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)     

Response of mother and infant squirrel monkeys to separation and disturbance

Plasma cortisol values were obtained from squirrel monkey mothers and infants after two types of brief separation: infant removed to a nearby cage and infant removed to a different room. Cortisol values were also obtained during basal conditions, and after 30 min exposure to an unfamiliar juvenile conspecific when mothers and infants were allowed to maintain contact. For either separation condition, both mothers and infants exhibited significant cortisol elevations, and overall, infants ‘corticoid values were much greater than mothers’. Behavioral measures were also obtained from mothers, who during both separations tended to show marked behavioral agitation. The partner's presence or absence during separation did not produce differential behavioral or corticoid responses by either mother or infant. However, the presence of the unfamiliar conspecific induced clearly significant cortisol elevations in the infant but only slight elevations in the mother.     

Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers

Effects of social stimuli on behavioral and physiological responses were examined in infant rhesus monkeys at 4 and 9 months of age. Infants and mothers were removed from the social group and housed as dyads. Following this period, infants were removed and separated under four counterbalanced conditions: (a) totally isolated--placed in a holding cage for 24 hr; (b) mother present, no contact--housed in a single cage in view of their mother, no contact; (c) mother present, contact--similar to above, with mother in proximity to the infant; and (d) peer present--separated but in proximity to a peer. In the first experiment, the infants rarely vocalized when totally isolated but showed high rates of vocalization in the presence of the mother, both with and without contact. In the mother-present conditions, they failed to show a plasma cortisol response. In contrast, totally isolated infants showed a significant elevation in plasma cortisol. At 9 months of age, these infants were separated for 3 days under two different conditions: mother present and totally isolated. Once again, the infants that were totally isolated showed little vocalization but significant elevations in plasma cortisol. In contrast, infants separated in the presence of their mothers showed high vocalization rates but no cortisol response. The concepts of protest and despair are discussed as they relate to behavioral and physiological differences observed following different separation paradigms.     

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.     

Multiple, brief maternal separations in the squirrel monkey: changes in hormonal and behavioral responsiveness

Infant squirrel monkeys had their mother removed from the home cage for 2 hr on 80 occasions between 12 and 31 weeks of age. The initial separation elicited high levels of infant vocalizations. By the second observation session (Separation 14), no vocal response to separation was observed. Plasma cortisol levels were markedly elevated at the beginning of the separation series, and there was a significant decline in this response by Separation 28, which was the next separation during which cortisol was monitored. However, there was no further decline, so that significant cortisol elevations were observed throughout the remainder of the separation series. At 35 weeks, the infants were separated one additional time and their responses were compared to those of a previously nonseparated control group. The control group vocalized more, but the two groups exhibited equivalent cortisol elevations. Observations of time spent riding on the mother during undisturbed conditions indicated that both groups developed independence from the mother at about the normal rate. Overall, the data show that brief separation from the mother can activate the infants' pituitary-adrenal system even when the infant has been separated 80 times previously, no longer appears behaviorally responsive to separation, is almost 9 months of age, and exhibits normal signs of independence from the mother.     

Behavioral and immunological consequences of brief mother-infant separation: a species comparison

The immediate behavioral and immunological consequences of a single 2-week maternal separation experience were studied in socially housed 7-month old bonnet and pigtail macaques. Maternal separation was associated with species dependent behavioral changes. Both species showed significant increases in ingestive behaviors associated with separation. Separated and matched controls showed an increase in disturbance behaviors (vocalization, startles, shaking, temper-tantrums) that subsided after 24-36 hours in control subjects, but continued, albeit with species-dependent patterns, in the separated monkeys. Allomaternal care of the separated bonnet infants but not the pigtail infants was associated with a progressive reduction of these disturbance behaviors during the separation period. Following a period of agitation, pigtail infants showed a depressive phase characterized by slouched, withdrawn postures and reduced motor activity. As a group, the separated infants of both species were not different from controls with respect to lymphocyte activation by mitogens, a measure of immunocompetence. However, when individual behavioral responses were considered, the change in lymphocyte activation during separation was significantly related to behavioral responses which reflected disturbance, such that the change in lymphocyte activation following in vitro stimulation with the mitogens phytohemagglutinin and Concanavalin A (markers of the immunocompetence of T lymphocytes) was related to levels of vocalization and time spent in slouched postures. The activation of B lymphocytes by pokeweed mitogen was not influenced by the separation experience nor was it associated with specific behavioral responses to separation. The importance of assessing the affective consequences of stressor is discussed.     

