Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder

Attention-deficit/hyperactivity disorder (ADHD) has been suggested to involve deficits in reward processing. We used functional magnetic resonance imaging (fMRI) to compare the neural responses to reward anticipation and outcomes in 10 adults with ADHD and 10 controls as they played a monetary incentive delay task. Adults with ADHD were unmedicated, and groups were matched for age, verbal IQ and smoking habits. Adults with ADHD showed decreased activation in the ventral striatum during the anticipation of gain, but increased activation of the orbitofrontal cortex in response to gain outcomes. Ventral striatal activation in adults with ADHD during gain anticipation was negatively correlated with self-rated symptoms of hyperactivity and impulsivity. These findings suggest that male adults with ADHD show neural signs of abnormal reward processing. Future studies will have to investigate whether these dysfunctional patterns might be normalized by treatment.

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

[2]  Michael X. Cohen,et al.  Different neural systems adjust motor behavior in response to reward and punishment , 2007, NeuroImage.

[3]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[4]  Ali A. Bonab,et al.  In Vivo Neuroreceptor Imaging in Attention-Deficit/Hyperactivity Disorder: A Focus on The Dopamine Transporter , 2005, Biological Psychiatry.

[5]  M. First,et al.  Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research version (SCID-I RV) , 2002 .

[6]  G H Glover,et al.  Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Jin Fan,et al.  Response inhibition in adolescents diagnosed with attention deficit hyperactivity disorder during childhood: an event-related FMRI study. , 2004, The American journal of psychiatry.

[8]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

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

[10]  M. Ernst,et al.  Neural substrates of decision making in adults with attention deficit hyperactivity disorder. , 2003, The American journal of psychiatry.

[11]  Brian Knutson,et al.  Linking nucleus accumbens dopamine and blood oxygenation , 2007, Psychopharmacology.

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

[13]  E. Sonuga-Barke,et al.  Psychological heterogeneity in AD/HD—a dual pathway model of behaviour and cognition , 2002, Behavioural Brain Research.

[14]  Steven W Anderson,et al.  Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex , 2006, Journal of the International Neuropsychological Society.

[15]  Jaap Oosterlaan,et al.  How specific is a deficit of executive functioning for Attention-Deficit/Hyperactivity Disorder? , 2002, Behavioural Brain Research.

[16]  G. Bush,et al.  Functional Neuroimaging of Attention-Deficit/Hyperactivity Disorder: A Review and Suggested Future Directions , 2005, Biological Psychiatry.

[17]  E. Bullmore,et al.  Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. , 1999, The American journal of psychiatry.

[18]  N. Makris,et al.  Structural Brain Imaging of Attention-Deficit/Hyperactivity Disorder , 2005, Biological Psychiatry.

[19]  A. Roberts,et al.  Primate orbitofrontal cortex and adaptive behaviour , 2006, Trends in Cognitive Sciences.

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

[21]  Larry J. Seidman,et al.  Functional MRI in attention-deficit hyperactivity disorder: Evidence for hypofrontality , 2005, Brain and Development.

[22]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[23]  V. Russell,et al.  A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. , 2005, The Behavioral and brain sciences.

[24]  E. Rolls,et al.  Different representations of pleasant and unpleasant odours in the human brain , 2003, The European journal of neuroscience.

[25]  Sarah Durston,et al.  A review of the biological bases of ADHD: what have we learned from imaging studies? , 2003, Mental retardation and developmental disabilities research reviews.

[26]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[27]  S. Kollins,et al.  Discriminative and participant-rated effects of methylphenidate in children diagnosed with attention deficit hyperactivity disorder (ADHD). , 1998, Experimental and clinical psychopharmacology.

[28]  B. Alsop,et al.  Sensitivity to reward frequency in boys with attention deficit hyperactivity disorder. , 1999, Journal of clinical child psychology.

[29]  Gordon D. Logan,et al.  The Ecological Validity of Delay Aversion and Response Inhibition as Measures of Impulsivity in AD/HD: A Supplement to the NIMH Multimodal Treatment Study of AD/HD , 2001, Journal of abnormal child psychology.

[30]  Edmund J. S. Sonuga-Barke,et al.  Causal Models of Attention-Deficit/Hyperactivity Disorder: From Common Simple Deficits to Multiple Developmental Pathways , 2005, Biological Psychiatry.

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

[32]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

[33]  P. Wender,et al.  The Wender Utah Rating Scale: an aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. , 1993, The American journal of psychiatry.

[34]  Brian Knutson,et al.  Ventral Striatal Hyporesponsiveness During Reward Anticipation in Attention-Deficit/Hyperactivity Disorder , 2007, Biological Psychiatry.

[35]  T. Robbins,et al.  Impulsive Choice Induced in Rats by Lesions of the Nucleus Accumbens Core , 2001, Science.

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