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Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction
Open accessAbstract
Both oxytocin (OT) and vasopressin (AVP) are known to modulate social behavior, and dysfunction in both systems has been postulated as a potential cause of certain psychiatric disorders that involve social behavioral deficits. In particular, there is growing interest in intranasal OT as a potential treatment for certain psychiatric disorders, and preliminary pre-clinical and clinical studies suggest efficacy in alleviating some of the associated symptoms. However, the vast majority of research participants in these studies have been male, and there is evidence for sexually differentiated effects of nonapeptides in both humans and non-human animals. To date, no study has investigated the effect of intranasal OT on brain function in human males and females within the same paradigm. Previously, in a randomized, placebo-controlled, double-blind fMRI study, we reported effects of intranasal OT and AVP on behavior and brain activity of human males as they played an interactive social game known as the Prisoner's Dilemma Game. Here, we present findings from an identical study in human females, and compare these with our findings from males. Overall, we find that both behavioral and neural responses to intranasal OT and AVP are highly sexually differentiated. In women, AVP increased conciliatory behavior, and both OT and AVP caused women to treat computer partners more like humans. In men, AVP increased reciprocation of cooperation from both human and computer partners. However, no specific drug effects on behavior were shared between men and women. During cooperative interactions, both OT and AVP increased brain activity in men within areas rich in OT and AVP receptors and in areas playing a key role in reward, social bonding, arousal and memory (e.g., the striatum, basal forebrain, insula, amygdala and hippocampus), whereas OT and AVP either had no effect or in some cases actually decreased brain activity in these regions in women. OT treatment rendered neural responses of males more similar to responses of females in the placebo group and vice versa, raising the prospect of an inverted u-shaped dose response to central OT levels. These findings emphasize the need to fully characterize the effects of intranasal OT and AVP in both males and females and at multiple doses before widespread clinical application will be warranted.
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In the citing paper
“This bias can be observed in much of the prior work on oxytocin in humans as well, with some neuroimaging studies indicating potential differences in the oxytocin system between sexes.13, 14, 47, 48, 49”
From Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women (2017) · cites this paper as [48]
In the citing paper
“This bias can be observed in much of the prior work on oxytocin in humans as well, with some neuroimaging studies indicating potential differences in the oxytocin system between sexes.13, 14, 47, 48, 49”
From Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women (2017) · cites this paper as [48]
In the citing paper
“These data have, however, found OT and AVP can have differential effects on neural activity (i.e., BOLD fMRI responses) and cognition, at least in some cases although the effects of OT are more robust [84; 86; 87; 88; 89; 90].”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [88]
In the citing paper
“The few studies that have compared the effects of intranasally administered OT and AVP in humans have reported that these peptides do not have opposing roles.”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [88]
In the citing paper
“In humans, intranasal VP had sex-specific effects during social communication and cooperation interactions”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Rilling et al., 2014
In the citing paper
“Intranasal OT increased the caudate/putamen response in males, whereas it decreased this response in females (Rilling et al., 2014).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Rilling et al., 2014
In the citing paper
“Sex differences were also found for the effect of OT on brain activation during reciprocated cooperation.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Rilling et al., 2014
In the citing paper
“previous research has shown that oxytocin effects can vary as a function of emotion regulation skills (Quirin et al., 2011), social context history of childhood maltreatment (Ebert et al., 2013; Flanagan et al., 2015), and sex (Ditzen et al., 2012; Rilling et al., 2014).”
From Augmenting Prolonged Exposure therapy for PTSD with intranasal oxytocin: a randomized, placebo-controlled pilot trial (2018) · cites this paper as Rilling et al., 2014
In the citing paper
“In healthy individuals, OT effects seem to follow an inverted u-shape (Rilling et al, 2014), with doses ~24 IU, resulting in more anxiolytic effects than higher doses of OT (Cardoso et al, 2013).”
From Intranasal oxytocin administration dampens amygdala reactivity towards emotional faces in male and female PTSD patients (2016) · cites this paper as Rilling et al, 2014
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“In the present study, only female participants were chosen, in line with emerging research that posits that when females take no oral contraceptives (or any other medication containing hormones) they are ideal subjects when it comes to OT research (Ditzen et al., 2013; Feldman, Gordon, & Zagoory-Sharon, 2010; Insel &…”
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“…re fl ects the well-documented four-to-one male bias in autism prevalence [63], future research is warranted to examine oxytocin-induced effects also in larger samples of girls with autism, especially given prior reports of sex-related differences in neural and behavioral responses to oxytocin [64].”
BackgroundFakhoury, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.02.026 · Cited by 21
“, 2001) and oxytocin (Rilling et al., 2014; Uhl-Bronner et al., 2005) in sexual dimorphism.”
