Connecting brain responsivity and real-world risk taking: Strengths and limitations of current methodological approaches

In line with the goal of limiting health risk behaviors in adolescence, a growing literature investigates whether individual differences in functional brain responses can be related to vulnerability to engage in risky decision-making. We review this body of work, investigate when and in what way findings converge, and provide best practice recommendations. We identified 23 studies that examined individual differences in brain responsivity and adolescent risk taking. Findings varied widely in terms of the neural regions identified as relating to risky behavior. This heterogeneity is likely due to the abundance of approaches used to assess risk taking, and to the disparity of fMRI tasks. Indeed, brain-behavior correlations were typically found in regions showing a main effect of task. However, results from a test of publication bias suggested that region of interest approaches lacked evidential value. The findings suggest that neural factors differentiating riskier teens are not localized to a single region. Therefore, approaches that utilize data from the entire brain, particularly in predictive analyses, may yield more reliable and applicable results. We discuss several decision points that researchers should consider when designing a study, and emphasize the importance of precise research questions that move beyond a general desire to address adolescent risk taking.

[1]  M. J. Meloy,et al.  Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. , 2004, Alcoholism, clinical and experimental research.

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

[3]  A. Banks Puberty* , 1958, Encyclopedia of Evolutionary Psychological Science.

[4]  Eva H. Telzer,et al.  The quality of adolescents' peer relationships modulates neural sensitivity to risk taking. , 2015, Social cognitive and affective neuroscience.

[5]  K. Fromme,et al.  Effects of Outcome Expectancies and Personality on Young Adults' Illicit Drug Use, Heavy Drinking, and Risky Sexual Behavior , 2000, Cognitive Therapy and Research.

[6]  Jillian E. Hardee,et al.  Neuroimaging Risk Markers for Substance Abuse: Recent Findings on Inhibitory Control and Reward System Functioning , 2015, Current Addiction Reports.

[7]  Adriana Galván,et al.  Meaningful Family Relationships: Neurocognitive Buffers of Adolescent Risk Taking , 2013, Journal of Cognitive Neuroscience.

[8]  B. Casey,et al.  Adolescence: What Do Transmission, Transition, and Translation Have to Do with It? , 2010, Neuron.

[9]  Matcheri S Keshavan,et al.  Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. , 2005, Alcoholism, clinical and experimental research.

[10]  L. Steinberg,et al.  Connecting Brain Responsivity and Real-World Risk taking: Strengths and Limitations of Current Methodological Approaches , 2017, bioRxiv.

[11]  Martin P Paulus,et al.  Neural activation during inhibition predicts initiation of substance use in adolescence. , 2011, Drug and alcohol dependence.

[12]  Adriana Galván,et al.  Beyond simple models of adolescence to an integrated circuit-based account: A commentary , 2015, Developmental Cognitive Neuroscience.

[13]  Jennifer H. Pfeifer,et al.  Learning to Play It Safe (or Not): Stable and Evolving Neural Responses during Adolescent Risky Decision-making , 2015, Journal of Cognitive Neuroscience.

[14]  N. Volkow,et al.  Neurocircuitry of Addiction , 2010, Neuropsychopharmacology.

[15]  Brian Knutson,et al.  Incentive-elicited Striatal Activation in Adolescent Children of Alcoholics , 2022 .

[16]  L. Wilbrecht,et al.  Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry , 2016, Psychoneuroendocrinology.

[17]  Mareike M. Menz,et al.  Lower ventral striatal activation during reward anticipation in adolescent smokers. , 2011, The American journal of psychiatry.

[18]  J. Block,et al.  Adolescent drug use and psychological health. A longitudinal inquiry. , 1990, The American psychologist.

[19]  David J. Paulsen,et al.  Neurocognitive Development of Risk Aversion from Early Childhood to Adulthood , 2012, Front. Hum. Neurosci..

[20]  Will M Aklin,et al.  Evaluation of behavioral measures of risk taking propensity with inner city adolescents. , 2005, Behaviour research and therapy.

[21]  Eva H. Telzer,et al.  Buffering effect of positive parent–child relationships on adolescent risk taking: A longitudinal neuroimaging investigation , 2015, Developmental Cognitive Neuroscience.

[22]  Eva H. Telzer,et al.  Neural mechanisms of impulse control in sexually risky adolescents , 2013, Developmental Cognitive Neuroscience.

[23]  Stephan F. Miedl,et al.  Risk taking and the adolescent reward system: a potential common link to substance abuse. , 2012, The American journal of psychiatry.

[24]  M. Paulus,et al.  Neural Predictors of Initiating Alcohol Use During Adolescence. , 2017, The American journal of psychiatry.

[25]  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.

[26]  B. Leigh Alcohol and Condom Use: A Meta-Analysis of Event-Level Studies , 2002, Sexually transmitted diseases.

