Neural pathways of embarrassment and their modulation by social anxiety

While being in the center of attention and exposed to other's evaluations humans are prone to experience embarrassment. To characterize the neural underpinnings of such aversive moments, we induced genuine experiences of embarrassment during person-group interactions in a functional neuroimaging study. Using a mock-up scenario with three confederates, we examined how the presence of an audience affected physiological and neural responses and the reported emotional experiences of failures and achievements. The results indicated that publicity induced activations in mentalizing areas and failures led to activations in arousal processing systems. Mentalizing activity as well as attention towards the audience were increased in socially anxious participants. The converging integration of information from mentalizing areas and arousal processing systems within the ventral anterior insula and amygdala forms the neural pathways of embarrassment. Targeting these neural markers of embarrassment in the (para-)limbic system provides new perspectives for developing treatment strategies for social anxiety disorders.

[1]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[2]  Clayton R. Critcher,et al.  Inferring Attitudes From Mindwandering , 2010, Personality & social psychology bulletin.

[3]  B. Weiner An attributional theory of achievement motivation and emotion. , 1985, Psychological review.

[4]  J. Lorberbaum,et al.  Neural correlates of speech anticipatory anxiety in generalized social phobia , 2004, Neuroreport.

[5]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[6]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[7]  Robin M. Kowalski,et al.  Impression management: A literature review and two-component model. , 1990 .

[8]  Rowland S. Miller Embarrassment: Poise and Peril in Everyday Life , 1996 .

[9]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[10]  D. Pine,et al.  Atypical modulation of medial prefrontal cortex to self-referential comments in generalized social phobia , 2011, Psychiatry Research: Neuroimaging.

[11]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[12]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[13]  C. Keysers,et al.  Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex , 2011, Human brain mapping.

[14]  Krishan Kumar,et al.  Public and private in thought and practice : perspectives on a grand dichotomy , 1998 .

[15]  K. Vogeley,et al.  Toward a second-person neuroscience 1 , 2013, Behavioral and Brain Sciences.

[16]  M. Irwin,et al.  Greater amygdala activity and dorsomedial prefrontal–amygdala coupling are associated with enhanced inflammatory responses to stress , 2015, Brain, Behavior, and Immunity.

[17]  F. Paulus,et al.  On the distinction of empathic and vicarious emotions , 2013, Front. Hum. Neurosci..

[18]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[19]  M. Bradley,et al.  The pupil as a measure of emotional arousal and autonomic activation. , 2008, Psychophysiology.

[20]  J. Smallwood,et al.  The restless mind. , 2006, Psychological bulletin.

[21]  Derek G. V. Mitchell,et al.  Caught in the act: The impact of audience on the neural response to morally and socially inappropriate behavior , 2006, NeuroImage.

[22]  R. Mattick,et al.  Development and validation of measures of social phobia scrutiny fear and social interaction anxiety. , 1998, Behaviour research and therapy.

[23]  S. Garrod,et al.  Brain-to-brain coupling: a mechanism for creating and sharing a social world , 2012, Trends in Cognitive Sciences.

[24]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[25]  T. Heatherton,et al.  Anterior cingulate cortex responds differentially to expectancy violation and social rejection , 2006, Nature Neuroscience.

[26]  J. Rubenfeld The Right of Privacy , 1989 .

[27]  F. Paulus,et al.  Mentalizing and the Role of the Posterior Superior Temporal Sulcus in Sharing Others' Embarrassment. , 2015, Cerebral cortex.

[28]  D. Stipek,et al.  A developmental analysis of elementary school-aged children's concepts of pride and embarrassment. , 1988, Child development.

[29]  J. Tangney,et al.  Moral emotions and moral behavior. , 2007, Annual review of psychology.

[30]  Herbert W. Marsh,et al.  A multidimensional, hierarchical model of self-concept: Theoretical and empirical justification , 1990 .

[31]  G. Rizzolatti,et al.  Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys , 2009, Science.

[32]  Richard Sennett,et al.  The Fall of Public Man , 1977 .

[33]  Jeffrey C. Cooper,et al.  The role of the posterior temporal and medial prefrontal cortices in mediating learning from romantic interest and rejection. , 2014, Cerebral cortex.

[34]  F. Paulus,et al.  When your friends make you cringe: social closeness modulates vicarious embarrassment-related neural activity. , 2016, Social cognitive and affective neuroscience.

[35]  Olga V. Demler,et al.  Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[36]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[37]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[38]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[39]  F. Paulus,et al.  Advancing the neuroscience of social emotions with social immersion , 2013, Behavioral and Brain Sciences.

[40]  Martin A. Lindquist,et al.  Brain mediators of cardiovascular responses to social threat Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity , 2009, NeuroImage.

[41]  T. Gilovich,et al.  The spotlight effect in social judgment: an egocentric bias in estimates of the salience of one's own actions and appearance. , 2000, Journal of personality and social psychology.

[42]  C. Mirabel-Sarron [Social anxiety]. , 2010, La Revue du praticien.

[43]  E. Leibenluft,et al.  The pathology of social phobia is independent of developmental changes in face processing. , 2011, The American journal of psychiatry.

[44]  R. Heimberg,et al.  Social anxiety and social anxiety disorder. , 2013, Annual review of clinical psychology.

[45]  A. Bandura Self-efficacy mechanism in human agency , 2024, Psihologìâ ì suspìlʹstvo.

[46]  M. Weissman,et al.  Social Phobia: Comorbidity and Morbidity in an Epidemiologic Sample , 1992 .

[47]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[48]  G. Rizzolatti,et al.  View-Based Encoding of Actions in Mirror Neurons of Area F5 in Macaque Premotor Cortex , 2011, Current Biology.

[49]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[50]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

[51]  Larry Ambrose,et al.  The power of feedback. , 2002, Healthcare executive.

[52]  A. Buss Self-consciousness and social anxiety , 1980 .

[53]  Erin B. McClure-Tone,et al.  Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. , 2008, Archives of general psychiatry.

[54]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[55]  Tilo Kircher,et al.  Your Flaws Are My Pain: Linking Empathy To Vicarious Embarrassment , 2011, PloS one.

[56]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  Erik D. Reichle,et al.  Meta-awareness, perceptual decoupling and the wandering mind , 2011, Trends in Cognitive Sciences.

[58]  W. Einhäuser,et al.  Fronto-insula network activity explains emotional dysfunctions in juvenile myoclonic epilepsy: Combined evidence from pupillometry and fMRI , 2015, Cortex.