Behavioral and hormonal effects of attachment object separation in surrogate-peer-reared and mother-reared infant rhesus monkeys

Mother-reared and surrogate-peer-reared rhesus monkeys were separated from their respective attachment objects at 6 months of age and tested for the following 9 weeks to determine their home cage behavior and their pituitary-adrenocortical responses to stress. Both groups displayed a strong immediate behavioral response to separation which was characterized by increases vocalization, increased locomotion, and decreased self-play. However, the surrogate-peer-reared infants showed a subsequent recovery in their levels of self-play whereas the mother-reared infants instead developed stereotypic behavior patterns such as repetitive pacing. The 2 groups displayed similar plasma cortisol responses to weekly sessions in an apparatus equipped with animated toy “monsters.” Mother-reared but not surrogate-peer-reared subjects, however, also manifested elevated cortisol levels when an animal in an adjacent cage was captured and removed for stress testing. Mother-reared infant monkeys thus responded in a stronger and more prolonged manner to the loss of their attachment object than surrogate-peer-reared infants. These results suggest that infant rhesus monkeys form stronger attachments to monkey mothers than to inanimate surrogate mothers, a phenomenon which has not been as clearly demonstrated using other indices of attachment strength.     

Pituitary-adrenal response to separation in mother and infant squirrel monkeys.

Pituitary-adrenal response in mother and infant squirrel monkeys following brief separation was assessed. Each mother and infant pair was tested under each of 3 conditions: (1) Basal; (2) Separation-Reunion; and (3) Separation. Samples were obtained from mothers and infants in the Separation and Separation-Reunion conditions 30 min following the initial disturbance. A similar paradigm was used to assess the effects of separation in surrogate-reared animals. The results indicate that mothers, infants, and surrogate-reared infants respond to 30-min separation with a substantial increase in plasma cortisol. The values obtained in the Separation-Reunion condition did not differ significantly from Basal values in any of the 3 groups, suggesting that the effect of separation on the pituitary-adrenal system is not due to the disturbance involved in the separation procedure. The response of surrogate-reared infants suggests that these infants develop similar attachments to the surrogate as normal infants to their own mothers.     

Physiological correlates of maternal separation in surrogate-reared infants: a study in altered attachment bonds.

Three pigtail infant monkeys (Macaca nemestrina) were separated from their mothers shortly after birth and raised in social isolation on cloth surrogates. At about 24 weeks of age they were surgically implanted with multichannel biotelemetry systems. Following the collection of baseline behavioral and physiological data, the cloth surrogates were removed for 4 days, then returned. The behavioral and physiological (heart rate, body temperature, sleep patterns) reaction to separation from the surrogate was much less intense than is the case in group-living pigtail infants that are separated from their mothers, suggesting that the attachment bond to a cloth surrogate may be different than the bond to a living mother in a social group. Heart rate mean values and variability were similar in surrogate-reared and mother-reared infants, suggesting a degree of environmental independence in heart rate regulation.     

Nocturnal sleep in isolation-reared monkeys: evidence for enviromental independence.

Thirteen all-night recordings were obtained from 3 infant pigtailed (Macaca nemestrina) monkeys raised on a cloth surrogate mother and under conditions of social isolation. Totally implantable biotelemetry systems were used to record the sleep physiology from the unrestrained animals. Sleep stages and night-to-night variability were virtually identical to values previously found in 8 mother-reared group-living infants. Sustained alterations in the early rearing enviroment, even though considerably modifying the organism's development, did not appear to result in differences in sleep organization.     

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.     

Brief separation elevates cortisol in mother and infant squirrel monkeys

The pituitary-adrenal response of mother and infant squirrel monkeys was assessed under basal conditions and after 5, 10, or 20 min of separation followed by 30 min of reunion. All separation conditions produced equal increments of cortisol (approximately 50%) in both mothers and infants. These increments were lower than would have occurred in the absence of reunion. These results extend previous reports that reunion ameliorates the psychoendocrine effects of separation and indicate that mother-infant attachment can be studied with shorter periods of separation than have been used customarily.     

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.     

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.     

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)     

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.     

