Oxytocin modulates fMRI responses to facial expression in macaques
Open accessAbstract
Significance: Oxytocin (OT), a mammalian hormone, may serve as a treatment for psychiatric disorders because of its beneficial effect on social behavior. Here, we found that in monkeys, OT selectively altered brain activity within multiple neural systems (visual perception, emotion, attention, and higher cognition function) and functional coupling between the amygdala and areas in the ventral visual pathway evoked by negative emotional expressions. Our findings provide key information for understanding the behavioral consequences of OT administration and 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 pharmacologic strategies for treating patients with dysfunctional social behavior.
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It has recently been demonstrated that intranasal oxytocin modulates amygdala responses in monkeys in a manner equivalent to humans.
“it has recently been demonstrated that IN-OT modulates amygdala responses in monkeys in a manner equivalent to humans (40).”
From Is there a Publication Bias in Behavioural Intranasal Oxytocin Research on Humans? Opening the File Drawer of One Laboratory (2016) · cites this paper as [40]
Several previous studies suggested that the effects of oxytocin and vasopressin result from activation of the opposite receptor.
“This concept is not new; several previous studies suggested that the effects of OT and AVP are a result of the activation of the ‘opposite’ receptor (4,80,86-89).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [80]
Intranasal oxytocin treatment in macaques can alter neural responses to emotional faces.
“It has also recently been shown that treatment with IN-OT in macaques can alter neural responses to emotional faces (80).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [80]
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“Despite a growing number of exogenous OT studies in macaques (e.g., Chang and Platt 2014; Ebitz et al. 2013; Liu et al. 2015), we know of no reports of sex differences, although this may be due to the necessity of small sample sizes (i.e., 2–6 individuals) and therefore insufficient power to detect…”
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Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
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“Likewise in rhesus monkeys, IN OT reduced the functional coupling between the amygdala and areas in the occipital and inferior temporal cortices but only when the subjects viewed aggressive or fearful faces (Liu et al., 2015).”
BackgroundThe Role of Oxytocin in Early-Life-Stress-Related Neuropsychiatric Disorders
Jin, Y., Song, D. F., Yan, Y., Quan, Z., & Qing, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310430 · Cited by 30 · see citing works
Romantic Love vs. Drug Addiction May Inspire a New Treatment for Addiction
Zou, Z., Song, H., Zhang, Y., & Zhang, X. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01436 · Cited by 28 · see citing works
Opportunities and challenges for intranasal oxytocin treatment studies in nonhuman primates
Bauman, M. D., Murai, T., Hogrefe, C. E., & Platt, M. L. (2018) · American Journal of Primatology · doi:10.1002/ajp.22913 · Cited by 25 · see citing works
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Oxytocin increases eye gaze in schizophrenia
Bradley, E. R., Seitz, A., Niles, A. N., Rankin, K. P., Mathalon, D. H., O'Donovan, A., & Woolley, J. D. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.07.039 · Cited by 22 · see citing works
Oxytocin improves the ability of dogs to follow informative pointing: a neuroemotional hypothesis
Macchitella, L., Stegagno, T., Giaconella, R., di Sorrentino, E. P., Schino, G., & Addessi, E. (2016) · RENDICONTI LINCEI · doi:10.1007/s12210-016-0579-6 · Cited by 22 · see citing works
“Several lines of evidence show that in non-human animals inhaled oxytocin reaches target brain areas and cerebrospinal fluid (e.g. mice and rats, Neumann et al. 2013; rhesus macaques, Chang et al. 2012; Liu et al. 2015).”
BackgroundOxytocin-Augmented Psychotherapy: Beware of Context
Hurlemann, R. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.188 · Cited by 22 · see citing works
Lu, X., Hu, Z., Xin, Y., Yang, T., Wang, Y., Zhang, P., Liu, N., & Jiang, Y. (2024) · Nature Communications · doi:10.1038/s41467-024-53968-x · Cited by 20 · see citing works
“After recovery, monkeys were trained to sit in a plastic restraintchairand fi xateatacentraltargetforlongdurationswiththeir heads fi xed, facing a screen on which visualstimuli were presented 57,58 .”
