Oxytocin modulates fMRI responses to facial expression in macaques

Liu, Ning; Hadj-Bouziane, Fadila; Jones, Katherine M.; Turchi, Janita; Averbeck, Bruno B.; Ungerleider, Leslie G.

doi:10.1073/pnas.1508097112

Cited by 57 publications

(50 citation statements)

References 57 publications

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“…Elevated oxytocin levels in both the CNS and periphery are most likely due to the direct effects of exogenous peptide administration, although it is impossible to rule out a contribution from endogenous oxytocin release (50). Finally, functional magnetic resonance imaging (fMRI) studies have demonstrated that intranasal oxytocin produces changes in the activity of several brain areas in humans and macaques (49,56,57), thus supporting other findings of the CNS effects of this neuromodulator (58).…”

Section: Discussionmentioning

confidence: 90%

Inhaled oxytocin increases positive social behaviors in newborn macaques

Simpson

Sclafani

Paukner

et al. 2014

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

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Early caregiver-infant interactions are critical for infants' socioemotional and cognitive development. Several hormones and neuromodulators, including oxytocin, affect these interactions. Exogenous oxytocin promotes social behaviors in several species, including human and nonhuman primates. Although exogenous oxytocin increases social function in adults-including expression recognition and affiliation-it is unknown whether oxytocin can increase social interactions in infants. We hypothesized that nebulized oxytocin would increase affiliative social behaviors and such effects would be modulated by infants' social skills, measured earlier in development. We also hypothesized that oxytocin's effects on social behaviors may be due to its anxiolytic effects. We tested these hypotheses in a blind study by nebulizing 7-to 14-d-old macaques (n = 28) with oxytocin or saline. Following oxytocin administration, infants' facial gesturing at a human caregiver increased, and infants' salivary oxytocin was positively correlated with the time spent in close proximity to a caregiver. Infants' imitative skill (measured earlier in development: 1-7 d of age) predicted oxytocin-associated increases in affiliative behaviors-lip smacking, visual attention to a caregiver, and time in close proximity to a caregiver-suggesting that infants with higher propensities for positive social interactions are more sensitive to exogenous oxytocin. Oxytocin also decreased salivary cortisol, but not stressrelated behaviors (e.g., scratching), suggesting the possibility of some anxiolytic effects. To our knowledge, this study provides the first evidence that oxytocin increases positive social behaviors in newborns. This information is of critical importance for potential interventions aimed at ameliorating inadequate social behaviors in infants with higher likelihood of developing neurodevelopmental disorder.imitation recognition | neonatal imitation | individual differences

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Section: Discussionmentioning

confidence: 90%

Inhaled oxytocin increases positive social behaviors in newborn macaques

Simpson

Sclafani

Paukner

et al. 2014

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

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“…OT is a well-known modulator of social behavior, and several imaging studies in humans and monkeys have implicated the amygdala in this process (28)(29)(30)(31)(41)(42)(43)(44)(45). Inhaled OT increases OT concentration in the central nervous system and enhances both prosocial preferences and social attention in rhesus macaques (33).…”

Section: Resultsmentioning

confidence: 99%

“…Inhaled OT increases OT concentration in the central nervous system and enhances both prosocial preferences and social attention in rhesus macaques (33). Recently, it has been demonstrated that OT administration modulates hemodynamic activity in the amygdala in rhesus macaques (30), and it has been hypothesized that the primate amygdala may express presynaptic OT receptors (46). If reward value-mirroring by the amygdala is critical for prosocial behavior, we reasoned that directly increasing OT levels in the amygdala would increase the likelihood that monkeys would make prosocial decisions.…”

Section: Resultsmentioning

confidence: 99%

“…BLA also signals social information, such as facial expressions and the direction of gaze, and has been implicated in theory of mind and emotional empathy (22)(23)(24)(25)(26). Notably, oxytocin (OT), a neurohypophysial hormone that modulates many social behaviors (27), appears to do so via the amygdala in humans and nonhuman primates (28)(29)(30). Intranasal OT reliably modulates hemodynamic activity in the amygdala in healthy humans (28,29,31), children with autism (32), and rhesus macaques (30).…”

mentioning

confidence: 99%

“…Notably, oxytocin (OT), a neurohypophysial hormone that modulates many social behaviors (27), appears to do so via the amygdala in humans and nonhuman primates (28)(29)(30). Intranasal OT reliably modulates hemodynamic activity in the amygdala in healthy humans (28,29,31), children with autism (32), and rhesus macaques (30). These changes in amygdala activity are related to social cognition.…”

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confidence: 99%

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Neural mechanisms of social decision-making in the primate amygdala

Chang

Fagan

Toda

et al. 2015

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

134

117

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Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.amygdala | social decision | value mirroring | oxytocin | hierarchical modeling H ow we treat others impacts not only their well-being but our own. Human society depends on cooperation, charity, and altruism, as well as institutions to regulate selfish biases. In humans, these behaviors involve perspective-taking, empathy, and theory of mind (1, 2), and the rudiments of these capacities appear to mediate complex social behavior in animals (3). Recent research has sketched a rough outline of the neural circuits that contribute to complex social behavior (4, 5). These comprise a set of domaingeneral brain areas, including the ventromedial prefrontal cortex and ventral striatum, that process information about reward and punishment and contribute to decision-making, and a set of specialized areas, including the temporoparietal junction and medial prefrontal cortex, that process specifically social information (4, 6). How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7-11).The amygdala, especially the basolateral division (BLA), has been implicated in both decision-making and social perception, inviting the possibility that it contributes to decision-making with respect to others (12)(13)(14)(15)(16)(17). This set of nuclei is well known for contributions to emotional experience and expression, especia...

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Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

Putnam

Young²,

Gothard

2018

American J Primatol

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Oxytocin (OT), a neuropeptide that acts in the brain as a neuromodulator, has been long known to shape maternal physiology and behavior in mammals, however its role in regulating social cognition and behavior in primates has come to the forefront only in the recent decade. Many of the current perspectives on the role of OT in modulating social behavior emerged first from studies in rodents, where invasive techniques with a high degree of precision have permitted the mechanistic dissection of OT-related behaviors, as well as their underlying neural circuits in exquisite detail. In parallel, behavioral and imaging studies in humans have suggested that brain OT may similarly influence human social behavior and neural activity. These studies in rodents and humans have spurred interest in the therapeutic potential of targeting the OT system to remedy deficits in social cognition and behavior that are present across numerous psychiatric disorders. Yet there remains a tremendous gap in our mechanistic understanding of the influence of brain OT on social neural circuitry between rodents and man. In fact, very little is known regarding the neural mechanisms by which exogenous or endogenous OT influences human social cognition, limiting its therapeutic potential. Here we discuss how non-human primates (NHPs) are uniquely positioned to now bridge the gaps in knowledge provided by the precise circuit-level approaches widely used in rodent models and the behavioral, imaging, and clinical studies in humans. This review provides a perspective on what has been achieved, and what can be expected from exploring the role of OT in shaping social behaviors in NHPs in the coming years.

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Oxytocin modulates fMRI responses to facial expression in macaques

Cited by 57 publications

References 57 publications

Inhaled oxytocin increases positive social behaviors in newborn macaques

Inhaled oxytocin increases positive social behaviors in newborn macaques

Neural mechanisms of social decision-making in the primate amygdala

Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

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