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

[28]  C. Raymond Bingham,et al.  Buffering Social Influence: Neural Correlates of Response Inhibition Predict Driving Safety in the Presence of a Peer , 2015, Journal of Cognitive Neuroscience.

[29]  Carrie L. Masten,et al.  Entering Adolescence: Resistance to Peer Influence, Risky Behavior, and Neural Changes in Emotion Reactivity , 2011, Neuron.

[30]  J. Hittner,et al.  Sensation seeking and alcohol use: a meta-analytic review. , 2006, Addictive behaviors.

[31]  Leif D. Nelson,et al.  p-Curve and Effect Size , 2014, Perspectives on psychological science : a journal of the Association for Psychological Science.

[32]  M. Rietschel,et al.  Neuropsychosocial profiles of current and future adolescent alcohol misusers , 2014, Nature.

[33]  M. V. van Aken,et al.  A meta-analysis on age differences in risky decision making: adolescents versus children and adults. , 2015, Psychological bulletin.

[34]  Joanna Jacobus,et al.  Altered white matter integrity in adolescent binge drinkers. , 2009, Alcoholism, clinical and experimental research.

[35]  T. Yarkoni Big Correlations in Little Studies: Inflated fMRI Correlations Reflect Low Statistical Power—Commentary on Vul et al. (2009) , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[36]  Eveline A. Crone,et al.  Structural brain development between childhood and adulthood: Convergence across four longitudinal samples , 2016, NeuroImage.

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

[38]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[39]  Leif D. Nelson,et al.  P-Curve: A Key to the File Drawer , 2013, Journal of experimental psychology. General.

[40]  Thomas J. H. Chen,et al.  The Reward Deficiency Syndrome: A Biogenetic Model for the Diagnosis and Treatment of Impulsive, Addictive and Compulsive Behaviors , 2000, Journal of psychoactive drugs.

[41]  L. Squeglia,et al.  Adolescence and drug use vulnerability: findings from neuroimaging , 2017, Current Opinion in Behavioral Sciences.

[42]  Adriana Galván,et al.  At risk of being risky: The relationship between “brain age” under emotional states and risk preference , 2017, Developmental Cognitive Neuroscience.

[43]  Sabine Peters,et al.  The link between testosterone and amygdala–orbitofrontal cortex connectivity in adolescent alcohol use , 2015, Psychoneuroendocrinology.

[44]  Carolyn R. Fallahi,et al.  Functional magnetic resonance imaging (fMRI) response to alcohol pictures predicts subsequent transition to heavy drinking in college students. , 2014, Addiction.

[45]  N. Volkow,et al.  Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers , 1993, Synapse.

[46]  Christian A. Rodriguez,et al.  Adolescent impatience decreases with increased frontostriatal connectivity , 2015, Proceedings of the National Academy of Sciences.

[47]  A. V. van Duijvenvoorde,et al.  Longitudinal Changes in Adolescent Risk-Taking: A Comprehensive Study of Neural Responses to Rewards, Pubertal Development, and Risk-Taking Behavior , 2015, The Journal of Neuroscience.

[48]  Maristela Monteiro,et al.  AUDIT - The alcohol use disorders identification test: guidelines for use in primary care. , 2001 .

[49]  Kathryn L. Modecki,et al.  Driving Under the Influence of Risky Peers: An Experimental Study of Adolescent Risk Taking , 2016 .

[50]  Brian A. Nosek,et al.  Power failure: why small sample size undermines the reliability of neuroscience , 2013, Nature Reviews Neuroscience.

[51]  M. Ernst,et al.  Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices , 2007, Neuropsychologia.

[52]  David J. Paulsen,et al.  Developmental Cognitive Neuroscience Regional Brain Activation Supporting Cognitive Control in the Context of Reward Is Associated with Treated Adolescents' Marijuana Problem Severity at Follow-up: a Preliminary Study , 2022 .

[53]  R. Poldrack Is “efficiency” a useful concept in cognitive neuroscience? , 2014, Developmental Cognitive Neuroscience.

[54]  Adriana Galván,et al.  The effects of poor quality sleep on brain function and risk taking in adolescence , 2013, NeuroImage.

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

[56]  Eva H. Telzer,et al.  Failure to retreat: Blunted sensitivity to negative feedback supports risky behavior in adolescents , 2017, NeuroImage.

[57]  Matt Field,et al.  Risk-taking but not response inhibition or delay discounting predict alcohol consumption in social drinkers. , 2010, Drug and alcohol dependence.

[58]  R. Adolphs,et al.  Building a Science of Individual Differences from fMRI , 2016, Trends in Cognitive Sciences.

[59]  Lauren E. Sherman,et al.  Peer Influence Via Instagram: Effects on Brain and Behavior in Adolescence and Young Adulthood. , 2018, Child development.

[60]  Mary Helen Immordino‐Yang,et al.  Neural correlates of adolescents’ viewing of parents’ and peers’ emotions: Associations with risk-taking behavior and risky peer affiliations , 2015, Social neuroscience.

