A bimodal neurophysiological study of motor control in attention-deficit hyperactivity disorder: A step towards core mechanisms?

Brain

Volumn 137, Issue 4, 2014, Pages 1156-1166

  Heinrich, Hartmut ^a,b   Hoegl, Thomas ^a   Moll, Gunther H ^a   Kratz, Oliver ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b Heckscher Klinikum   (Germany)

Author keywords

attention deficit hyperactivity disorder; correlational analysis; event related potentials; motor control; transcranial magnetic stimulation

Indexed keywords

ADOLESCENT; ARTICLE; ASSOCIATION; ATTENTION DEFICIT DISORDER; CHILD; CLINICAL ARTICLE; COGNITION; CONTINGENT NEGATIVE VARIATION; CONTROLLED STUDY; DISCRIMINANT ANALYSIS; EVENT RELATED POTENTIAL; EXCITABILITY; FEMALE; HUMAN; INHIBITION (PSYCHOLOGY); INTERNEURON; MALE; MOTOR CONTROL; MOTOR CORTEX; NEUROPHYSIOLOGY; PRIORITY JOURNAL; REACTION TIME; REST; SCHOOL CHILD; TASK PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION; EVOKED RESPONSE; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADOLESCENT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CHILD; EVOKED POTENTIALS; FEMALE; HUMANS; MALE; MOTOR ACTIVITY; REACTION TIME; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84897850619     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu029     Document Type: Article

References (63)