Effect of surrogate–administered punishment on surrogate contact in infant squirrel monkeys

Three experiments were conducted in which surrogate-reared infant squirrel monkeys were exposed to punishment in the form of pressurized air emitted from the bodies of the surrogates. Punishment was administered irregularly during the day between the ages of 6 and 34 weeks, under different schedules of random presentation and at different parameters of the airblast stimulus. Physical contact with the surrogate was recorded separately for day and night activity. The results of all experiments were consistent in showing that punished infants spent less time than did nonpunished controls in contacting their surrogates during the daytime throughout the entire period of study. Nighttime scores were less consistent, but showed the same trend in 2 of the experiments. The results also suggested that different subtypes of squirrel monkeys are inherently different in their degree of surrogate contact, with monkeys of the Bolivian type spending more time in contact than those of either Peruvian or Colombian descent.     

Contrasting responses to intruders and to involuntary separation by monogamous and polygynous New World monkeys

The strength and quality of the relationship between heterosexual pairmates were compared in two species of New World monkeys, the polygynous squirrel monkey (Saimiri) and the monogamous titi monkey (Callicebus). This was accomplished by measuring behavioral and adrenocortical responses to intruders and to involuntary separation from the pairmate. The species diverged sharply in their responses to these conditions. For titi monkeys, the presence of an intruder resulted in a marked increase in behavioral signs of agitation, which were more prominent in the subject of the same sex as the intruder. Most male titi monkeys showed an increase in plasma cortisol in the presence of a male intruder; this pattern was not seen in their response to a female intruder. Female titi monkeys showed no consistent pattern of adrenocortical response to intruders of either sex. For squirrel monkeys, the presence of an intruder resulted in increased frequency of displays in male subjects, but not in female subjects. Both sexes showed a reliable reduction in plasma cortisol, below basal levels, in the presence of a female intruder, whereas no effect on cortisol was produced by a male intruder. Titi monkeys, but not squirrel monkeys, responded to separation with a significant increase in plasma cortisol and in behavioral indices of agitation or distress.     

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

Infant guinea pigs recently were found to respond to brief maternal separation with an increase in plasma cortisol levels. The present experiments were conducted to further characterize this response and compare it with the cortisol separation response previously observed in primates. In Experiment 1, separation of guinea pig pups from their mothers did not elevate the plasma cortisol levels of the pups at either 30 or 180 min when they remained alone in their home cages during the separation. Experiment 2 showed that cortisol levels of pups placed alone in a novel cage were greater at 30, 90, and 180 min than were those of pups placed in the cages together with their mothers. In contrast, the separated pups vocalized more than did pups tested with their mothers during the initial 30 min only. In Experiment 3, pups raised on inanimate surrogates responded less intensely to rearing-figure separation in terms of both cortisol and vocalizations than did mother-reared controls. Taken together, these results indicate both differences (response to home cage separation) and similarities (dissociation of cortisol and vocalization responses, effect of surrogate separation) in the separation responses of guinea pig and primate infants. The guinea pig model may provide a useful adjunct to primate studies for examining particular issues concerning physiological effects of brief separation from an attachment object.     

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.     

Postnatal foraging demands alter adrenocortical activity and psychosocial development

Mother squirrel monkeys stop carrying infants at earlier ages in high-demand (HD) conditions where food is difficult to find relative to low-demand (LD) conditions. To characterize these transitions in psychosocial development, from 10- to 21-weeks postpartum we collected measures of behavior, adrenocortical activity, and social transactions coded for initiator (mother or infant), goal (make-contact or break-contact), and outcome (success or failure). Make-contact attempts were most often initiated by HD infants, but mothers often opposed these attempts and less than 50% were successful. Break-contact attempts were most often initiated by LD infants, but mothers often opposed these attempts and fewer LD than HD infant break-contact attempts were successful. Plasma levels of cortisol were significantly higher in HD than LD mothers, but differences in adrenocortical activity were less consistent in their infants. HD and LD infants also spent similar amounts of time nursing on their mothers and feeding on solid foods. By rescheduling some transitions in development (carry→self-transport), and not others (nursing→self-feeding), mothers may have partially protected infants from the immediate impact of an otherwise stressful foraging task. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 285–291, 1998     

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.     

