Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques ( Macaca mulatta )
Open accessAbstract
People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.
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Four studies raised oxytocin concentrations above 20 pg/ml from basal levels below 5 pg/ml; Dal Monte et al. reported a rise to 80 pg/ml after nasal spray but no significant rise with a nebuliser, and Modi et al. reported a 100-fold plasma increase in macaques to more than 300 pg/ml and a rise to about 60 pg/ml after nebuliser application.
“Of the above-mentioned studies, four (20,22,24,25) achieved oxytocin concentrations in excess of 20pg/ml from basal levels of <5pg/ml, while Dal Monte et al. reported a rise to 80pg/ml after nasal spray, but no significant rise with a nebulariser (23).Modi et al. reported a 100-fold increase in plasma in the macaque (to >300pg/ml), and a rise to ~60pg/ml (from 10pg/ml) after nebulariser”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [24]
Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredIn two macaques given 25 IU intranasal oxytocin, CSF oxytocin increased from about 20 to about 50 pg/ml at 35 minutes.
“Chang et al. gave 25IU oxytocin to two macaques, and reported a rise in CSF from ~20 to ~50pg/ml at 35min (24).”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [24]
The Results say two male macaques received 25 IU intranasal oxytocin, and the CSF OT Protocol says CSF was sampled on average 35 minutes after inhalation began. The Methods report an approximately 2.5-fold rise in CSF oxytocin, consistent with 20 to 50 pg/mL, but our copy does not state those absolute concentrations. (LLM, conf=0.84)
Experimental — accuracy not yet measuredNeuropeptides gain access to the brain following intranasal administration.
“neuropeptides have been shown to gain access to the brain following intranasal administration (Born et al., 2002;Chang et al., 2012).”
From Sex-specific effects of intranasal oxytocin on autonomic nervous system and emotional responses to couple conflict (2013) · cites this paper as Chang et al., 2012
IN-OXT treatment increases gaze following, increases socially oriented gaze, and alters social attention in a wide variety of contexts in macaques.
“This work provides anatomical support for other findings in macaques, which indicate that IN-OXT treatment increases gaze following67, increases socially oriented gaze68, and alters social attention in a wide variety of contexts69–74.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [68]
OT increases reward allocation to a partner monkey.
“OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al., 2012).”
From Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys (2016) · cites this paper as Chang et al., 2012
The expected period of rise in OT levels is 20-45 min.
“This way the expected period of rise in OT levels (20–45 min) coincided with the post-treatment viewing period (Chang et al., 2012; Dal Monte et al., 2014b).”
From Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys (2016) · cites this paper as Chang et al., 2012
Animal studies in rodents and nonhuman primates have shown central elevations of OT concentration 30 min after intranasal administration.
“Behavioral testing began 30 min after each treatment, given that animal studies in both rodents (53) and nonhuman primate (54, 55) have shown central elevations of OT concentration after 30 min from intranasal administration.”
From Oxytocin under opioid antagonism leads to supralinear enhancement of social attention (2017) · cites this paper as [54]
Intranasal administration of 24 IU OT increases OT levels in cerebrospinal fluid in nonhuman primates.
“This dose, administered intranasally, has been shown in nonhuman primates to increase OT levels in cerebrospinal fluid significantly (54) and to modulate social behavior (65), as well as to affect brain activity (66) and phasic activity of the parasympathetic nervous system (67) in humans.”
From Oxytocin under opioid antagonism leads to supralinear enhancement of social attention (2017) · cites this paper as [54]
In rhesus macaques, three studies found that intranasal oxytocin treatment impacts social visual attention and looking behaviours across a variety of tasks.
“In rhesus macaques, three studies have found that treatment with IN-OT impacts social visual attention and looking behaviours in a variety of tasks (77-79).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [77]
The intranasal dose administered in the present study has been associated with changes in central function in humans, and similar or smaller doses of oxytocin or vasopressin have been associated with elevations in peptide levels in the cerebrospinal fluid in humans or macaques of no more than approximately 55 pg/ml or up to 0.005% of the administered dose.
“The intranasal dose administered in the present study has been associated with changes in central function in humans 58, and similar or smaller doses of oxytocin or vasopressin (24–48 IU for oxytocin; 40–80 IU for vasopressin) have been associated with elevations in peptide levels in the cerebrospinnal fluid in humans or macaques of no more than approximately 55 pg/ml in actual levels 70, 71, 72,”
From The Analgesic Effect of Oxytocin in Humans: A Double‐Blind, Placebo‐Controlled Cross‐Over Study Using Laser‐Evoked Potentials (2016) · cites this paper as [73]
In rhesus macaques, subjects that engaged in a food sharing task showed first greater selfish choices and after 2 h greater prosocial choices after inhaling oxytocin.
“In rhesus macaques, for example, Chang et al. (2012) found that subjects that engaged in a food sharing task showed first greater selfish choices and after 2 h greater prosocial choices after inhaling oxytocin.”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Chang et al., 2012
In some studies oxytocin only increases positive perceptions or social motivations toward others, and in other studies it also amplifies pre-existing social motivations or perceptions, whether positive or negative.