BackgroundResultOxytocin and vasopressin modulation of prisoner’s dilemma strategies
Neto, M. L., Antunes, M. C. D. S., Lopes, M. C., Ferreira, D. M. S., Rilling, J. K., & Prata, D. P. (2020) · Journal of Psychopharmacology · doi:10.1177/0269881120913145 · Cited by 23
“The present sample is included in previous reports which follow the same protocol (Chen et al., 2016; Feng et al., 2015; Rilling et al., 2012, 2014).”
InfluentialSelf-citationVoncken, M. J., Dijk, C., Stöhr, F., Niesten, I. J. M., Schruers, K. R. J., & Kuypers, K. P. C. (2021) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2021.07.005 · Cited by 20
Sippel, L. M., Flanagan, J. C., Holtzheimer, P. E., Maria, M. M. M., Brady, K. T., & Joseph, J. E. (2021) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2021.111368 · Cited by 21
Sex differences in stress reactivity after intranasal oxytocin in recreational cannabis users
Reed, S. C., Haney, M., Manubay, J. M., Campagna, B. R., Reed, B., Foltin, R. W., & Evans, S. M. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.11.008 · Cited by 20
“, 2015) and humans (e.g., Cardoso et al., 2012; Flanagan et al., 2018; Kubzansky et al., 2012; Rilling et al., 2014; Xu et al., 2017) have demonstrated that the effects of i.”
Oxytocin and vasopressin increase male-directed threats and vocalizations in female macaques
Jiang, Y., & Platt, M. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-36332-0 · Cited by 20
Oxytocin strengthens the link between provocation and aggression among low anxiety people
Pfundmair, M., Reinelt, A., DeWall, C. N., & Feldmann, L. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.04.025 · Cited by 19
Levin, S. B. (2021) · doi:10.1093/oso/9780190051495.001.0001 · Cited by 18
Berger, R., Hurlemann, R., Shamay‐Tsoory, S., Kanterman, A., Brauser, M., Gorni, J., Luhmann, M., Schramm, E., Schultz, J., Philipsen, A., et al. (2024) · Psychotherapy and Psychosomatics · doi:10.1159/000538752 · Cited by 22
Oxytocin: Coevolution of human and domesticated animals
Herbeck, Y. E., Gulevich, R. G., Shepeleva, D. V., & Grinevich, V. (2017) · Russian Journal of Genetics Applied Research · doi:10.1134/s2079059717030042 · Cited by 18
Dose-Dependent and Lasting Influences of Intranasal Vasopressin on Face Processing in Men
Price, D., Burris, D., Cloutier, A., Thompson, C. B., Rilling, J. K., & Thompson, R. R. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00220 · Cited by 18
Self-citationOxytocin conditions trait-based rule adherence
Gross, J., & Dreu, C. K. W. D. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw138 · Cited by 19
“Administration of oxytocin can differentially affect the behaviour of males and females (Rilling et al., 2014; Yao et al., 2014) and might interact with menstrual cycle and usage of contraceptives.”
BackgroundCoenjaerts, M., Adrovic, B., Trimborn, I., Philipsen, A., Hurlemann, R., & Scheele, D. (2023) · Scientific Reports · doi:10.1038/s41598-023-29754-y · Cited by 17
Emerging Frontiers in Social Neuroendocrinology and the Study of Nonapeptides
Ondrasek, N. R. (2016) · Ethology · doi:10.1111/eth.12493 · Cited by 19
Frazier, I. R., Lin, T., Liu, P., Skarsten, S. N., Feifel, D., & Ebner, N. C. (2021) · Psychology and Aging · doi:10.1037/pag0000545 · Cited by 18
“Previous work that found oxytocin-induced modulatory effects on insula activity in response to untrustworthiness used facial images to depict game partners (Chen et al., 2016; Rilling et al., 2014).”
BackgroundInfluentialA common variant in OXTR rs53576 impacts topological patterns of brain functional networks
Wang, J., Zhang, Y., Zhu, D., Yang, Z., Liu, F., Qin, W., Zhu, J., Liu, B., Jiang, T., & Yu, C. (2019) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-019-01414-5 · Cited by 16
Arginine Vasopressin, Synaptic Plasticity, and Brain Networks
Winklewski, P. J., Marcinkowska, A. B., & Biancardi, V. C. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220222143532 · Cited by 16
Vehlen, A., Kellner, A., Normann, C., Heinrichs, M., & Domes, G. (2023) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2023.01.016 · Cited by 18
Genomic conflicts and sexual antagonism in human health: insights from oxytocin and testosterone
Mökkönen, M., & Crespi, B. J. (2015) · Evolutionary Applications · doi:10.1111/eva.12244 · Cited by 18
“mutual cooperation in males, decreases them in females Rilling et al. (2014)”
BackgroundFear or greed? Oxytocin regulates inter-individual conflict by enhancing fear in men
Zheng, H., Kendrick, K. M., & Yu, R. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.07.003 · Cited by 16
“ration and even temper deliberate greed (De Dreu et al., 2014; Rilling et al., 2014).”
