Adrenocortical activity during conditions of brief social separation in preweaning rats

doi:10.1016/0163-1047(90)91231-Y

Behavioral and Neural Biology

Volume 54, Issue 1, July 1990, Pages 42-55

https://doi.org/10.1016/0163-1047(90)91231-Y Get rights and content

Rat pups (18 days of age) placed into a novel test cage for 30 min exhibited greater concentrations of plasma corticosterone if alone than if with the biological mother regardless of whether she was conscious or anesthetized. Pups tested with a conscious nonlactating female had higher corticosterone levels than did pups tested with their own conscious mother. Anesthetizing the adult stimulus females eliminated this differential effect. Further, pups isolated in the home cage for 30 min exhibited corticosterone elevations as great as those of pups placed into a novel environment. However, pups left in the home cage with the mother for 30 min displayed corticosterone elevations similar to those of pups isolated in the home cage. In contrast, if pups were left in the home cage with both the mother and the littermates corticosteroid levels were reduced. These results indicate that, under certain conditions, brief separation from the mother can elevate plasma corticosterone levels in the 18-day-old rat. The differential effect of the biological mother and the nonlactating female appears attributable to differences in the behavior of the adult females. Finally, brief isolation from all littermates was also found to evoke a plasma corticosterone response.

References (24)

CoeC.L. et al.
Mother-infant attachment in the squirrel monkey: Adrenal response to separation
Behavioral Biology
(1978)
CooverG.D. et al.
Corticosterone “basal levels” and response to ether anesthesia in rats on a water deprivation regimen
Physiology and Behavior
(1979)
HennessyM.B.
Both prevention of physical contact and removal of distal cues mediate cortisol and vocalization responses of guinea pig pups to maternal separation in a novel environment
Physiology and Behavior
(1988)
HoferM.A.
The effects of brief maternal separations on behavior and heart rate of two week old rat pups
Physiology and Behavior
(1973)
LeonM. et al.
Maternal pheromone: Discrimination by preweanling albino rats
Physiology and Behavior
(1971)
SapolskyR.M. et al.
Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsiveness period
Brain Research Reviews
(1986)
TakahashiL.K. et al.
Stressor controllability during pregnancy influences pituitary—adrenal hormone concentrations and analgesic responsiveness in offspring
Physiology and Behavior
(1988)
DavidsonJ.M. et al.
Feedback regulation of adrenocorticotropin secretion in “basal” and “stress” conditions: Acute and chronic effects of intrahypothalamic corticoid implantation
Endocrinology
(1968)
HennessyM.B. et al.
Factors influencing cortisol and behavioral responses to maternal separation in guinea pigs
Behavioral Neuroscience
(1989)
HennessyM.B. et al.
Hormonal and behavioral attachment responses in infant guinea pigs
Developmental Psychobiology
(1987)

HepperP.G.

Parental recognition in the rat

The Quarterly Journal of Experimental Psychology

(1986)

HoferM.A.

