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A Spatiotemporal Profile of In Vivo Cerebral Blood Flow Changes Following Intranasal Oxytocin in Humans
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BACKGROUND: Animal and human studies highlight the role of oxytocin in social cognition and behavior and the potential of intranasal oxytocin (IN-OT) to treat social impairment in individuals with neuropsychiatric disorders such as autism. However, extensive efforts to evaluate the central actions and therapeutic efficacy of IN-OT may be marred by the absence of data regarding its temporal dynamics and sites of action in the living human brain. METHODS: In a placebo-controlled study, we used arterial spin labeling to measure IN-OT-induced changes in resting regional cerebral blood flow (rCBF) in 32 healthy men. Volunteers were blinded regarding the nature of the compound they received. The rCBF data were acquired 15 min before and up to 78 min after onset of treatment onset (40 IU of IN-OT or placebo). The data were analyzed using mass univariate and multivariate pattern recognition techniques. RESULTS: We obtained robust evidence delineating an oxytocinergic network comprising regions expected to express oxytocin receptors, based on histologic evidence, and including core regions of the brain circuitry underpinning social cognition and emotion processing. Pattern recognition on rCBF maps indicated that IN-OT-induced changes were sustained over the entire posttreatment observation interval (25-78 min) and consistent with a pharmacodynamic profile showing a peak response at 39-51 min. CONCLUSIONS: Our study provides the first visualization and quantification of IN-OT-induced changes in rCBF in the living human brain unaffected by cognitive, affective, or social manipulations. Our findings can inform theoretical and mechanistic models regarding IN-OT effects on typical and atypical social behavior and guide future experiments (e.g., regarding the timing of experimental manipulations).
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![Figure 3 Statistical parametric maps for the four clusters showing a signi fi cant Treatment (intranasal oxytocin [ n 5 16], placebo [ n 5 16]) 3 Period (baseline, after administration) interaction ( F contrast) over the entire observation interval of 25 -78 minutes following the onset of treatment. Inserted graphs plot the extracted ( fi rst eigenvariate), F contrast adjusted rCBF values for each cluster to illustrate the interaction effect. Error bars represent SE. The right-hand side of each image corresponds to the participant ' s right side. Slice numbers indicate Montreal Neurological Institute coordinates. rCBF, regional cerebral blood fl ow.](/paper-figures/8774c7994d3a4925acb734a10321b3c5/a-spatiotemporal-profile-of-in-vivo-cerebral-blood-flow-changes-following-figure-3.png)
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“doubt has been cast on the extent to which intranasal OXT crosses the blood-brain barrier (Neumann et al., 2013;Paloyelis et al., 2014;Striepens et al., 2013).”
From Oxytocin increases attention to the eyes and selectively enhances self-reported affective empathy for fear (2017) · cites this paper as Paloyelis et al., 2014
In the citing paper
“Furthermore, there are uncertainties regarding the site and mechanism of action of exogenous intranasal oxytocin in humans due to lack of suitable radio tracers (Paloyelis et al., 2016).”
From Meta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions (2017) · cites this paper as Paloyelis et al., 2016
In the citing paper
“intranasal administration of oxytocin has been shown to modulate neural responses in brain regions involved in threat detection and reward processing (Ma et al., 2016b; Paloyelis et al., 2016; Wang et al., 2017; Liu et al., 2019).”
From Oxytocin promotes coordinated out-group attack during intergroup conflict in humans (2019) · cites this paper as Paloyelis et al., 2016
In the citing paper
“A recent elegant study using arterial spin labeling showed that IN-OT increases the levels of cerebral blood flow of key regions of the SBN such as ventral striatum, amygdala, hippocampus, caudate nucleus, anterior and middle cingulate cortices, anterior insula, ventral tegmental area (VTA), inferior frontal gyrus, inferior parietal cortex, and superior temporal gyrus (Paloyelis et al. 2016).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Paloyelis et al. 2016
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Effects of intranasal oxytocin in food intake and craving: A meta-analysis of clinical trials
Chen, C., Chiang, Y.-C., Kuo, T., Tam, K., & Loh, E. (2021) · Clinical Nutrition · doi:10.1016/j.clnu.2021.08.011 · Cited by 24
Martins, D., Davies, C., Micheli, A. D., Oliver, D., Krawczun-Rygmaczewska, A., Fusar‐Poli, P., & Paloyelis, Y. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00890-7 · Cited by 27
