Disorder‐specific dysfunctions in patients with attention‐deficit/hyperactivity disorder compared to patients with obsessive‐compulsive disorder during interference inhibition and attention allocation

Background: Abnormalities in inhibitory control and underlying fronto‐striatal networks is common to both attention deficit hyperactivity disorder (ADHD) and obsessive‐compulsive‐disorder (OCD). The aim of this study was to investigate disorder‐specific abnormalities in neural networks mediating interference inhibition and selective attention. Method: Event‐related functional magnetic resonance imaging (fMRI) was used to compare brain activation of boys with ADHD (18), with OCD (10), and healthy boys during (20) during a Simon task that measures interference inhibition and controls for and therefore comeasures attention allocation. Results: During interference inhibition, both patient groups shared mesial frontal dysfunction compared to controls. Disorder‐specific dysfunctions were observed in OCD patients in dorsolateral prefrontal cortex during the oddball condition and in ADHD patients in inferior parietal lobe during interference inhibition and in caudate and posterior cingulate during the simpler oddball condition. The decreased activation in caudate and cingulate in ADHD was furthermore negatively correlated with ADHD symptoms and positively with OCD behavioral traits. Conclusions: The study shows that ADHD and OCD patients have shared but also disorder‐specific brain dysfunctions during interference inhibition and attention allocation. Both disorders shared dysfunction in mesial frontal cortex. Disorder‐specific dysfunctions, however, were observed in dorsolateral prefrontal cortex in OCD patients and in caudate, cingulate, and parietal brain regions in ADHD patients. The disorder‐specific dissociation of striato‐cingulate activation that was increased in OCD compared to ADHD patients, was furthermore inversely related to the symptomatology of the two disorders, and may potentially reflect differential dopamine modulation of striatal brain regions. Hum Brain Mapp, 2011. © 2010 Wiley‐Liss, Inc.

[1]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[2]  V. Giampietro,et al.  A functional magnetic resonance imaging study of inhibitory control in obsessive-compulsive disorder , 2009, Psychiatry Research: Neuroimaging.

[3]  R. Halari,et al.  Impulsiveness as a timing disturbance: neurocognitive abnormalities in attention-deficit hyperactivity disorder during temporal processes and normalization with methylphenidate , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  Rozmin Halari,et al.  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. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[5]  D. Veltman,et al.  Paediatric obsessive–compulsive disorder, a neurodevelopmental disorder? Evidence from neuroimaging , 2009, Neuroscience & Biobehavioral Reviews.

[6]  Hui Zhang,et al.  Cluster mass inference via random field theory , 2009, NeuroImage.

[7]  E. Bullmore,et al.  Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: The orbitofronto-striatal model revisited , 2008, Neuroscience & Biobehavioral Reviews.

[8]  D. Gitelman,et al.  The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. , 2008, Cerebral cortex.

[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]  J. Krause,et al.  SPECT and PET of the dopamine transporter in attention-deficit/hyperactivity disorder , 2008, Expert review of neurotherapeutics.

[11]  P. McGuire,et al.  Brain activation in paediatric obsessive-compulsive disorder during tasks of inhibitory control , 2008, British Journal of Psychiatry.

[12]  Chi-Hua Chen,et al.  Neurocognitive endophenotypes of obsessive-compulsive disorder. , 2007, Brain : a journal of neurology.

[13]  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.

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

[15]  K. Rubia,et al.  Impaired response inhibition in obsessive compulsive disorder , 2007, European Psychiatry.

[16]  Y. Ryu,et al.  Dopamine Transporter Density in the Basal Ganglia in Obsessive-Compulsive Disorder, Measured with [123I]IPT SPECT before and after Treatment with Serotonin Reuptake Inhibitors , 2007, Neuropsychobiology.

[17]  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.

[18]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[19]  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.

[20]  Michael P Milham,et al.  The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[21]  Nora D. Volkow,et al.  Effects of expectation on the brain metabolic responses to methylphenidate and to its placebo in non-drug abusing subjects , 2006, NeuroImage.

[22]  Trevor W Robbins,et al.  Motor inhibition and cognitive flexibility in obsessive-compulsive disorder and trichotillomania. , 2006, The American journal of psychiatry.

[23]  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.

[24]  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.

[25]  J. Jolles,et al.  The effect of acute tryptophan depletion on the BOLD response during performance monitoring and response inhibition in healthy male volunteers , 2006, Psychopharmacology.