Self-citationFacial Expressions Evoke Differential Neural Coupling in Macaques
Liu, N., Hadj‐Bouziane, F., Moran, R., Ungerleider, L. G., & Ishai, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv345 · Cited by 19 · see citing works
Self-citationFace perception: computational insights from phylogeny
Behrmann, M., & Avidan, G. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.01.006 · Cited by 18 · see citing works
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“Animal models provide invaluable opportunity to examine oxytocin effects in a highly controlled experimental condition and gain insight into the underlying mechanisms of oxytocin role in primate cognition [13,16,26,39,50,52].”
Taubert, J., Flessert, M., Liu, N., & Ungerleider, L. G. (2019) · Scientific Reports · doi:10.1038/s41598-019-51422-3 · Cited by 16 · see citing works
Self-citationOxytocin reduces the link between neural and affective responses after social exclusion
Petereit, P., Rinn, C., Stemmler, G., & Mueller, E. M. (2019) · Biological Psychology · doi:10.1016/j.biopsycho.2019.05.002 · Cited by 15 · see citing works
Intranasal oxytocin modulates higher order social cognition in body dysmorphic disorder
Fang, A., Lawson, E. A., & Wilhelm, S. (2019) · Depression and Anxiety · doi:10.1002/da.22876 · Cited by 14 · see citing works
“Oxytocin is a promising therapeutic agent, as it plays amajor role in mediating socioemotional processing in animals and humans (Liu et al., 2015; MacDonald & Feifel, 2013).”
Differences in how macaques monitor others: Does serotonin play a central role?
Weinberg‐Wolf, H., & Chang, S. W. C. (2019) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1494 · Cited by 14 · see citing works
“…Platt, 2012), regulate social vigilance (Ebitz, Watson, & Platt, 2013; Landman, Sharma, Sur, & Desimone, 2014) and differentially impact attention and brain activation to different facial expressions (Domes, Steiner, Porges, & Heinrichs, 2013; Liu et al., 2015; Parr, Modi, Siebert, & Young, 2013).”
The role of oxytocin on peaceful associations and sociality in mammals
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Festante, F., Rayson, H., Paukner, A., Kaburu, S., Toschi, G., Fox, N. A., & Ferrari, P. F. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.100950 · Cited by 12 · see citing works
Behavioral screening tools for identifying autism in macaques: existing and promising tests
Qin, D., Wu, S., Chen, Y., & Hu, X. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.12.018 · Cited by 11 · see citing works
Probing the processing of facial expressions in monkeys via time perception and eye tracking
Liu, X., 中国科学院深圳先进技术研究院深港脑科学创新研究院, 广. 深. 5., Gan, L., Zhang, Z., Yu, P., Dai, J., 中国科学院深圳先进技术研究院脑认知与脑疾病研究所, 广. 深. 5., 广东省脑连接图谱重点实验室, 广. 深., 中国科学院深圳先进技术研究院医学人工智能研究中心, 广. 深. 5., & 中国科学院大学, 北. 1. (2023) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2023.003 · Cited by 10 · see citing works
Fu, K., Xu, S., Zhang, Z., Liu, D. C., Xu, T., Zhang, Y., Zhou, F., Zhang, X., Lan, C., Wang, J., et al. (2025) · Advanced Science · doi:10.1002/advs.202503251 · Cited by 11 · see citing works
The neural origin for asymmetric coding of surface color in the primate visual cortex
Wu, Y., Zhao, M., Deng, H., Wang, T., Xin, Y., Dai, W., Huang, J., Zhou, T., Sun, X., Liu, N., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-44809-y · Cited by 10 · see citing works
“After recovery, subjects were trainedtositinaplasticrestraintchairand fi xateonacentraltargetfor long durations with their heads fi xed, facing a screen on which visual stimuli were presented 56,57 .”
