Sandra G. Wiener

Psychoneuroendocrinology of Stress: A Psychobiological Perspective

Publisher Summary This chapter discusses specific psychological variables that are involved in the regulation of the Pituitary–Adrenal (P–A) activity and specific aspects of the psychological variables that can selectively affect and regulate the secretion of gonadal hormones. The influence of psychological factors on P–A hormones is bidirectional. The psychological stimuli not only participate in activating this system but also effectively inhibit it. This inhibition is manifested either by reduced elevations of plasma corticoids during aversive stimulation or by an actual decrease in circulating levels of corticoids. This effect is particularly pronounced when the predictable or reinforcing stimulus involves consummatory events. Apart from induced stress, feedback is another factor involved in this process. Feedback refers to stimuli or information occurring after a behavioral response has been made in reaction to an event. These stimuli may be used to convey information to the responding organism indicating that it has made the correct response to a noxious event. The field of neuroendocrinology has made tremendous advances in the past few decades in identifying many chemical substances that qualify as hormones not only in the pituitary and peripheral organs but also in the central nervous system.

PSYCHOENDOCRINE ASPECTS OF MOTHER-INFANT RELATIONSHIPS IN NONHUMAN PRIMATES

Studies will be presented which examine the physiological and behavioral responses of squirrel monkeys and rhesus macaques following disruptions of mother-infant relationships. Reliable increases in circulating levels of plasma cortisol occur following separation of the infant from its mother. The presence of familiar conspecifics during the time of separation reduces the pituitary-adrenal response, compared to that elicited by total isolation. Visual access to the mother during separation also ameliorates the plasma cortisol response. However, when infants are separated in the presence of unfamiliar conspecifics, the physiological response is exaggerated compared to animals which are totally isolated. The behavior expressed by the infant during separation, particularly separation-induced vocalizations, is not concordant with this physiological index of affect. The rate of vocalization produced when the infant has visual access to the mother was higher than when the infant was totally isolated. However, when allowed access to familiar conspecifics, the rate of vocalization was lower than during total isolation, with no vocalization produced while the separated infant was in the unfamiliar social group. The curvilinear relationship between vocalization and the physiological index of arousal has led to a revision of the traditional concept that separation-induced infant vocalization is reflective of distress. These data support the hypothesis that vocalizations may serve as a coping response that reduces the physiological indices of arousal. Social interaction with familiar cospecifics may serve as a non-vocal coping response (e.g., proximity contact to other monkeys) which also reduces the behavioral and physiological responses to maternal separation.

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

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; and 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.

Temporal and social factors influencing behavioral and hormonal responses to separation in mother and infant squirrel monkeys

The behavioral and hormonal responses of mother and infant squirrel monkeys (Saimiri sciureus) were examined to assess temporal and environmental factors that influence the response to separation. In two experiments evaluating the effects of 1-, 3-, 6-, and 24-hr separations, it was found that signs of infant behavioral agitation decreased over time, whereas adrenocortical activation persisted or even increased. Moreover, two separation environments were shown to differentially affect behavioral and hormonal responses. Separated infants vocalized significantly more when their mothers were proximal than when isolated, but showed lower cortisol levels in the adjacent separation than in the total-isolation condition. These data indicate that the intensity of the infants calling response cannot be used to predict internal state (as reflected by cortisol levels). Furthermore, vocalization rate is highly dependent upon contingent stimuli, such as the presence of maternal cues. Following separation, the mothers also showed elevated cortisol levels. However, both the magnitude and pattern of the response differed considerably from that of the infant.

Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus).

This study extends an examination of the behavioral and pituitary-adrenal responses of infant squirrel monkeys (Saimiri sciureus) separated from their mothers under different environmental conditions to another physiological system by measuring the metabolites of the central monoamines found in the cerebrospinal fluid (CSF). This study included spectrographic examination of the vocalizations emitted by the infant during separation. Infants were separated from their mothers for 24 hr under 3 conditions: Home, infant remained in its home cage after removal of mother; adjacent, infant was placed in a cage adjacent to its mother; and total, infant was totally isolated. The behavioral results indicated that the number of calls emitted differed with condition (adjacent greater than total greater than home), and the peak frequency of the calls and number of multiple calls was greatest in the total condition. Plasma cortisol elevations after separation differentiated the conditions of separation (total greater than adjacent greater than home greater than base). The elevations in the CSF catecholamine metabolites (3-methoxy-4-hydroxyphenylglycol and homovanillic acid) were also sensitive to the conditions of separation (total greater than adjacent greater than base). These results are discussed in the context of coping theory.

Primate Vocalization: A Psychobiological Approach.

