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Oxytocin improves behavioural and neural deficits in inferring others’ social emotions in autism
Abstract
Recent studies have suggested oxytocin's therapeutic effects on deficits in social communication and interaction in autism spectrum disorder through improvement of emotion recognition with direct emotional cues, such as facial expression and voice prosody. Although difficulty in understanding of others' social emotions and beliefs under conditions without direct emotional cues also plays an important role in autism spectrum disorder, no study has examined the potential effect of oxytocin on this difficulty. Here, we sequentially conducted both a case-control study and a clinical trial to investigate the potential effects of oxytocin on this difficulty at behavioural and neural levels measured using functional magnetic resonance imaging during a psychological task. This task was modified from the Sally-Anne Task, a well-known first-order false belief task. The task was optimized for investigation of the abilities to infer another person's social emotions and beliefs distinctively so as to test the hypothesis that oxytocin improves deficit in inferring others' social emotions rather than beliefs, under conditions without direct emotional cues. In the case-control study, 17 males with autism spectrum disorder showed significant behavioural deficits in inferring others' social emotions (P = 0.018) but not in inferring others' beliefs (P = 0.064) compared with 17 typically developing demographically-matched male participants. They also showed significantly less activity in the right anterior insula and posterior superior temporal sulcus during inferring others' social emotions, and in the dorsomedial prefrontal cortex during inferring others' beliefs compared with the typically developing participants (P < 0.001 and cluster size > 10 voxels). Then, to investigate potential effects of oxytocin on these behavioural and neural deficits, we conducted a double-blind placebo-controlled crossover within-subject trial for single-dose intranasal administration of 24 IU oxytocin in an independent group of 20 males with autism spectrum disorder. Behaviourally, oxytocin significantly increased the correct rate in inferring others' social emotions (P = 0.043, one-tail). At the neural level, the peptide significantly enhanced the originally-diminished brain activity in the right anterior insula during inferring others' social emotions (P = 0.004), but not in the dorsomedial prefrontal cortex during inferring others' beliefs (P = 0.858). The present findings suggest that oxytocin enhances the ability to understand others' social emotions that have also required second-order false belief rather than first-order false beliefs under conditions without direct emotional cues in autism spectrum disorder at both the behaviour and neural levels.
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In the citing paper
“OT relieves social deficits observed in ASD and augments insular activity and connectivity22,23, suggesting a mechanistic relationship between OT, insula and social cognition.”
From Insular cortex mediates approach and avoidance responses to social affective stimuli (2018) · cites this paper as [22]
In the citing paper
“Imaging studies have provided preliminary evidence that oxytocin influences the ability to understand others’ mental and emotional states by enhancing activation of brain regions within the empathy network, such as the anterior insula50.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [50]
In the citing paper
“Moreover, previous studies showing oxytocin effects on emotion recognition, empathy, or face processing in adults with ASD had an average sample size of 21.5 participants48,50,51,86–88.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [50]
In the citing paper
“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 [50]
In the citing paper
“IN-OT enhances emotion recognition and theory of mind in ASD (Aoki et al. 2014; Guastella et al. 2010), and gaze to the eyes in ASD and in healthy subjects (Auyeung et al. 2015).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Aoki et al. 2014
In the citing paper
“At the neural level, IN-OT enhances anterior insula activity during inference of others’ emotions (Aoki et al. 2014).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Aoki et al. 2014
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Metadata
- Authors
- Aoki, Y., Yahata, N., Watanabe, T., Takano, Y., Kawakubo, Y., Kuwabara, H., Iwashiro, N., Natsubori, T., Inoue, H., Suga, M., Takao, H., Sasaki, H., Gonoi, W., Kunimatsu, A., Kasai, K., & Yamasue, H.
- Affiliations
- The University of Tokyo (JP)
- Japan Science and Technology Agency (JP)
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-08-22
- Volume
- 137
- Issue
- 11
- Pages
- 3073-3086
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2065016435
- Semantic Scholar
- d4ecae6caeeae9ee79c364d86b5653566d456221
- Cited by
- 187
- References
- 89
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 15 · 2023: 12 · 2022: 8 · 2021: 14 · 2020: 15 · 2019: 12 · 2018: 20 · 2017: 26 · 2016: 20 · 2015: 32 · 2014: 1
- FWCI
- 39.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science (26250024)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- oxytocin, autism spectrum disorder, false belief understanding, second-order false belief, Sally-Anne task, anterior insula, posterior superior temporal sulcus, dorsomedial prefrontal cortex, intranasal administration, social cognition, placebo-controlled crossover trial, case-control study, social communication deficits
- MeSH terms
- Adult, Cerebral Cortex, Child Development Disorders, Pervasive, Double-Blind Method, Emotions, Empathy, Facial Expression, Humans, Magnetic Resonance Imaging, Male, Oxytocin, Placebos, Social Perception, Case-Control Studies, Treatment Outcome, Cross-Over Studies, Young Adult, Theory of Mind, Functional Neuroimaging
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