Adolescents’ risky decision-making activates neural networks related to social cognition and cognitive control processes

This study examines by means of functional magnetic resonance imaging the neural mechanisms underlying adolescents’ risk decision-making in social contexts. We hypothesize that the social context could engage brain regions associated with social cognition processes and developmental changes are also expected. Sixty participants (adolescents: 17–18, and young adults: 21–22 years old) read narratives describing typical situations of decision-making in the presence of peers. They were asked to make choices in risky situations (e.g., taking or refusing a drug) or ambiguous situations (e.g., eating a hamburger or a hotdog). Risky as compared to ambiguous scenarios activated bilateral temporoparietal junction (TPJ), bilateral middle temporal gyrus (MTG), right medial prefrontal cortex, and the precuneus bilaterally; i.e., brain regions related to social cognition processes, such as self-reflection and theory of mind (ToM). In addition, brain structures related to cognitive control were active [right anterior cingulate cortex (ACC), bilateral dorsolateral prefrontal cortex (DLPFC), bilateral orbitofrontal cortex], whereas no significant clusters were obtained in the reward system (ventral striatum). Choosing the dangerous option involved a further activation of control areas (ACC) and emotional and social cognition areas (temporal pole). Adolescents employed more neural resources than young adults in the right DLPFC and the right TPJ in risk situations. When choosing the dangerous option, young adults showed a further engagement in ToM related regions (bilateral MTG) and in motor control regions related to the planning of actions (pre-supplementary motor area). Finally, the right insula and the right superior temporal gyrus were more activated in women than in men, suggesting more emotional involvement and more intensive modeling of the others’ perspective in the risky conditions. These findings call for more comprehensive developmental accounts of decision-making in social contexts that incorporate the role of emotional and social cognition processes.

[1]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[2]  A. Aleman,et al.  Self-reflection and the brain: A theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia , 2010, Neuroscience & Biobehavioral Reviews.

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

[4]  W. Güth,et al.  An experimental analysis of ultimatum bargaining , 1982 .

[5]  G. Glover,et al.  Risk-taking and the adolescent brain: who is at risk? , 2007, Developmental science.

[6]  Sarah-Jayne Blakemore,et al.  Imaging brain development: The adolescent brain , 2012, NeuroImage.

[7]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  E. A. Berg,et al.  A simple objective technique for measuring flexibility in thinking. , 1948, The Journal of general psychology.

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

[10]  J. Rilling,et al.  The neuroscience of social decision-making. , 2011, Annual review of psychology.

[11]  T. Braver,et al.  Anterior Cingulate and the Monitoring of Response Conflict: Evidence from an fMRI Study of Overt Verb Generation , 2000, Journal of Cognitive Neuroscience.

[12]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[13]  W. Krieg.  Functional Neuroanatomy , 1953, Springer Series in Experimental Entomology.

[14]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[15]  Evelyn C. Ferstl,et al.  The extended language network: A meta‐analysis of neuroimaging studies on text comprehension , 2008, Human brain mapping.

[16]  Michael P. Milham,et al.  Distinct neural mechanisms of risk and ambiguity: A meta-analysis of decision-making , 2006, NeuroImage.

[17]  Nelson Cowan,et al.  The development of working memory , 1997 .

[18]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[19]  R. Saxe,et al.  What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind , 2010, Neuropsychologia.

[20]  Geoffrey Bird,et al.  Development during Adolescence of the Neural Processing of Social Emotion , 2009, Journal of Cognitive Neuroscience.

[21]  P. Glimcher,et al.  Title: the Neural Representation of Subjective Value under Risk and Ambiguity 1 2 , 2009 .

[22]  Iroise Dumontheil,et al.  Developmental influences on the neural bases of responses to social rejection: Implications of social neuroscience for education , 2011, NeuroImage.

[23]  P. Montague.  Neuroeconomics: a view from neuroscience. , 2007, Functional neurology.

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

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

[26]  A. Sanfey.  Social Decision-Making : Insights from Game Theory and Neuroscience , 2022 .

[27]  T. Robbins,et al.  Decision-making in the adolescent brain , 2012, Nature Neuroscience.

[28]  L. Steinberg.  Risk Taking in Adolescence: What Changes, and Why? , 2004, Annals of the New York Academy of Sciences.

[29]  L. Johnston.  It's the thought that counts-- , 1994 .

[30]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[31]  Amishi P. Jha,et al.  Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain , 2005, NeuroImage.

[32]  Evelyn C. Ferstl,et al.  Time, space and emotion: fMRI reveals content-specific activation during text comprehension , 2007, Neuroscience Letters.

[33]  Serge A. R. B. Rombouts,et al.  Social exclusion and punishment of excluders: Neural correlates and developmental trajectories , 2012, NeuroImage.

[34]  S. Carey,et al.  Understanding other minds: linking developmental psychology and functional neuroimaging. , 2004, Annual review of psychology.