BackgroundSchuh‐Hofer, S., Eichhorn, N., Grinevich, V., & Treede, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00161 · Cited by 16
Jarnecke, A. M., Barden, E. P., Back, S. E., Brady, K. T., & Flanagan, J. C. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.10.003 · Cited by 16
“For example, sex differences in OT response have been extensively documented (Ditzen et al., 2013; Flanagan et al., 2018a; Lynn et al., 2014; Rilling et al., 2014).”
BackgroundTesting for ‘Anthropomorphization’: A Case for Mixed Methods in Human-Robot Interaction
Damholdt, M. F., Vestergaard, C., & Seibt, J. (2020) · Springer series on bio- and neurosystems · doi:10.1007/978-3-030-42307-0_8 · Cited by 16
Blending oxytocin and dopamine with everyday creativity
Chong, A., Tolomeo, S., Yue, X., Angeles, D. C., Cheung, M. W. ‐., Becker, B., Lai, P. S., Lei, Z., Malavasi, F., Tang, Q., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-95724-x · Cited by 16
Marazziti, D., Diep, P.-T., Carter, C. S., & Carbone, M. G. (2022) · Current Medicinal Chemistry · doi:10.2174/0929867329666220727120646 · Cited by 16
Effects of oxytocin administration on salivary sex hormone levels in autistic and neurotypical women
Procyshyn, T. L., Lombardo, M. V., Lai, M., Bonnie Auyeung, B., Crockford, S. K., Deakin, J., Soubramanian, S., Sule, A., Baron‐Cohen, S., & Bethlehem, R. A. I. (2020) · Molecular Autism · doi:10.1186/s13229-020-00326-5 · Cited by 16
The effect of intranasal oxytocin on social reward processing in humans: a systematic review
Kraus, J., Výborová, E., & Silani, G. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1244027 · Cited by 16
Coenjaerts, M., Trimborn, I., Adrovic, B., Stoffel‐Wagner, B., Cahill, L. F., Philipsen, A., Hurlemann, R., & Scheele, D. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119689 · Cited by 17
“8 recognition memory of negative stimuli and insula activity to subsequently remembered negative items in men and that it would produce the opposite effect in women (Rilling et al., 2014).”
BackgroundEffects of oxytocin administration and conditioned oxytocin on brain activity: An fMRI study
Skvortsova, A., Veldhuijzen, D. S., de Rover, M., Pacheco‐López, G., Bakermans‐Kranenburg, M. J., van IJzendoorn, M. H., Chavannes, N. H., van Middendorp, H., & Evers, A. W. M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0229692 · Cited by 17
Imaging neuropeptide effects on human brain function
Lefèvre, A., Hurlemann, R., & Grinevich, V. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2899-6 · Cited by 16
Current rodent models for the study of empathic processes
Cox, S. S., & Reichel, C. M. (2020) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000590 · Cited by 15
“There is overwhelming evidence in human studies linking oxytocin to several components of empathy (Domes et al., 2007; Hurlemann et al., 2010; Decety, 2011; Theodoridou et al., 2013; Christov-Moore et al., 2014; Rilling et al., 2014; Jones et al., 2017; Ebert and Brüne, 2018; Uysal et al., 2020).”
BackgroundWang, J., Zhang, P., Li, W., Qin, W., Liu, F., Xu, J., Xu, Q., Zhu, D., Ye, Z., & Yu, C. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa198 · Cited by 14
Social affective behaviors among female rats involve the basolateral amygdala and insular cortex
Djerdjaj, A., Rieger, N. S., Brady, B. H., Carey, B. N., Ng, A. J., & Christianson, J. P. (2023) · PLoS ONE · doi:10.1371/journal.pone.0281794 · Cited by 14
“Sex differences in the oxytocin system are common [57, 75] and there are age [56, 58, 64] and maternal [76] factors that affect cortical oxytocin receptor functions.”
BackgroundTseng, H. C., Chi, M. H., Lee, L.-T., Tsai, H. C., Lee, I. H., Chen, K. C., Yang, Y. K., & Chen, P. S. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.12.011 · Cited by 14
“Sex difference in the neural and behavioral response to oxytocin administration during human social interaction associations has also been reported (Rilling et al., 2014).”