“Finally, in some studies oxytocin only increases positive perceptions or social motivations toward others (Chang et al., 2012; Shamay-Tsoory et al., 2013) and in other studies it also amplifies pre-existing social motivations or perceptions, whether positive or negative (De Dreu, 2012).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Chang et al., 2012
Inhaled oxytocin arrives in the behaviorally-relevant parts of the brain in mice and rats and in the CSF in rhesus monkeys, although the exact route remains elusive.
“More recently, Neumann et al. (2013) in mice and rats, and Chang et al. (2012) in rhesus monkeys showed that inhaled oxytocin arrives in the behaviorally-relevant parts of the brain and in the CSF, respectively, although the exact route remains elusive.”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Chang et al., 2012
Oxytocin release may depend more on an individual's social perception of an interaction than on the properties of the interaction itself.
“That oxytocin release may depend more on an individuals' social perception of an interaction than on the properties of the interaction itself mirrors other studies on human and non-human primates which suggest that inhaled oxytocin changes individuals' perception or motivation toward a social context (Chang et al., 2012; Parr et al., 2013, for reviews see: Bartz et al., 2011; Olff et al., 2013).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Chang et al., 2012
Studies using exogenous oxytocin have highlighted that a possible effect of oxytocin is to change individuals' social motivations or perceptions of a current social context, such that individuals that inhale oxytocin compared with those that do not become more affiliative, attentive, prosocial or empathetic to the same social stimuli.
“Studies using exogenous oxytocin have highlighted how a possible effect of oxytocin is to change individuals' social motivations or perceptions of a current social context, such that individuals that inhale oxytocin compared with those that do not, become more affiliative, attentive, prosocial or empathetic to the same social stimuli (e.g., Bartz et al., 2011; Chang et al., 2012; Parr et al., 2013”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Chang et al., 2012
In monkeys, intranasal oxytocin or oxytocin intake via a nebulizer at 25 or 48 IU increased cerebrospinal fluid oxytocin concentration compared with placebo.
“Also, in monkeys, IN-OT or OT intake via a nebulizer (25 or 48 IU) increased OT CSF concentration compared to placebo (Chang et al. 2012; Dal Monte et al. 2014; Modi et al. 2014).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Chang et al. 2012
In nonhuman primates, exogenous inhaled oxytocin promotes social donation behavior.
“In nonhuman primates, exogenous inhaled oxytocin promotes social donation behavior 26 and focal infusion of oxytocin into the amygdala significantly increases prosocial decisions 7 .”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [26]
IN-OT promotes social exploration, enhances social motivation, and attenuates social vigilance in nonhuman primate models.
“There is accumulated research on the role of IN-OT in promoting social exploration, enhancing social motivation and attenuating social vigilance in nonhuman primate models (Chang et al. 2012; Chang and Platt 2014; Ebitz and Platt 2013; Parr et al. 2013; Putnam et al. 2016).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Chang et al. 2012
Only a small amount of intranasally administered oxytocin reaches the brain.
“It is estimated that only a small amount of intranasally administered oxytocin reaches the brain.33, 34, 46, 47”
From Oxytocin efficacy is modulated by dosage and oxytocin receptor genotype in young adults with high-functioning autism: a 24-week randomized clinical trial (2016) · cites this paper as [46]
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).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
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).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
When choosing between allocating juice rewards to a recipient monkey and no one at all, exogenous OT enhances the baseline prosocial bias in rhesus macaques.
“When choosing between allocating juice rewards to a recipient monkey and no one at all, exogenous OT enhances the baseline prosocial bias (Fig. 2A).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
Inhaled OT significantly increases reaction times when actor monkeys choose between donating juice rewards to the recipient monkey and no one.
“Furthermore, inhaled OT significantly increases reaction times when the actor monkeys choose between donating juice rewards to the recipient monkey and no one (Chang et al., 2012) (Fig. 2C), inviting the possibility that OT promotes prosocial choices by increasing internal deliberative processing in rhesus macaques.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
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).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
Amplified prosocial preference following OT is accompanied by an increase in gaze shifts to the recipient monkeys' face region.
“Amplified prosocial preference is accompanied by an increase in gaze shifts to the recipient monkeys’ face region following OT (Fig. 2B).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
OT-treated actor monkeys do not increase gaze shifts to recipient monkeys when juice rewards are delivered by the experimenter (cued condition).
“Critically, the OT-treated actors do not increase such gaze shifts to the recipient monkeys when the juice rewards are delivered to the recipients by the experimenter (i.e., cued condition) (Chang et al., 2012).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
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.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
The nebulized inhalation method is efficacious for delivering OT to the CNS in alert rhesus macaques prior to experimental tasks.
“The efficacy of the nebulized inhalation method for delivering OT to the CNS in alert rhesus macaques prior to experimental tasks (Chang et al., 2012; Modi et al., in press) makes it easier to compare neurophysiological results from animal studies with behavioral or neuroimaging results obtained from both healthy people and those with neuropsychiatric disorders.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2012
Prosocial responses occur through multiple processes both within and across species, some of which may be modified by OXT while others may not (this study).
“Ultimately, prosocial responses occur through multiple processes both within and across species, some of which may be modified by OXT (Brosnan, Talbot, et al., 2015; Chang et al., 2012; Mustoe et al., 2015) while others may not (this study).”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Chang et al., 2012
The exact transnasal-CNS route remains unknown, and the proportion of OXT that actually reaches the CNS is exceptionally small relative to the given dose.
