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Cited by 71Neuroendocrine regulation and behaviorPrimate Behavior and EcologyHuman-Animal Interaction Studies

Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology

Open access
Chang, Steve W.C., Platt, Michael L.·2014·Brain Research
DOI 10.1016/j.brainres.2013.11.006PMC PMC4017005
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Abstract

Converging evidence from humans and non-human animals indicates that the neurohypophysial hormone oxytocin (OT) evolved to serve a specialized function in social behavior in mammals. Although OT-based therapies are currently being evaluated as remedies for social deficits in neuropsychiatric disorders, precisely how OT regulates complex social processes remains largely unknown. Here we describe how a non-human primate model can be used to understand the mechanisms by which OT regulates social cognition and thereby inform its clinical application in humans. We focus primarily on recent advances in our understanding of OT-mediated social cognition in rhesus macaques (Macaca mulatta), supplemented by discussion of recent work in humans, other primates, and rodents. Together, these studies endorse the hypothesis that OT promotes social exploration both by amplifying social motivation and by attenuating social vigilance.

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Written from the paper’s full text.

TL;DR

This review argues that oxytocin (OT) promotes social exploration in rhesus macaques by amplifying social motivation and attenuating social vigilance, with implications for treating human social deficits. It synthesizes non-human primate, human, and rodent evidence to propose rhesus macaques as a translational model for understanding and safely developing OT therapies.

Key findings

  • Inhaled/nebulized OT reaches the CNS in rhesus macaques: oronasal administration increased OT concentration in cerebrospinal fluid measured at 30 min post-delivery, whereas another laboratory reported that intranasal spray did not elevate CSF OT in rhesus macaques.
  • OT amplifies pre-existing social preferences in a context-specific way: it enhanced prosocial bias when actors chose between rewarding a recipient versus no one, increased gaze shifts to the recipient’s face, and increased reaction times during prosocial choices; however, when choosing between rewarding self versus recipient, OT amplified self-regarding preference and nearly eliminated prosocial choices.
  • OT reduces social vigilance: it selectively reduced viewing of dominant monkey faces, eliminated privileged processing of dominant faces, attenuated distraction by unfamiliar monkey faces, and in another study reduced attention to emotional facial expressions while enhancing attention to direct-gaze faces.
  • Early social experience is linked to OT: nursery-reared male rhesus macaques had significantly reduced baseline CSF OT, but not CSF AVP, compared with mother-reared peers; mother-reared monkeys showed more affiliative and less aggressive behavior later (18–36 months), and neglected human children showed reduced urinary OT later (average age 4.5 years).

Methods

  • Narrative review synthesizing recent advances in OT-mediated social cognition in rhesus macaques, supplemented by work in humans, other primates, and rodents.
  • Draws on cited studies using nebulized/inhaled OT and CSF measurement, a social reward-allocation paradigm, social vigilance tasks, receptor distribution studies, and amygdala-focused human neuroimaging and animal work.
  • No new experimental data are reported; the main analysis is a conceptual synthesis endorsing the hypothesis that OT promotes social exploration by amplifying social motivation and attenuating social vigilance.

Limitations

  • The paper states that precise dosing to the brain via intranasal or inhaled OT is virtually impossible to determine, and that future animal studies should estimate how much OT reaches the brain.
  • The paper states that chronic OT treatment safety and efficacy are understudied, that OT can evoke antisocial or aggressive behaviors depending on context, and that primate OT receptor distribution and binding affinities remain unresolved and require new ligands.
  • The paper notes that developmental correlations may be confounded by variables other than rearing style, including HPA system contributions, and that whether urinary OT reflects central oxytonergic function remains undetermined; as a narrative review, it also does not systematically assess evidence quality or publication bias.

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Integrity signals

Registry

Crossref · 10.1016/j.brainres.2013.11.006

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 97 cited sources checked · 0 supported · 0 flagged

  • Findingcitation

    Inhaled oronasal administration of OT increases its concentration in the cerebrospinal fluid (CSF) in rhesus macaques, measured at 30 min post-delivery.

    “Using a pediatric nebulizer, we recently showed that inhaled oronasal administration of OT increases its concentration in the cerebrospinal fluid (CSF), measured at 30 min post-delivery (Chang et al., 2012) (Fig. 1B).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chang et al., 2012 source

      Not checked in the free run.