Intergenerational effects of mother's early rearing experience on offspring treatment and socioemotional development

This longitudinal study spans two generations of rhesus monkeys. First, the study investigates the effects of early rearing experiences on the maternal behavior of first-generation mothers (rates of premature infant rejection) and, second, the study investigates the effects of maternal rejection on the behavior of second-generation infants. Rhesus macaque mother–infant dyads (Macaca mulatta—N = 176) were observed twice weekly, with each session lasting 300 s. First-generation mothers were raised in one of three conditions: as mother-reared controls (MR; [n = 95]), in peer groups (PR; raised without adults but with constant access to three same-aged peers [n = 49]), or with an inanimate surrogate (SPR; raised with an inanimate fleece-covered, surrogate mother and limited daily peer-group interactions [n = 32]). Second-generation infants were all raised by their differentially reared mothers and statistically grouped into one of two groups: those that were rejected by their mothers beginning at a more-typical weaning age (controls), starting in the third month of life (n = 108), and those that were prematurely rejected, with mothers showing rejections before the third month of infant life (n = 68). Overall, PR mothers exhibited the highest rates of premature infant rejection, except for month 1 of infant life, when SPR mothers exhibited the highest rates of rejection. Intriguingly, after month 1, SPR mothers showed high rates of infant cradling and seldom rejected their infants. Independent of their mothers’ early rearing environment, prematurely rejected infants displayed more aggression and passive vigilance, and were cradled and groomed less by their mothers, and there was evidence that the overall rates of rejection after the first 2 months of life had a cumulative negative effect on the developing infant. Post hoc analyses of plasma cortisol levels showed that the prematurely rejected infants had higher cortisol concentrations, suggesting a high level of stress in the prematurely rejected infants. These results suggest that maternal presence during infancy has long-term effects on a female's future maternal skills which, in turn, have intergenerational consequences for the socioemotional development of second-generation infants.     

Social rearing effects on HPA axis activity over early development and in response to stress in rhesus monkeys

Previous studies have found evidence of behavioral and psychophysiological differences between nonhuman primates reared in different social environments, however, few of these have employed longitudinal study of the animals over early development. In this study, HPA axis activity was assessed via measurement of ACTH and cortisol values over the first 6 months of life and in response to two stressful housing transitions in 48 infant rhesus monkeys that were either mother- or peer-reared. ACTH and cortisol values declined over the first 6 months in both rearing groups. Peer-reared monkeys showed lower levels of ACTH over the first 6 months of life than mother-reared, but the rearing groups did not differ in basal cortisol values over this period. Mother-reared animals showed a greater ACTH response to the mild stress of being moved to a new cage, and male monkeys showed higher values than females. Mother-reared animals showed the largest cortisol increase in response to the caging transition. Both groups showed increases in ACTH and cortisol in response to the more severe stress of separation from their rearing partners and housing with unfamiliar agemates. Mother-reared animals again showed the largest increase in ACTH in response to these events, but increases in cortisol were similar among both sexes and rearing groups. These results suggest an interaction of sex and rearing history in response to stressful events. © 1993 John Wiley & Sons Inc.     

Behavioral development and maternal care in tufted capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) from birth through seven months.

Fourteen infant capuchins and eight squirrel monkeys reared by their mothers in captive species-typical social groups were observed from birth through 7 months. Motoric altriciality of the neonatal capuchin relative to the squirrel monkey is a key feature of behavioral differences between the species in the first few months after birth. Infants of the two species differed substantially in age at onset of independent locomotion, the developmental profile of independent activities, and the overall amount and rate of particular social activities. Capuchins displayed a lag of 7 weeks relative to squirrel monkeys in the pattern of increasing time spent alone; lags in other indices of independent activity and exploratory behaviors were also evident, although not as clear-cut. The species also differed substantially in the nature and frequency of social interactions between infants and others. Capuchins, especially later-born infants of multiparous mothers, experienced a more socially interactive infancy than squirrel monkeys. Contrasts in behavioral developmental and infant care in the two species are related to the timing and duration of the weaning process.     

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.