“the exact transnasal-CNS route remains unknown, and the proportion of OXT that actually reaches the CNS is exceptionally small relative to the given dose (Born et al., 2002; Chang et al., 2012; Striepens et al., 2013; Dal Monte et al., 2014; Modi et al., 2014).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Chang et al., 2012
Intranasal administration rapidly upregulates OT levels in the brain and plasma during the timeframe of behavioral testing, and OT clears the system several hours after testing.
“These results suggest that intranasal administration rapidly upregulates OT levels in the brain and plasma during the timeframe of behavioral testing, and that OT clears the system several hours after testing.”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Chang et al., 2012
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Oxytocin and neurophysin in plasma and CSF during suckling in the guinea-pig
Robinson, I. C. A. F., & Jones, P. M. (2008) · Neuroendocrinology · doi:10.1159/000123278 · Cited by 69 · see citing works
Maestripieri, D. (2007) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226501215.001.0001 · Cited by 59 · see citing works
Oxytocin and Vasopressin: Social Neuropeptides
Stein, D. J. (2009) · CNS Spectrums · doi:10.1017/s1092852900023841 · Cited by 24 · see citing works
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Research works printed but not linked: 1
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Toward a second-person neuroscience
Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000660 · Cited by 1,510 · see citing works
Neumann, I. D., & Landgraf, R. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.08.004 · Cited by 954 · see citing works
The neurobiology of rewards and values in social decision making
Ruff, C. C., & Fehr, E. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3776 · Cited by 716 · see citing works
Intranasal Oxytocin: Myths and Delusions
Leng, G., & Ludwig, M. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.003 · Cited by 615 · see citing works
Striepens, N., Kendrick, K. M., Hanking, V., Landgraf, R., Wüllner, U., Maier, W., & Hurlemann, R. (2013) · Scientific Reports · doi:10.1038/srep03440 · Cited by 452 · see citing works
Guastella, A. J., Hickie, I. B., McGuinness, M. M., Otis, M., Woods, E. A., Disinger, H. M., Chan, H.-K., Chen, T. F., & Banati, R. B. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.11.019 · Cited by 357 · see citing works
“Interspecies differences in nasal cavity structure limit the ability to extrapolate findings of nasal spray peptide absorption studies in non-humans (e.g., monkeys, rats; (DeSesso, 1993; Chang et al., 2012)) onto humans.”
BackgroundOxytocin enhances brain function in children with autism
Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., Lucas, M. V., Eilbott, J. A., Zagoory-Sharon, O., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312857110 · Cited by 336 · see citing works
“Intranasal OT can increase central (40) or peripheral (42) OT concentrations or both (43).”
BackgroundNeuronal reference frames for social decisions in primate frontal cortex
Chang, S. W. C., Gariépy, J.-F., & Platt, M. L. (2013) · Nature Neuroscience · doi:10.1038/nn.3287 · Cited by 336 · see citing works
Self-citationPsychobiology of social support: The social dimension of stress buffering
Ditzen, B., & Heinrichs, M. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139008 · Cited by 298 · see citing works
“…that intranasally administered neuropeptides reach the brain (for vasopressin, see Born et al., 2002; with regard to oxytocin, see recent data from Chang et al., 2012), several studies have investigated the effects of oxytocin (and to a lesser extent of vasopressin ) intranasal administration on…”
Quintana, D. S., Lischke, A., Grace, S., Scheele, D., Ma, Y., & Becker, B. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00864-7 · Cited by 263 · see citing works
Lee, M. R., Scheidweiler, K. B., Diao, X. X., Akhlaghi, F., Cummins, A., Huestis, M. A., Leggio, L., & Averbeck, B. B. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.27 · Cited by 235 · see citing works
Prefrontal–amygdala circuits in social decision-making
Gangopadhyay, P., Chawla, M., Monte, O. D., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00738-9 · Cited by 247 · see citing works
Kinetics and dose dependency of intranasal oxytocin effects on amygdala reactivity
Spengler, F. B., Schultz, J., Scheele, D., Essel, M., Maier, W., Heinrichs, M., & Hurlemann, R. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.04.015 · Cited by 229 · see citing works
“CSF 35, 40, and 60 minutes after aerosolized or intranasal OXT administration [25 IU (28), 48 IU (29), and 24 IU (30), respectively].”
MethodUnderstanding Social Hierarchies: The Neural and Psychological Foundations of Status Perception
Koski, J. E., Xie, H., & Olson, I. R. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1013223 · Cited by 184 · see citing works
“Conversely, an increase in the hormone oxytocin promotes more affiliative behavior (Chang, Barter, Ebitz, Watson, & Platt, 2012), which may promote status attainment in some species (Newton-fisher, 2004; de Waal, 1986).”
Groppe, S. E., Gossen, A., Rademacher, L., Hahn, A., Westphal, L., Gründer, G., & Spreckelmeyer, K. N. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.023 · Cited by 218 · see citing works
“Specifically, findings that oxytocin enhances the frequency of attention shifts toward the eye region of a face (5,15,16) suggest that oxytocin alters the readiness of the brain to orient to socially meaningful stimuli.”
BackgroundOxytocin promotes social bonding in dogs
Romero, T., Nagasawa, M., Mogi, K., Hasegawa, T., & Kikusui, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1322868111 · Cited by 221 · see citing works
“Similar to human (30) and recent nonhuman primate studies (31), the OT treatment was administered nasally, a minimally stressful method.”
ResultGenetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220 · see citing works
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“In rhesus macaques, three studies have found that treatment with IN-OT impacts social visual attention and looking behaviours in a variety of tasks (77-79).”
BackgroundProsocial behaviour in animals: the influence of social relationships, communication and rewards
Cronin, K. A. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.08.009 · Cited by 205 · see citing works
“…responses in some studies raise the intriguing suggestion that actors experience the rewards of others when providing benefits to close social partners, providing one proximate mechanism that facilitates prosocial responses between close social partners (de Waal et al. 2008; Chang et al. 2012).”
BackgroundFreeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185 · see citing works
“More recently, IN-OT administration in rhesus macaques has been shown to increase central OT concentrations (Chang et al., 2012) (Modi et al., 2014) and to affect a variety of social behaviors including increasing gaze to the eye region of monkey faces (Ebitz et al., 2013), increasing both selfish…”
BackgroundInfluentialCrockford, C., Deschner, T., Ziegler, T. E., & Wittig, R. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00068 · Cited by 187 · see citing works
Oxytocin improves behavioral and electrophysiological deficits in a novel Shank3-deficient rat
Harony-Nicolas, H., Kay, M., Hoffmann, J. D., Klein, M. E., Bozdagi-Gunal, O., Riad, M., Daskalakis, N. P., Sonar, S., Castillo, P. E., Hof, P. R., et al. (2017) · eLife · doi:10.7554/elife.18904 · Cited by 168 · see citing works
“The peptide oxytocin is a powerful regulator of mammalian social behavior, which has been shown to improve various aspects of social cognition and social behavior in human and non-human primates, by increasing social memory, enhancing social reward, and modulating social attention (Chang et al., 2012; Guastella et al.…”
BackgroundA neural circuit covarying with social hierarchy in macaques
Noonan, M. P., Sallet, J., Mars, R. B., Neubert, F. X., O'Reilly, J. X., Andersson, J. L., Mitchell, A. S., Bell, A. H., Miller, K. L., & Rushworth, M. F. S. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001940 · Cited by 183 · see citing works
“Whether such interactions also occur in primates is unknown, although there is evidence that social reward is also related to oxytocin levels in macaques [30].”
BackgroundCSF and blood oxytocin concentration changes following intranasal delivery in macaque
Dal Monte, O., Noble, P. L., Turchi, J., Cummins, A., & Averbeck, B. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103677 · Cited by 177 · see citing works
“5 mL) was obtained from the cisterna magna, as was done in the Chang et al study [25], using a sterile single-use needle.”
BackgroundMethodResultInfluentialMacDonald, K., & Feifel, D. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00035 · Cited by 181 · see citing works
“…2012), support for the direct-to-brain notion comes from recent studies in primates that found that IN OT doubles CSF OT levels within 35 min (Chang et al., 2012), strong evidence of central penetration, given that extant evidence supports that endogenous OT in the CSF derives from central…”
Intranasal administration of oxytocin: behavioral and clinical effects, a review
Veening, J. G., & Olivier, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.012 · Cited by 169 · see citing works
“The results of the three IN-OT experiments in monkeys in the literature (Chang et al., 2012; Parker et al., 2005; Smith et al., 2010) are completely in line with the human data (see Section 3.”
ResultInfluentialNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157 · see citing works
“Reaction times, the time from the onset of decisions to movement onset, were computed using a 20 °/s velocity threshold criterion (7, 33, 34).”
InfluentialAffiliation, empathy, and the origins of theory of mind
Seyfarth, R. M., & Cheney, D. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301223110 · Cited by 160 · see citing works
“Proc Natl Acad Sci USA 109(42):16980–16985.”
BackgroundNeuroethology of primate social behavior
Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301213110 · Cited by 157 · see citing works
“Recently, we demonstrated that OT inhaled via a nebulizer effectively penetrates the central nervous system in rhesus macaques (97) (Fig.”
BackgroundFeldman, R., & Bakermans-Kranenburg, M. J. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.02.011 · Cited by 160 · see citing works
“Similarly, [66_TD$DIFF]OT administration increased OT levels in CSF in rhesus monkeys [44].”
Oxytocin and Pain Perception: From Animal Models to Human Research
Boll, S., de Minas, A. C. A., Raftogianni, A., Herpertz, S. C., & Grinevich, V. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.041 · Cited by 137 · see citing works
The neuroethology of friendship
Brent, L. J. N., Chang, S. W. C., Gariépy, J., & Platt, M. L. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12315 · Cited by 138 · see citing works
Blevins, J. E., & Baskin, D. G. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.05.023 · Cited by 132 · see citing works
“Regardless, it is encouraging that the intranasal route of administration has yielded positive prosocial effects in nonhuman primates [208], male and female individuals with schizophrenia [227,228], and inmen andwomenwho experience social rejection [229].”
BackgroundOxytocin blunts social vigilance in the rhesus macaque
Ebitz, R. B., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305230110 · Cited by 132 · see citing works
“In rhesus macaques, intranasalOT increases the number of rewards amonkey chooses to deliver to another monkey when there is no cost to himself, but also enhances a selfish bias when there is an option to reward himself (4).”