[35]  Carlo Contoreggi,et al.  Risky decision making and the anterior cingulate cortex in abstinent drug abusers and nonusers. , 2005, Brain research. Cognitive brain research.

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

[37]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

[38]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[39]  D. A. Grant,et al.  A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. , 1948, Journal of experimental psychology.

[40]  J L Collins,et al.  Youth Risk Behavior Surveillance--United States, 1997. State and Local YRBSS Coordinators. , 1998, The Journal of school health.

[41]  Ingrid R. Olson,et al.  Social cognition and the anterior temporal lobes , 2010, NeuroImage.

[42]  Susan Whitfield-Gabrieli,et al.  Brain regions for perceiving and reasoning about other people in school-aged children. , 2009, Child development.

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

[44]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[45]  Carrie L. Masten,et al.  Neural correlates of direct and reflected self-appraisals in adolescents and adults: when social perspective-taking informs self-perception. , 2009, Child development.

[46]  Riitta Hari,et al.  The compassionate brain: humans detect intensity of pain from another's face. , 2006, Cerebral cortex.

[47]  R. Mar.  The neural bases of social cognition and story comprehension. , 2011, Annual review of psychology.

[48]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[49]  Kathrin Cohen Kadosh,et al.  The social brain in adolescence: Evidence from functional magnetic resonance imaging and behavioural studies , 2011, Neuroscience & Biobehavioral Reviews.

[50]  Connie Lim,et al.  Youth risk behavior surveillance--United States, 2007. , 2008, Morbidity and mortality weekly report. Surveillance summaries.

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

[52]  Leah H. Somerville,et al.  A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues , 2010, Brain and Cognition.

[53]  L. Fellows,et al.  Dorsal Medial Prefrontal Cortex Plays a Necessary Role in Rapid Error Prediction in Humans , 2008, The Journal of Neuroscience.

[54]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[55]  M. Ernst,et al.  Neurobiology of the development of motivated behaviors in adolescence: A window into a neural systems model , 2009, Pharmacology Biochemistry and Behavior.

[56]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[57]  Graham Hitch,et al.  The Development of Working Memory , 1992 .

[58]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[59]  Serge A R B Rombouts,et al.  Changing Brains, Changing Perspectives , 2011, Psychological science.

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

[61]  Joshua W. Brown,et al.  A computational model of risk, conflict, and individual difference effects in the anterior cingulate cortex , 2008, Brain Research.

[62]  L. Steinberg.  A dual systems model of adolescent risk-taking. , 2010, Developmental psychobiology.

[63]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[64]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[65]  H. Damasio,et al.  The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers , 2005, Trends in Cognitive Sciences.

[66]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[67]  L. Siegel,et al.  The development of working memory in normally achieving and subtypes of learning disabled children. , 1989, Child development.

[68]  Serge A. R. B. Rombouts,et al.  Adolescent risky decision-making: Neurocognitive development of reward and control regions , 2010, NeuroImage.

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

[70]  T. Robbins,et al.  Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making , 2008, Brain : a journal of neurology.

[71]  L. Somerville,et al.  Braking and Accelerating of the Adolescent Brain. , 2011, Journal of research on adolescence : the official journal of the Society for Research on Adolescence.

[72]  E. Crone,et al.  Brain Regions Mediating Flexible Rule Use during Development , 2006, The Journal of Neuroscience.

[73]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[74]  Lorena R. R. Gianotti,et al.  Disruption of Right Prefrontal Cortex by Low-Frequency Repetitive Transcranial Magnetic Stimulation Induces Risk-Taking Behavior , 2006, The Journal of Neuroscience.

[75]  B. Luna,et al.  What has fMRI told us about the Development of Cognitive Control through Adolescence? , 2010, Brain and Cognition.

[76]  M. Banich,et al.  Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model. , 2008, Developmental psychology.

[77]  E. Halgren,et al.  Responses of Human Anterior Cingulate Cortex Microdomains to Error Detection, Conflict Monitoring, Stimulus-Response Mapping, Familiarity, and Orienting , 2005, The Journal of Neuroscience.

[78]  Hidenao Fukuyama,et al.  Pre-SMA actively engages in conflict processing in human: A combined study of epicortical ERPs and direct cortical stimulation , 2013, Neuropsychologia.

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

[80]  G. Glover,et al.  Earlier Development of the Accumbens Relative to Orbitofrontal Cortex Might Underlie Risk-Taking Behavior in Adolescents , 2006, The Journal of Neuroscience.

[81]  Laurence Steinberg,et al.  Peer influence on risk taking, risk preference, and risky decision making in adolescence and adulthood: an experimental study. , 2005, Developmental psychology.

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

[83]  Cara L. Wong,et al.  The function of the anterior temporal lobe: A review of the empirical evidence , 2012, Brain Research.