Intranasal oxytocin enhances socially-reinforced learning in rhesus monkeys

Parr, Lisa A.

doi:10.3389/fnbeh.2014.00278

Cited by 21 publications

(17 citation statements)

References 39 publications

(65 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This study is interesting because the participants were Chinese and, unlike studies in Caucasians, the Placebo condition was characterized by decreased performance after social compared to nonsocial reinforcement. However, IN-OT reversed this and resulted in enhanced learning in the social compared to nonsocial conditions, consistent with previous studies in both humans and monkeys (Hurlemann et al, 2010; Parr, 2014). The aforementioned studies focused primarily on the connectivity between the amygdala and the rest of the brain due to its well-established role in processing emotionally-salient stimuli.…”

supporting

confidence: 91%

“…In nonhuman primates, OT receptors have been found in brain regions involved in detecting the salience of visual stimuli and regulating attention to them, including the superior colliculus, pulvinar, and nucleus basalis of Meynert (Freeman et al, 2014). Although only a few studies have focused on the effects of IN-OT on social behavior and cognition in nonhuman primates, they have broadly replicated many of the findings from human IN-OT studies, including increased attention to the eyes in faces (Ebitz et al, 2013; Dal Monte et al, 2014), enhanced socially-reinforced learning (Parr, 2014), and reduced attention to negative, threatening or potential dangerous stimuli (Chang et al, 2013; Parr et al, 2013). Together, these findings support the general idea that IN-OT influences prosocial behavior by increasing the salience and rewarding quality of mild or moderately arousing social stimuli, while reducing vigilance towards highly arousing, negative stimuli.…”

mentioning

confidence: 95%

“…Because of its prosocial effects, we hypothesized that IN-OT will enhance connectivity between the ACC and amygdala, thus reducing social inhibition (Blackford et al, 2014). Because IN-OT has also been shown to enhance the rewarding quality of social stimuli in both humans and macaques (Hu et al, 2015; Hurlemann et al, 2010; Parr, 2014), we predicted that it would enhance the functional connectivity between the ventral striatum and other core regions within the SN.…”

mentioning

confidence: 99%

See 2 more Smart Citations

Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward

Parr

Mitchell

Hecht

2018

American J Primatol

Self Cite

View full text Add to dashboard Cite

In primates, resting state functional neuroimaging (rsfcMRI) has identified several large-scale, intrinsic brain networks, including the salience network (SN), which is involved in detecting stimulus salience. Intranasal oxytocin (IN-OT) has been shown to modulate the salience and rewarding quality of social stimuli in mammals and numerous studies have shown that it can affect the functional connectivity between brain regions. Less is known, however, about how these effects unfold over time following IN-OT administration. This study used rsfcMRI in anesthetized rhesus macaques to track temporal changes in the functional connectivity between brain regions involved in the SN, including the anterior cingulate cortex (ACC), anterior insula (AI), amygdala (amy), and ventral striatum (vstr), lasting three hours after IN-OT or Placebo (saline) administration. We found significant temporal changes in the functional connectivity between all regions associated with treatment condition. IN-OT increased the functional connectivity between AI_vstr, ACC_amy (right hemisphere), ACC_vstr (left hemisphere), and amy_vstr (right hemisphere), but reduced the functional connectivity between ACC_AI, and the AI_amygdala. These results suggest that IN-OT may dampen salience detection in rhesus monkeys, consistent with previous findings of reduced social vigilance, while enhancing the connectivity between the SN and regions involved in processing reward.

show abstract

supporting

confidence: 91%

mentioning

confidence: 95%

mentioning

confidence: 99%

See 1 more Smart Citation

Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward

Parr

Mitchell

Hecht

2018

American J Primatol

Self Cite

View full text Add to dashboard Cite

show abstract

“…When administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images (Dal Monte et al, 2014a; Ebitz et al, 2013) and communicative gesturing in rhesus infants (Simpson et al, 2014). OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al, 2012). These results in non-human primates replicate similar findings in humans (Guastella et al, 2008; Hurlemann et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys

Putnam

Roman

Zimmerman

et al. 2016

Psychoneuroendocrinology

View full text Add to dashboard Cite

Gaze following is a basic building block of social behavior that has been observed in multiple species, including primates. The absence of gaze following is associated with abnormal development of social cognition, such as in autism spectrum disorders (ASD). Some social deficits in ASD, including the failure to look at eyes and the inability to recognize facial expressions, are ameliorated by intranasal administration of oxytocin (IN-OT). Here we tested the hypothesis that IN-OT might enhance social processes that require active engagement with a social partner, such as gaze following. Alternatively, IN-OT may only enhance the perceptual salience of the eyes, and may not modify behavioral responses to social signals. To test this hypothesis, we presented four monkeys with videos of conspecifics displaying natural behaviors. Each video was viewed multiple times before and after the monkeys received intranasally either 50 IU of OT or saline. We found that despite a gradual decrease in attention to the repeated viewing of the same videos (habituation), IN-OT consistently increased the frequency of gaze following saccades. Further analysis confirmed that these behaviors did not occur randomly, but rather predictably in response to the same segments of the videos. These findings suggest that in response to more naturalistic social stimuli IN-OT enhances the propensity to interact with a social partner rather than merely elevating the perceptual salience of the eyes. In light of these findings, gaze following may serve as a metric for pro-social effects of oxytocin that target social action more than social perception.

show abstract

“…Thus, the monkey may be an ideal animal model to explore the development of OT-based pharmacologic strategies for treating patients with dysfunctional social behavior. including vicarious as well as self-reinforcement (20), social vigilance (22), socially reinforced learning (26), and attention to facial features and expressions (21,24). However, how OT exerts its effects on brain activity in monkeys remains unclear.…”

mentioning

confidence: 99%

Oxytocin modulates fMRI responses to facial expression in macaques

Liu¹,

Hadj-Bouziane²,

Jones³

et al. 2015

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

View full text Add to dashboard Cite

Increasing evidence has shown that oxytocin (OT), a mammalian hormone, modifies the way social stimuli are perceived and the way they affect behavior. Thus, OT may serve as a treatment for psychiatric disorders, many of which are characterized by dysfunctional social behavior. To explore the neural mechanisms mediating the effects of OT in macaque monkeys, we investigated whether OT would modulate functional magnetic resonance imaging (fMRI) responses in face-responsive regions (faces vs. blank screen) evoked by the perception of various facial expressions (neutral, fearful, aggressive, and appeasing). In the placebo condition, we found significantly increased activation for emotional (mainly fearful and appeasing) faces compared with neutral faces across the faceresponsive regions. OT selectively, and differentially, altered fMRI responses to emotional expressions, significantly reducing responses to both fearful and aggressive faces in face-responsive regions while leaving responses to appeasing as well as neutral faces unchanged. We also found that OT administration selectively reduced functional coupling between the amygdala and areas in the occipital and inferior temporal cortex during the viewing of fearful and aggressive faces, but not during the viewing of neutral or appeasing faces. Taken together, our results indicate homologies between monkeys and humans in the neural circuits mediating the effects of OT. Thus, the monkey may be an ideal animal model to explore the development of OT-based pharmacological strategies for treating patients with dysfunctional social behavior.oxytocin | neuroimaging | nonhuman primate | social stimuli I n the last decade, oxytocin (OT), a mammalian hormone, has become one of the most studied peptides of the neuroendocrine system. In humans, accumulating evidence has demonstrated that OT affects a wide range of social behavior and cognition, including perception, recognition and memory of social stimuli (1-5), socially reinforced learning (6), and more complex sociocognitive behaviors [e.g., trust (7,8), cooperation (9), generosity (10), and empathy (6, but see ref. 11)]. Therefore, it has been proposed that OT may serve as a treatment for various disorders with dysfunctional social behavior, such as autism spectrum disorders, antisocial personality disorder, and schizophrenia (for review, see ref. 12). A recent study found that OT enhances brain activity for socially meaningful stimuli but attenuates activity for nonsocially meaningful stimuli in children with autism spectrum disorders (13). Although these studies suggest very promising prospects of OT for clinical use, the neural mechanisms underlying OT's modulatory effects remain elusive. To understand these mechanisms, it is important to investigate the effect of OT on brain activity, especially in regions involved in social behavior and cognition.Functional magnetic resonance imaging (fMRI) has been the major approach to investigating altered brain activation patterns in response to OT in humans. OT may affect the per...

show abstract

Intranasal oxytocin enhances socially-reinforced learning in rhesus monkeys

Cited by 21 publications

References 39 publications

Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward

Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward

Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys

Oxytocin modulates fMRI responses to facial expression in macaques

Contact Info

Product

Resources

About