Distinguishing Adolescents With ADHD From Their Unaffected Siblings and Healthy Comparison Subjects by Neural Activation Patterns During Response Inhibition

Dysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response inhibition measures do not consistently differentiate affected from unaffected individuals. The authors therefore investigated neural correlates of...

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Veröffentlicht in:The American journal of psychiatry Jg. 172; H. 7; S. 674
Hauptverfasser: van Rooij, Daan, Hoekstra, Pieter J, Mennes, Maarten, von Rhein, Daniel, Thissen, Andrieke J A M, Heslenfeld, Dirk, Zwiers, Marcel P, Faraone, Stephen V, Oosterlaan, Jaap, Franke, Barbara, Rommelse, Nanda, Buitelaar, Jan K, Hartman, Catharina A
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States 01.07.2015
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ISSN:1535-7228, 1535-7228
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Abstract Dysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response inhibition measures do not consistently differentiate affected from unaffected individuals. The authors therefore investigated neural correlates of response inhibition and the familial nature of these neural correlates. Functional MRI measurements of neural activation during the stop-signal task and behavioral measures of response inhibition were obtained in adolescents and young adults with ADHD (N=185), their unaffected siblings (N=111), and healthy comparison subjects (N=124). Stop-signal task reaction times were longer and error rates were higher in participants with ADHD, but not in their unaffected siblings, while reaction time variability was higher in both groups than in comparison subjects. Relative to comparison subjects, participants with ADHD and unaffected siblings had neural hypoactivation in frontal-striatal and frontal-parietal networks, whereby activation in inferior frontal and temporal/parietal nodes in unaffected siblings was intermediate between levels of participants with ADHD and comparison subjects. Furthermore, neural activation in inferior frontal nodes correlated with stop-signal reaction times, and activation in both inferior frontal and temporal/parietal nodes correlated with ADHD severity. Neural activation alterations in ADHD are more robust than behavioral response inhibition deficits and explain variance in response inhibition and ADHD severity. Although only affected participants with ADHD have deficient response inhibition, hypoactivation in inferior frontal and temporal-parietal nodes in unaffected siblings supports the familial nature of the underlying neural process. Activation deficits in these nodes may be useful as endophenotypes that extend beyond the affected individuals in the family.
AbstractList Dysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response inhibition measures do not consistently differentiate affected from unaffected individuals. The authors therefore investigated neural correlates of response inhibition and the familial nature of these neural correlates.OBJECTIVEDysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response inhibition measures do not consistently differentiate affected from unaffected individuals. The authors therefore investigated neural correlates of response inhibition and the familial nature of these neural correlates.Functional MRI measurements of neural activation during the stop-signal task and behavioral measures of response inhibition were obtained in adolescents and young adults with ADHD (N=185), their unaffected siblings (N=111), and healthy comparison subjects (N=124).METHODSFunctional MRI measurements of neural activation during the stop-signal task and behavioral measures of response inhibition were obtained in adolescents and young adults with ADHD (N=185), their unaffected siblings (N=111), and healthy comparison subjects (N=124).Stop-signal task reaction times were longer and error rates were higher in participants with ADHD, but not in their unaffected siblings, while reaction time variability was higher in both groups than in comparison subjects. Relative to comparison subjects, participants with ADHD and unaffected siblings had neural hypoactivation in frontal-striatal and frontal-parietal networks, whereby activation in inferior frontal and temporal/parietal nodes in unaffected siblings was intermediate between levels of participants with ADHD and comparison subjects. Furthermore, neural activation in inferior frontal nodes correlated with stop-signal reaction times, and activation in both inferior frontal and temporal/parietal nodes correlated with ADHD severity.RESULTSStop-signal task reaction times were longer and error rates were higher in participants with ADHD, but not in their unaffected siblings, while reaction time variability was higher in both groups than in comparison subjects. Relative to comparison subjects, participants with ADHD and unaffected siblings had neural hypoactivation in frontal-striatal and frontal-parietal networks, whereby activation in inferior frontal and temporal/parietal nodes in unaffected siblings was intermediate between levels of participants with ADHD and comparison subjects. Furthermore, neural activation in inferior frontal nodes correlated with stop-signal reaction times, and activation in both inferior frontal and temporal/parietal nodes correlated with ADHD severity.Neural activation alterations in ADHD are more robust than behavioral response inhibition deficits and explain variance in response inhibition and ADHD severity. Although only affected participants with ADHD have deficient response inhibition, hypoactivation in inferior frontal and temporal-parietal nodes in unaffected siblings supports the familial nature of the underlying neural process. Activation deficits in these nodes may be useful as endophenotypes that extend beyond the affected individuals in the family.CONCLUSIONSNeural activation alterations in ADHD are more robust than behavioral response inhibition deficits and explain variance in response inhibition and ADHD severity. Although only affected participants with ADHD have deficient response inhibition, hypoactivation in inferior frontal and temporal-parietal nodes in unaffected siblings supports the familial nature of the underlying neural process. Activation deficits in these nodes may be useful as endophenotypes that extend beyond the affected individuals in the family.
Dysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response inhibition measures do not consistently differentiate affected from unaffected individuals. The authors therefore investigated neural correlates of response inhibition and the familial nature of these neural correlates. Functional MRI measurements of neural activation during the stop-signal task and behavioral measures of response inhibition were obtained in adolescents and young adults with ADHD (N=185), their unaffected siblings (N=111), and healthy comparison subjects (N=124). Stop-signal task reaction times were longer and error rates were higher in participants with ADHD, but not in their unaffected siblings, while reaction time variability was higher in both groups than in comparison subjects. Relative to comparison subjects, participants with ADHD and unaffected siblings had neural hypoactivation in frontal-striatal and frontal-parietal networks, whereby activation in inferior frontal and temporal/parietal nodes in unaffected siblings was intermediate between levels of participants with ADHD and comparison subjects. Furthermore, neural activation in inferior frontal nodes correlated with stop-signal reaction times, and activation in both inferior frontal and temporal/parietal nodes correlated with ADHD severity. Neural activation alterations in ADHD are more robust than behavioral response inhibition deficits and explain variance in response inhibition and ADHD severity. Although only affected participants with ADHD have deficient response inhibition, hypoactivation in inferior frontal and temporal-parietal nodes in unaffected siblings supports the familial nature of the underlying neural process. Activation deficits in these nodes may be useful as endophenotypes that extend beyond the affected individuals in the family.
Author Buitelaar, Jan K
Hoekstra, Pieter J
Mennes, Maarten
Heslenfeld, Dirk
van Rooij, Daan
Faraone, Stephen V
Oosterlaan, Jaap
Hartman, Catharina A
Franke, Barbara
von Rhein, Daniel
Thissen, Andrieke J A M
Zwiers, Marcel P
Rommelse, Nanda
Author_xml – sequence: 1
  givenname: Daan
  surname: van Rooij
  fullname: van Rooij, Daan
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  givenname: Pieter J
  surname: Hoekstra
  fullname: Hoekstra, Pieter J
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  givenname: Maarten
  surname: Mennes
  fullname: Mennes, Maarten
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 4
  givenname: Daniel
  surname: von Rhein
  fullname: von Rhein, Daniel
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  givenname: Andrieke J A M
  surname: Thissen
  fullname: Thissen, Andrieke J A M
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  givenname: Dirk
  surname: Heslenfeld
  fullname: Heslenfeld, Dirk
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  givenname: Marcel P
  surname: Zwiers
  fullname: Zwiers, Marcel P
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 8
  givenname: Stephen V
  surname: Faraone
  fullname: Faraone, Stephen V
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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  surname: Oosterlaan
  fullname: Oosterlaan, Jaap
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 10
  givenname: Barbara
  surname: Franke
  fullname: Franke, Barbara
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 11
  givenname: Nanda
  surname: Rommelse
  fullname: Rommelse, Nanda
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 12
  givenname: Jan K
  surname: Buitelaar
  fullname: Buitelaar, Jan K
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
– sequence: 13
  givenname: Catharina A
  surname: Hartman
  fullname: Hartman, Catharina A
  organization: From the Department of Psychiatry, University Medical Center, University of Groningen, Groningen, the Netherlands; the Department of Cognitive Neuroscience, the Department of Psychiatry, and the Department of Human Genetics, Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Center Nijmegen, Nijmegen, the Netherlands; the Department of Psychology, VU University Amsterdam, Amsterdam, the Netherlands; and the Department of Psychiatry and the Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, N.Y
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Snippet Dysfunctional response inhibition is a key executive function impairment in attention deficit hyperactivity disorder (ADHD). Still, behavioral response...
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StartPage 674
SubjectTerms Adolescent
Attention - physiology
Attention Deficit Disorder with Hyperactivity - diagnosis
Attention Deficit Disorder with Hyperactivity - genetics
Attention Deficit Disorder with Hyperactivity - physiopathology
Brain Mapping
Cerebral Cortex - physiopathology
Executive Function
Female
Follow-Up Studies
Humans
Impulsive Behavior - physiology
Inhibition (Psychology)
Magnetic Resonance Imaging
Male
Neuropsychological Tests
Psychomotor Performance - physiology
Reaction Time - physiology
Reference Values
Title Distinguishing Adolescents With ADHD From Their Unaffected Siblings and Healthy Comparison Subjects by Neural Activation Patterns During Response Inhibition
URI https://www.ncbi.nlm.nih.gov/pubmed/25615565
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