Shared and disorder-specific prefrontal abnormalities in boys with pure attention-deficit/hyperactivity disorder compared to boys with pure CD during interference inhibition and attention allocation.

BACKGROUND Inhibitory and attention deficits have been suggested to be shared problems of disruptive behaviour disorders. Patients with attention deficit hyperactivity disorder (ADHD) and patients with conduct disorder (CD) show deficits in tasks of attention allocation and interference inhibition. However, functional magnetic resonance imaging (fMRI) of inhibitory and attention control has only been investigated in patients with ADHD, including comorbidity with CD, finding fronto-striatal and temporo-parietal dysfunction. This study investigates differences and commonalities in functional neural networks mediating interference inhibition and attention allocation between medication-naïve children and adolescents with pure CD and those with pure ADHD. METHODS Event-related fMRI was used to compare brain activation of 13 boys with non-comorbid CD, 20 boys with non-comorbid ADHD and 20 healthy comparison boys during a Simon task that measures interference inhibition and controls for attention allocation, thus tapping into interference inhibition and selective attention networks. RESULTS During interference inhibition, both patient groups shared reduced activation compared to controls in right superior temporal lobe and in predominantly right precuneus. During the oddball condition, both patient groups showed reduced activation compared to healthy control children in right medial prefrontal lobe. However, only ADHD patients showed a disorder-specific under-activation compared to the other two groups in an extensive activation cluster in left inferior prefrontal cortex. CONCLUSIONS This study shows shared dysfunction in both patients groups in right hemispheric temporal and parietal brain regions during interference inhibition and in right dorsolateral prefrontal cortex during attention allocation. Ventrolateral prefrontal dysfunction, however, was specific to ADHD and not observed in patients with CD in the context of attention allocation. The findings suggest that the typically reduced functional activation in patients with ADHD in ventrolateral prefrontal cortex may be specific to the disorder, at least when compared to patients with CD.

[1]  E. Taylor,et al.  Neuropsychological analyses of impulsiveness in childhood hyperactivity , 2001, British Journal of Psychiatry.

[2]  V. Hesselbrock,et al.  Brain maturation and subtypes of conduct disorder: interactive effects on p300 amplitude and topography in male adolescents. , 2003, Journal of the American Academy of Child and Adolescent Psychiatry.

[3]  Brian Toone,et al.  Task-specific hypoactivation in prefrontal and temporoparietal brain regions during motor inhibition and task switching in medication-naive children and adolescents with attention deficit hyperactivity disorder. , 2006, The American journal of psychiatry.

[4]  K. Rubia,et al.  Conduct Problems in Adolescence: Three Domains of Inhibition and Effect of Gender , 2006, Developmental neuropsychology.

[5]  Nicole M Dudukovic,et al.  Altered neural substrates of cognitive control in childhood ADHD: evidence from functional magnetic resonance imaging. , 2005, The American journal of psychiatry.

[6]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[7]  M. Brammer,et al.  Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. , 2005, The American journal of psychiatry.

[8]  J L Bradshaw,et al.  Fronto-parietal activation in attention-deficit hyperactivity disorder, combined type: functional magnetic resonance imaging study. , 2005, The British journal of psychiatry : the journal of mental science.

[9]  Vincent Giampietro,et al.  Dissociated functional brain abnormalities of inhibition in boys with pure conduct disorder and in boys with pure attention deficit hyperactivity disorder. , 2008, The American journal of psychiatry.

[10]  Manuel F. Casanova,et al.  Reduced temporal lobe volume in early onset conduct disorder , 2004, Psychiatry Research: Neuroimaging.

[11]  Wei Li,et al.  Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[12]  T A Carpenter,et al.  Colored noise and computational inference in neurophysiological (fMRI) time series analysis: Resampling methods in time and wavelet domains , 2001, Human brain mapping.

[13]  T. Banaschewski,et al.  Questioning inhibitory control as the specific deficit of ADHD – evidence from brain electrical activity , 2004, Journal of Neural Transmission.

[14]  J. Kwon,et al.  Frontal P300 Decrement and Executive Dysfunction in Adolescents with Conduct Problems , 2001, Child psychiatry and human development.

[15]  Erik Willcutt,et al.  Towards an understanding of unique and shared pathways in the psychopathophysiology of ADHD. , 2005, Developmental science.

[16]  Vinod Menon,et al.  Parietal attentional system aberrations during target detection in adolescents with attention deficit hyperactivity disorder: event-related fMRI evidence. , 2006, The American journal of psychiatry.

[17]  Gereon R. Fink,et al.  Dysfunctional Attentional Networks in Children with Attention Deficit/Hyperactivity Disorder: Evidence from an Event-Related Functional Magnetic Resonance Imaging Study , 2006, Biological Psychiatry.

[18]  Rozmin Halari,et al.  Disorder-specific dissociation of orbitofrontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure ADHD during sustained attention. , 2009, The American journal of psychiatry.

[19]  P. Fenwick,et al.  The Aetiology of Aggression in Temporal-Lobe Epilepsy , 1988, British Journal of Psychiatry.

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

[21]  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.

[22]  Michael J. Brammer,et al.  Temporal Lobe Dysfunction in Medication-Naïve Boys With Attention-Deficit/Hyperactivity Disorder During Attention Allocation and Its Relation to Response Variability , 2007, Biological Psychiatry.

[23]  Aribert Rothenberger,et al.  Association of ADHD and conduct disorder--brain electrical evidence for the existence of a distinct subtype. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[24]  R. Goodman.  The Strengths and Difficulties Questionnaire: a research note. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[25]  M. Brammer,et al.  Progressive increase of frontostriatal brain activation from childhood to adulthood during event‐related tasks of cognitive control , 2006, Human brain mapping.

[26]  R. Barry,et al.  A review of electrophysiology in attention-deficit/hyperactivity disorder: II. Event-related potentials , 2003, Clinical Neurophysiology.

[27]  W. Iacono,et al.  P3 event-related potential amplitude and the risk for disinhibitory disorders in adolescent boys. , 2002, Archives of general psychiatry.

[28]  Godfrey D Pearlson,et al.  An FMRI auditory oddball study of combined-subtype attention deficit hyperactivity disorder. , 2007, The American journal of psychiatry.

[29]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[30]  Richard Rowe,et al.  Conduct disorder and oppositional defiant disorder in a national sample: developmental epidemiology. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[31]  V. Hesselbrock,et al.  Subtypes of Family History and Conduct Disorder: Effects on P300 During the Stroop Test , 1999, Neuropsychopharmacology.

[32]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[33]  E. Taylor,et al.  Performance of Children with Attention Deficit Hyperactivity Disorder (ADHD) on a Test Battery of Impulsiveness , 2007, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[34]  Philipp Sterzer,et al.  Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder , 2005, Biological Psychiatry.

[35]  Keith M. Shafritz,et al.  The effects of methylphenidate on neural systems of attention in attention deficit hyperactivity disorder. , 2004, The American journal of psychiatry.