Contributions of Reward Sensitivity to Ventral Striatum Activity Across Adolescence and Early Adulthood

It was examined how ventral striatum responses to rewards develop across adolescence and early adulthood and how individual differences in state‐ and trait‐level reward sensitivity are related to these changes. Participants (aged 8–29 years) were tested across three waves separated by 2 years (693 functional MRI scans) in an accelerated longitudinal design. The results confirmed an adolescent peak in reward‐related ventral striatum, specifically nucleus accumbens, activity. In early to mid‐adolescence, increases in reward activation were related to trait‐level reward drive. In mid‐adolescence to early adulthood decreases in reward activation were related to decreases in state‐level hedonic reward pleasure. This study demonstrates that state‐ and trait‐level reward sensitivity account for reward‐related ventral striatum activity in different phases of adolescence and early adulthood.

[1]  E. Crone,et al.  Changing brains: how longitudinal functional magnetic resonance imaging studies can inform us about cognitive and social-affective growth trajectories. , 2015, Wiley interdisciplinary reviews. Cognitive science.

[2]  M. Ernst,et al.  Longitudinal study of striatal activation to reward and loss anticipation from mid-adolescence into late adolescence/early adulthood , 2014, Brain and Cognition.

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

[4]  Sabine Peters,et al.  Gambling for self, friends, and antagonists: Differential contributions of affective and social brain regions on adolescent reward processing , 2014, NeuroImage.

[5]  Eveline A. Crone,et al.  A cross-sectional and longitudinal analysis of reward-related brain activation: Effects of age, pubertal stage, and reward sensitivity , 2014, Brain and Cognition.

[6]  M F Huque,et al.  Some comments on frequently used multiple endpoint adjustment methods in clinical trials. , 1997, Statistics in medicine.

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

[8]  Beatriz Luna,et al.  Modulation of reward-related neural activation on sensation seeking across development , 2017, NeuroImage.

[9]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

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

[11]  Daniel Brandeis,et al.  Cognitive flexibility in adolescence: Neural and behavioral mechanisms of reward prediction error processing in adaptive decision making during development , 2015, NeuroImage.

[12]  Jin Fan,et al.  Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[13]  M. Phillips,et al.  Healthy adolescents' neural response to reward: associations with puberty, positive affect, and depressive symptoms. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[14]  G. Schwarz Estimating the Dimension of a Model , 1978 .

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

[16]  M. Delgado,et al.  The social brain and reward: social information processing in the human striatum. , 2014, Wiley interdisciplinary reviews. Cognitive science.

[17]  Bregtje Gunther Moor,et al.  Developmental Cognitive Neuroscience Testosterone Levels Correspond with Increased Ventral Striatum Activation in Response to Monetary Rewards in Adolescents , 2022 .

[18]  J. Fudge,et al.  A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes , 2009, Neuroscience & Biobehavioral Reviews.

[19]  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.

[20]  Beatriz Luna,et al.  Longitudinal Growth Curves of Brain Function Underlying Inhibitory Control through Adolescence , 2013, The Journal of Neuroscience.

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

[22]  Gail M. Rosenbaum,et al.  The Influences of Described and Experienced Information on Adolescent Risky Decision Making. , 2017, Developmental review : DR.

[23]  R. Zatorre,et al.  Anatomically distinct dopamine release during anticipation and experience of peak emotion to music , 2011, Nature Neuroscience.

[24]  Uwe Sunde,et al.  Relative versus absolute income, joy of winning, and gender: Brain imaging evidence , 2011 .

[25]  Adriana Galvan,et al.  Adolescent development of the reward system , 2022 .

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

[27]  H. Akaike A new look at the statistical model identification , 1974 .

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

[29]  N. Sadato,et al.  Processing of Social and Monetary Rewards in the Human Striatum , 2008, Neuron.

[30]  Stefan Kaiser,et al.  Neural reward processing is modulated by approach- and avoidance-related personality traits , 2010, NeuroImage.

[31]  R. Dahl Adolescent Brain Development: A Period of Vulnerabilities and Opportunities. Keynote Address , 2004, Annals of the New York Academy of Sciences.

[32]  J. Dreher,et al.  Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies , 2013, Neuroscience & Biobehavioral Reviews.

[33]  K. Lim,et al.  Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence. , 2012, Developmental psychology.

[34]  E. Crone,et al.  Reward-related neural responses are dependent on the beneficiary. , 2014, Social cognitive and affective neuroscience.

[35]  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.

[36]  Adriana Galván,et al.  Ventral striatum activation to prosocial rewards predicts longitudinal declines in adolescent risk taking , 2013, Developmental Cognitive Neuroscience.

[37]  Eva H. Telzer,et al.  Developmental Cognitive Neuroscience Dopaminergic Reward Sensitivity Can Promote Adolescent Health: a New Perspective on the Mechanism of Ventral Striatum Activation , 2022 .

[38]  E. Crone,et al.  What motivates adolescents? Neural responses to rewards and their influence on adolescents’ risk taking, learning, and cognitive control , 2016, Neuroscience & Biobehavioral Reviews.

[39]  T. White,et al.  Neurobehavioral evidence for changes in dopamine system activity during adolescence , 2010, Neuroscience & Biobehavioral Reviews.

[40]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[41]  Serge A R B Rombouts,et al.  What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. , 2010, Cerebral cortex.

[42]  H. Demaree,et al.  You bet: How personality differences affect risk-taking preferences , 2008 .

[43]  T. Perneger What's wrong with Bonferroni adjustments , 1998, BMJ.