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      Oxytocin Facilitates Empathic- and Self-embarrassment Ratings by Attenuating Amygdala and Anterior Insula Responses

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          Abstract

          The hypothalamic neuropeptide oxytocin has been reported to enhance emotional empathy in association with reduced amygdala activation, although to date studies have not investigated empathy for individuals expressing self-conscious, moral emotions which engage mentalizing as well as emotion processing networks. In the current randomized, double-blind placebo controlled functional MRI experiment in 70 male and female subjects we have therefore investigated the effects of intranasal oxytocin (40 IU) on behavioral and neural responses to embarrassment experienced by others or by self. Results showed that oxytocin significantly increased ratings of both empathic and self-embarrassment and concomitantly decreased skin conductance response, activation in the right amygdala and insula but not in the medial prefrontal cortex. The amygdala effects of oxytocin were associated with the magnitude of the skin conductance response and trait anxiety scores. Overall our results demonstrate that oxytocin increases ratings of self- and other embarrassment and that this is associated with reduced physiological arousal and activity in neural circuits involved in emotional arousal. The neural effects of oxytocin were more pronounced stronger in individuals with high trait anxiety suggesting that it may particularly reduce their anxiety in embarrassing situations.

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          Most cited references52

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          Oxytocin modulates neural circuitry for social cognition and fear in humans.

          In non-human mammals, the neuropeptide oxytocin is a key mediator of complex emotional and social behaviors, including attachment, social recognition, and aggression. Oxytocin reduces anxiety and impacts on fear conditioning and extinction. Recently, oxytocin administration in humans was shown to increase trust, suggesting involvement of the amygdala, a central component of the neurocircuitry of fear and social cognition that has been linked to trust and highly expresses oxytocin receptors in many mammals. However, no human data on the effects of this peptide on brain function were available. Here, we show that human amygdala function is strongly modulated by oxytocin. We used functional magnetic resonance imaging to image amygdala activation by fear-inducing visual stimuli in 15 healthy males after double-blind crossover intranasal application of placebo or oxytocin. Compared with placebo, oxytocin potently reduced activation of the amygdala and reduced coupling of the amygdala to brainstem regions implicated in autonomic and behavioral manifestations of fear. Our results indicate a neural mechanism for the effects of oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.
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            Oxytocin improves "mind-reading" in humans.

            The ability to "read the mind" of other individuals, that is, to infer their mental state by interpreting subtle social cues, is indispensable in human social interaction. The neuropeptide oxytocin plays a central role in social approach behavior in nonhuman mammals. In a double-blind, placebo-controlled, within-subject design, 30 healthy male volunteers were tested for their ability to infer the affective mental state of others using the Reading the Mind in the Eyes Test (RMET) after intranasal administration of 24 IU oxytocin. Oxytocin improved performance on the RMET compared with placebo. This effect was pronounced for difficult compared with easy items. Our data suggest that oxytocin improves the ability to infer the mental state of others from social cues of the eye region. Oxytocin might play a role in the pathogenesis of autism spectrum disorder, which is characterized by severe social impairment.
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              Is there a core neural network in empathy? An fMRI based quantitative meta-analysis.

              Whilst recent neuroimaging studies have identified a series of different brain regions as being involved in empathy, it remains unclear concerning the activation consistence of these brain regions and their specific functional roles. Using MKDA, a whole-brain based quantitative meta-analysis of recent fMRI studies of empathy was performed. This analysis identified the dACC-aMCC-SMA and bilateral anterior insula as being consistently activated in empathy. Hypothesizing that what are here termed affective-perceptual and cognitive-evaluative forms of empathy might be characterized by different activity patterns, the neural activations in these forms of empathy were compared. The dorsal aMCC was demonstrated to be recruited more frequently in the cognitive-evaluative form of empathy, whilst the right anterior insula was found to be involved in the affective-perceptual form of empathy only. The left anterior insula was active in both forms of empathy. It was concluded that the dACC-aMCC-SMA and bilateral insula can be considered as forming a core network in empathy, and that cognitive-evaluative and affective-perceptual empathy can be distinguished at the level of regional activation. Copyright © 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                25 September 2018
                2018
                : 9
                : 572
                Affiliations
                MOE Key Laboratory for Neuroinformation, Clinical Hospital of Chengdu Brain Science Institute, University of Electronic Science and Technology of China , Chengdu, China
                Author notes

                Edited by: James A. Carr, Texas Tech University, United States

                Reviewed by: Ben Nephew, Worcester Polytechnic Institute, United States; Aldo Lucion, Universidade Federal do Rio Grande do Sul (UFRGS), Brazil

                *Correspondence: Benjamin Becker ben_becker@ 123456gmx.de

                This article was submitted to Neuroendocrine Science, a section of the journal Frontiers in Endocrinology

                Article
                10.3389/fendo.2018.00572
                6190868
                ba289ca8-a83b-45cf-b227-aeb4a4e1d4b5
                Copyright © 2018 Geng, Zhao, Zhou, Ma, Yao, Becker and Kendrick.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 12 June 2018
                : 06 September 2018
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 72, Pages: 10, Words: 7850
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31530032
                Award ID: 91632117
                Categories
                Endocrinology
                Original Research

                Endocrinology & Diabetes
                oxytocin,empathy,embarrassment,anxiety,insula,amygdala,prefrontal cortex,sex differences

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