Adaptive coding of the value of social cues with oxytocin, an fMRI study in autism spectrum disorder
Abstract
The neuropeptide oxytocin (OT) is one of the major targets of research in neuroscience, with respect to social functioning. Oxytocin promotes social skills and improves the quality of face processing in individuals with social dysfunctions such as autism spectrum disorder (ASD). Although one of OT's key functions is to promote social behavior during dynamic social interactions, the neural correlates of this function remain unknown. Here, we combined acute intranasal OT (IN-OT) administration (24 IU) and fMRI with an interactive ball game and a face-matching task in individuals with ASD (N = 20). We found that IN-OT selectively enhanced the brain activity of early visual areas in response to faces as compared to non-social stimuli. OT inhalation modulated the BOLD activity of amygdala and hippocampus in a context-dependent manner. Interestingly, IN-OT intake enhanced the activity of mid-orbitofrontal cortex in response to a fair partner, and insula region in response to an unfair partner. These OT-induced neural responses were accompanied by behavioral improvements in terms of allocating appropriate feelings of trust toward different partners' profiles. Our findings suggest that OT impacts the brain activity of key areas implicated in attention and emotion regulation in an adaptive manner, based on the value of social cues.
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Oxytocin is released during social interaction between humans.
“Oxytocin is released during social interaction between humans.”
From The Oxytocinergic System as a Mediator of Anti-stress and Instorative Effects Induced by Nature: The Calm and Connection Theory (2021) · cites this paper as Andari et al., 2016
Administration of synthetic oxytocin enhances activity in brain areas linked to wellbeing, reward, and social activity.
“These studies have shown that administration of synthetic oxytocin enhances the activity in brain areas linked to wellbeing, reward, and social activity (Andari et al., 2016; Bethlehem et al., 2017).”
From The Oxytocinergic System as a Mediator of Anti-stress and Instorative Effects Induced by Nature: The Calm and Connection Theory (2021) · cites this paper as Andari et al., 2016
Most randomized clinical trials have found some oxytocin effects on ASD symptoms and brain function, but not all trials have reported effects.
“While most randomized clinical trials have found some oxytocin effects on ASD symptoms33,50–52 and brain function50–52,80,81, not all trials have reported effects82.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [81]
IN-OT enhanced BOLD activity of visual areas (inferior occipital lobe) during perception of players' faces in individuals with ASD playing the social ball-toss game.
“More recently, in an fMRI study, individuals with ASD playing the social ball-toss game showed enhanced BOLD activity of visual areas (inferior occipital lobe) during the perception of players’ faces following IN-OT intake (Andari et al. 2016), a finding that is in line with the OT-dependent attention increase to social cues.”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Andari et al. 2016
Cites
How do you feel — now? The anterior insula and human awareness
(Bud) Craig, A. D. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2555 · Cited by 6,657 · see citing works
Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690 · see citing works
The NimStim set of facial expressions: Judgments from untrained research participants.
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., Marcus, D. J., Westerlund, A., Casey, B., & Nelson, C. (2009) · Psychiatry Research · doi:10.1016/j.psychres.2008.05.006 · Cited by 3,454 · see citing works
Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans
Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., Gruppe, H., Mattay, V. S., Gallhofer, B., & Meyer-Lindenberg, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-05.2005 · Cited by 1,639 · see citing works
Social effects of oxytocin in humans: context and person matter
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.002 · Cited by 1,572 · see citing works
Dissociation of reward anticipation and outcome with event-related fMRI
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00016 · Cited by 1,300 · see citing works
Oxytocin improves “mind-reading” in humans
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.015 · Cited by 1,298 · see citing works
The Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict Among Humans
De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., Van Kleef, G. A., Baas, M., Ten Velden, F. S., Van Dijk, E., & Feith, S. W. W. (2010) · Science · doi:10.1126/science.1189047 · Cited by 1,148 · see citing works
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Promoting social behavior with oxytocin in high-functioning autism spectrum disorders.