Scientific inquiry, for the most part, can be described as parochial. Not only are there clear demarcations between broad disciplinary categories (i.e., anatomy, physiology, psychology), but subspecialties are common within disciplines. Modern technology has made possible a trend toward greater and greater specialization. In fact, there are now areas of scientific investigation that did not exist a few years ago. This increasing specialization and its concomitant reductionism is not without its pitfalls and problems. There is a tendency to move away from the basic evolutionary concept of living organisms as organized systems functioning and adapting within an ecosystem. The laboratory scientist often ignores the inherent organization of living systems in favor of an intense pursuit of his or her particular chosen bit of the biological puzzle. However, there are still disciplines that not only subscribe to the notion of living organisms as organized systems but have made a valiant attempt to bring this concept under laboratory scrutiny. Often, in order to identify these endeavors, a technique is used to combine two or three words into one. Thus, we have several flourishing disciplines described as psychoneuroimmunology, psychoneuroendocrinology, neurochemistry, physiosociology, and so on. For the investigator who attempts a more integrated approach to the broad biological and psychological universe, the demands are heavy. He or she is faced with the need to maintain credibility in several disciplines, each of which is advancing at an accelerated pace. However, we feel that the value of an integrated approach that crosses traditional disciplinary lines will be illustrated in a small way by this article and, we hope, by the series of articles presented in this symposium section of Child Development.

Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother-infant relationships

This study was designed to determine the behavioral and pituitary-adrenal responses of squirrel monkey mother-infant dyads reared under different housing conditions to either 1- or 6-hr separations. Dyads were reared either in an individual cage or in social groups of 3 mother-infant dyads. The two separation conditions consisted of removing either the mother or the infant to a novel test cage while the other member remained in the home cage. Group-reared infants displayed lower levels of plasma cortisol, movement, and vocalization when they remained in the home cage during separation compared to their responses in the novel cage. However, individually-reared infants displayed high cortisol and activity levels in both separation environments, and vocalization levels were higher at 1 hr in the home cage than in the novel cage. These results indicate that familiarity with the separation environment, per se, does not attenuate the behavioral or physiological responses of infants, but that familiar conspecifics, even in the absence of alloparenting, can benefit an infant during separation from its mother. Two additional test conditions assessed the responses of mother-infant dyads when they were only momentarily separated and then immediately reunited in either the home cage or a novel cage. Reunion in the home cage evoked no cortisol or behavioral responses, but reunion in a novel cage resulted in significant elevations in infant cortisol levels and time in contact with the mother. The corticoid response of the mothers differed from their infants during separations.(ABSTRACT TRUNCATED AT 250 WORDS)

Psychoendocrine Responses of Mother and Infant Monkeys to Disturbance and Separation

In mammalian and avian species, it is essential that the young maintain at least periodic contact with their mother in order to obtain nurturance and warmth. This contact is ensured through the development of emotional dependency or attachment, as well as by the complementary distress reaction that occurs following sudden or forced separation of mother and infant. During the last several years, our laboratory has investigated this response as a way of evaluating how mother and infant primates cope with stressful situations. This research not only has generated new information on the nature of attachment processes in nonhuman primates but has also provided a unique way of determining how young organisms cope with stress. In addition to demonstrating that social relationships are important in the mediation of stress and coping, we have found that the concepts developed in the stress literature have a surprising degree of applicability to an understanding of the dynamics of mother-infant relationships.

ACTH and Corticosterone Secretion in Rats following Removal of the Neurointermediate Lobe of the Pituitary Gland

Surgical removal of the neurointermediate lobe of the pituitary gland (NIL-X) in the rat resulted in two abnormalities in ACTH secretion: (1) plasma ACTH and corticosterone levels were elevated in the morning and over a 24-hour period compared with levels in control (NIL-C) rats, and (2) although NIL-X and NIL-C rats had acute increases in plasma ACTH and corticosterone of equal magnitude after interoceptive stimuli (hemorrhage, surgery), NIL-X rats demonstrated markedly smaller elevations in plasma levels of these hormones after neurotropic stimuli (noise, novel environment). This subnormal adrenocortical response of NIL-X rats was not due to an impairment in perception of a neurotropic stimulus; these rats had normal latencies to paw licking and to jumping off a heated surface, yet smaller increases in plasma corticosterone after the stimulus. The impairment in ACTH response was not related to stimulus intensity, as NIL-X and NIL-C rats had equal ACTH and corticosterone secretion during both low and high levels of insulin-induced hypoglycemia. NIL-X rats demonstrated a significant elevation in daily water intake, although hematocrit, plasma Na+, K+, osmolality and protein were normal. Significant diurnal rhythms in plasma corticosterone levels and in water intake were maintained as well. The elevated morning plasma ACTH levels, the blunted hormone increases after noise, and the increase in water intake persisted in NIL-X rats 2 months after surgery. These data indicate that removal of the NIL results in (1) chronic elevations in basal ACTH and corticosterone secretion, and (2) chronic impairment in adrenocortical responses to neurotropic stimuli, but not to interoceptive stimuli. The deficit is not due to impaired perceptual capacity nor to the intensity of the stimulus.

Physiological Consequences of Maternal Separation and Loss in the Squirrel Monkey

As the chapters in this volume indicate, the squirrel monkey has been a valuable subject in many areas of research. One area in which the squirrel monkey has been particularly popular is in the investigation of developmental issues. Our laboratory has found it to be the subject of choice for two reasons. First, the specificity and duration of the emotional bond between mother and infant make the squirrel monkey a good model for the study of attachment processes. Second, the resiliency of the infant and its high adrenocortical hormone levels are extremely conducive to experiments on the effects of psychological and environmental perturbations that occur early in life. Here we will review a series of studies on the physiological consequences of maternal separation in infant squirrel monkeys, and also discuss some of the factors that can ameliorate the deleterious hormonal and immunological effects of maternal loss.