BackgroundMethodResultInfluentialBonding after trauma: on the role of social support and the oxytocin system in traumatic stress
Olff, M. (2012) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v3i0.18597 · Cited by 131 · see citing works
Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques
Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., & Parr, L. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.011 · Cited by 129 · see citing works
“This route has been shown to elicit effects on social behavior and perception in monkeys in three separate studies (Chang et al., 2012; Ebitz et al., 2013; Parr et al., 2013).”
Plasma and CSF oxytocin levels after intranasal and intravenous oxytocin in awake macaques
Freeman, S. M., Samineni, S., Allen, P. C., Stockinger, D., Bales, K. L., Hwa, G. G. C., & Roberts, J. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.01.014 · Cited by 128 · see citing works
Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions
Parr, L. A., Modi, M., Siebert, E., & Young, L. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.011 · Cited by 124 · see citing works
“This method has been proven effective in delivering OT to the central nervous system in rhesus monkeys (Chang et al., 2012; Modi et al., submitted).”
BackgroundMethodResultInfluentialOverview of human oxytocin research
Kendrick, K. M., Guastella, A. J., & Becker, B. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_19 · Cited by 121 · see citing works
Oxytocin and social functioning
Jones, C., Barrera, I., Brothers, S., Ring, R., & Wahlestedt, C. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.2/cjones · Cited by 132 · see citing works
Kosaka, H., Okamoto, Y., Munesue, T., Yamasue, H., Inohara, K., Fujioka, T., Anme, T., Orisaka, M., Ishitobi, M., Jung, M., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.152 · Cited by 117 · see citing works
Neural Mechanisms of Social Cognition in Primates
Wittmann, M. K., Lockwood, P. L., & Rushworth, M. F. S. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-061450 · Cited by 113 · see citing works
“…monkeys rarely sacrifice their own rewards to deliver reward to others (Chang et al. 2012, 2013), they prefer rewarding others compared to no one (Chang et al. 2012, 2013, 2015) as well as rewarding both themselves and another monkey compared to rewarding themselves alone (Ballesta & Duhamel…”
BackgroundOpposing effects of oxytocin on moral judgment in males and females
Scheele, D., Striepens, N., Kendrick, K. M., Schwering, C., Noelle, J., Wille, A., Schlaepfer, T. E., Maier, W., & Hurlemann, R. (2014) · Human Brain Mapping · doi:10.1002/hbm.22605 · Cited by 112 · see citing works
“However, it also increased giving vicarious rewards to other monkeys when self-reward was not an option [Chang et al., 2012].”
BackgroundDitzen, B., Nater, U. M., Schaer, M., La Marca, R., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss083 · Cited by 111 · see citing works
“However, neuropeptides have been shown to gain access to the brain following intranasal administration (Born et al., 2002; Chang et al., 2012).”
BackgroundInfluentialQuintana, D. S., Guastella, A. J., Westlye, L. T., & Andreassen, O. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.166 · Cited by 107 · see citing works
Are there specialized circuits for social cognition and are they unique to humans?
Rushworth, M. F., Mars, R. B., & Sallet, J. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.013 · Cited by 117 · see citing works
Smith, A. S., Korgan, A. C., & Young, W. S. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104324 · Cited by 107 · see citing works
A Review of Oxytocin’s Effects on the Positive, Negative, and Cognitive Domains of Schizophrenia
Feifel, D., Shilling, P. D., & MacDonald, K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.025 · Cited by 110 · see citing works
“For example, Probabilistic Learning, a task used to measure cross-species reinforcement learning (56), and could be used to test the effects of OT in an animal model with relevance to anhedonia (45).”
BackgroundMethodRole of oxytocin signaling in the regulation of body weight
Blevins, J. E., & Ho, J. M. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-013-9260-x · Cited by 108 · see citing works
A brief history of oxytocin and its role in modulating psychostimulant effects
Carson, D. S., Guastella, A. J., Taylor, E. R., & McGregor, I. S. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881112473788 · Cited by 105 · see citing works
“Nasal routes of administration may overcome these problems for other polypeptides (AVP and insulin) but research has been slow in providing direct evidence for OT penetrating the brain via the intranasal route (Born et al., 2002; see Chang et al., 2012 for very preliminary data in monkeys).”
BackgroundSocial Decision-Making and the Brain: A Comparative Perspective
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.007 · Cited by 105 · see citing works
Evolutionarily conserved role of oxytocin in social fear contagion in zebrafish
Akinrinade, I. D., Kareklas, K., Teles, M. C., Reis, T. K., Gliksberg, M., Petri, G., Levkowitz, G., & Oliveira, R. F. (2023) · Science · doi:10.1126/science.abq5158 · Cited by 101 · see citing works
Oxytocin for the treatment of drug and alcohol use disorders
Lee, M. R., & Weerts, E. M. (2016) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000258 · Cited by 105 · see citing works
“It is clear, however, that intranasal administration of OT results in elevated CSF levels of OT in humans (Born et al., 2002; Striepens et al., 2013), nonhuman primates (Chang et al., 2012; dal Monte et al., 2014; Modi et al., 2014; Freeman et al., 2016), and rodents (Neumann et al., 2013).”
BackgroundIntranasal oxytocin effects on social cognition: A critique
Evans, S. L., Dal Monte, O., Noble, P., & Averbeck, B. B. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.008 · Cited by 97 · see citing works
“Limited data has shown increased levels of central OT after nasal administration, in two rhesus macaques (Chang et al., 2012).”
