Earlier Development of the Accumbens Relative to Orbitofrontal Cortex Might Underlie Risk-Taking Behavior in Adolescents

Adolescence has been characterized by risk-taking behaviors that can lead to fatal outcomes. This study examined the neurobiological development of neural systems implicated in reward-seeking behaviors. Thirty-seven participants (7–29 years of age) were scanned using event-related functional magnetic resonance imaging and a paradigm that parametrically manipulated reward values. The results show exaggerated accumbens activity, relative to prefrontal activity in adolescents, compared with children and adults, which appeared to be driven by different time courses of development for these regions. Accumbens activity in adolescents looked like that of adults in both extent of activity and sensitivity to reward values, although the magnitude of activity was exaggerated. In contrast, the extent of orbital frontal cortex activity in adolescents looked more like that of children than adults, with less focal patterns of activity. These findings suggest that maturing subcortical systems become disproportionately activated relative to later maturing top–down control systems, biasing the adolescent's action toward immediate over long-term gains.

[1]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

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

[3]  H. Duvernoy,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply , 1999 .

[4]  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.

[5]  K. Kunz,et al.  Dissociating Striatal and Hippocampal Function Developmentally with a Stimulus–Response Compatibility Task , 2002, The Journal of Neuroscience.

[6]  Masato Inoue,et al.  Correspondence of cue activity to reward activity in the macaque orbitofrontal cortex , 2005, Neuroscience Letters.

[7]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[8]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[9]  G. Glover,et al.  The Role of Ventral Frontostriatal Circuitry in Reward-Based Learning in Humans , 2005, The Journal of Neuroscience.

[10]  S. Hyman,et al.  Addiction and the brain: The neurobiology of compulsion and its persistence , 2001, Nature Reviews Neuroscience.

[11]  Camelia M. Kuhnen,et al.  The Neural Basis of Financial Risk Taking , 2005, Neuron.

[12]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[13]  E. Bullmore,et al.  Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI , 2000, Neuroscience & Biobehavioral Reviews.

[14]  T. Robbins,et al.  Dissociable Contributions of the Orbitofrontal and Infralimbic Cortex to Pavlovian Autoshaping and Discrimination Reversal Learning: Further Evidence for the Functional Heterogeneity of the Rodent Frontal Cortex , 2003, The Journal of Neuroscience.

[15]  Abraham Z. Snyder,et al.  The Feasibility of a Common Stereotactic Space for Children and Adults in fMRI Studies of Development , 2002, NeuroImage.

[16]  Norio Ozaki,et al.  No association between monoamine oxidase A promoter polymorphism and personality traits in Japanese females , 2005, Neuroscience Letters.

[17]  D. Yurgelun-Todd,et al.  Trajectories of Adolescent Emotional and Cognitive Development: Effects of Sex and Risk for Drug Use , 2004, Annals of the New York Academy of Sciences.

[18]  G. Laviola,et al.  Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models , 1999, Neuroscience & Biobehavioral Reviews.

[19]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[20]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[21]  A. Bechara.  Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective , 2005, Nature Neuroscience.

[22]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[23]  Gary H Glover,et al.  Improved combination of spiral‐in/out images for BOLD fMRI , 2004, Magnetic resonance in medicine.

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

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

[26]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[27]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[28]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[29]  S. Petersen,et al.  Developmental changes in human cerebral functional organization for word generation. , 2005, Cerebral cortex.

[30]  Brian Knutson,et al.  Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults , 2004, The Journal of Neuroscience.

[31]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[32]  F. McGlone,et al.  Dopamine Transmission in the Human Striatum during Monetary Reward Tasks , 2004, The Journal of Neuroscience.

[33]  Tobias Sommer,et al.  Evidence of Developmental Differences in Implicit Sequence Learning: An fMRI Study of Children and Adults , 2004, Journal of Cognitive Neuroscience.

[34]  Douglas C. Noll,et al.  A pediatric functional MRI study of prefrontal activation during performance of a Go-No-Go task , 1996, NeuroImage.

[35]  A. Dickinson,et al.  Classical conditioning in animals. , 1978, Annual review of psychology.

[36]  D. Rosenberg,et al.  Changes in the dopaminergic innervation of monkey prefrontal cortex during late postnatal development: A tyrosine hydroxylase immunohistochemical study , 1994, Biological Psychiatry.

[37]  N. Kraus,et al.  The time course of auditory perceptual learning: neurophysiological changes during speech‐sound training , 1998, Neuroreport.

[38]  Daniel A. Gottlieb.  Acquisition with partial and continuous reinforcement in rat magazine approach. , 2005, Journal of experimental psychology. Animal behavior processes.

[39]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

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

[41]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[42]  K. Doya,et al.  A Neural Correlate of Reward-Based Behavioral Learning in Caudate Nucleus: A Functional Magnetic Resonance Imaging Study of a Stochastic Decision Task , 2004, The Journal of Neuroscience.

[43]  Michael Koch,et al.  Dopamine in the orbitofrontal cortex regulates operant responding under a progressive ratio of reinforcement in rats , 2004, Neuroscience Letters.

[44]  J. O'Doherty,et al.  Dissociating Valence of Outcome from Behavioral Control in Human Orbital and Ventral Prefrontal Cortices , 2003, The Journal of Neuroscience.

[45]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[46]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  S. Haber.  The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[48]  Aziz M. Ulug,et al.  Differential cingulate and caudate activation following unexpected nonrewarding stimuli , 2004, NeuroImage.

[49]  M. Umemiya,et al.  A Calcium-Dependent Feedback Mechanism Participates in Shaping Single NMDA Miniature EPSCs , 2001, The Journal of Neuroscience.

[50]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[51]  S. Inati,et al.  An fMRI study of reward-related probability learning , 2005, NeuroImage.

[52]  M. Delgado,et al.  Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents , 2004, Biological Psychiatry.

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

[54]  Sylvia M. L. Cox,et al.  Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward , 2005, The Journal of Neuroscience.

[55]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[56]  Lawrence R. Frank,et al.  Functional MRI of Global and Local Processing in Children , 2002, NeuroImage.

[57]  D. Rosenberg,et al.  Postnatal maturation of the dopaminergic innervation of monkey prefrontal and motor cortices: A tyrosine hydroxylase immunohistochemical analysis , 1995, The Journal of comparative neurology.

[58]  J. Swanson,et al.  Dopamine in drug abuse and addiction: results from imaging studies and treatment implications , 2004, Molecular Psychiatry.

[59]  T. Hare,et al.  Changes in cerebral functional organization during cognitive development , 2005, Current Opinion in Neurobiology.

[60]  A. Tversky,et al.  The framing of decisions and the psychology of choice. , 1981, Science.

[61]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[62]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[63]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

[64]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[65]  Daniel A. Gottlieb.  Acquisition with partial and continuous reinforcement in pigeon autoshaping , 2004, Learning & behavior.

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

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

[68]  J. W. Aldridge,et al.  Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards. , 2004, The Journal of neuroscience : the official journal of the Society for Neuroscience.