Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta).

Bayart, Françoise; Hayashi, Kevin T.; Faull, Kym F.; Barchas, Jack D.; Levine, Seymour

doi:10.1037/0735-7044.104.1.98

Cited by 110 publications

(66 citation statements)

References 19 publications

(19 reference statements)

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“…Maternal presence has a strong regulatory influence on the ANS and HPA axis in rodents and primates (11,43), and insecure attachment is associated with elevated cortisol reactivity and vagal withdrawal in young children (44,45). Moreover, placement before 24 months in BEIP is also associated with substantially greater odds of developing a secure attachment (42), indicating a similar sensitive period for attachment security as we observe for cortisol reactivity and vagal regulation.…”

Section: Discussionsupporting

confidence: 57%

“…Rhesus and squirrel monkeys exposed to prolonged early-life maternal deprivation exhibit elevated basal levels of cortisol (7-9), enhanced glucocorticoid feedback sensitivity (10), and heightened cortisol reactivity to social stress in some studies (11,12), but lower basal cortisol and reduced cortisol reactivity in others (9,13,14). The effect of maternal deprivation on SNS development in nonhuman primates has been studied infrequently.…”

mentioning

confidence: 99%

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Causal effects of the early caregiving environment on development of stress response systems in children

McLaughlin

Sheridan

Tibu³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

381

330

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Disruptions in stress response system functioning are thought to be a central mechanism by which exposure to adverse early-life environments influences human development. Although early-life adversity results in hyperreactivity of the sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis in rodents, evidence from human studies is inconsistent. We present results from the Bucharest Early Intervention Project examining whether randomized placement into a family caregiving environment alters development of the autonomic nervous system and HPA axis in children exposed to early-life deprivation associated with institutional rearing. Electrocardiogram, impedance cardiograph, and neuroendocrine data were collected during laboratorybased challenge tasks from children (mean age = 12.9 y) raised in deprived institutional settings in Romania randomized to a highquality foster care intervention (n = 48) or to remain in care as usual (n = 43) and a sample of typically developing Romanian children (n = 47). Children who remained in institutional care exhibited significantly blunted SNS and HPA axis responses to psychosocial stress compared with children randomized to foster care, whose stress responses approximated those of typically developing children. Intervention effects were evident for cortisol and parasympathetic nervous system reactivity only among children placed in foster care before age 24 and 18 months, respectively, providing experimental evidence of a sensitive period in humans during which the environment is particularly likely to alter stress response system development. We provide evidence for a causal link between the early caregiving environment and stress response system reactivity in humans with effects that differ markedly from those observed in rodent models.childhood adversity | early-life stress | HPA axis | autonomic nervous system | stress reactivity D isruptions in stress response system functioning are thought to be a central mechanism by which exposure to adverse early-life environments influences human development. This idea is borne out in rodent models, where the effects of early-life adversity on the development of stress response systems have been well characterized. Exposure to early-life adversityinvolving repeated and prolonged separation of a pup from its mother-results in hyperreactivity of the sympathetic nervous system (SNS) and the hypothalamic-pituitary-adrenal (HPA) axis in adolescence and adulthood and elevations in anxiety, fearful behaviors, and hypervigilance (1-4). Stress exposure in mature rodents is associated with immediate, but not lasting, changes in stress response systems (5, 6), suggesting the presence of an early sensitive period when exposure to adverse environments results in long-term changes in physiological stress response system functioning.

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Section: Discussionsupporting

confidence: 57%

mentioning

confidence: 99%

Causal effects of the early caregiving environment on development of stress response systems in children

McLaughlin

Sheridan

Tibu³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

381

330

View full text Add to dashboard Cite

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“…Normal infants physically separated from their mothers respond with species-typical protest behaviors (Sackett, 1970;Bayart et al, 1990) and immediately seek proximity to their mothers (Sackett et al, 1967;Suomi et al, 1973Suomi et al, , 1983. Furthermore, separation paradigms in which the mother is visible but not physically accessible, such as in the mother preference test used in this study, provoke severe behavioral distress responses, as indicated by increased vocalizations (Seay and Harlow, 1965;Levine et al, 1984).…”