Prosocial Choice in Rats Depends on Food-Seeking Behavior Displayed by Recipients
Márquez, C., Rennie, S. M., Costa, D. F., & Moita, M. A. P. (2015) · Current Biology · doi:10.1016/j.cub.2015.05.018 · Cited by 99 · see citing works
“Interestingly, vicarious reward signals are modulated by oxytocin in monkeys [48].”
Specialized medial prefrontal–amygdala coordination in other-regarding decision preference
Monte, O. D., Chu, C.-C. J., Fagan, N. A., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0593-y · Cited by 99 · see citing works
Evidence for Intranasal Oxytocin Delivery to the brain: Recent Advances and Future Perspectives
Quintana, D. S., Smerud, K. T., Andreassen, O. A., & Djupesland, P. G. (2018) · Therapeutic Delivery · doi:10.4155/tde-2018-0002 · Cited by 94 · see citing works
Freeman, S. M., Palumbo, M. C., Lawrence, R. H., Smith, A. L., Goodman, M. M., & Bales, K. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0315-3 · Cited by 82 · see citing works
Calcagnoli, F., Kreutzmann, J. C., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.019 · Cited by 92 · see citing works
Hu, J., Qi, S., Becker, B., Luo, L., Gao, S., Gong, Q., Hurlemann, R., & Kendrick, K. M. (2015) · Human Brain Mapping · doi:10.1002/hbm.22760 · Cited by 91 · see citing works
“…[Guastella et al., 2013; Striepens et al., 2011], the experimental paradigm started 45 min after OXT or PLC treatment which is estimated to allow maximum increased concentrations of the peptide to occur within the cerebrospinal fluid [Born et al., 2002; Chang et al., 2012; Striepens et al., 2014].”
MethodWatson, K. K., & Platt, M. L. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-21 · Cited by 90 · see citing works
“Even in the (famously despotic) rhesus macaque, inhaled OT has the effect of increasing prosocial decisions in non-competitive contexts as well as attention to another individual [26].”
BackgroundOxytocin effects in schizophrenia: Reconciling mixed findings and moving forward
Bradley, E., & Woolley, J. D. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.007 · Cited by 88 · see citing works
“Research involving administration of oxytocin has increased dramatically over the last decade, and studies in non-human primates demonstrating that intranasal oxytocin can elevate oxytocin concentrations in the cerebrospinal fluid (CSF) (Chang et al., 2012; Dal Monte et al., 2014; Modi et al., 2014a) have supported th…”
InfluentialOxytocin modulates social value representations in the amygdala
Liu, Y., Li, S., Lin, W., Li, W., Yan, X., Wang, X., Pan, X., Rutledge, R. B., & Ma, Y. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0351-1 · Cited by 89 · see citing works
Adaptations for social cognition in the primate brain
Platt, M. L., Seyfarth, R. M., & Cheney, D. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0096 · Cited by 87 · see citing works
Learning About Oxytocin: Pharmacologic and Behavioral Issues
Chini, B., Leonzino, M., Braida, D., & Sala, M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.08.029 · Cited by 87 · see citing works
“the same study, CSF OT levels doubled within 35 minutes (43), thus supporting the idea that endogenous OT in the CSF comes”
Potential of Oxytocin in the Treatment of Schizophrenia
Shilling, P. D., & Feifel, D. (2016) · CNS Drugs · doi:10.1007/s40263-016-0315-x · Cited by 82 · see citing works
“While direct proof that IN-administered OT enters the brain is lacking, several recent reports provide unequivocal evidence that IN OT invokes increased OT levels in the CNS of humans [94], primates [95], and rats [96], whether it be by the exogenous peptide entering the CNS or by stimulation of endogenous OT release…”
BackgroundHippocampal deficits in neurodevelopmental disorders
Li, Y., Shen, M., Stockton, M. E., & Zhao, X. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.10.001 · Cited by 84 · see citing works
Inhaled oxytocin increases positive social behaviors in newborn macaques
Simpson, E. A., Sclafani, V., Paukner, A., Hamel, A. F., Novak, M. A., Meyer, J. S., Suomi, S. J., & Ferrari, P. F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402471111 · Cited by 82 · see citing works
“Unlike other routes of administration (e. g., intranasal, intravenous), nebulizing oxytocin may allow oxytocin molecules to be absorbed into the CNS through the nasal mucosa (54, 55), making it one of the most effective routes of administration (50).”
BackgroundResultInfluentialOxytocin enhances attention to the eye region in rhesus monkeys
Dal Monte, O., Noble, P. L., Costa, V. D., & Averbeck, B. B. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00041 · Cited by 80 · see citing works
“ORIGINAL RESEARCH ARTICLE published: 03 March 2014 doi: 10.3389/fnins.2014.00041 Oxytocin enhances attention to the eye region in rhesus monkeys”
BackgroundMethodResultInfluentialNeural mechanisms necessary for empathy-related phenomena across species
Paradiso, E., Gazzola, V., & Keysers, C. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.005 · Cited by 78 · see citing works
Oxytocin in Schizophrenia: Pathophysiology and Implications for Future Treatment
Goh, K. K., Chen, C.-H., & Lane, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042146 · Cited by 78 · see citing works
“The oxytocin treatment significantly modulates social perception by reducing the attention to a negative facial expression [67] and to social reward by promoting prosocial donation behavior [68] in rhesus monkeys (Macaca mulatta).”
