Development of social fear after amygdalectomy in infant rhesus monkeys

Thompson, Carl I.; Schwartzbaum, J. S.; Harlow, Harry F.

doi:10.1016/0031-9384(69)90088-2

Cited by 45 publications

(44 citation statements)

References 17 publications

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“…A subtle, but distinct, alternative explanation for their lack of reaction is that the amygdala-lesioned infants were actually so secure in their attachment to their mother that visual access to their mothers was sufficient to alleviate the distress response during physical separation in the unfamiliar environment. However, given the overall lack of fear exhibited by amygdala-lesioned infants during exposure to novel environments (Thompson et al, 1969) and unfamiliar objects (Prather et al, 2001) without their mothers present, we favor the interpretation that the amygdala-lesioned infants simply fail to identify potential danger, whether or not the mother is present.…”

Section: Discussionmentioning

confidence: 61%

“…b, Bars represent the group average frequency of approaches Ϯ SEM per 120 sec trial. Asterisks denote significant onetailed paired t tests ( p Ͻ 0.05) (Thompson et al, 1969;Prather et al, 2001), neonatal amygdala lesions result in abnormal fear of conspecifics. Given that situations invoking fear or anxiety in young primates cause the subject to seek contact with its attachment figure (Mason and Capitanio, 1988), one can reasonably propose that the increased motherinfant contact time of the amygdala-lesioned infants may reflect an early mechanism of coping with the fear evoked by the presence of other conspecifics.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, infant macaques without an amygdala respond to unthreatening social interactions with heightened fear behaviors (Thompson et al, 1969;Prather et al, 2001). Although it is unclear why amygdala lesions result in decreased social fear responses in mature subjects and increased social fear responses in immature subjects, it is clear that amygdala lesions consistently disrupt the ability to correctly evaluate potential social danger (novel adult social partner), or lack thereof (unthreatening infant social partner), and respond appropriately.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

Bauman¹,

Lavenex²,

Mason³

et al. 2004

J. Neurosci.

111

145

View full text Add to dashboard Cite

show abstract

“…For example, neonatal amygdala lesions in rodents have been shown to result in severe changes in social behavior (Daenen et al, 2002;Hanlon and Sutherland, 2000). In primates, Thompson and colleagues (Thompson and Towfighi, 1976;Thompson et al, 1968, Thompson et al, 1969 showed that bilateral amygdala lesions (created by aspiration) made during the third postnatal month leave subjects affectively and socially impaired. After surgery, operated monkeys displayed more fear responses during social encounters than did control monkeys with whom they were paired, and the fear responses made by the operated monkeys were most profound whenever control animals became more active.…”

Section: Maturation Of the Orbitofrontal-limbic Circuit And Severity mentioning

confidence: 97%

The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism

Bachevalier

Loveland

2006

Neuroscience & Biobehavioral Reviews

357

267

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“…Additional studies suggest that these social deficits are related to difficulties assessing and responding to threatening stimuli. (Thompson, 1981;Thompson et al, 1969Thompson et al, , 1977Thompson and Towfighi, 1976) Evidence of a progressive deficit in social and emotional behavior after selective neonatal injuries to the amygdala was replicated by , who examined the development of social interactions of monkeys amygdalectomized during the first postnatal month. Their findings indicated that early damage to the amygdala results in progressively profound changes in affective responses and social behavior, and these changes persisted into adulthood.…”

Section: Neurodevelopmental Model Of Socioemotional Deficit: Neonatalmentioning

confidence: 99%

Non-Human Primates: Model Animals for Developmental Psychopathology

Nelson

Winslow

2008

Neuropsychopharmacol

100

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Non-human primates have been used to model psychiatric disease for several decades. The success of this paradigm has issued from comparable cognitive skills, brain morphology, and social complexity in adult monkeys and humans. Recently, interest in biological psychiatry has focused on similar brain, social, and emotional developmental processes in monkeys. In part, this is related to evidence that early postnatal experiences in human development may have profound implications for subsequent mental health. Non-human primate studies of postnatal phenomenon have generally fallen into three basic categories: experiential manipulation (largely manipulations of rearing), pharmacological manipulation (eg drug-induced psychosis), and anatomical localization (defined by strategic surgical damage). Although these efforts have been very informative each of them has certain limitations. In this review we highlight general findings from the non-human primate postnatal developmental literature and their implications for primate models in psychiatry. We argue that primates are uniquely capable of uncovering interactions between genes, environmental challenges, and development resulting in altered risk for psychopathology.

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Development of social fear after amygdalectomy in infant rhesus monkeys

Cited by 45 publications

References 17 publications

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

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

The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism

Non-Human Primates: Model Animals for Developmental Psychopathology

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