Imitation promotes affiliation in infant macaques at risk for impaired social behaviors

Sclafani, Valentina; Paukner, Annika; Suomi, Stephen J.; Ferrari, Pier Francesco

doi:10.1111/desc.12237

Cited by 24 publications

(18 citation statements)

References 80 publications

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“…infant macaques (16,17), among healthy children (1), and in children with autistic spectrum disorder (18)(19)(20)(21). The evidence presented here, which links synchrony to dopamine, provides initial evidence that dopamine is involved in the prosocial effects of synchrony.…”

Section: Discussionmentioning

confidence: 69%

Dopamine in the medial amygdala network mediates human bonding

Atzil

Touroutoglou

Rudy

et al. 2017

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

116

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Research in humans and nonhuman animals indicates that social affiliation, and particularly maternal bonding, depends on reward circuitry. Although numerous mechanistic studies in rodents demonstrated that maternal bonding depends on striatal dopamine transmission, the neurochemistry supporting maternal behavior in humans has not been described so far. In this study, we tested the role of central dopamine in human bonding. We applied a combined functional MRI-PET scanner to simultaneously probe mothers' dopamine responses to their infants and the connectivity between the nucleus accumbens (NAcc), the amygdala, and the medial prefrontal cortex (mPFC), which form an intrinsic network (referred to as the "medial amygdala network") that supports social functioning. We also measured the mothers' behavioral synchrony with their infants and plasma oxytocin. The results of this study suggest that synchronous maternal behavior is associated with increased dopamine responses to the mother's infant and stronger intrinsic connectivity within the medial amygdala network. Moreover, stronger network connectivity is associated with increased dopamine responses within the network and decreased plasma oxytocin. Together, these data indicate that dopamine is involved in human bonding. Compared with other mammals, humans have an unusually complex social life. The complexity of human bonding cannot be fully captured in nonhuman animal models, particularly in pathological bonding, such as that in autistic spectrum disorder or postpartum depression. Thus, investigations of the neurochemistry of social bonding in humans, for which this study provides initial evidence, are warranted.arly social bonding with a primary caregiver is necessary for mental and physical health, whereas the absence of such bonding is a clear risk factor for adult illness (1). However, despite potentially enormous implications, to date the science of mother-infant bonding relies mostly on nonhuman animal models.Research on nonhuman animals indicates that maternal bonding involves the nucleus accumbens (NAcc), amygdala, and medial prefrontal cortex (mPFC). In rodents, oxytocin and dopamine act in the amygdala and NAcc (2) to regulate maternal appetitive behaviors. In humans, functional MRI (fMRI) studies have verified that NAcc activity increases consistently when mothers gaze at their infants (3). Moreover, the NAcc and amygdala activity have been linked to the quality of maternal behavior (4). Mothers who were sensitive to their infants' cues for social engagement and who adjusted their own behavior to meet those needs (referred to as "mother-infant synchrony"), showed greater activations in the left NAcc and lower activation in the right amygdala when viewing films of their infants than did nonsynchronous mothers (4). In agreement with the animal studies, oxytocin has been implicated in human maternal behavior, so that synchronous mothers show a stronger link between levels of circulating plasma oxytocin and NAcc fMRI activations when viewing films of their in...

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Section: Discussionmentioning

confidence: 69%

Dopamine in the medial amygdala network mediates human bonding

Atzil

Touroutoglou

Rudy

et al. 2017

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

116

View full text Add to dashboard Cite

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“…With regard to mirroring, given that this behaviour increases the engagement and affiliation of recipients, including infant primates313233, the question arises whether its positive effect on the development of infant social expressiveness in our study was of this generic, motivational, kind. This seems unlikely, because only maternal mirroring of social, but not non-social, behaviours increased subsequent infant social expressiveness.…”

Section: Discussionmentioning

confidence: 95%

The functional architecture of mother-infant communication, and the development of infant social expressiveness in the first two months

Murray

Pascalis

Bozicevic

et al. 2016

Sci Rep

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121

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By two-three months, infants show active social expressions during face-to-face interactions. These interactions are important, as they provide the foundation for later emotional regulation and cognition, but little is known about how infant social expressiveness develops. We considered two different accounts. One emphasizes the contingency of parental responsiveness, regardless of its form; the other, the functional architecture account, emphasizes the preparedness of both infants and parents to respond in specific ways to particular forms of behaviour in their partner. We videotaped mother-infant interactions from one to nine weeks, and analysed them with a micro-analytic coding scheme. Infant social expressiveness increased through the nine-week period, particularly after 3 weeks. This development was unrelated to the extent of maternal contingent responsiveness, even to infant social expressions. By contrast, specific forms of response that mothers used preferentially for infant social expressions-mirroring, marking with a smile- predicted the increase in these infant behaviours over time. These results support a functional architecture account of the perceptual and behavioural predispositions of infants and parents that allow young infants to capitalize on relatively limited exposure to specific parental behaviours, in order to develop important social capacities.

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“…We chose macaques because they share many aspects of human physiology, development, cognition, and social complexity (Phillips et al 2014) and exhibit pronounced individual differences in sociality across development (Dettmer et al 2016; Sclafani et al 2016). We tested macaque infants reared in a neonatal nursery by human caretakers, a population at risk for impaired social behaviors (e.g., Sclafani et al 2015; Winslow, 2003), and who therefore may benefit the most from OT interventions. We chose to test one-month-olds to assess infants when they were still beginning to develop working memory and gaze following; therefore, an intervention would have the potential to produce positive changes in these skills.…”

mentioning

confidence: 99%

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

et al. 2016

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Rationale Exogenous oxytocin administration is widely reported to improve social cognition in human and nonhuman primate adults. Risk factors of impaired social cognition, however, emerge in infancy. Early interventions—when plasticity is greatest—are critical to reverse negative outcomes. Objective We tested the hypothesis that oxytocin may exert similar positive effects on infant social cognition, as in adults. To test this idea, we assessed the effectiveness of acute, aerosolized oxytocin on two foundational social cognitive skills: working memory (i.e., ability to briefly hold and process information) and social gaze (i.e., tracking the direction of others’ gaze) in one-month-old nursery-reared macaque monkeys (Macaca mulatta). We did not predict sex differences, but we included sex as a factor in our analyses to test whether our effects would be generalizable across both males and females. Results In a double-blind, placebo-controlled design, we found that females were more socially skilled at baseline compared to males, and that oxytocin improved working memory and gaze following, but only in males. Conclusions These sex differences, while unexpected, may be due to interactions with gonadal steroids and may be relevant to sexually dimorphic disorders of social cognition, such as male-biased autism spectrum disorder, for which oxytocin has been proposed as a potential treatment. In sum, we report the first evidence that oxytocin may influence primate infant cognitive abilities. Moreover, these behavioral effects appear sexually dimorphic, highlighting the importance of considering sex differences. Oxytocin effects observed in one sex may not be generalizable to the other sex.

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Imitation promotes affiliation in infant macaques at risk for impaired social behaviors

Cited by 24 publications

References 80 publications

Dopamine in the medial amygdala network mediates human bonding

Dopamine in the medial amygdala network mediates human bonding

The functional architecture of mother-infant communication, and the development of infant social expressiveness in the first two months

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

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