Self-citationLiu, N., Behrmann, M., Turchi, J. N., Avidan, G., Hadj‐Bouziane, F., & Ungerleider, L. G. (2022) · Nature Communications · doi:10.1038/s41467-022-34451-x · Cited by 9 · see citing works
Self-citationOxytocin and cardiometabolic interoception: Knowing oneself affects ingestive and social behaviors
Smith, J. A., Eikenberry, S. A., Scott, K. A., Baumer-Harrison, C., de Lartigue, G., de Kloet, A. D., & Krause, E. G. (2022) · Appetite · doi:10.1016/j.appet.2022.106054 · Cited by 8 · see citing works
Methylation of OXT and OXTR genes, central oxytocin, and social behavior in female macaques
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“with aerosolized OXT or focal injections) generally show OXT to have a prosocial and/or anxiolytic effect in behavioral paradigms (Chang et al., 2012, 2015; Dal Monte et al., 2014b; Liu et al., 2015; Parr et al., 2013; Simpson et al., 2014).”
BackgroundOxytocin differentially modulates the early neural responses to faces and non-social stimuli
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“Changes in both amygdala activity and connectivity are associated with intranasal-OT (Liu et al. , 2015; Wang et al. , 2017; Grace et al. , 2018; Tully et al. , 2018), with marked reductions in the activity elicited by fearful faces (Kirsch et al. , 2005; Dodhia et al. , 2014; Grace et al. , 2018)…”
BackgroundNeue Einblicke in die Psychobiologie altruistischer Entscheidungen
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Unraveling the role of oxytocin in the motivational structure of conflict
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Brain serotonin, oxytocin, and their interaction: Relevance for eating disorders
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“Animal research indicated that in addition to modulating brain activity (Febo and Ferris, 2014; Liu et al., 2015), OT affects the maturation of various brain regions (e.g., amygdala, hippocampus, hypothalamus, neocortex) across the lifespan, with higher contribution for subcortical regional…”
Shared and Unique Neural Codes for Biological Motion Perception in Humans and Macaque Monkeys
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“The frequency of reward would be increased as the duration of fixation increased (Liu et al., 2022; Liu et al., 2015; Liu et al., 2013).”
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Self-citationIn Memory of Leslie G. Ungerleider
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Self-citationHormonal and behavioural responses to visual social cues in common marmosets (Callithrix jacchus)
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Evaluating Pupillometry as a Tool for Assessing Facial and Emotional Processing in Nonhuman Primates
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Tracking effects of oxytocin crossing the blood brain barrier in vivo and in vitro
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La importancia de la oxitocina en el vínculo entre perros y personas
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“…& Church, 2015), mejora el procesamiento facial y el reconocimiento de las emociones en humanos (Kis, Kemerle, Hernádi, & Topál, 2013) y macacos (Liu et al., 2015), aumenta el acicalamiento social hacia compañeros estresados en ratones de las praderas ( Microtus ochrogaster ) (Burkett et al.,…”
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Parallel processing of distinct facial signals for the rapid evaluation of social agents
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- Authors
- Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G.
- Affiliations
- National Institutes of Health (US)
- Section on Neurocircuitry, Laboratory of Brain and Cognition, NIMH, NIH, Bethesda, MD 20892;
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-05-26
- Volume
- 112
- Issue
- 24
- Pages
- E3123-30
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4475931
- OpenAlex
- W1498619577
- Cited by
- 65
- References
- 60
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 8 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 2 · 2019: 9 · 2018: 6 · 2017: 5 · 2016: 12 · 2015: 2 · 2014: 2
- FWCI
- 13.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin, facial expression perception, emotional face processing, amygdala, inferior temporal cortex, occipital cortex, functional connectivity, macaque, social behavior, mental illness
- MeSH terms
- Administration, Intranasal, Amygdala, Animals, Behavior, Animal, Cerebral Cortex, Emotions, Facial Expression, Macaca mulatta, Magnetic Resonance Imaging, Male, Oxytocin, Social Behavior, Social Perception, Functional Neuroimaging
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