Longitudinal Changes in Prefrontal Cortex Activation Underlie Declines in Adolescent Risk Taking

Adolescence is a critical developmental phase during which risk-taking behaviors increase across a variety of species, raising the importance of understanding how brain changes contribute to such behaviors. While the prefrontal cortex is thought to influence adolescent risk taking, the specific ways in which it functions are unclear. Using longitudinal functional magnetic resonance imaging in human adolescents, we found that ventrolateral prefrontal cortex (VLPFC) activation decreased during an experimental risk-taking task over time, with greater declines in VLPFC associated with greater declines in self-reported risky behavior. Furthermore, greater decreases in functional coupling between the medial prefrontal cortex (MPFC) and ventral striatum over time were associated with decreases in self-reported risky behavior. Thus, disparate roles of the VLPFC and MPFC modulate longitudinal declines in adolescent risk taking. SIGNIFICANCE STATEMENT Adolescence is a developmental period marked by steep increases in risk-taking behavior coupled with dramatic brain changes. Although theories propose that the prefrontal cortex (PFC) may influence adolescent risk taking, the specific ways in which it functions remain unclear. We report the first longitudinal functional magnetic resonance imaging study to examine how neural activation during risk taking changes over time and contributes to adolescents' real-life risk-taking behavior. We find that longitudinal declines in activation of the ventrolateral PFC are linked to declines in adolescent risk taking, whereas the medial PFC influences adolescent risk taking via its functional neural coupling with reward-related regions. This is the first study to identify the mechanism by which different regions of the PFC disparately contribute to declines in risk taking.

[1]  Beatriz Luna,et al.  The Maturation of Task Set-Related Activation Supports Late Developmental Improvements in Inhibitory Control , 2009, The Journal of Neuroscience.

[2]  T. Achenbach.  Integrative Guide for the 1991 CBCL/4-18, Ysr, and Trf Profiles , 1991 .

[3]  H. Kraemer,et al.  How can we learn about developmental processes from cross-sectional studies, or can we? , 2000, The American journal of psychiatry.

[4]  James R. Booth,et al.  Neural development of selective attention and response inhibition , 2003, NeuroImage.

[5]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[6]  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.

[7]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[8]  S. Rombouts,et al.  Developmental Cognitive Neuroscience How Stable Is Activation in the Amygdala and Prefrontal Cortex in Adolescence? a Study of Emotional Face Processing across Three Measurements , 2022 .

[9]  Sandra Jazbec,et al.  Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents , 2005, NeuroImage.

[10]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[11]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[12]  Hongtu Zhu,et al.  A developmental fMRI study of self‐regulatory control , 2006, Human brain mapping.

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

[14]  John A. Detre,et al.  Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI Study of the Balloon Analog Risk Task (BART) , 2008, NeuroImage.

[15]  Michael G. Hardin,et al.  Triadic model of the neurobiology of motivated behavior in adolescence , 2005, Psychological Medicine.

[16]  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.

[17]  G. Laviola,et al.  Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence , 2003, Neuroscience & Biobehavioral Reviews.

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

[19]  Jan R. Wessel,et al.  Chronometric Electrical Stimulation of Right Inferior Frontal Cortex Increases Motor Braking , 2013, The Journal of Neuroscience.

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

[21]  L. Spear.  The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

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

[23]  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.

[24]  M. Brammer,et al.  Linear age‐correlated functional development of right inferior fronto‐striato‐cerebellar networks during response inhibition and anterior cingulate during error‐related processes , 2007, Human brain mapping.

[25]  J. Mumford,et al.  Greater risk sensitivity of dorsolateral prefrontal cortex in young smokers than in nonsmokers , 2013, Psychopharmacology.

[26]  Gregory L. Stuart,et al.  Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). , 2002, Journal of experimental psychology. Applied.

[27]  I. Franken,et al.  Parental rearing behavior prospectively predicts adolescents' risky decision-making and feedback-related electrical brain activity. , 2013, Developmental science.

[28]  S. Holland,et al.  Neural Correlates of Risky Decision Making in Adolescents With and Without Traumatic Brain Injury Using the Balloon Analog Risk Task , 2012, Developmental neuropsychology.

[29]  A. Wagner,et al.  Annals of the New York Academy of Sciences Cognitive Control and Right Ventrolateral Prefrontal Cortex: Reflexive Reorienting, Motor Inhibition, and Action Updating , 2022 .

[30]  Stacey B. Daughters,et al.  Reliability and Validity of the Youth Version of the Balloon Analogue Risk Task (BART–Y) in the Assessment of Risk-Taking Behavior Among Inner-City Adolescents , 2007, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[31]  Todd A. Hare,et al.  A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry , 2013, The Journal of Neuroscience.

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

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

[34]  Susan B Perlman,et al.  Developing connections for affective regulation: age-related changes in emotional brain connectivity. , 2011, Journal of experimental child psychology.

[35]  Adriana Galván,et al.  Neural sensitivity to eudaimonic and hedonic rewards differentially predict adolescent depressive symptoms over time , 2014, Proceedings of the National Academy of Sciences.