1. Albrecht B, Brandeis D, Uebel H, Valko L, Heinrich H, Drechsler R, et al. Familiality of neural preparation and response control in childhood attention deficit-hyperactivity disorder. Psychol Med 2013; 43: 1997-2011.
2. Bacci A, Huguenard JR, Prince DA. Modulation of neocortical inter-neurons: extrinsic influences and exercises in self-control. Trends Neurosci 2005; 28: 602-10.
3. Banaschewski T, Brandeis D. Annotation: what electrical brain activity tells us about brain function that other techniques cannot tell us-a child psychiatric perspective. J Child Psychol Psychiatry 2007; 48: 415-35.
4. Banaschewski T, Brandeis D, Heinrich H, Albrecht B, Brunner E, Rothenberger A. Association of ADHD and conduct disorder-brain electrical evidence for the existence of a distinct subtype. J Child Psychol Psychiatry 2003; 44: 356-76.
5. Banaschewski T, Hollis C, Oosterlaan J, Roeyers H, Rubia K, Willcutt E, et al. Towards an understanding of unique and shared pathways in the psychopathophysiology of ADHD. Dev Sci 2005; 8: 132-40.
6. Bansal R, Staib LH, Laine AF, Hao X, Xu D, Liu J, et al. Anatomical brain images alone can accurately diagnose chronic neuropsychiatric illnesses. PLoS One 2012; 7: e50698.
7. Barkley RA. Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 1997; 121: 65-94.
8. Beste C, Dziobek I, Hielscher H, Willemssen R, Falkenstein M. Effects of stimulus-response compatibility on inhibitory processes in Parkinson's disease. Eur J Neurosci 2009; 29: 855-60.
9. Brandeis D, Banaschewski T, Baving L, Georgiewa P, Blanz B, Warnke A, et al. Multicenter P300 brain mapping of impaired attention to cues in hyperkinetic children. J Am Acad Child Adolesc Psychiatry 2002; 41: 990-8.
10. Brookes K, Xu X, Chen W, Zhou K, Neale B, Lowe N, et al. The analysis of 51 genes in DSM-IV combined type attention deficit hyperactivity disorder: association signals in DRD4, DAT1 and 16 other genes. Mol Psychiatry 2006; 11: 934-53.
11. Buchmann J, Gierow W, Weber S, Hoeppner J, Klauer T, Benecke R, et al. Restoration of disturbed intracortical motor inhibition and facilitation in attention deficit hyperactivity disorder children by methyl-phenidate. Biol Psychiatry 2007; 62: 963-9.
12. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, et al. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 2002; 288: 1740-8.
13. Castellanos FX, Tannock R. Neuroscience of attention-deficit/hyperactiv- ity disorder: the search for endophenotypes. Nat Rev Neurosci 2002; 3: 617-28.
14. Constantinidis C, Williams GV, Goldman-Rakic PS. A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 2002; 5: 175-80.
15. Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, et al. Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. Am J Psychiatry 2012; 169: 1038-55.
16. Del Campo N, Chamberlain SR, Sahakian BJ, Robbins TW. The roles of dopamine and noradrenaline in the pathophysiology and treatment of attention-deficit/hyperactivity disorder. Biol Psychiatry 2011; 69: e145-57.
17. Doehnert M, Brandeis D, Schneider G, Drechsler R, Steinhausen HC. A neurophysiological marker of impaired preparation in an 11-year follow-up study of attention-deficit/hyperactivity disorder (ADHD). J Child Psychol Psychiatry 2012; 54: 260-70.
18. Döpfner M, Lehmkuhl G. DISYPS-KJ-Diagnostik-System für psychische Störungen im Kindes-und Jugendalter. Bern: Hans Huber; 2000.
19. Durston S, Van Belle J, De Zeeuw P. Differentiating fronto-striatal and fronto-cerebellar circuits in ADHD. Biol Psychiatry 2011; 69: 1178-84.
20. Edden RA, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH. Reduced GABA concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 2012; 69: 750-53.
21. Floeter MK, Rothwell JC. Releasing the brakes before pressing the gas pedal. Neurology 1999; 53: 664-5.
22. Gao WJ, Wang Y, Goldman-Rakic PS. Dopamine modulation of periso-matic and peridendritic inhibition in prefrontal cortex. J Neurosci 2003; 23: 1622-30.
23. Gilbert DL, Isaacs KM, Augusta M, Macneil LK, Mostofsky SH. Motor cortex inhibition: a marker of ADHD behavior and motor development in children. Neurology 2011; 76: 615-21.
24. Gilbert DL, Sallee FR, Zhang J, Lipps TD, Wassermann EM. Transcranial magnetic stimulation-evoked cortical inhibition: a consistent marker of attention-deficit/hyperactivity disorder scores in tourette syndrome. Biol Psychiatry 2005; 57: 1597-1600.
25. Gratton G, Coles MG, Donchin E. A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 1983; 55: 468-84.
26. Groom MJ, Scerif G, Liddle PF, Batty MJ, Liddle EB, Roberts KL, et al. Effects of motivation and medication on electrophysiological markers of response inhibition in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 2010; 67: 624-31.
27. Hart H, Radua J, Mataix-Cols D, Rubia K. Meta-analysis of fMRI studies of timing in attention-deficit hyperactivity disorder (ADHD). Neurosci Biobehav Rev 2012; 36: 2248-56.
28. Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. Arch Gen Psychiatry 2013; 70: 185-98.
29. Heinrich H, Dickhaus H, Rothenberger A, Heinrich V, Moll GH. Single-sweep analysis of event-related potentials by wavelet networks-methodological basis and clinical application. IEEE Trans Biomed Eng 1999; 46: 867-79.
30. Heise KF, Steven B, Liuzzi G, Thomalla G, Jonas M, Müller-Vahl K, et al. Altered modulation of intracortical excitability during movement preparation in Gilles de la Tourette syndrome. Brain 2010; 133: 580-90.
31. Hoegl T, Heinrich H, Albrecht B, Diruf M, Moll GH, Kratz O. Interplay of neuronal processes during response inhibition: results from a combined event-related potentials (ERPs)/transcranial magnetic stimulation (TMS): study on methylphenidate. Int J Psychophysiol 2011; 81: 99-106.