BackgroundAdvances in nonhuman primate models of autism: Integrating neuroscience and behavior
Bauman, M. D., & Schumann, C. M. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.07.021 · Cited by 71 · see citing works
“Initial studies carried out in adult nonhuman primates demonstrated that inhaled OT in rhesus monkeys penetrates the CNS [207] and increases pro-social behaviors in a reward allocation test [208].”
Chang, S. W. C., & Platt, M. L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.006 · Cited by 71 · see citing works
“2B) (Chang et al., 2012).”
BackgroundMethodInfluentialOxytocin increases VTA activation to infant and sexual stimuli in nulliparous and postpartum women
Gregory, R., Cheng, H., Rupp, H. A., Sengelaub, D. R., & Heiman, J. R. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.12.009 · Cited by 72 · see citing works
“Additionally, intranasal oxytocin administration has been shown to increase oxytocin levels in the cerebral spinal fluid of non-human primates (Chang et al., 2012), suggesting that central effects are possible.”
Cavanaugh, J., Mustoe, A. C., Taylor, J. H., & French, J. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.06.020 · Cited by 72 · see citing works
“, 2013) and rhesus macaques (Chang et al., 2012) In rats and mice, OT levels were increased in microdialysates from the hippocampus and amygdala, and plasma, 30—60 min after intranasal administration (Neumann et al.”
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
“1338Evidence suggests both OT and specific social contexts are crit1339ically important for the expression of prosocial preferences among 1340primates (Brosnan et al., 2015; Chang et al., 2012; Mustoe et al., 13412015).”
Buttner, A. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.029 · Cited by 67 · see citing works
“Similarly, intranasal OT administration also generally enhances prosocial behavior in nonhuman primates (Chang et al., 2012; Mustoe et al., 2015; Parr et al., 2013), and higher endogenous levels of peripheral OT have been found to be associated with certain affiliative behaviors, including food…”
Oxytocin modulates fMRI responses to facial expression in macaques
Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508097112 · Cited by 65 · see citing works
“First, previous studies have demonstrated that intranasally administered OT could enter the central nervous system (20, 35, 36) and then bind to OT receptors there.”
BackgroundMethodInfluentialJiang, Y., & Platt, M. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-25607-1 · Cited by 66 · see citing works
Zhao, W., Yao, S., Li, Q., Geng, Y., Ma, X., Luo, L., Xu, L., & Kendrick, K. M. (2016) · Human Brain Mapping · doi:10.1002/hbm.23190 · Cited by 65 · see citing works
“The experimental paradigm started 45 min after OXT or PLC treatment, which is estimated to allow increased concentrations of the peptide to occur within the cerebrospinal fluid [Born et al., 2002; Chang et al., 2012].”
MethodHorta, M., Kaylor, K., Feifel, D., & Ebner, N. C. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.012 · Cited by 62 · see citing works
“, breath-powered devices, nebulizers) are being explored as they constitute more controlled methods of intranasal delivery to central targets (Chang et al., 2012; Quintana et al., 2016).”
BackgroundPaloyelis, Y., Krahé, C., Maltezos, S., Williams, S. C., Howard, M. A., & Fotopoulou, A. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12347 · Cited by 61 · see citing works
ASD and Genetic Associations with Receptors for Oxytocin and Vasopressin—AVPR1A, AVPR1B, and OXTR
Francis, S. M., Kim, S., Kistner‐Griffin, E., Guter, S. J., Cook, E. H., & Jacob, S. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00516 · Cited by 62 · see citing works
“While the relationship between these neuropeptide systems and behaviors are complex (Appenrodt et al., 1998; Chang et al., 2012), in general, OT facilitates prosocial and “approaching” behaviors, social memory and recognition, and reduction in anxiety and reaction to stressors (Carter, 1998;…”
BackgroundFerris, C. F., Yee, J. R., Kenkel, W. M., Dumais, K. M., Moore, K., Veenema, A. H., Kulkarni, P. P., Perkybile, A. M., & Carter, C. S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00245 · Cited by 60 · see citing works
“While several studies have claimed elevations in CSF levels of OT following intranasal OT administration (Chang et al., 2012; Neumann et al., 2013; Striepens et al., 2013; Modi et al., 2014), it is not possible to distinguish OT released from endogenous stores, from OT given peripherally.”
BackgroundDo marmosets care to share? Oxytocin treatment reduces prosocial behavior toward strangers
Mustoe, A. C., Cavanaugh, J., Harnisch, A. M., Thompson, B. E., & French, J. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.015 · Cited by 59 · see citing works
“Notwithstanding these potential limitations, and the small sample size of individual marmosets, the prosocial behavior following OXT treatments appears to be socially-specific, suggesting that cues from the social partner may be influencing prosocial behavior within the marmoset dyads, which is an important considerat…”
BackgroundInfluentialOxytocin and cardioprotection in diabetes and obesity
Jankowski, M., Broderick, T. L., & Gutkowska, J. (2016) · BMC Endocrine Disorders · doi:10.1186/s12902-016-0110-1 · Cited by 59 · see citing works
“35 min post-treatment [54–56].”
