Decreased ventral anterior cingulate cortex activity is associated with reduced social pain during emotional support

Abstract People feel psychological pain when they are excluded, and this pain is often attenuated when emotional support is received. It is therefore likely that a specific neural mechanism underlies the detection of social exclusion. Similarly, specific neural mechanisms may underlie the beneficial effects of emotional support. Although neuroimaging researchers have recently examined the neural basis of social pain, there is presently no agreement as to which part of the anterior cingulate cortex (ACC) is involved in the perception and modulation of social pain. We hypothesized that activity in those brain regions that are associated with social pain would be correlated with decrements in social pain induced by emotional support. To examine the effects of emotional support on social pain caused by exclusion, we conducted an fMRI study in which participants played a virtual ball-tossing game. Participants were initially included and later excluded from the game. In the latter half of the session from which participants were excluded, participants received emotionally supportive text messages. We found that emotional support led to increased activity in the left lateral/medial prefrontal cortices and some temporal regions. Those individuals who experienced greater attenuation of social pain exhibited lower ventral ACC and higher left lateral prefrontal cortex activation. These results suggest that the ventral ACC underlies social pain, and that emotional support enhances prefrontal cortex activity, which in turn may lead to a weakened affective response.

[1]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[2]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[3]  Niall Bolger,et al.  Effects of social support visibility on adjustment to stress: experimental evidence. , 2007, Journal of personality and social psychology.

[4]  Takashi Hanakawa,et al.  The neural basis of social tactics: An fMRI study , 2006, NeuroImage.

[5]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[6]  M. Leary,et al.  Hurt feelings: The neglected emotion. , 2001 .

[7]  Hubert Preissl,et al.  Influence of social support and emotional context on pain processing and magnetic brain responses in fibromyalgia. , 2004, Arthritis and rheumatism.

[8]  Matthew D. Lieberman,et al.  Neural pathways link social support to attenuated neuroendocrine stress responses , 2007, NeuroImage.

[9]  Marie T Banich,et al.  Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function. , 2007, Psychophysiology.

[10]  T. J. Berndt,et al.  Children's Perceptions of Friendships as Supportive Relationships. , 1986 .

[11]  K. Williams,et al.  Cyberostracism: effects of being ignored over the Internet. , 2000, Journal of personality and social psychology.

[12]  James K Rilling,et al.  The neural correlates of theory of mind within interpersonal interactions , 2004, NeuroImage.

[13]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[14]  M. Leary,et al.  Why does social exclusion hurt? The relationship between social and physical pain. , 2005, Psychological bulletin.

[15]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[16]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[17]  Matthew D. Lieberman,et al.  Why rejection hurts: a common neural alarm system for physical and social pain , 2004, Trends in Cognitive Sciences.

[18]  J. Gross,et al.  Emotional suppression: physiology, self-report, and expressive behavior. , 1993, Journal of personality and social psychology.

[19]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[20]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[21]  Christopher D. Frith,et al.  Imaging the Intentional Stance in a Competitive Game , 2002, NeuroImage.

[22]  R. Baumeister,et al.  Does Social Exclusion Motivate Interpersonal Reconnection ? Resolving the “ Porcupine Problem ” , 2006 .

[23]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[24]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[25]  T. Wills,et al.  Stress, social support, and the buffering hypothesis. , 1985, Psychological bulletin.

[26]  R. Thornhill,et al.  The evolution of psychological pain. , 1989 .

[27]  J. Desmond,et al.  Hemispheric asymmetry for emotional stimuli detected with fMRI , 1998, Neuroreport.

[28]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[29]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[30]  A. Meltzoff,et al.  Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain , 2006, Neuropsychologia.

[31]  R. Lazarus,et al.  SHORT-CIRCUITING OF THREAT BY EXPERIMENTALLY ALTERING COGNITIVE APPRAISAL. , 1964, Journal of abnormal psychology.

[32]  J. Gross Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. , 1998, Journal of personality and social psychology.

[33]  Rick Richardson,et al.  How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence , 2004 .

[34]  R. Kessler,et al.  Invisible support and adjustment to stress. , 2000, Journal of personality and social psychology.

[35]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[36]  Claus Lamm,et al.  The Neural Substrate of Human Empathy: Effects of Perspective-taking and Cognitive Appraisal , 2007, Journal of Cognitive Neuroscience.

[37]  J. Decety,et al.  To what extent do we share the pain of others? Insight from the neural bases of pain empathy , 2006, Pain.

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

[39]  Richard J. Davidson,et al.  PSYCHOLOGICAL SCIENCE Research Article Lending a Hand Social Regulation of the Neural Response to Threat , 2022 .

[40]  M. Leary,et al.  Social Support and Experimental Pain , 2003, Psychosomatic medicine.

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

[42]  V. Helgeson,et al.  Two Important Distinctions in Social Support: Kind of Support and Perceived Versus Received1 , 1993 .

[43]  Daniel Houser,et al.  A functional imaging study of cooperation in two-person reciprocal exchange , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Luke J. Chang,et al.  Sex specificity of ventral anterior cingulate cortex suppression during a cognitive task , 2007, Human brain mapping.