Chen, Y., Li, Q., Zhang, Q., Kou, J., Zhang, Y., Cui, H., Wernicke, J., Montag, C., Becker, B., Kendrick, K. M., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.589878 · Cited by 26
Lussier, D., Cruz‐Almeida, Y., & Ebner, N. C. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00338 · Cited by 21
Shcherbinin, S., Doyle, O., Zelaya, F. O., Simoni, S. D., Mehta, M. A., & Schwarz, A. J. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4021-z · Cited by 21
Martins, D., Leslie, M. R., Rodan, S., Zelaya, F. O., Treasure, J. L., & Paloyelis, Y. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00871-w · Cited by 21
Imaging clinically relevant pain states using arterial spin labeling
Loggia, M. L., Segerdahl, A. R., Howard, M. A., & Tracey, I. (2019) · PAIN Reports · doi:10.1097/pr9.0000000000000750 · Cited by 23
Zhao, W., Geng, Y., Luo, L., Zhao, Z., Ma, X., Xu, L., Yao, S., & Kendrick, K. M. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00272 · Cited by 20
Schultebraucks, K., Maslahati, T., Wingenfeld, K., Hellmann‐Regen, J., Kraft, J., Kownatzki, M., Behnia, B., Ripke, S., Otte, C., & Roepke, S. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01247-4 · Cited by 23
Leslie, M., Leppanen, J., Paloyelis, Y., Nazar, B. P., & Treasure, J. (2019) · Journal of neuroendocrinology · doi:10.1111/jne.12771 · Cited by 19
Tully, J., Sethi, A., Griem, J., Paloyelis, Y., Craig, M., Williams, S., Murphy, D., Blair, J., & Blackwood, N. (2023) · Nature Mental Health · doi:10.1038/s44220-023-00067-3 · Cited by 18
Embodied Precision: Intranasal Oxytocin Modulates Multisensory Integration
Crucianelli, L., Paloyelis, Y., Ricciardi, L., Jenkinson, P. M., & Fotopoulou, A. (2018) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01366 · Cited by 20
Victory is its own reward: oxytocin increases costly competitive behavior in schizophrenia
Bradley, E., Brustkern, J., Coster, L. D., van den Bos, W., McClure, S. M., Seitz, A., & Woolley, J. D. (2019) · Psychological Medicine · doi:10.1017/s0033291719000552 · Cited by 21
Mekhael, A. A., Bent, J. E., Fawcett, J. M., Campbell, T. S., Aguirre‐Camacho, A., Farrell, A., & Rash, J. A. (2023) · Canadian Journal of Pain · doi:10.1080/24740527.2023.2191114 · Cited by 19
A phase II randomised controlled trial of intranasal oxytocin in anorexia nervosa
Maguire, S., Kesby, A., Brownlow, R. S., Hunt, G. E., Kim, M., McAulay, C., Grisham, J. R., McGregor, I. S., Suraev, A. S., Kevin, R. C., et al. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107032 · Cited by 17
Chen, Y., Zou, H., Hou, X., Lan, C., Wang, J., Qing, Y., Chen, W., Yao, S., & Kendrick, K. M. (2023) · eLife · doi:10.7554/elife.85847 · Cited by 18
Lan, C., Liu, C., Li, K., Zhao, Z., Yang, J., Ma, Y., Scheele, D., Yao, S., Kendrick, K. M., & Becker, B. (2022) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyac037 · Cited by 18
Ali, Z. A., Yasseen, A. A., Al-Dujaili, A. H., Al-Karaqully, A. J., McAllister, K. A., & Jumaah, A. S. (2022) · PLoS ONE · doi:10.1371/journal.pone.0265217 · Cited by 17
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
Metadata
- Authors
- Paloyelis, Y., Doyle, O. M., Zelaya, F. O., Maltezos, S., Williams, S. C., Fotopoulou, A., & Howard, M. A.
- Affiliations
- King's College London (GB)
- University College London (GB)
- Corresponding author
- Paloyelis, Yannis
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 79
- Issue
- 8
- Pages
- 693-705
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2021223630
- Cited by
- 187
- References
- 154
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 12 · 2023: 10 · 2022: 12 · 2021: 16 · 2020: 41 · 2019: 20 · 2018: 14 · 2017: 19 · 2016: 13
- FWCI
- 22.75
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Biological Psychiatry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Portal (King's College London) (publishedVersion, cc-by)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Economic and Social Research Council fellowship (ES/K009400/1)
- Volkswagen Foundation “European Platform for Life Sciences, Mind Sciences and Humanities” (II/85 069)
- Institute for the Study of Affective Neuroscience/Hope for Depression Research Foundation (to AF)
- European Research Council Starting Investigator Award (ERC-2012-STG GA313755)
- 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 › Neuropeptides and Animal Physiology
- Keywords
- intranasal oxytocin, regional cerebral blood flow, arterial spin labeling, oxytocin receptor, social cognition, emotional processing, pharmacodynamics, autism spectrum disorder, social dysfunction, spatiotemporal dynamics
- MeSH terms
- Administration, Intranasal, Brain, Brain Mapping, Central Nervous System Agents, Cerebrovascular Circulation, Humans, Magnetic Resonance Imaging, Male, Oxytocin, Pattern Recognition, Automated, Rest, Multivariate Analysis, Single-Blind Method, Young Adult
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