Influence of the maternal surrogate on pituitary–adrenal activity and behavior of infant squirrel monkeys

Squirrel monkey infants reared on surrogates showed an increase in vocalizations, but no change in plasma cortisol levels when the surrogate was removed from the home cage for .5 hr. When the infant was exposed to novelty during separation, there was a further increase in vocalizations, as well as increases in movement and plasma cortisol. Placing the surrogate with the infant in the novel environment reduced the behavioral reaction and led to high levels of infant-surrogate contact; however, plasma cortisol levels were as high at .5 hr as when the infant was in the novel environment alone. With longer (2–4 hr) exposures to the novel room, cortisol elevations were attenuated by the presence of the surrogate. When the infant was alone, levels of cortisol, but not protest behavior, increased with length of exposure to the novel room. These results indicate that the physiological reaction to separation procedures in infant primates may not be safely inferred from behavioral responses, and, together with earlier findings, suggest a deficiency in the attachment of surrogate-reared infants.     

The influence of maternal separation on plasma concentrations of ACTH, epinephrine, and norepinephrine in guinea pig pups

Preweaning guinea pigs were placed into a test cage either alone or with their mother for 10, 30, or 90 min, or were placed into the cage alone for 24 hr. At 30 and 90 min, pups exhibited higher plasma levels of ACTH if alone than if with the mother. This effect was not apparent at 10 min, and ACTH levels of pups tested alone were no longer greater than baseline levels at 24 hr. These results provide further evidence that brief maternal separation can serve as a potent stimulus for activation of the hypothalamo-pituitary-adrenal system in this species. Plasma epinephrine and norepinephrine concentrations of pups tested alone were not significantly greater than those of pups tested with their mothers. But, pups tested alone for 10 and 30 min did show an elevation of epinephrine and norepinephrine over baseline levels. That is, the combined influence of separation and other aspects of the manipulation (e.g., exposure to novelty) evoked sympathetic responses. In addition, the number of vocalizations emitted by pups during the first 30 min of isolation in the test cage was positively correlated with concentrations of ACTH, epinephrine, and norepinephrine following 24 hr of this procedure, but not following 90 min or at baseline. Thus, the initial behavioral response appears to be predictive of the levels of both hypothalamo-pituitary-adrenal and sympathetic activity 24 hr after separation is initiated.     

Responses of infant Titi monkeys,Callicebus moloch,to removal of one or both parents: Evidence for paternal attachment

The response to parental separation in infant titi monkeys was evaluated. Separation from the mother for 1 hr did not elicit an adrenocortical response from the infant unless the father was also removed. Separation from the father elicited a significant elevation in adrenocortical activity even when the mother remained with the infant during the separation period. Infants showed the highest cortisol levels and vocalization rates when both parents were removed and the infant remained alone in the living cage for 1 hr. As in previous research, infants maintained higher levels of contact with the father than with the mother. The results indicate that in this monogamous New World primate, the father is the primary attachment figure for the developing infant. © 1995 Johnv Wiley & Sons, Inc.     

Response of bonnet macaque dyads to an acute foraging task under different motivational conditions.

To explore behavioral patterns in bonnet macaque mother-infant dyads under environmental challenge, the motivation of infants to contact their mothers during a 1-hr foraging period was manipulated in two ways. First, sessions were given in which the infants were separated from their mothers for 3 hr prior to the foraging period. Second, sessions were given in which the infants were allowed access to food prior to the foraging period, thereby presumably reducing their motivation to separate from mother to seek food for themselves during the foraging period. Neither manipulation resulted in heightened conflict within the dyads. Separation of the infants prior to the foraging period did result, in general, in mothers forfeiting foraging task engagement to attend to their infants. The extent to which a mother exhibited this pattern correlated with her level of foraging effectiveness.     

Social and environmental factors influencing mother-infant separation-reunion in squirrel monkeys

Sixteen squirrel monkey mother and infant dyads were housed in groups of two. They were separated and then immediately reunited in their familiar home cage or in a novel environment, either in conjunction with the second mother-infant dyad, or as a single manipulated pair. Behavioral observations of both dyads were made during the 30-min period following these manipulations; blood samples were then taken for cortisol assay. Mothers' locomotor activity increased when a single dyad was manipulated in the home cage and decreased in the novel environment where proximity between the pairs increased. Cortisol levels varied significantly across conditions, with mothers and infants responding to different stimuli. Mothers responded primarily to social disruption, including separation from the other dyad, and infants responded most clearly to novelty and separation from the other dyad. No significant differences were observed over base levels when both mother and infant pairs were reunited in the home cage, indicating that changes were not due to the disturbance involved in the separation procedure.     

