Dataset Information

Oxytocin Differentially Modulates Amygdala Responses during Top-Down and Bottom-Up Aversive Anticipation.

ABSTRACT: The ability to successfully regulate negative emotions such as fear and anxiety is vital for mental health. Intranasal administration of the neuropeptide oxytocin (OXT) has been shown to reduce amygdala activity but to increase amygdala-prefrontal cortex connectivity during exposure to threatening stimuli suggesting that it may act as an important modulator of emotion regulation. The present randomized, between-subject, placebo-controlled pharmacological study combines the intranasal administration of OXT with functional magnetic resonance imaging (fMRI) during an explicit emotion regulation paradigm in 65 healthy male participants to investigate the modulatory effects of OXT on both bottom-up and top-down emotion regulation. OXT attenuates the activation in the posterior insular cortex and amygdala during anticipation of top-down regulation of predictable threat stimuli in participants with high trait anxiety. In contrast, OXT enhances amygdala activity during the bottom-up anticipation of unpredictable threat stimuli in participants with low trait anxiety. OXT may facilitate top-down goal-directed attention by attenuating amygdala activity in high anxiety individuals, while promoting bottom-up attention/vigilance to unexpected threats by enhancing amygdala activity in low anxiety individuals. OXT may thus have the potential to promote an adaptive balance between bottom-up and top-down attention systems depending on an individual's trait anxiety level.

SUBMITTER: Xin F

PROVIDER: S-EPMC7435249 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Oxytocin Differentially Modulates Amygdala Responses during Top-Down and Bottom-Up Aversive Anticipation.

Xin Fei F Zhou Xinqi X Dong Debo D Zhao Zhongbo Z Yang Xi X Wang Qianqian Q Gu Yan Y Kendrick Keith M KM Chen Antao A Becker Benjamin B

Advanced science (Weinheim, Baden-Wurttemberg, Germany) 20200701 16

The ability to successfully regulate negative emotions such as fear and anxiety is vital for mental health. Intranasal administration of the neuropeptide oxytocin (OXT) has been shown to reduce amygdala activity but to increase amygdala-prefrontal cortex connectivity during exposure to threatening stimuli suggesting that it may act as an important modulator of emotion regulation. The present randomized, between-subject, placebo-controlled pharmacological study combines the intranasal administrat ...[more]

PMID: 32832361

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Project description:BackgroundIn the last decade, accumulative evidence has shown that oxytocin can modulate social perception in typically developed individuals and individuals diagnosed with autism. While several studies show that oxytocin (OT) modulates neural activation in social-related neural regions, the mechanism that underlies OT effects in ASD is not fully known yet. Despite evidence from animal studies on connections between the oxytocinergic system and excitation/inhibition neural balance, the influence of OT on oscillatory responses among individuals with ASD has been rarely examined. To bridge these gaps in knowledge, we investigated the effects of OT on both social and non-social stimuli while focusing on its specific influence on the neural connectivity between three socially related neural regions-the left and right fusiform and the medial frontal cortex.MethodsTwenty-five adolescents with ASD participated in a wall-established social task during a randomized, double-blind placebo-controlled MEG and OT administration study. Our main task was a social-related task that required the identification of social and non-social-related pictures. We hypothesized that OT would modulate the oscillatory connectivity between three pre-selected regions of interest to be more adaptive to social processing. Specifically, we focused on alpha and gamma bands which are known to play an important role in face processing and top-down/bottom-up balance.ResultsCompared to placebo, OT reduced the connectivity between the medial frontal cortex and the fusiform in the low gamma more for social stimuli than for non-social ones, a reduction that was correlated with individuals' performance in the task. Additionally, for both social and non-social stimuli, OT increased the connectivity in the alpha and beta bands.LimitationsSample size was determined based on sample sizes previously reported in MEG in clinical populations, especially OT administration studies in combination with neuroimaging in ASD. We were limited in our capability to recruit for such a study, and as such, the sample size was not based on a priori power analysis. Additionally, we limited our analyses to specific neural bands and regions. To validate the current results, future studies may be needed to explore other parameters using whole-brain approaches in larger samples.ConclusionThese results suggest that OT influenced social perception by modifying the communication between frontal and posterior regions, an attenuation that potentially impacts both social and non-social early perception. We also show that OT influences differ between top-down and bottom-up processes, depending on the social context. Overall, by showing that OT influences both social-related perception and overall attention during early processing stages, we add new information to the existing understanding of the impact of OT on neural processing in ASD. Furthermore, by highlighting the influence of OT on early perception, we provide new directions for treatments for difficulties in early attentional phases in this population. Trial registration Registered on October 27, 2021-Retrospectively registered, https://clinicaltrials.gov/ct2/show/record/NCT05096676 (details on clinical registration can be found in www.Clinicaltrialgov , unique identifier: NCT05096676 ).

Dataset Information

Oxytocin Differentially Modulates Amygdala Responses during Top-Down and Bottom-Up Aversive Anticipation.

Publications

Oxytocin Differentially Modulates Amygdala Responses during Top-Down and Bottom-Up Aversive Anticipation.

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