Neural responses to exclusion predict susceptibility to social influence.

PURPOSE Social influence is prominent across the lifespan, but sensitivity to influence is especially high during adolescence and is often associated with increased risk taking. Such risk taking can have dire consequences. For example, in American adolescents, traffic-related crashes are leading causes of nonfatal injury and death. Neural measures may be especially useful in understanding the basic mechanisms of adolescents' vulnerability to peer influence. METHODS We examined neural responses to social exclusion as potential predictors of risk taking in the presence of peers in recently licensed adolescent drivers. Risk taking was assessed in a driving simulator session occurring approximately 1 week after the neuroimaging session. RESULTS Increased activity in neural systems associated with the distress of social exclusion and mentalizing during an exclusion episode predicted increased risk taking in the presence of a peer (controlling for solo risk behavior) during a driving simulator session outside the neuroimaging laboratory 1 week later. These neural measures predicted risky driving behavior above and beyond self-reports of susceptibility to peer pressure and distress during exclusion. CONCLUSIONS These results address the neural bases of social influence and risk taking; contribute to our understanding of social and emotional function in the adolescent brain; and link neural activity in specific, hypothesized, regions to risk-relevant outcomes beyond the neuroimaging laboratory. Results of this investigation are discussed in terms of the mechanisms underlying risk taking in adolescents and the public health implications for adolescent driving.

[1]  Thomas A. Dingus,et al.  Peer influence predicts speeding prevalence among teenage drivers. , 2012, Journal of safety research.

[2]  M. Leary,et al.  Self-esteem as an interpersonal monitor: The sociometer hypothesis. , 1995 .

[3]  John D. Lee,et al.  Handbook of Driving Simulation for Engineering, Medicine and Psychology: An Overview , 2011 .

[4]  Sarah-Jayne Blakemore,et al.  Development of the social brain in adolescence , 2012, Journal of the Royal Society of Medicine.

[5]  L. Hawkley,et al.  Loneliness and Health: Potential Mechanisms , 2002, Psychosomatic medicine.

[6]  M. Lieberman.  Social Cognitive Neuroscience , 2010 .

[7]  Allan F Williams,et al.  Teenage drivers: patterns of risk. , 2003, Journal of safety research.

[8]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[9]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  Daniel Romer,et al.  Adolescent risk taking, impulsivity, and brain development: implications for prevention. , 2010, Developmental psychobiology.

[11]  R. Dantzer.  The Psychology of Fear and Stress, J.A. Gray (Ed.). Cambridge University Press, Cambridge (1987), viii and 422 pp, ISBN 0-521-27098-7 , 1989 .

[12]  James D. Larson,et al.  Peer relationships in adolescence. , 2009 .

[13]  Allan F Williams,et al.  Characteristics of teens-with-teens fatal crashes in the United States, 2005-2010. , 2014, Journal of safety research.

[14]  A. Pradhan,et al.  Experimental effects of injunctive norms on simulated risky driving among teenage males. , 2014, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[15]  K. Berridge.  From prediction error to incentive salience: mesolimbic computation of reward motivation , 2012, The European journal of neuroscience.

[16]  Bruce Simons-Morton,et al.  The observed effects of teenage passengers on the risky driving behavior of teenage drivers. , 2005, Accident; analysis and prevention.

[17]  Gary G Berntson,et al.  Loneliness in everyday life: cardiovascular activity, psychosocial context, and health behaviors. , 2003, Journal of personality and social psychology.

[18]  L. Steinberg,et al.  Handbook of adolescent psychology , 2009 .

[19]  Thomas E. Nichols,et al.  Handbook of Functional MRI Data Analysis: Index , 2011 .

[20]  B. Skinner.  Operant Behavior , 2021, Encyclopedia of Evolutionary Psychological Science.

[21]  R. Saxe,et al.  Making sense of another mind: The role of the right temporo-parietal junction , 2005, Neuropsychologia.

[22]  J. Allen,et al.  The two faces of adolescents' success with peers: adolescent popularity, social adaptation, and deviant behavior. , 2005, Child development.

[23]  N. Eisenberger.  The Neural Bases of Social Pain: Evidence for Shared Representations With Physical Pain , 2012, Psychosomatic medicine.

[24]  T. Dingus,et al.  Crash and risky driving involvement among novice adolescent drivers and their parents. , 2011, American journal of public health.

[25]  Thomas E. Nichols,et al.  Comprar Handbook Of Functional Mri Data Analysis | R. Poldrack | 9780521517669 | Cambridge University Press , 2011 .

[26]  R. Folmer.  rTMS for Tinnitus , 2012, Front. Hum. Neurosci..

[27]  Ethan Kross,et al.  Social rejection shares somatosensory representations with physical pain , 2011, Proceedings of the National Academy of Sciences.

[28]  L. Steinberg.  A Social Neuroscience Perspective on Adolescent Risk-Taking. , 2008, Developmental review : DR.

[29]  G. Loewenstein,et al.  Neural Predictors of Purchases , 2007, Neuron.

[30]  D. de Waard,et al.  Handbook of driving simulation for engineering, medicine and psychology , 2011 .

[31]  Matthew D. Lieberman,et al.  Identifying the What, Why, and How of an Observed Action: An fMRI Study of Mentalizing and Mechanizing during Action Observation , 2011, Journal of Cognitive Neuroscience.