32. Hoegl T, Heinrich H, Barth W, Lösel F, Moll GH, Kratz O. Time course analysis of motor excitability in a response inhibition task according to the level of hyperactivity and impulsivity in children with ADHD. PLoS One 2012; 7: e46066.
33. Kratz O, Diruf MS, Studer P, Gierow W, Buchmann J, Moll GH, et al. Effects of methylphenidate on motor system excitability in a response inhibition task. Behav Brain Funct 2009; 5: 12.
34. Kratz O, Studer P, Barth W, Wangler S, Hoegl T, Heinrich H, et al. Seizure in a nonpredisposed individual induced by single-pulse tran-scranial magnetic stimulation. J ECT 2011a; 27: 48-50.
35. Kratz O, Studer P, Malcherek S, Erbe K, Moll GH, Heinrich H. Attentional processes in children with ADHD: an event-related potential study using the attention network test. Int J Psychophysiol 2011b; 81: 82-90.
36. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol 1993; 471: 501-19.
37. Liddle EB, Hollis C, Batty MJ, Groom MJ, Totman JJ, Liotti M, et al. Task-related default mode network modulation and inhibitory control in ADHD: effects of motivation and methylphenidate. J Child Psychol Psychiatry 2011; 52: 761-71.
38. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004; 5: 793-807.
39. Moll GH, Heinrich H, Trott GE, Wirth S, Bock N, Rothenberger A. Children with comorbid attention-deficit-hyperactivity disorder and tic disorder: evidence for additive inhibitory deficits within the motor system. Ann Neurol 2001; 49: 393-96.
40. Moll GH, Heinrich H, Trott G, Wirth S, Rothenberger A. Deficient intra-cortical inhibition in drug-naive children with attention-deficit hyper-activity disorder is enhanced by methylphenidate. Neurosci Lett 2000; 284: 121-5.
41. Moll GH, Heinrich H, Rothenberger A. Transcranial magnetic stimulation in child psychiatry: disturbed motor system excitability in hypermotoric syndromes. Dev Sci 2002; 5: 381-91.
42. Moll GH, Wischer S, Heinrich H, Tergau F, Paulus W, Rothenberger A. Deficient motor control in children with tic disorder: evidence from transcranial magnetic stimulation. Neurosci Lett 1999; 272: 37-40.
43. Nieuwenhuis S, Aston-Jones G, Cohen JD. Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychol Bull 2005; 131: 510-32.
44. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9: 97-113.
45. Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M, et al. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 2008; 586: 325-51.
46. Sara SJ, Bouret S. Orienting and reorienting: the locus coeruleus mediates cognition through arousal. Neuron 2012; 76: 130-41.
47. Sergeant JA. Modeling attention-deficit/hyperactivity disorder: a critical appraisal of the cognitive-energetic model. Biol Psychiatry 2005; 57: 1248-55.
48. Shaw P, Lerch J, Greenstein D, Sharp W, Clasen L, Evans A, et al. Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 2006; 63: 540-9.
49. Smith JL, Johnstone SJ, Barry RJ. Aiding diagnosis of attention-deficit/hyperactivity disorder and its subtypes: discriminant function analysis of event-related potential data. J Child Psychol Psychiatry 2003; 44: 1067-75.
50. Sohn YH, Wiltz K, Hallett M. Effect of volitional inhibition on cortical inhibitory mechanisms. J Neurophysiol 2002; 88: 333-8.
51. Solanto MV, Abikoff H, Sonuga-Barke E, Schachar R, Logan GD, Wigal T, 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. J Abnorm Child Psychol 2001; 29: 215-28.
52. Sonuga-Barke EJ. The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev 2003; 27: 593-604.
53. Sonuga-Barke E, Bitsakou P, Thompson M. Beyond the dual pathway model: evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2010; 49: 345-55.
54. Soto O, Valls-Solé J, Kumru H. Paired-pulse transcranial magnetic stimulation during preparation for simple and choice reaction time tasks. J Neurophysiol 2010; 104: 1392-1400.
55. Stinear CM, Coxon JP, Byblow WD. Primary motor cortex and movement prevention: where Stop meets Go. Neurosci Biobehav Rev 2009; 33: 662-73.
56. Thome J, Ehlis AC, Fallgatter AJ, Krauel K, Lange KW, Riederer P, et al. Biomarkers for attention-deficit/hyperactivity disorder (ADHD). A consensus report of the WFSBP task force on biological markers and the World Federation of ADHD. World J Biol Psychiatry 2012; 13: 379-400.
57. Uebel H, Albrecht B, Asherson P, Börger NA, Butler L, Chen W, et al. Performance variability, impulsivity errors and the impact of incentives as gender-independent endophenotypes for ADHD. J Child Psychol Psychiatry 2010; 51: 210-8.
58. Waldvogel D, van Gelderen P, Muellbacher W, Ziemann U, Immisch I, Hallett M. The relative metabolic demand of inhibition and excitation. Nature 2000; 406: 995-8.
59. Winterer G, Weinberger DR. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 2004; 27: 683-90.
60. Yordanova J, Albrecht B, Uebel H, Kirov R, Banaschewski T, Rothenberger A, et al. Independent oscillatory patterns determine performance fluctuations in children with attention deficit/hyperactivity disorder. Brain 2011; 134: 1740-50.
61. Yordanova J, Banaschewski T, Kolev V, Woerner W, Rothenberger A. Abnormal early stages of task stimulus processing in children with attention-deficit hyperactivity disorder-evidence from event-related gamma oscillations. Clin Neurophysiol 2001; 112: 1096-108.
62. Ziemann U, Paulus W, Rothenberger A. Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 1997a; 154: 1277-84.
63. Ziemann U, Tergau F, Bruns D, Baudewig J, Paulus W. Changes in human motor cortex excitability induced by dopaminergic and anti-dopaminergic drugs. Electroencephalogr Clin Neurophysiol 1997b; 105: 430-37.