The relationship between affective responses in preseparation episodes and patterns of attachment behaviors in the strange situation

Fifty-six first born Japanese 12-month-old infants were observed in the Strange Situation and the relationship between affective responses in the preseparation episodes and patterns of attachment behaviors in the following episodes was examined. In the preseparation episodes, 18 infants were rated as displaying distress (HS) and 38 infants did not display distress (LS). HS infants were acutely distressed in the separation episodes, and did not easily recover from distress even after regaining close physical contact with mother in the reunion episodes. In contrast, LS infants did not show distress in the first separation and reunion episodes. Although they were distressed in the second separation, they recovered more easily than HS infants in the second reunion episode. Resistant behaviors in the second reunion were observed more frequently and were stronger in HS infants than LS infants. Eighty-three percent of B4 and C were HS infants and 84% of B were LS infants. These results indicated that the affective responses in the preseparation episodes could predict the patterns of attachment behaviors in the following episodes.     

Total cortisol,free cortisol,and growth hormone associated with brief social separation experiences in young macaques

Many behavioral, immunological, and physiological consequences of brief maternal separation in bonnet (Macaca radiata) and pigtail monkeys (Macaca nemistrina) have been documented. However, the impact of social separation on plasma cortisol and growth hormone is unknown for these particular species. In the present study, the behavioral and endocrinological consequences of a 2-week maternal separation in socially housed infant bonnet and pigtail monkeys were followed. In seven pairs (separated and matched control) of bonnet and six pairs of pigtail infants, plasma was obtained under baseline, separated, and reunion conditions twice weekly for the duration of the study. Blood samples were obtained from both infants of the pair in approximately 10 min. Plasma total cortisol, free cortisol, and growth hormone were measured in these samples. Focal animal behavioral observations were made on all subjects twice daily throughout the study period. In both species, total cortisol and free cortisol rose immediately following maternal separation in comparison to the matched nonseparated controls and returned to basal levels (e.g., that of matched non-separted controls) following reunion with the mother. In contrast, plasma growth hormone rose only in the pigtail infants over a time course that peaked around the time of reunion. Multiple regression techniques indicated for the first week of separation, in the separated but not control subjects, that mean plasma free and total cortisol was positively related to distress behaviors (vocalization and postural slouch) observed during this week and negatively related to social behaviors (play and proximity to others) noted during the same period. In contrast, plasma growth hormone was related to both species and sex of the subjects but unrelated to behavioral variables. © 1995 John Wiley & Sons, Inc.     

Insulin responses and glucose levels in plasma and cerebrospinal fluid during fasting and refeeding in the rat

The present experiments were designed to investigate the rate of penetration of insulin from the plasma into the cerebrospinal fluid (CSF) during 24 hr of fasting and refeeding in the light phase. The results show that under these conditions basal CSF-immunoreactive insulin (IRI) levels were positively correlated with plasma IRI levels. Basal plasma IRI fell during a fast but was similar to prefast control after one day of refeeding. Although CSF-IRI levels rose during glucose infusion, CSF-IRI was not elevated by glucose during a fast. During refeeding, CSF-IRI responses returned toward control, prefeeding values. This study suggests a decreased transport of insulin from plasma to CSF during fasting. The lower CSF-IRI levels achieved under these conditions may determine meal size by allowing larger meals after a fast.     

Attachment quality is related to the synchrony of mother and infant monitoring patterns

We investigated whether attachment quality is related to infant–mother dyadic patterns in monitoring animated social situations. Sixty 12-month-old infants and their mothers participated in an eye-tracking study in which they watched abstractly depicted distress interactions involving the separation of a “baby” and a “parent” character followed by reunion or further separation of the two characters. We measured infants’ and their mothers’ relative fixation duration to the two characters in the animations. We found that infant attachment disorganization moderated the correspondence between the monitoring patterns of infant–mother dyads during the final part of the animations resulting in reunion or separation. Organized infants and their mothers showed complementary monitoring patterns: the more the mothers focused their attention on the “baby” character, the more the infants focused their attention on the “parent” character, and vice versa. Disorganized infant–mother dyads showed the opposite pattern although the correlation was nonsignificant: mothers and their infants focused on the same character. The attachment-related differences in the nature of the synchrony in the attentional processes of infants and their mothers suggest that by 12 months the dyads’ representations of social situations reflect their shared social–emotional experiences.     