Section: Discussionmentioning

confidence: 99%

The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys

Bauman¹,

Lavenex²,

Mason³

et al. 2004

J. Neurosci.

111

145

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As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, we examined the development of mother-infant interactions in 24 macaque monkeys who received either bilateral amygdala or hippocampus ibotenic acid lesions, or a sham surgical procedure at 2 weeks of age. After surgery, the infants were returned to their mothers and reared with daily access to small social groups. Behavioral observations of the infants in dyads (mother-infant pairs alone), tetrads (two mother-infant pairs), and social groups (six mother-infant pairs and one adult male) revealed species-typical mother-infant interactions for all lesion conditions, with the exception of increased physical contact time between the amygdala-lesioned infants and their mothers. Immediately after permanent separation from their mothers at 6 months of age, the infants were tested in a mother preference test that allowed the infants to choose between their mother and another familiar adult female. Unlike control and hippocampus-lesioned infants, the amygdala-lesioned infants did not preferentially seek proximity to their mother, nor did they produce distress vocalizations. Given the normal development of mother-infant interactions observed before weaning, we attribute the behavior of the amygdala-lesioned infants during the preference test to an impaired ability to perceive potential danger (i.e., separation from their mother in a novel environment), rather than to a disruption of the mother-infant relationship. These results are consistent with the view that the amygdala is not essential for fundamental aspects of social behavior but is necessary to evaluate potentially dangerous situations and to coordinate appropriate behavioral responses.

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“…One possible explanation for sertraline's loss of effectiveness, consistent with our hypotheses, is that stress overrode the pharmacological effects of sertraline. In primates, social stress increases CNS serotonin turnover rate (Bayart et al 1990). This is particularly true during aggressive encounters (Higley et al 1996a).…”

Section: J Higley Et Almentioning

confidence: 99%

The Serotonin Reuptake Inhibitor Sertraline Reduces Excessive Alcohol Consumption in Nonhuman Primates: Effect of Stress

Higley

Hasert²,

Suomi³

et al. 1998

Neuropsychopharmacology

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Many monkeys that are reared without adult influence, with only peers, voluntarily consume alcohol in amounts producing intoxication on a relatively regular basis. Using a cross-over design, eight adolescent, peer-reared rhesus monkeys were allowed unfettered access to an 8.4% ethanol solution and treated with 20 mg/kgA large number of preclinical studies have reported high rates of alcohol consumption among animals with reduced central nervous system (CNS) serotonin functioning (for reviews, see Sellers et al. 1992;LeMarquand et al. 1994b). Among humans, clinical studies show evidence of reduced CNS serotonin functioning in subjects at risk for or who exhibit early onset alcohol abuse and alcoholism (for recent reviews see LeMarquand et al. 1994a;Litten et al. 1996;Pettinati 1996). Some recent studies show that selective serotonin reuptake inhibitors (SSRIs) are promising as adjunctive pharmacological treatment for maintenance of abstinence (see LeMarquand et al. 1994b). Preclinical studies with rodents show that the SSRIs reduce alcohol consumption (LeMarquand et al. 1994b). Similarly, in a number of small scale studies, SSRIs have shown promise as an adjunct treatment for alcohol abuse and alcoholism (LeMarquand et al. 1994a;Pettinati 1996). The controlled studies conducted by Gorelick (1989) and Kranzler et al. (1995) showed, however, that fluoxetine was ineffective in promoting maintenance of abstinence among treatment-seeking alcoholics. More recently, researchers used a controlled study to demonstrate that citalopram was efficacious in promoting maintenance 18 , NO . 6 of abstinence among early-onset, violent male alcoholics thought to have reduced central serotonin functioning (Tiihonen et al. 1996). Because of the conflicting reports on the efficacy of the SSRIs in the maintenance of abstinence, we decided to investigate sertraline as a potential treatment for excessive alcohol intake, using a nonhuman primate model with monkeys known to have reduced central serotonin functioning (Higley et al. 1996d,e). Furthermore, we designed the study specifically to examine the role that stress plays in excessive alcohol consumption among nonhuman primates and to test the efficacy of sertraline in mitigating the effects of stress on alcohol consumption.Until recently, it was widely believed that nonhuman primates would not voluntarily consume alcohol in appreciable quantities (e.g., Mello and Mendelson 1971;Meisch et al. 1975;Crowley et al. 1983); consequently, they were not typically used in research on alcohol abuse. More recent studies have shown, however, that for many species of primates, many (but not all) subjects will freely consume alcohol in quantities that produce pharmacological effects when an alcohol solution is palatable (Higley et al. 1991;Higley 1996;Higley and Linnoila 1997). Within some species, such as rhesus macaques and other Old World primate species, some individual subjects will routinely consume sufficient quantities of alcohol to produce blood levels exceeding the limits of legal in...

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Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta).

Cited by 110 publications

References 19 publications

Causal effects of the early caregiving environment on development of stress response systems in children

Causal effects of the early caregiving environment on development of stress response systems in children

The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys

The Serotonin Reuptake Inhibitor Sertraline Reduces Excessive Alcohol Consumption in Nonhuman Primates: Effect of Stress

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