[61]  T. Braver,et al.  Cognitive Neuroscience Approaches to Individual Differences in Working Memory and Executive Control: Conceptual and Methodological Issues , 2010 .

[62]  S. Tapert,et al.  Longitudinal changes in white matter integrity among adolescent substance users. , 2012, Alcoholism, clinical and experimental research.

[63]  Riitta Parkkola,et al.  Risk-Taking Behavior in a Computerized Driving Task: Brain Activation Correlates of Decision-Making, Outcome, and Peer Influence in Male Adolescents , 2015, PloS one.

[64]  J. Brooks-Gunn,et al.  New perspectives on adolescent risk behavior: Betwixt and between: Sexuality in the context of adolescent transitions , 1998 .

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

[66]  Gregory R. Samanez-Larkin,et al.  Caudate responses to reward anticipation associated with delay discounting behavior in healthy youth , 2013, Developmental Cognitive Neuroscience.

[67]  Laurence Steinberg,et al.  The Teenage Brain , 2013 .

[68]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[69]  A. Bechara,et al.  Abnormal affective decision making revealed in adolescent binge drinkers using a functional magnetic resonance imaging study. , 2013, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[70]  Monica Luciana,et al.  Neural networks involved in adolescent reward processing: An activation likelihood estimation meta-analysis of functional neuroimaging studies , 2015, NeuroImage.

[71]  W. Bickel,et al.  Longitudinal Associations Among Religiousness, Delay Discounting, and Substance Use Initiation in Early Adolescence. , 2015, Journal of research on adolescence : the official journal of the Society for Research on Adolescence.

[72]  A. Simmons,et al.  Adolescents' fMRI activation to a response inhibition task predicts future substance use. , 2013, Addictive behaviors.

[73]  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.

[74]  Cuda,et al.  Adolescent Children of Alcoholics. , 1993, Adolescent medicine.

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

[76]  S. Tapert,et al.  A longitudinal examination of adolescent response inhibition: neural differences before and after the initiation of heavy drinking , 2013, Psychopharmacology.

[77]  D. Hommer,et al.  Imaging brain response to reward in addictive disorders , 2011, Annals of the New York Academy of Sciences.

[78]  Ashley R. Smith,et al.  The dual systems model: Review, reappraisal, and reaffirmation , 2015, Developmental Cognitive Neuroscience.

[79]  James M. Bjork,et al.  Developmental Cognitive Neuroscience Who Are Those " Risk-taking Adolescents " ? Individual Differences in Developmental Neuroimaging Research , 2022 .

[80]  Sabine Peters,et al.  Nucleus accumbens response to rewards and testosterone levels are related to alcohol use in adolescents and young adults , 2015, Developmental Cognitive Neuroscience.

[81]  R. Dahl,et al.  The developmental neuroscience of adolescence: Revisiting, refining, and extending seminal models , 2015, Developmental Cognitive Neuroscience.

[82]  R. Poldrack Inferring Mental States from Neuroimaging Data: From Reverse Inference to Large-Scale Decoding , 2011, Neuron.

[83]  J. Ioannidis,et al.  Potential Reporting Bias in fMRI Studies of the Brain , 2013, PloS one.

[84]  Scott A. Jones,et al.  Reduced cerebellar brain activity during reward processing in adolescent binge drinkers , 2015, Developmental Cognitive Neuroscience.

[85]  R. Poldrack,et al.  Mind the gap: bridging economic and naturalistic risk-taking with cognitive neuroscience , 2011, Trends in Cognitive Sciences.

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

[87]  S. Tapert,et al.  Adolescent marijuana users have elevated risk-taking on the balloon analog risk task , 2014, Journal of psychopharmacology.

[88]  Vince D. Calhoun,et al.  Prediction of Individual Differences from Neuroimaging Data , 2017, NeuroImage.

[89]  Paul J. C. Adachi,et al.  Examining the link between adolescent brain development and risk taking from a social–developmental perspective , 2013, Brain and Cognition.

[90]  A. Galván,et al.  Behavioral and neural correlates of loss aversion and risk avoidance in adolescents and adults , 2013, Developmental Cognitive Neuroscience.

[91]  Eva H. Telzer,et al.  Links between parental depression and longitudinal changes in youths' neural sensitivity to rewards. , 2016, Social cognitive and affective neuroscience.

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

[93]  Ashley R. Smith,et al.  Psychosocial problems and recruitment of incentive neurocircuitry: Exploring individual differences in healthy adolescents , 2011, Developmental Cognitive Neuroscience.

[94]  F. Filbey,et al.  Adolescent risk-taking and resting state functional connectivity , 2014, Psychiatry Research: Neuroimaging.

[95]  M. Rietschel,et al.  Determinants of Early Alcohol Use In Healthy Adolescents: The Differential Contribution of Neuroimaging and Psychological Factors , 2012, Neuropsychopharmacology.