Hormonal and behavioral attachment responses in infant guinea pigs

Infant guinea pigs, 11/12 and 18/19 days of age, exhibited high rates of vocalizing and increases in plasma concentrations of cortisol when separated from their mothers for 30 min in a novel environment (unfamiliar cage in an unfamiliar room). Levels of vocalizations and plasma cortisol were significantly reduced when the pup was exposed to the novel environment with its own conscious or anesthetized mother, but not when it was exposed with an unfamiliar anesthetized lactating female. Pups spent equivalent amounts of time in physical contact with their own conscious mother, their own anesthetized mother and an unfamiliar anesthetized lactating female. Unexpectedly, when the unfamiliar cage was placed in an environmental chamber during separation, pups showed negligible increases in vocalizations and plasma cortisol levels, even when administered footshock just prior to exposure. These findings demonstrate that guinea pig pups exhibit adrenocorticoid as well as behavioral responses to maternal separation, provide further evidence for the existence of filial attachment in this species, and document an unexpected role of the test environment in determining responses during maternal separation. The guinea pig may afford a rodent model for examining the effects of attachment-object separation on the activity of the pituitary-adrenal system.     

Alterations of ventricular pH alter water intake and food consumption in rats

The pH of third ventricular CSF was altered by infusing acidic or alkaline solution of artificial cerebrospinal fluid (aCSF) through chronically implanted stainless steel cannula. In two separate group of rats (n = 18 each) water and food consumptions were recorded 30 min, 1 hr, and 24 hr after intraventricular infusions of the modified aCSF solutions having pH 6.0, 8.0 and 7.4 (control). On raising the CSF pH, water intake increased in all three observations. Feeding was not affected in the observations taken after 30 min and 1 hr, but significantly reduced food consumption was observed 24 hr after the infusions. Lowering of pH had no effect either on dipsogenic or feeding response. The CSF pH correlated positively with drinking in all three observations. Since dipsogenic and feeding responses are centrally regulated by ion sensitive cells, it may be presumed that altered CSF pH influenced the activities of the sensors by altering ionic conductance across their membranes.     

The role of peers in modifying behavioral distress and pituitary-adrenal response to a novel environment in year-old rhesus monkeys

The effects of a peer's presence were examined for 9 mother-reared rhesus monkeys (mean age=12 months). Subjects were captured from their social groups and placed in single cages for 24 hr under each of 4 conditions: Alone, with Mother, with a Peer from the Same Group, or with a Peer from a Different Group. Plasma cortisol and behavioral data were obtained. Thirty min after capture the presence of a peer from a different social group produced elevations in plasma cortisol greater than those observed in all but the Alone condition. This effect was not apparent 24 hr later. Furthermore, by 22 hr after capture the presence of a peer from either social group significantly reduced agitated behavior, as compared to responses observed when subjects were housed alone. These subjects thus readily habituated to the less familiar peer to whom they initially responded. Physical contact and whoo calling clearly differentiated responses to peer from mother, suggesting that the calming effect of a peer's presence was not sufficient that the peer serve as a surrogate attachment figure. The results indicate the role of peer conspecifics in modifying responses to stressful situations in young group-reared rhesus monkeys.     

Ventrobasal thalamus necessary for visually-released defensive boxing of rat

Pituitary-adrenal response in mother and infant squirrel monkeys was assessed following either 30 min separation or 5, 15 and 30 min after a brief separation and reunion of mother and infant. Basal (undisturbed) samples were also obtained. The results revealed that there was an increment (28%) in plasma cortisol levels in the separation-reunion condition. This change was slight however when compared to the changes in plasma cortisol following separation (120%). A second experiment assessed plasma cortisol levels in mothers and infants that were reunited following a 30 min separation. Blood samples obtained 30 min after reunion indicated that the plasma cortisol levels in mothers had returned to basal levels, whereas the infants remained highly elevated during this period. Thus the effects of reunion following a very brief separation show the operation of an inhibitory process which occurs as a result of the interaction between mother and infant. Reunion following a longer separation appears to be more effective in reducing the pituitary-adrenal response in the mother than in the infant.     

Maternal and nutritional contributions to infant rats' activational responses to ingestion

Infant rats deprived of food, maternal care, and the opportunity to suckle display a dramatic behavioral activation and vigorously ingest when provided milk through oral cannulas. These experiments assessed which components of deprivation are important in producing these responses to milk. Nutritional deprivation alone, with or without the presence of an active maternal female, appears to be sufficient to produce ingestion. Behavioral activation, on the other hand, appears to require both nutritional deprivation and deprivation from a maternal female. The effect of maternal stimulation on later behavioral reactivity was not a function of the pups' opportunity to suckle. However, active maternal stimulation was more effective in preventing activation than was passive maternal stimulation (e.g., thermotactile and olfactory stimulation). Stimulation provided by an active, nonlactating mother was effective in preventing behavioral activation, but the effect was short-lived, lasting only 2 hr after the pup was removed from the mother's care. This series of studies thus reveals that identified components of maternal separation have dissociable effects on appetitively motivated behaviors in infant rats.