  • Findingcitation

    Oronasal nebulization of OT amplifies self-regarding and other-regarding preferences in rhesus macaques.

    “Oronasal nebulization of OT amplifies these self-regarding and other-regarding preferences in rhesus macaques (Chang et al., 2012).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chang et al., 2012 source

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  • Findingcitation

    OT selectively reduces species-typical tendencies to view the faces of dominant monkeys, a threatening but highly informative stimulus, in male rhesus macaques.

    “When monkeys choose whether to acquire different types of visual information about the local social context (viewing different social images), OT selectively reduces species-typical tendencies to view the faces of dominant monkeys, a threatening but highly informative stimulus (Fig. 3A).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ebitz et al., 2013 source

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  • Findingcitation

    OT substantially attenuates species-typical distraction by the peripheral flash of images of unfamiliar monkey faces, indexed by a reduction in gaze deflection towards them.

    “Moreover, OT substantially attenuates species-typical distraction by the peripheral flash of images of unfamiliar monkey faces, indexed by a reduction in gaze deflection towards them (Fig. 3C).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ebitz et al., 2013 source

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  • Findingcitation

    When choosing between delivering juice rewards to themselves and to the recipients, inhaled OT amplifies the self-regarding preference, essentially eliminating the small number of prosocial choices in this competitive context.

    “By contrast, when choosing between delivering juice rewards to themselves and to the recipients, inhaled OT amplifies the self-regarding preference (i.e., delivering juice to only themselves over only the recipients), essentially eliminating the small number of prosocial choices in this competitive context (Fig. 2A).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chang et al., 2012 source

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  • May combine two claims. 17
  • Classified as probably not a substantial claim. 10

  • May combine two claims.

    Findingcitation

    Inhaled OT eliminates the privileged processing for dominant faces over other images, effectively slowing monkeys down when making this particular decision.

    “Inhaled OT also eliminates the privileged processing for dominant faces over other images, effectively slowing monkeys down when making this particular decision (Fig. 3B).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ebitz et al., 2013 source

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  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Precisely how OT regulates complex social processes remains largely unknown.

    “precisely how OT regulates complex social processes remains largely unknown.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisenone given

    OT-based therapies are currently being evaluated as remedies for social deficits in neuropsychiatric disorders.

    “Although OT-based therapies are currently being evaluated as remedies for social deficits in neuropsychiatric disorders, precisely how OT regulates complex social processes remains largely unknown.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Inhaled administration of aerosolized OT effectively elevates OT levels in the CSF in rhesus macaques, but intranasal spray does not.

    “Subsequent work in primates from another laboratory reported that the inhaled administration of aerosolized OT effectively elevates OT levels in the CSF in rhesus macaques, but the application of intranasal spray, which has been the standard method in studies in humans, does not (Modi et al., in press).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Modi et al., in press

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  • May combine two claims.

    Interpretationnone given

    OT promotes social exploration both by amplifying social motivation and by attenuating social vigilance.

    “Together, these studies endorse the hypothesis that OT promotes social exploration both by amplifying social motivation and by attenuating social vigilance.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In highly social animals, ancestral functions of OT have been co-opted to serve social functions, such as promoting maternal behavior, pair-bonding, affiliative behaviors, in-group bias, reducing social vigilance, and amplifying other-regarding behaviors.

    “In highly social animals, these ancestral functions of OT have been co-opted to serve social functions, such as promoting maternal behavior (Champagne et al., 2001; Pedersen et al., 1982), fostering pair-bonding and affiliative behaviors (Cushing and Carter, 2000; Smith et al., 2010; Snowdon et al., 2010; Young and Wang, 2004), encouraging in-group bias (Dreu et al., 2010), reducing social vigil”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Champagne et al., 2001 source

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    • cites Pedersen et al., 1982 source

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    • cites Cushing and Carter, 2000

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  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Rodent models permit exquisitely fine dissection of neural pathways but lack the behavioral complexity of human social function.