Rupp, H. A., James, T. W., Ketterson, E. D., Sengelaub, D. R., Ditzen, B., & Heiman, J. R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.10.007 · Cited by 57 · see citing works
“A recent study in primates demonstrated increased levels of oxytocin measured in CSF after oxytocin spray inhalation (Chang et al., 2012), supporting the possibility of central effects.”
Marmosets as model species in neuroscience and evolutionary anthropology
Burkart, J. M., & Finkenwirth, C. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.09.003 · Cited by 60 · see citing works
Oxytocin under opioid antagonism leads to supralinear enhancement of social attention
Dal Monte, O., Piva, M., Anderson, K. M., Tringides, M., Holmes, A. J., & Chang, S. W. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702725114 · Cited by 55 · see citing works
Oxytocin and opioid addiction revisited: old drug, new applications
Zanos, P., Georgiou, P., Weber, C. D., Robinson, F., Kouimtsidis, C., Niforooshan, R., & Bailey, A. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13757 · Cited by 54 · see citing works
Oxytocin and vasopressin inhibit hyper-aggressive behaviour in socially isolated mice
Tan, O., Musullulu, H., Raymond, J. S., Wilson, B. B., Langguth, M., & Bowen, M. T. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.016 · Cited by 56 · see citing works
Putnam, P. T., Roman, J. M., Zimmerman, P. E., & Gothard, K. M. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.05.016 · Cited by 53 · see citing works
“OT also enhances socially reinforced learning (Parr, 2014), and increases reward allocation to a partner monkey (Chang et al., 2012).”
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
Oxytocin—a social peptide? Deconstructing the evidence
Leng, G., Leng, R., & Ludwig, M. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0055 · Cited by 48 · see citing works
Comparative connectomics of the primate social brain
Yokoyama, C., Autio, J. A., Ikeda, T., Sallet, J., Mars, R. B., Essen, D. C. V., Glasser, M. F., Sadato, N., & Hayashi, T. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118693 · Cited by 45 · see citing works
“, 1991); oxytocin and vasopressin have been linked to prosociality and social attention in monkeys and humans (Chang et al., 2012; Ebitz et al., 2013; Hovey et al., 2020; Jiang and Platt, 2018a, 2018b; Liu et al., 2015); endorphins have shown to play a role in grooming (Dunbar, 2010; Keverne et al.”
BackgroundAmygdala response to negative images in postpartumvsnulliparous women and intranasal oxytocin
Rupp, H. A., James, T. W., Ketterson, E. D., Sengelaub, D. R., Ditzen, B., & Heiman, J. R. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss100 · Cited by 44 · see citing works
Ma, X., Luo, L., Geng, Y., Zhao, W., Zhang, Q., & Kendrick, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00266 · Cited by 43 · see citing works
“There is evidence for increased CSF concentrations of OXT following intranasal application in humans (Striepens et al., 2013) and monkeys (Chang et al., 2012), and other similar peptides in humans (Born et al., 2002), and it is generally considered that OXT given intranasally crosses the…”
BackgroundMethodEffect of distracting faces on visual selective attention in the monkey
Landman, R., Sharma, J., Sur, M., & Desimone, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420167111 · Cited by 43 · see citing works
“The latency of our behavioral effect of OT (∼70 min) is in line with previously reported behavioral effects (peaking at 110 min) using the same nebulization method (50).”
BackgroundResultMustoe, A. C., Harnisch, A. M., Hochfelder, B., Cavanaugh, J., & French, J. A. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.025 · Cited by 40 · see citing works
“Ultimately, prosocial responses occur through multiple processes, both within and across species, and some may be modified by OXT (Brosnan, Talbot, et al., 2015; Chang et al., 2012; Mustoe et al., 2015) while others may not (this study).”
BackgroundOxytocin regulates reunion affiliation with a pairmate following social separation in marmosets
Cavanaugh, J., Mustoe, A. C., & French, J. A. (2018) · American Journal of Primatology · doi:10.1002/ajp.22750 · Cited by 41 · see citing works
“The recent surge of research aimed at determining the efficacy and mechanisms of intranasal OT in human and non-human primates (Chang et al., 2012; Dal Monte et al., 2014; Freeman et al., 2016; Lee et al., 2017; Modi, Connor-Stroud, Landgraf, Young, & Parr, 2014; Striepens et al., 2013) has found…”
Background
- Authors
- Chang, S. W. C., Barter, J. W., Ebitz, R. B., Watson, K. K., & Platt, M. L.
- Affiliations
- Duke University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-01-03
- Volume
- 109
- Issue
- 3
- Pages
- 959-964
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3271866
- OpenAlex
- W2134524153
- Cited by
- 252
- References
- 49
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 6 · 2023: 6 · 2022: 11 · 2021: 15 · 2020: 8 · 2019: 24 · 2018: 27 · 2017: 24 · 2016: 25 · 2015: 20 · 2014: 28 · 2013: 27 · 2012: 12
- FWCI
- 41.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH086712, R01MH086712, R01MH095894)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- oxytocin, vicarious reinforcement, self-reinforcement, social donations, prosocial behavior, selfishness, rhesus monkeys, social attention, reward sensitivity, social cognition, primate social behavior
- MeSH terms
- Administration, Intranasal, Animals, Decision Making, Humans, Macaca mulatta, Oxytocin, Reinforcement, Psychology, Reward, Time Factors, Inhalation Exposure
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