Shaping forces within early social relationships

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In vertebrate animals, exposure of developing young to noxious or threatening stimuli can profoundly shape their morphology, physiology, and behavior throughout life, with the potential to impact fitness. Many of these effects are mediated in part by activation of the hypothalamo-pituitary-adrenal (HPA) axis, which produces a substantial rise in glucocorticoids following exposure to such stimuli during critical periods of development (Hennessy and Weinberg, 1990; Lynn and Kern, 2014; Pravosudov and Kitaysky, 2006; Rensel et al., 2010; Schoech et al., 2011). Elevations of glucocorticoids early in life can alter a variety of phenotypic characteristics in developing young (Lindström, 1999; Love et al., 2013; Monaghan, 2008; Schoech et al., 2011).
Early life experiences can affect the function of the hypothalamo-pituitary-adrenal (HPA) axis of vertebrates, with potential fitness consequences later in life. In altricial species, for example, variation in parental behavior, e.g. brooding or feeding, can modify the activity of the HPA axis of the young by altering their exposure to noxious stimuli as the young develop in the nest. We have shown that a drop in the body temperature of eastern bluebird (Sialia sialis) chicks, such as occurs when females are away from the nest, elevates their blood corticosterone levels. If repeated during the early days of their development, cooling bouts also reduce the chicks’ later corticosterone secretion in response to handling. Thus, variation in maternal behavior has the capacity to shape the function of the chicks’ HPA axis. To better understand how maternal absence from the nest activates the HPA axis of bluebird chicks, we experimentally mimicked the cooling that occurs when the female is away from the nest, and investigated a) the age at which the HPA axis becomes capable of responding to cooling by increasing corticosterone secretion, b) whether corticosterone secretion remains elevated throughout long periods of cooling, and c) whether fasting (also potentially associated with maternal absence) interacts with cooling to affect corticosterone secretion. Cooling for 18 min significantly elevated circulating corticosterone levels of chicks as young as 4 days post-hatch, indicating that their HPA axis is sensitive to cooling very early in life. Corticosterone levels remained elevated throughout longer bouts of cooling. However, a 1-hr period of fasting had no effect on corticosterone secretion, regardless of whether chicks were cooled or not. Collectively, these data demonstrate that variation in maternal brooding behavior can substantially modify the corticosterone profiles of chicks during early postnatal development, and that chick temperature is likely the main driver of this.
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Infants frequently show signs of distress when separated from their mothers (Ainsworth et al., 1978; Harlow and Harlow, 1965) such as vocalizations, changes in locomotion and in self-directed behavior. Such reactions which diminish or stop when the contact with the mother is restored are commonly taken as indicating the existence and intensity of mother–child attachment in both humans (Ainsworth et al., 1978; Bowlby, 1984) and other mammals (Hennessy and Weinberg, 1990; Wiener et al., 1990). Isolating guinea pig pups increase the production of high-pitched whistles and cortisol levels.
Guinea pig pups produce typical distress whistles when isolated. Whistles’ frequency is decreased or abolished when they contact with the mother and, to a lesser degree, a sibling or even an unfamiliar female, is regained. Those non-aggressive companions were considered social support providers for reducing pup physiological stress responses and whistling rate in an unfamiliar environment. However, what would happen if the isolated pup would be in contact with an adult male, normally indifferent to pups, in such distress situation? The role of attachment and familiarity to males in promoting changes in distress responses of isolated pups was verified. Tests consisted of separating three week old pups from their family, in a familiar or an unfamiliar environment, and introducing a conspecific in the cage after one minute (mother, sibling, father or a strange male). Whistling and other behaviors were compared between the alone period and the accompanied period. Main factors were prior presence/absence of father (pups were raised with father until testing or only for the first week after birth), sex of pup, novelty of test environment and companion. It was verified that (1) all conspecifics reduced whistling rate (F_4,88 = 77.89, p < 0.001), but pups behaved differently with different conspecifics; (2) suppression of isolation induced behavior did not necessarily occur because of previous attachment (e.g., pups in the PAF condition spent more time pausing, F_1,22 = 7.68, p < 0.05, less time in passive contact with companions, F_1,22 = 10.63, p < 0.01, and ate/drank less, F_1,22 = 6.18, p < 0.05). It was concluded that the suppression of pup's isolation induced behavior by companions must not be used alone as a measure of attachment. It must be seen in an evolutionary perspective where the presence of any conspecific represents security offering self-protective behavior cues as finding a place to hide, and providing dilution effect against predation.
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The case that many researchers make is that isolation itself is a stressor, and as such should not be used as a control. Indeed, many studies have shown that maternal separation (isolating pups from dam) and neonatal isolation (isolating pups from dam and other pups) are significant stressors, evoking ultrasonic vocalizations and inducing CORT release in pups (Hennessy and Weinberg, 1990; Kehne et al., 1991; Kuhn et al., 1990; Levine et al., 1991; McCormick et al., 1998; Viau et al., 1996). In addition, acute isolation of group-housed rats also induces CORT, which is taken as a clear indication of stress (Takatsu-Coleman et al., 2013).
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Protracted or repeated activation of the hypothalamic–pituitary–adrenocortical (HPA) system is associated with a variety of physical and psychological pathologies. Studies dating back to the 1970s have documented many cases in which the presence of a social companion can moderate HPA responses to stressors. However, there also are many cases in which this “social buffering” of the HPA axis is not observed. An examination of the literature indicates that the nature of the relationship between individuals is crucial in determining whether or not social buffering of the HPA response will occur. Other factors that affect social buffering, either directly or by influencing the social relationship, include the social organization of the species, previous experience, gender, integration into a social unit, and the developmental stage at which individuals are examined. Current evidence suggests that social buffering involves mechanisms acting at more than one level of the CNS. It is suggested that, in addition to promoting health, social buffering may have evolved to direct the establishment of social relationships, and to facilitate developmental transitions in social interactions appropriate for different life stages.
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: The work was supported by Grants BNS-8701620 and 8822240 from the National Science Foundation and a Biomedical Sciences Seed Grant from Wright State University to M.B.H., and by Grants MA-8040 and MA-9730 from the Medical Research Council of Canada to J.W. Portions of these data were presented at the 1988 meeting of the Midwest Psychological Association.

¹: The authors thank Anne Tamborski, Susan Suchy, Kevin Fung, and Gretta D'Alquen for technical assistance, and Sally Mendoza for her helpful comments on an earlier draft of this manuscript.

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Adrenocortical activity during conditions of brief social separation in preweaning rats

Behavioral Biology

Physiology and Behavior

Physiology and Behavior

Physiology and Behavior

Physiology and Behavior

Brain Research Reviews

Physiology and Behavior

Feedback regulation of adrenocorticotropin secretion in “basal” and “stress” conditions: Acute and chronic effects of intrahypothalamic corticoid implantation

Endocrinology

Factors influencing cortisol and behavioral responses to maternal separation in guinea pigs

Behavioral Neuroscience

Hormonal and behavioral attachment responses in infant guinea pigs

Developmental Psychobiology

Parental recognition in the rat

The Quarterly Journal of Experimental Psychology

Shaping forces within early social relationships