Andari, E., Duhamel, J.-R., Zalla, T., Herbrecht, E., Leboyer, M., & Sirigu, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910249107 · Cited by 941 · see citing works
Self-citationOxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856 · see citing works
What does the amygdala contribute to social cognition
Adolphs, R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05445.x · Cited by 836 · see citing works
Oxytocin increases gaze to the eye region of human faces
Guastella, A. J., Mitchell, P. B., & Dadds, M. R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.06.026 · Cited by 798 · see citing works
Hare, T. A., O'Doherty, J., Camerer, C. F., Schultz, W., & Rangel, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1309-08.2008 · Cited by 792 · see citing works
Sescousse, G., Caldú, X., Segura, B., & Dreher, J.-C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.002 · Cited by 782 · see citing works
Oxytocin induces maternal behavior in virgin female rats
Pedersen, C. A., Ascher, J. A., Monroe, Y. L., & Prange, A. J. (1982) · Science · doi:10.1126/science.7071605 · Cited by 770 · see citing works
Oxytocin-gaze positive loop and the coevolution of human-dog bonds
Nagasawa, M., Mitsui, S., En, S., Ohtani, N., Ohta, M., Sakuma, Y., Onaka, T., Mogi, K., & Kikusui, T. (2015) · Science · doi:10.1126/science.1261022 · Cited by 753 · see citing works
Intranasal Administration of Oxytocin Increases Envy and Schadenfreude (Gloating)
Shamay-Tsoory, S. G., Fischer, M., Dvash, J., Harari, H., Perach-Bloom, N., & Levkovitz, Y. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.009 · Cited by 542 · see citing works
Brain processing of visual sexual stimuli in human males
Redouté, J., Stoléru, S., Grégoire, M., Costes, N., Cinotti, L., Lavenne, F., Bars, D. L., Forest, M., & Pujol, J. (2000) · Human Brain Mapping · doi:10.1002/1097-0193(200011)11:3 · Cited by 538 · see citing works
Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans
Gamer, M., Zurowski, B., & Büchel, C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000985107 · Cited by 487 · see citing works
The role of the occipital face area in the cortical face perception network
Pitcher, D., Walsh, V., & Duchaine, B. (2011) · Experimental Brain Research · doi:10.1007/s00221-011-2579-1 · Cited by 399 · see citing works
Loup, F., Tribollet, E., Dubois-Dauphin, M., & Dreifuss, J. J. (1991) · Brain Research · doi:10.1016/0006-8993(91)90345-v · Cited by 378 · see citing works
Oxytocin 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
An Anxiolytic Action of Oxytocin is Enhanced by Estrogen in the Mouse
MCCARTHY, M. M., MCDONALD, C. H., BROOKS, P. J., & GOLDMAN, D. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00212-0 · Cited by 328 · see citing works
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., & Pagnoni, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.013 · Cited by 303 · see citing works
Oxytocin, vasopressin and pair bonding: implications for autism
Hammock, E. A. D., & Young, L. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1939 · Cited by 289 · see citing works
Chen, F. S., Kumsta, R., von Dawans, B., Monakhov, M., Ebstein, R. P., & Heinrichs, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113079108 · Cited by 268 · see citing works
Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder
Domes, G., Heinrichs, M., Kumbier, E., Grossmann, A., Hauenstein, K., & Herpertz, S. C. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.007 · Cited by 255 · see citing works
Oxytocin facilitates protective responses to aversive social stimuli in males
Striepens, N., Scheele, D., Kendrick, K. M., Becker, B., Schäfer, L., Schwalba, K., Reul, J., Maier, W., & Hurlemann, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208852109 · Cited by 242 · see citing works
Oxytocin and social motivation
Gordon, I., Martin, C., Feldman, R., & Leckman, J. F. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.007 · Cited by 211 · see citing works
Skuse, D. H., Lori, A., Cubells, J. F., Lee, I., Conneely, K. N., Puura, K., Lehtimäki, T., Binder, E. B., & Young, L. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302985111 · Cited by 207 · see citing works
Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence
Bosch, O. J. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0085 · Cited by 194 · see citing works
Freeman, 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
WILLIAMS, J. R., CARTER, C. S., & INSEL, T. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34393.x · Cited by 147 · see citing works
Shamay-Tsoory, S. G., Abu-Akel, A., Palgi, S., Sulieman, R., Fischer-Shofty, M., Levkovitz, Y., & Decety, J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.015 · Cited by 123 · see citing works
Theta Signal as the Neural Signature of Social Exclusion
Cristofori, I., Moretti, L., Harquel, S., Posada, A., Deiana, G., Isnard, J., Mauguı̀ere, F., & Angela Sirigu, B. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs236 · Cited by 93 · see citing works
Social neuroscience: The social brain, oxytocin, and health
Norman, G. J., Hawkley, L. C., Cole, S. W., Berntson, G. G., & Cacioppo, J. T. (2011) · Social Neuroscience · doi:10.1080/17470919.2011.568702 · Cited by 72 · see citing works
Barthélémy, C. (2014) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-013-0516-5 · Cited by 1 · see citing works
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Intranasal oxytocin in the treatment of autism spectrum disorders: A multilevel meta-analysis
Huang, Y., Huang, X., Ebstein, R. P., & Yu, R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.028 · Cited by 119 · see citing works
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Yamasue, H., & Domes, G. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_24 · Cited by 109 · see citing works
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Li, T., Chen, X., Mascaro, J., Haroon, E., & Rilling, J. K. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.01.006 · Cited by 105 · see citing works
Wang, D., Yan, X., Li, M., & Ma, Y. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx085 · Cited by 86 · see citing works
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Kanat, M., Spenthof, I., Riedel, A., van Elst, L. T., Heinrichs, M., & Domes, G. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.67 · Cited by 70 · see citing works
Grahn, P., Ottosson, J., & Uvnäs-Moberg, K. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.617814 · Cited by 46 · see citing works
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- Authors
- Andari, E., Richard, N., Leboyer, M., & Sirigu, A.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Corresponding author
- Andari, Elissar
- Venue
- Cortex
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 76
- Pages
- 79-88
- ISSN
- 0010-9452 (ISSN-L)
- OpenAlex
- W2253101848
- Cited by
- 62
- References
- 39
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 3 · 2022: 12 · 2021: 10 · 2020: 7 · 2019: 4 · 2018: 7 · 2017: 11 · 2016: 2
- FWCI
- 12.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cortex (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Keywords
- oxytocin, autism spectrum disorder, social cues, face processing, amygdala, hippocampus, orbitofrontal cortex, insula, trust, social interaction, emotion regulation, early visual areas, intranasal administration
- MeSH terms
- Autism Spectrum Disorder, Administration, Intranasal, Amygdala, Cues, Emotions, Female, Humans, Interpersonal Relations, Magnetic Resonance Imaging, Male, Oxytocin, Social Behavior
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