    “Conversely, rodent models permit exquisitely fine dissection of these neural pathways but lack the behavioral complexity of human social function.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Rhesus macaques display basic aspects of complex social behaviors typically considered uniquely human, including social imitation, prosocial behaviors, and understanding others' perceptions.

    “Critically, rhesus macaques display basic aspects of complex social behaviors that are typically considered ‘uniquely human’ (Frith and Frith, 2007; Saxe, 2006). These include social imitation (Ferrari et al., 2006; Subiaul, 2004), prosocial behaviors (Chang et al., 2011; Masserman et al., 1964), as well as understanding others’ perceptions (Flombaum and Santos, 2005; Santos et al., 2006).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Frith and Frith, 2007 source

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    • cites Ferrari et al., 2006 source

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    • cites Chang et al., 2011 source

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  • May combine two claims.

    Interpretationcitation

    The anxiolytic, approach-promoting, and tolerance-enhancing roles of OT may serve as foundational substrates that promote social exploration and interaction while suppressing social avoidance.

    “The anxiolytic, approach-promoting, and tolerance-enhancing roles of OT (Amico et al., 2004; Averbeck, 2010; Heinrichs et al., 2003; Kemp and Guastella, 2010; Neumann et al., 2000a; Riem et al., 2011; Ring et al., 2006; Uvnäs-Moberg et al., 1994; Waldherr and Neumann, 2007; Yoshida et al., 2009; Young, 2002) may serve as foundational substrates that promote social exploration and interaction while”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Amico et al., 2004 source

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    • cites Heinrichs et al., 2003 source

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    • cites Kemp and Guastella, 2010

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  • May combine two claims.

    Interpretationcitation

    Reducing social vigilance state could free up cognitive resources and promote social exploration.

    “Reducing social vigilance state in turn could free up cognitive resources and promote social exploration (Ebitz et al., 2013).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ebitz et al., 2013 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    OT promotes prosocial choices by increasing internal deliberative processing in rhesus macaques.

    “inviting the possibility that OT promotes prosocial choices by increasing internal deliberative processing in rhesus macaques.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Inhaled OT selectively reduces attention to emotional facial expressions while enhancing attention to faces with direct gaze in rhesus macaques.

    “Consistent with the role of OT in reducing social vigilance state, another recent study in rhesus macaques reported that inhaled OT selectively reduces attention to emotional facial expressions while enhancing attention to faces with direct gaze (Parr et al., 2013) (Fig. 3D), which is a threatening gesture in macaques.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Parr et al., 2013 source

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  • May combine two claims.

    Interpretationcitation

    OT may facilitate social interactions by lowering social vigilance and reducing social stress.

    “Taken together, these findings suggest that OT may facilitate social interactions by lowering social vigilance and reducing social stress (Carter, 1998; Chang et al., 2013b; Ebitz et al., 2013; Neumann et al., 2000b; Uvnäs-Moberg et al., 1994).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Carter, 1998 source

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    • cites Ebitz et al., 2013 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Urinary OT levels after grooming behaviors predicted the strength of social bonds among partners in wild chimpanzees, and this effect was not explained by genetic relatedness.

    “A recent study in wild chimpanzees (Pan troglodytes) measured urinary OT levels after grooming bouts with different partners (Crockford et al., 2013). urinary OT levels after grooming behaviors predicted the strength of social bonds among the partners, and, surprisingly, this effect was not explained by genetic relatedness.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Crockford et al., 2013 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In rats, some of the regions with high densities of OT receptor include the olfactory nucleus, hypothalamic regions, and the central amygdala.

    “In rats, some of the regions with high densities of OT receptor include the olfactory nucleus, hypothalamic regions, and the central amygdala (Tribollet and Barberis, 1996; Tribollet et al., 1992).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Tribollet and Barberis, 1996

      Not checked in the free run.

    • cites Tribollet et al., 1992 source

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  • May combine two claims.

    Interpretationreasoning

    Reduced vigilance might play a permissive role in social approach behavior, favoring increased attention to faces and eyes and subsequent enhancements in social cognition.

    “Based on these results, we conjecture that reduced vigilance might play a permissive role in social approach behavior, favoring increased attention to faces and eyes and subsequent enhancements in social cognition.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Ebitz et al., 2013 source

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    • cites Chang et al., 2012 source

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  • May combine two claims.