[32]  K. Williams,et al.  When inclusion costs and ostracism pays, ostracism still hurts. , 2006, Journal of personality and social psychology.

[33]  J. Panksepp,et al.  The biology of social attachments: opiates alleviate separation distress. , 1978, Biological psychiatry.

[34]  J. Gerris,et al.  Developmental analysis of social cognitive and behavioral differences between popular and rejected children , 1994 .

[35]  J. Gray,et al.  Brain systems that mediate both emotion and cognition. , 1990 .

[36]  L. Somerville.  The Teenage Brain , 2013 .

[37]  E. Crone,et al.  Understanding adolescence as a period of social–affective engagement and goal flexibility , 2012, Nature Reviews Neuroscience.

[38]  J. Cacioppo,et al.  Beyond Bipolar Conceptualizations and Measures: The Case of Attitudes and Evaluative Space , 1997, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[39]  L. Hawkley,et al.  Loneliness predicts increased blood pressure: 5-year cross-lagged analyses in middle-aged and older adults. , 2010, Psychology and aging.

[40]  L. Steinberg,et al.  Adolescent Development , 2001, Journal of Cognitive Education and Psychology.

[41]  Jeff K. Caird,et al.  Twelve Practical and Useful Questions about Driving Simulation , 2011 .

[42]  Judith Lynne Charlton,et al.  Simulator Validity: Behaviors Observed on the Simulator and on the Road , 2011 .

[43]  G. Fernández,et al.  Reinforcement Learning Signal Predicts Social Conformity , 2009, Neuron.

[44]  Noah J. Goldstein,et al.  Social influence: compliance and conformity. , 2004, Annual review of psychology.

[45]  A. Cillessen,et al.  Peer rejection and HPA activity in middle childhood: friendship makes a difference. , 2011, Child development.

[46]  L. Steinberg,et al.  Age differences in resistance to peer influence. , 2007, Developmental psychology.

[47]  Jennifer H. Pfeifer,et al.  Adolescent social cognitive and affective neuroscience: past, present, and future. , 2012, Social cognitive and affective neuroscience.

[48]  M. Leary,et al.  Calibrating the sociometer: the relationship between interpersonal appraisals and state self-esteem. , 1998, Journal of personality and social psychology.

[49]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[50]  Sarah-Jayne Blakemore,et al.  Social brain development and the affective consequences of ostracism in adolescence , 2010, Brain and Cognition.

[51]  Joseph P. Forgas,et al.  The Social Outcast : Ostracism, Social Exclusion, Rejection, and Bullying , 2005 .

[52]  S. Fiske,et al.  The Handbook of Social Psychology , 1935 .

[53]  A. Galván,et al.  Peer influence in involuntary social groups: Lessons from research on bullying. , 2008 .

[54]  W. Gardner,et al.  The Social Monitoring System: Enhanced Sensitivity to Social Cues as an Adaptive Response to Social Exclusion. , 2005 .

[55]  Sarah-Jayne Blakemore,et al.  Is adolescence a sensitive period for sociocultural processing? , 2014, Annual review of psychology.

[56]  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.

[57]  S. Blakemore.  The social brain in adolescence , 2008, Nature Reviews Neuroscience.

[58]  Eva H. Telzer,et al.  Time spent with friends in adolescence relates to less neural sensitivity to later peer rejection. , 2012, Social cognitive and affective neuroscience.

[59]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[60]  Emily B. Falk,et al.  An imaging genetics approach to understanding social influence , 2012, Front. Hum. Neurosci..

[61]  Monica Hoyos Flight.  Axon guidance: A developmental switch , 2010, Nature Reviews Neuroscience.

[62]  Elliot T. Berkman,et al.  Beyond Brain Mapping , 2013, Current directions in psychological science.

[63]  R. Davidson,et al.  Anterior brain electrical asymmetries in response to reward and punishment. , 1992, Electroencephalography and clinical neurophysiology.

[64]  Carrie L. Masten,et al.  Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. , 2009, Social cognitive and affective neuroscience.

[65]  Ronald E. Dahl,et al.  Pubertal development and behavior: Hormonal activation of social and motivational tendencies , 2010, Brain and Cognition.

[66]  Gregory S. Berns,et al.  Neural mechanisms of the influence of popularity on adolescent ratings of music , 2010, NeuroImage.

[67]  E. Leibenluft,et al.  The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology , 2005, Psychological Medicine.

[68]  Adriana Galvan,et al.  The adolescent brain. , 2008, Developmental review : DR.

[69]  Nicholas B. Allen,et al.  Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders , 2012, Trends in Cognitive Sciences.

[70]  Brian Knutson,et al.  Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation , 2006, Neuron.

[71]  T. E. Dielman,et al.  Susceptibility to Peer Pressure, Self-Esteem, and Health Locus of Control as Correlates of Adolescent Substance Abuse , 1987, Health education quarterly.

[72]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

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

[74]  Jing Wang,et al.  Using the U.S. National Household Travel Survey to estimate the impact of passenger characteristics on young drivers' relative risk of fatal crash involvement. , 2010, Accident; analysis and prevention.

[75]  L. Steinberg,et al.  Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. , 2011, Developmental science.

[76]  William E. Moore,et al.  Risk-taking and social exclusion in adolescence: Neural mechanisms underlying peer influences on decision-making , 2013, NeuroImage.