[26]  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.

[27]  Caroline F. Zink,et al.  Human striatal activation reflects degree of stimulus saliency , 2006, NeuroImage.

[28]  R. Elliott,et al.  Serotonergic modulation of neuronal responses to behavioural inhibition and reinforcing stimuli: an fMRI study in healthy volunteers , 2006, The European journal of neuroscience.

[29]  Thomas Villmann,et al.  Serotonin and dopamine transporter imaging in patients with obsessive–compulsive disorder , 2005, Psychiatry Research: Neuroimaging.

[30]  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.

[31]  Rebecca Elliott,et al.  The Effect of Citalopram Pretreatment on Neuronal Responses to Neuropsychological Tasks in Normal Volunteers: An fMRI Study , 2005, Neuropsychopharmacology.

[32]  François Chollet,et al.  Chronic administration of selective serotonin reuptake inhibitor (SSRI) paroxetine modulates human motor cortex excitability in healthy subjects , 2005, NeuroImage.

[33]  Kazuko Yoshioka,et al.  A functional MRI comparison of patients with obsessive–compulsive disorder and normal controls during a Chinese character Stroop task , 2005, Psychiatry Research: Neuroimaging.

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

[35]  T. Yoshiura,et al.  Brain activation of patients with obsessive-compulsive disorder during neuropsychological and symptom provocation tasks before and after symptom improvement: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[36]  W. Gehring,et al.  Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder , 2005, Biological Psychiatry.

[37]  Cynthia H. Y. Fu,et al.  Tryptophan depletion reduces right inferior prefrontal activation during response inhibition in fast, event-related fMRI , 2005, Psychopharmacology.

[38]  K. Kiehl,et al.  Dysfunctional action monitoring hyperactivates frontal–striatal circuits in obsessive–compulsive disorder: an event-related fMRI study , 2005, NeuroImage.

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

[40]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[41]  Jesse G. Brand,et al.  Fluoxetine increases relative metabolic rate in prefrontal cortex in impulsive aggression , 2004, Psychopharmacology.

[42]  H. Westenberg,et al.  Low level of dopaminergic D2 receptor binding in obsessive-compulsive disorder , 2004, Biological Psychiatry.

[43]  G. Pagnoni,et al.  Human Striatal Responses to Monetary Reward Depend On Saliency , 2004, Neuron.

[44]  Y. Ryu,et al.  Dopamine transporter density of basal ganglia assessed with [123I]IPT SPET in obsessive-compulsive disorder , 2003, European Journal of Nuclear Medicine and Molecular Imaging.

[45]  B. J. Casey,et al.  Differential patterns of striatal activation in young children with and without ADHD , 2003, Biological Psychiatry.

[46]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[47]  R. Barry,et al.  A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography , 2003, Clinical Neurophysiology.

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

[49]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

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

[51]  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.

[52]  E. Bullmore,et al.  Mapping Motor Inhibition: Conjunctive Brain Activations across Different Versions of Go/No-Go and Stop Tasks , 2001, NeuroImage.

[53]  M. Carlsson On the role of cortical glutamate inobsessive‐compulsive disorder and attention‐deficit hyperactivity disorder, two phenomenologically antithetical conditions , 2000, Acta psychiatrica Scandinavica.

[54]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[55]  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.

[56]  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.

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

[58]  W. Goodman,et al.  Children's Yale-Brown Obsessive Compulsive Scale: reliability and validity. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[59]  J. Biederman,et al.  Comorbidity of juvenile obsessive-compulsive disorder with disruptive behavior disorders. , 1996, Journal of the American Academy of Child and Adolescent Psychiatry.

[60]  T. Achenbach Manual for the child behavior checklist/4-18 and 1991 profile , 1991 .

[61]  C. Edelbrock,et al.  Manual for the Child: Behavior Checklist and Revised Child Behavior Profile , 1983 .

[62]  C. Reynolds,et al.  What i think and feel: A revised measure of children's manifest anxiety , 1978, Journal of abnormal child psychology.

[63]  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.

[64]  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.

[65]  S. Faraone,et al.  Clinical correlates of obsessive compulsive disorder in children and adolescents referred to specialized and non‐specialized clinical settings , 2000, Depression and anxiety.

[66]  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.

[67]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[68]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[69]  P. Birleson The validity of depressive disorder in childhood and the development of a self-rating scale: a research report. , 1981, Journal of child psychology and psychiatry, and allied disciplines.