    Premisecitation

    Inhaling OT reduces BOLD activation in the amygdala when viewing or associating aversive social stimuli, during trust formation, in response to pain, and in response to infant crying.

    “Human functional neuroimaging studies have shown that inhaling OT reduces BOLD (blood-oxygen-level dependent) activation in the amygdala when viewing or associating aversive social stimuli (Kirsch, 2005; Petrovic et al., 2008), during trust formation (Baumgartner et al., 2008), in response to pain (Singer et al., 2008), and in response to infant crying (Riem et al., 2011).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Kirsch, 2005 source

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    • cites Petrovic et al., 2008 source

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    • cites Baumgartner et al., 2008 source

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  • May combine two claims.

    Premisecitation

    OT inhalation reduces amygdala activation when viewing fearful faces but increases amygdala activation when viewing happy faces.

    “Furthermore, OT inhalation reduces amygdala activation when viewing fearful faces but increases amygdala activation when viewing happy faces (Gamer et al., 2010).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Gamer et al., 2010 source

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  • May combine two claims.

    Premisecitation

    Neurons in the primate amygdala signal motivational values and are causally implicated in reward-guided learning.

    “Moreover, neurons in the primate amygdala signal motivational values and is causally implicated in reward-guided learning (Baxter and Murray, 2002; Paton et al., 2006).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Baxter and Murray, 2002

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    • cites Paton et al., 2006 source

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  • May combine two claims.

    Interpretationreasoning

    OT modulates context-specific processing associated with both negative and positive valence in the amygdala, consistent with the encoding of both positive and negative motivational values by the primate amygdala neurons.

    “These findings suggest that OT modulates context-specific processing associated with both negative and positive valence in the amygdala, consistent with the encoding of both positive and negative motivational values by the primate amygdala neurons (Belova et al., 2007; Paton et al., 2006).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Belova et al., 2007 source

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    • cites Paton et al., 2006 source

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  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Using non-human primates, researchers can administer OT at a regular interval (e.g., daily or weekly) in the same subjects over a long time period (e.g., months or years) to estimate the efficacy and safety of repeated OT treatments in humans.

    “Using non-human primates, researchers can administer OT at a regular interval (e.g., daily or weekly) in the same subjects over a long time period (e.g., months or years) to estimate the efficacy and safety of repeated OT treatments in humans.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: More research is necessary to fully and safely develop and implement OT treatment protocols for social deficits.
    • Rests on an assumption: The majority of OT studies to date have focused on establishing the effects of acute OT on specific social functions.
    • Rests on an assumption: Chronic OT studies are practically difficult and sometimes ethically questionable in human subjects.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    This OT-mediated autonomic circuit might also be utilized for regulating social vigilance.

    “This OT-mediated autonomic circuit might be also utilized for regulating social vigilance.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationreasoning

    It is feasible to record neuronal activity or measure hemodynamic responses regularly over time in such studies in order to evaluate efficacy and safety at the neurophysiological level.

    “It is also feasible to record neuronal activity or measure hemodynamic responses regularly over time in such studies in order to evaluate efficacy and safety at the neurophysiological level.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: More research is necessary to fully and safely develop and implement OT treatment protocols for social deficits.
    • Rests on an assumption: The majority of OT studies to date have focused on establishing the effects of acute OT on specific social functions.
    • Rests on an assumption: Chronic OT studies are practically difficult and sometimes ethically questionable in human subjects.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    It is feasible to conduct other physiological measurements every month to assess inflammatory processes, including urine and blood analysis to measure cytokine and C-reactive protein levels.

    “Furthermore, it is also feasible to conduct other physiological measurements every month to assess inflammatory processes, including urine and blood analysis to measure cytokine and C-reactive protein levels.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: More research is necessary to fully and safely develop and implement OT treatment protocols for social deficits.
    • Rests on an assumption: The majority of OT studies to date have focused on establishing the effects of acute OT on specific social functions.
    • Rests on an assumption: Chronic OT studies are practically difficult and sometimes ethically questionable in human subjects.

  • May combine two claims.

    Premisecitation

    Gender-specific effects of OT have been documented numerously in prairie voles (Microtus ochrogaster) and are centrally-mediated based on ventricular peptide manipulation experiments.

