Neural substrates of the influence of emotional cues on cognitive control in risk-taking adolescents

Adolescence is a period characterised by increases in risk-taking. This behaviour has been associated with an imbalance in the integration of the networks involved in cognitive control and motivational processes. We examined whether the influence of emotional cues on cognitive control differs between adolescents who show high or low levels of risk-taking behaviour. Participants who scored especially high or low on a risky decision task were subsequently administered an emotional go/no-go fMRI task comprising angry, happy and calm faces. Both groups showed decreased cognitive control when confronted with appetitive and aversive emotional cues. Activation in the inferior frontal gyrus (IFG) increased in line with the cognitive control demands of the task. Though the risk taking groups did not differ in their behavioural performance, functional connectivity analyses revealed the dorsal striatum plays a more central role in the processing of cognitive control in high than low risk-takers. Overall, these findings suggest that variance in fronto-striatal circuitry may underlie individual differences in risk-taking behaviour.

[1]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[2]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[3]  Verena D. Schmittmann,et al.  Qgraph: Network visualizations of relationships in psychometric data , 2012 .

[4]  S. Blakemore,et al.  The Developmental Mismatch in Structural Brain Maturation during Adolescence , 2014, Developmental Neuroscience.

[5]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[6]  René S. Kahn,et al.  Functional differences in emotion processing during adolescence and early adulthood , 2014, NeuroImage.

[7]  K. Thomas,et al.  Inhibitory control during emotional distraction across adolescence and early adulthood. , 2013, Child development.

[8]  Connie Lim,et al.  Youth risk behavior surveillance - United States, 2011. , 2012, Morbidity and mortality weekly report. Surveillance summaries.

[9]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[10]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[11]  N. Tottenham,et al.  Not all risk taking behavior is bad: Associative sensitivity predicts learning during risk taking among high sensation seekers. , 2013, Personality and individual differences.

[12]  James N. Porter,et al.  Age-related changes in the intrinsic functional connectivity of the human ventral vs. dorsal striatum from childhood to middle age , 2014, Developmental Cognitive Neuroscience.

[13]  C. Carver,et al.  Anger is an approach-related affect: evidence and implications. , 2009, Psychological bulletin.

[14]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[15]  Jennifer H. Pfeifer,et al.  The audacity of specificity: Moving adolescent developmental neuroscience towards more powerful scientific paradigms and translatable models , 2015, Developmental Cognitive Neuroscience.

[16]  Gang Chen,et al.  Adolescents, Adults and Rewards: Comparing Motivational Neurocircuitry Recruitment Using fMRI , 2010, PloS one.

[17]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[18]  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.

[19]  Joshua M. Smyth,et al.  The amygdala: An agent of change in adolescent neural networks , 2013, Hormones and Behavior.

[20]  G. Glover,et al.  Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task , 2008, Biological Psychiatry.

[21]  Laurence Steinberg,et al.  Peers Increase Late Adolescents' Exploratory Behavior and Sensitivity to Positive and Negative Feedback. , 2016, Journal of research on adolescence : the official journal of the Society for Research on Adolescence.

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

[23]  C. Geier.  Adolescent cognitive control and reward processing: Implications for risk taking and substance use , 2013, Hormones and Behavior.

[24]  Elliot T. Berkman,et al.  Putting the brakes on the brakes: negative emotion disrupts cognitive control network functioning and alters subsequent stopping ability , 2016, Experimental Brain Research.

[25]  Adriana Galvan,et al.  Enhanced Striatal Sensitivity to Aversive Reinforcement in Adolescents versus Adults , 2013, Journal of Cognitive Neuroscience.

[26]  M. Delgado,et al.  Reward‐Related Responses in the Human Striatum , 2007, Annals of the New York Academy of Sciences.

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

[28]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[29]  Paolo Maria Russo,et al.  Impulsivity and Reward Sensitivity differentially influence affective and deliberative risky decision making , 2012 .

[30]  K. Velanova,et al.  Immaturities in Reward Processing and Its Influence on Inhibitory Control in Adolescence , 2009, Cerebral cortex.

[31]  J. Grose-Fifer,et al.  Attentional capture by emotional faces in adolescence , 2010, Advances in cognitive psychology.

