPA-axis",
author = "Jessica Raper and Mark Wilson and Mar Sanchez and Machado, {Christopher J.} and Jocelyne Bachevalier",
year = "2013",
month = "7",
doi = "10.1016/j.psyneuen.2012.10.008",
language = "English (US)",
volume = "38",
pages = "1021--1035",
journal = "Psychoneuroendocrinology",
issn = "0306-4530",
publisher = "Elsevier Limited",
number = "7",

}

TY - JOUR

T1 - Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys

AU - Raper, Jessica

AU - Wilson, Mark

AU - Sanchez, Mar

AU - Machado, Christopher J.

AU - Bachevalier, Jocelyne

PY - 2013/7

Y1 - 2013/7

N2 - The current study examined the long-term effects of neonatal amygdala lesions on emotional and hypothalamic-pituitary-adrenal (HPA) axis reactivity to an acute stressor in rhesus monkeys. Rhesus monkeys received either bilateral MRI-guided ibotenic acid amygdala (Neo-Aibo; n=. 6) or sham (Neo-C; n=. 7) lesions between 7 and 14 days of age. Emotional reactivity was assessed using the Human Intruder paradigm at 2 months, 4.5 months, and 6-8 years of age, whereas stress neuroendocrine response was only assessed in adulthood (6-8 years). The modulation of defensive and emotional behaviors based on the gaze direction of the intruder emerged between 2 and 4 months of age in surrogate-peer reared sham-operated infant monkeys, as already shown for mother-reared infants. Although neonatal amygdala lesions did not impair the ability to exhibit defensive and emotional behaviors, it altered the modulation of these responses based on the intruder's gaze direction. The changes in emotional reactivity after neonatal amygdala lesions emerged in infancy and persisted throughout adulthood when they were associated with a reduction of basal cortisol levels and a blunted cortisol response to the stressor. These changes are reminiscent of those found after adult-onset amygdala lesions, demonstrating little functional compensation following early amygdala damage.

AB - The current study examined the long-term effects of neonatal amygdala lesions on emotional and hypothalamic-pituitary-adrenal (HPA) axis reactivity to an acute stressor in rhesus monkeys. Rhesus monkeys received either bilateral MRI-guided ibotenic acid amygdala (Neo-Aibo; n=. 6) or sham (Neo-C; n=. 7) lesions between 7 and 14 days of age. Emotional reactivity was assessed using the Human Intruder paradigm at 2 months, 4.5 months, and 6-8 years of age, whereas stress neuroendocrine response was only assessed in adulthood (6-8 years). The modulation of defensive and emotional behaviors based on the gaze direction of the intruder emerged between 2 and 4 months of age in surrogate-peer reared sham-operated infant monkeys, as already shown for mother-reared infants. Although neonatal amygdala lesions did not impair the ability to exhibit defensive and emotional behaviors, it altered the modulation of these responses based on the intruder's gaze direction. The changes in emotional reactivity after neonatal amygdala lesions emerged in infancy and persisted throughout adulthood when they were associated with a reduction of basal cortisol levels and a blunted cortisol response to the stressor. These changes are reminiscent of those found after adult-onset amygdala lesions, demonstrating little functional compensation following early amygdala damage.

KW - Amygdala

KW - Development

KW - Emotion

KW - HPA-axis

UR - http://www.scopus.com/inward/record.url?scp=84877925554&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84877925554&partnerID=8YFLogxK

U2 - 10.1016/j.psyneuen.2012.10.008

DO - 10.1016/j.psyneuen.2012.10.008

M3 - Article

C2 - 23148887

AN - SCOPUS:84877925554

VL - 38

SP - 1021

EP - 1035

JO - Psychoneuroendocrinology

JF - Psychoneuroendocrinology

SN - 0306-4530

IS - 7

ER -