    “Such gender-specific effects of OT have been documented numerously in prairie voles (Microtus ochrogaster), and are verified to be centrally-mediated based on ventricular peptide manipulation experiments.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bales and Carter, 2003

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    • cites Cushing and Carter, 2000

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    • cites Insel and Hulihan, 1995 source

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  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given

    Non-human primates will be valuable for monitoring the efficacy and safety of repeated OT administrations continuously for months and even years at the behavioral as well as neuronal level in a controlled setting.

    “Finally, non-human primates will be valuable for monitoring the efficacy and safety of repeated OT administrations continuously for months and even years at the behavioral as well as neuronal level in a controlled setting.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Rhesus macaques are tolerant to controlled experiments with an extremely high number of repeated trials (~1000 trials per day).
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  • The paper relies on this without support.

    Cerebrospinal fluid OT concentration provides a valid index of central OT function relevant to social behavior.

    “In rhesus macaques, baseline CSF OT levels, but not CSF AVP levels, are significantly reduced in males raised in a nursery compared to peers raised by their mothers (Winslow et al., 2003) (Fig. 1C), confirming a specialized role of OT in early social development.”

  • The paper relies on this without support.

    The behavioral effects of inhaled or intranasal OT on social cognition in rhesus macaques are mediated by central OT rather than peripheral mechanisms.

    “Using a pediatric nebulizer, we recently showed that inhaled oronasal administration of OT increases its concentration in the cerebrospinal fluid (CSF), measured at 30 min post-delivery (Chang et al., 2012) (Fig. 1B).”

  • The paper relies on this without support.

    More research is necessary to fully and safely develop and implement OT treatment protocols for social deficits.

    “Without doubt, more research is necessary to fully and safely develop and implement OT treatment protocols for social deficits.”

  • The paper relies on this without support.

    The majority of OT studies to date have focused on establishing the effects of acute OT on specific social functions.

    “In particular, determining the efficacy and safety of chronic OT treatment is a top priority because the majority of OT studies to date have focused on establishing the effects of acute OT on specific social functions.”

  • The paper relies on this without support.

    Chronic OT studies are practically difficult and sometimes ethically questionable in human subjects.

    “Unfortunately, chronic studies are practically difficult and sometimes ethically questionable in human subjects.”

  • The paper relies on this without support.

    Most of the rudimentary forms of complex human cognition are present in rhesus macaques.

    “Arguably, most of the rudimentary forms of complex human cognition are present in these animals.”

  • The paper relies on this without support.

    Rhesus macaques are tolerant to controlled experiments with an extremely high number of repeated trials (~1000 trials per day).

    “Furthermore, rhesus macaques are also tolerant to controlled experiments with an extremely high number of repeated trials (~1000 trials per day) allowing precise quantifications of behaviors as well as how these behaviors are related to underlying neuronal activity, which by nature is often highly variable.”
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References 125 · Cited by 71

Authors
Chang, S. W. C., & Platt, M. L.
Affiliations
Duke University (US)
Corresponding author
Chang, Steve W.C.
ORCID
Venue
Brain Research
Publisher
Elsevier BV
Published
2014-09
Volume
1580
Pages
57-68
ISSN
0006-8993 (ISSN-L)
DOI
10.1016/j.brainres.2013.11.006
PMC
PMC4017005
OpenAlex
W2036644048
Semantic Scholar
edcc32128a7eed2ed74eb54ea6b6bd8a05abeedf
Cited by
71
References
125
Citations by year
2026: 3 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 7 · 2021: 8 · 2020: 4 · 2019: 6 · 2018: 9 · 2017: 11 · 2016: 3 · 2015: 8 · 2014: 5
FWCI
0.71
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute for Mental Health (K99-MH099093, R01-MH086712)
  • Department of Defense (W81XWH-11-1-0584)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
Keywords
oxytocin, social cognition, rhesus monkeys, social motivation, social vigilance, social exploration, neuropsychiatric disorders, nonhuman primate model, neurohypophyseal hormones, evolution of social behavior
MeSH terms
Animals, Mental Disorders, Brain, Cognition, Humans, Macaca mulatta, Oxytocin, Social Behavior

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