BackgroundIntranasal oxytocin modulates the salience network in aging
Liu, P., Lin, T., Feifel, D., & Ebner, N. C. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119045 · Cited by 13
Intranasal Oxytocin Failed to Affect Chimpanzee (Pan troglodytes) Social Behavior
Proctor, D. P., Calcutt, S. E., Burke, K., & de Waal, F. Β. Μ. (2016) · Animal Behavior and Cognition · doi:10.12966/abc.04.08.2016 · Cited by 14
“Additionally, there is some indication that intranasal oxytocin affects human males and females differently (Rilling et al., 2014).”
Effects of Intranasal Oxytocin on Emotion Recognition in Korean Male: A Dose-Response Study
Shin, N. Y., Park, H. Y., Jung, W. H., & Kwon, J. S. (2018) · Psychiatry Investigation · doi:10.30773/pi.2018.02.19 · Cited by 14
Haram, M., Bettella, F., Brandt, C. L., Quintana, D. S., Nerhus, M., Bjella, T., Djurovic, S., Westlye, L. T., Andreassen, O. A., Melle, I., et al. (2016) · BJPsych Open · doi:10.1192/bjpo.bp.116.003376 · Cited by 13
Deng, G., Ai, H., Qin, L., Xu, J., Feng, C., & Xu, P. (2022) · Psychological Medicine · doi:10.1017/s0033291722002483 · Cited by 12
“, 2011), as well as risky decision making, cooperation, and prosocial behaviors (Feng, Qin, Luo, & Xu, 2020; Feng et al., 2015; Neto et al., 2020; Patel et al., 2015; Rilling et al., 2014).”
BackgroundSabino, A. D. V., Chagas, M. H. N., & Osório, F. L. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05493-0 · Cited by 13
“Also, all participants were male, which hinders the generalization of the findings presented to women, as previous studies have shown that the action of OXT can be modulated by gender (Rilling et al. 2014; Scheele et al. 2014).”
ResultProcyshyn, T. L., Lombardo, M. V., Lai, M., Jassim, N., Bonnie Auyeung, B., Crockford, S. K., Deakin, J., Soubramanian, S., Sule, A., Terburg, D., et al. (2022) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsac016 · Cited by 14
“Importantly, several studies have found the effect of oxytocin on amygdala activation in female participants to be opposite to that originally reported in all-male samples (Rilling et al. , 2014; Luo et al. , 2017; Lieberz et al. , 2020).”
Oxytocin and the Punitive Hub—Dynamic Spread of Cooperation in Human Social Networks
Li, S., Ma, S., Wang, D., Zhang, H., Li, Y., Wang, J., Li, J., Zhang, B., Gross, J., Dreu, C. K. W. D., et al. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2303-21.2022 · Cited by 13
“…only male central players to avoid potential confounding factors associated with sex differences in oxytocin effects ( Fischer-Shofty et al., 2013; Rilling et al., 2014), consistent with previous studies examining oxytocin effects on social cognition and cooperation (De Dreu et al., 2010; Ma et…”
ResultPolk, R. J., Horta, M., Lin, T., Porges, E. C., Ojeda, M., Nazarloo, H. P., Carter, C. S., & Ebner, N. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0048 · Cited by 12
Metadata
- Authors
- Rilling, J. K., DeMarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., Haroon, E., Thompson, R., Ditzen, B., Patel, R., & Pagnoni, G.
- Affiliations
- Emory University (US)
- University of Kansas (US)
- Bowdoin College (US)
- University of Modena and Reggio Emilia (IT)
- Corresponding author
- Rilling, James K.
- ORCID
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 39
- Pages
- 237-248
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3842401
- OpenAlex
- W2129575907
- Cited by
- 343
- References
- 54
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 13 · 2023: 16 · 2022: 19 · 2021: 38 · 2020: 35 · 2019: 50 · 2018: 35 · 2017: 35 · 2016: 32 · 2015: 28 · 2014: 17
- FWCI
- 38.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- Funders
- National Institute of Mental Health (R01 MH084068-01A1)
- National Center for Research Resources
- Yerkes Regional Primate Research Center (2P51RR000165-51)
- National Institutes of Health
- Presbyterian Historical Society (UL1 RR025008)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- oxytocin, vasopressin, sex differences, intranasal administration, social interaction, prisoner's dilemma game, cooperation, conciliation, social bonding, reward processing, brain activity, nonapeptide, mental illness
- MeSH terms
- Administration, Intranasal, Adolescent, Arginine Vasopressin, Brain, Cooperative Behavior, Double-Blind Method, Female, Game Theory, Humans, Image Processing, Computer-Assisted, Interpersonal Relations, Magnetic Resonance Imaging, Male, Oxytocin, Sex Characteristics, Social Behavior, Young Adult, Functional Neuroimaging
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