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

[33]  M. Toplak,et al.  Executive and motivational inhibition: Associations with self-report measures related to inhibition , 2009, Consciousness and Cognition.

[34]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[35]  Gary H. Glover,et al.  The bivalent side of the nucleus accumbens , 2009, NeuroImage.

[36]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

[37]  Karl J. Friston,et al.  A critique of functional localisers , 2006, NeuroImage.

[38]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[39]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

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

[41]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[42]  Susanne E. Baumgartner,et al.  The Relationship Between Media Multitasking and Executive Function in Early Adolescents , 2014 .

[43]  Denis Cousineau,et al.  Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method , 2005 .

[44]  John J. B. Allen,et al.  Anger and frontal brain activity: EEG asymmetry consistent with approach motivation despite negative affective valence. , 1998, Journal of personality and social psychology.

[45]  Will M Aklin,et al.  Evaluation of the Balloon Analogue Risk Task (BART) as a predictor of adolescent real-world risk-taking behaviours. , 2003, Journal of adolescence.

[46]  Todd A. Hare,et al.  Frontostriatal Maturation Predicts Cognitive Control Failure to Appetitive Cues in Adolescents , 2011, Journal of Cognitive Neuroscience.

[47]  B. Casey,et al.  Changes in cortico-subcortical and subcortico-subcortical connectivity impact cognitive control to emotional cues across development. , 2016, Social cognitive and affective neuroscience.

[48]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[49]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[50]  Daniel S Pine,et al.  Probing the neural correlates of anticipated peer evaluation in adolescence. , 2009, Child development.

[51]  Hiroki M. Morimoto,et al.  Functional dissociation in right inferior frontal cortex during performance of go/no-go task. , 2009, Cerebral cortex.

[52]  Russell A. Poldrack,et al.  Spatiotemporal activity estimation for multivoxel pattern analysis with rapid event-related designs , 2012, NeuroImage.

[53]  M. Phillips,et al.  Annotation: Development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[54]  Adriana Galván,et al.  Teens Impulsively React rather than Retreat from Threat , 2014, Developmental Neuroscience.

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

[56]  Ellen Leibenluft,et al.  A Developmental Examination of Amygdala Response to Facial Expressions , 2008, Journal of Cognitive Neuroscience.

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

[58]  E. Weber,et al.  Affective and deliberative processes in risky choice: age differences in risk taking in the Columbia Card Task. , 2009, Journal of experimental psychology. Learning, memory, and cognition.

[59]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[60]  M. Laubach,et al.  Neuronal correlates of instrumental learning in the dorsal striatum. , 2009, Journal of neurophysiology.

[61]  M. Van der Linden,et al.  Emotional Modulation of the Ability to Inhibit a Prepotent Response During Childhood , 2012, Developmental neuropsychology.

[62]  John Skvoretz,et al.  Node centrality in weighted networks: Generalizing degree and shortest paths , 2010, Soc. Networks.

[63]  B. Casey.  Beyond simple models of self-control to circuit-based accounts of adolescent behavior. , 2015, Annual review of psychology.

[64]  J. Halperin,et al.  Does the emotional go/no-go task really measure behavioral inhibition? Convergence with measures on a non-emotional analog. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

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

[66]  J. Sweeney,et al.  The Emergence of Collaborative Brain Function: fMRI Studies of the Development of Response Inhibition , 2004, Annals of the New York Academy of Sciences.

[67]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[68]  E. Nelson,et al.  Social re-orientation and brain development: An expanded and updated view , 2015, Developmental Cognitive Neuroscience.

[69]  L. Krabbendam,et al.  The potential adverse effect of energy drinks on executive functions in early adolescence , 2014, Front. Psychol..

[70]  Melissa T. Buelow,et al.  Test–Retest Reliability of Common Behavioral Decision Making Tasks , 2018, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[71]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[72]  Russell A. Poldrack,et al.  Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses , 2012, NeuroImage.

[73]  Beatriz Luna,et al.  Developmental changes in brain function underlying the influence of reward processing on inhibitory control , 2011, Developmental Cognitive Neuroscience.

[74]  A. Galván.  The Teenage Brain , 2013 .

[75]  Eric J. Johnson,et al.  Mindful judgment and decision making. , 2009, Annual review of psychology.

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

[77]  A. Richardson,et al.  A Critique of , 2009 .