Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates

doi:10.1016/0306-4530(83)90019-7

Psychoneuroendocrinology

Volume 8, Issue 4, 1983, Pages 401-409

https://doi.org/10.1016/0306-4530(83)90019-7 Get rights and content

Abstract

Mother and infant squirrel monkeys were subjected to a series of brief separations in order to evaluate how behavioral and physiological responses change following multiple exposures to stress. Beginning when the infants reached three months of age, their behavioral and hormonal responses were assessed during six 1-hr separations; an additional five dyads served as controls for the effect of repeated disturbance. The separated infants showed a marked and progressive decrease in distress calling across time, but no change was observed in the high levels of agitated activity or the plasma cortisol response to separation. This finding questions the traditional use of distress vocalizations as a measure of stress and indicates that certain types of behavior can change independently of physiological arousal responses, which may continue to occur even after repeated exposures to stress.

References (38)

M.R. Gunnar et al.
Behavioral and pituitary-adrenal responses during a prolonged separation period in infant rhesus macaques
Psychoneuroendocrinology
(1981)
G.W. Kraemer et al.
Interactions of pharmacological agents which alter biogenic amine metabolism and depression
J. Affect. Disorders
(1979)
Y. Spencer-Booth et al.
Effects of 6 days separation from mother in 18- to 32-week-old rhesus monkeys
Anim. Behav.
(1971)
R. Ader
Adrenocortical function and the measurement of emotionality
Ann. N.Y. Acad. Sci.
(1969)
J. Bowlby
C.L. Coe et al.
Normal responses to mother-infant separation in nonhuman primates
C.L. Coe et al.
Hormonal response to stress in the squirrel monkey (Saimiri sciureus)
Neuroendocrinology
(1978)
C.L. Coe et al.
Psychoendocrine responses of mother and infant monkeys to disturbance and separation
S.E. File
The rat corticosterone response: habituation and modification by chlordiazepoxide
Physiol. Behav.
(1982)
P.M. Groves et al.
Habituation: a dual process theory
Psychol. Rev.
(1970)

J.R. Hansen et al.

Urinary levels of epinephrine and norepinephrine in parachutist trainees

J.W. Hennessy et al.

Influence of experiential factors and gonadal hormones on pituitary-adrenal response of the mouse to novelty and electric shock

J. comp. Physiol. Psychol.

(1977)

J.W. Hennessy et al.

Stress, arousal, and the pituitary-adrenal system: a psychoendocrine hypothesis

S.D. Hill et al.

Effects of artificial mothers and visual experience on adrenal responsiveness of infant monkeys

Devl Psychobiol.

(1973)

M.A. Hofer

Parental contributions to the development of their offspring

I.C. Kaufman et al.

The reaction to separation in infant monkeys: anaclitic depression and conservation withdrawal

Psychosom. Med.

(1967)

I.C. Kaufman et al.

Depression can be induced in a bonnet macaque infant

Psychosom. Med.

(1978)

W. Klemm et al.

A routine method for the radioimmunoassay of plasma cortisol without chromatography

R. Kvetnansky et al.

Adrenal and urinary catecholamines during adaptation to repeated immobilization stress

Endocrinology

(1970)

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ReportBehavioral, but not physiological, adaptation to repeated separation in mother and infant primates

Abstract

Psychoneuroendocrinology

J. Affect. Disorders

Anim. Behav.

Adrenocortical function and the measurement of emotionality

Ann. N.Y. Acad. Sci.

Normal responses to mother-infant separation in nonhuman primates

Hormonal response to stress in the squirrel monkey (Saimiri sciureus)

Neuroendocrinology

Psychoendocrine responses of mother and infant monkeys to disturbance and separation

The rat corticosterone response: habituation and modification by chlordiazepoxide

Physiol. Behav.

Habituation: a dual process theory

Psychol. Rev.

Urinary levels of epinephrine and norepinephrine in parachutist trainees

Influence of experiential factors and gonadal hormones on pituitary-adrenal response of the mouse to novelty and electric shock

J. comp. Physiol. Psychol.

Stress, arousal, and the pituitary-adrenal system: a psychoendocrine hypothesis

Effects of artificial mothers and visual experience on adrenal responsiveness of infant monkeys

Devl Psychobiol.

Parental contributions to the development of their offspring

The reaction to separation in infant monkeys: anaclitic depression and conservation withdrawal

Psychosom. Med.

Depression can be induced in a bonnet macaque infant

Psychosom. Med.

A routine method for the radioimmunoassay of plasma cortisol without chromatography

Adrenal and urinary catecholamines during adaptation to repeated immobilization stress

Endocrinology

Report
Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates