Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents

Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.

[1]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[2]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[3]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[4]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[5]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

[6]  N. Ryan,et al.  K-SADS-PL. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[7]  N. Emery,et al.  The cognitive neuroscience of social behaviour , 2005 .

[8]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[9]  Dae-Shik Kim,et al.  Origin of Negative Blood Oxygenation Level—Dependent fMRI Signals , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[10]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[11]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[12]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[13]  W. Gardner,et al.  Adolescents' AIDS risk taking: a rational choice perspective. , 1990, New directions for child development.

[14]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

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

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

[17]  Marc N. Potenza,et al.  Neurodevelopment, Impulsivity, and Adolescent Gambling , 2004, Journal of Gambling Studies.

[18]  J. Arnett.  Adolescent storm and stress, reconsidered. , 1999, The American psychologist.

[19]  Edmund T Rolls,et al.  Convergence of sensory systems in the orbitofrontal cortex in primates and brain design for emotion. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[20]  Clay B. Holroyd,et al.  Errors in reward prediction are re£ected in the event-related brain potential , 2003 .

[21]  H. Duvernoy.  The Human Brain , 1999, Springer Vienna.

[22]  Jeffrey A Lieberman,et al.  Neuropsychological correlates of hippocampal volumes in patients experiencing a first episode of schizophrenia. , 2002, The American journal of psychiatry.

[23]  M. First,et al.  The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. , 1992, Archives of general psychiatry.

[24]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[25]  A. Phillips,et al.  Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior , 2003, Neuroscience & Biobehavioral Reviews.

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

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

[28]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

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

[30]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[32]  Christopher S. Monk,et al.  Choice selection and reward anticipation: an fMRI study , 2004, Neuropsychologia.

[33]  Deborah A Yurgelun-Todd,et al.  Cognitive Correlates of Medial Temporal Lobe Development across Adolescence: A Magnetic Resonance Imaging Study , 2003, Perceptual and motor skills.

[34]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[35]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[37]  E. Zarahn.  Testing for Neural Responses during Temporal Components of Trials with BOLD fMRI , 2000, NeuroImage.

[38]  T. Robbins,et al.  Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates , 2004, Neuroscience & Biobehavioral Reviews.

[39]  M. Hersen,et al.  Reliability of the Structured Clinical Interview for DSM-III-R: an evaluative review. , 1994, Comprehensive Psychiatry.

[40]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[41]  W. Schultz.  Getting Formal with Dopamine and Reward , 2002, Neuron.

[42]  T. Wills,et al.  Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger's theory. , 1994, Journal of substance abuse.

[43]  T. Robbins,et al.  Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats. , 2002, Behavioral neuroscience.

[44]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[45]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[46]  D. Kahneman,et al.  Functional Imaging of Neural Responses to Expectancy and Experience of Monetary Gains and Losses tasks with monetary payoffs , 2001 .

[47]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

[48]  J. Arnett.  Reckless behavior in adolescence: A developmental perspective , 1992 .

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

[50]  M. Raichle.  Behind the scenes of functional brain imaging: a historical and physiological perspective. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  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.

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

[53]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[54]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[55]  A. Damasio.  The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  JaneR . Taylor,et al.  Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. , 2003, The American journal of psychiatry.

[57]  A. Bechara.  The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage , 2004, Brain and Cognition.

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

[59]  William D S Killgore,et al.  Sex-specific developmental changes in amygdala responses to affective faces , 2001, Neuroreport.

[60]  D. Almeida,et al.  Risky Business , 1995 .

[61]  Kathleen M. Thomas,et al.  Amygdala response to facial expressions in children and adults , 2001, Biological Psychiatry.

[62]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[63]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[64]  Christian Kaufmann,et al.  Functional MRI during sleep: BOLD signal decreases and their electrophysiological correlates , 2004, The European journal of neuroscience.

[65]  Margo Wilson,et al.  Competitiveness, risk taking, and violence: the young male syndrome , 1985, Ethology and Sociobiology.

[66]  M Ashtari,et al.  Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. , 1999, Archives of general psychiatry.

[67]  D. Pine,et al.  The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. , 1998, Archives of general psychiatry.

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