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Behavioural Treatment Increases Activity in the Cognitive Neuronal Networks in Children with Attention Deficit/Hyperactivity Disorder

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Abstract

Response cost and token approach (RCT) within the scope of a summer camp training is an effective treatment program for attention deficit hyperactivity disorder (ADHD). It is likely that intensive RCT training influences networks responsible for ADHD symptoms. Functional magnetic resonance imaging (fMRI) was carried out in 12 children with ADHD before and after the RCT program and in 12 healthy control children twice. For fMRI, a Go/No-go paradigm was used to investigate the influence of RCT training on attention and impulsivity. The No-go condition revealed only weak activation in the dorsal part of the anterior cingulate cortex (ACC), parietal and dorsolateral prefrontal cortex (DLPFC) before the training in children with ADHD compared to healthy children. However, this activation in these brain regions was significantly more pronounced after the training. This increase in hemodynamic response cannot be attributed merely to repetition of the measurement since the effect was not observed in healthy children. The increase in hemodynamic response in the ACC and right DLPFC was significantly associated with a reduction in response time variability and clinical symptoms in ADHD patients. After the RCT training, the children with ADHD demonstrated more pronounced activation of cortical structures which are typically related to response monitoring and self-control. It seems likely that children with ADHD learned more cognitive control in a continuous performance task as was revealed by both neuropsychological outcome and fMRI.

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References

  • American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington

    Google Scholar 

  • Aron AR, Poldrack RA (2005) The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1285–1292

    Article  PubMed  Google Scholar 

  • Aron AR, Gluck MA, Poldrack RA (2006) Long-term test-retest reliability of functional MRI in a classification learning task. NeuroImage 29:1000–1006

    Article  PubMed  Google Scholar 

  • Banaschewski T, Brandeis D (2007) Annotation: what electrical brain activity tells us about brain function that other techniques cannot tell us-a child psychiatric perspective. J Child Psychol Psychiatry 48:415–435

    Article  PubMed  Google Scholar 

  • Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94

    Article  PubMed  CAS  Google Scholar 

  • Beauregard M, Levesque J (2006) Functional magnetic resonance imaging investigation of the effects of neurofeedback training on the neural bases of selective attention and response inhibition in children with attention-deficit/hyperactivity disorder. Appl Psychophysiol Biofeedback 31:3–20

    Article  PubMed  Google Scholar 

  • Biederman J, Faraone SV (2005) Attention-deficit hyperactivity disorder. Lancet 366:237–248

    Article  PubMed  Google Scholar 

  • Booth JR, Burman DD, Meyer JR, Lei Z, Trommer BL, Davenport ND, Li W, Parrish TB, Gitelman DR, Mesulam MM (2005) Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). J Child Psychol Psychiatry 46:94–111

    Article  PubMed  Google Scholar 

  • Broshek DK, Jeffrey TB (2000) The halstead-reitan neuropsychological test battery. In: Groth-Marnat G (ed) Neuropsychological assessment in clinical practice: a guide to test interpretation and integration. Wiley, New York

    Google Scholar 

  • Bush G, Spencer TJ, Holmes J, Shin LM, Valera EM, Seidman LJ, Makris N, Surman C, Aleardi M, Mick E, Biederman J (2008) Functional magnetic resonance imaging of methylphenidate and placebo in attention-deficit/hyperactivity disorder during the multi-source interference task. Arch Gen Psychiatry 65:102–114

    Article  PubMed  CAS  Google Scholar 

  • Castellanos FX, Sonuga-Barke EJ, Scheres A, Di Martino A, Hyde C, Walters JR (2005) Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biol Psychiatry 57:1416–1423

    Article  PubMed  Google Scholar 

  • Chamberlain SR, Hampshire A, Muller U, Rubia K, Del Campo N, Craig K, Regenthal R, Suckling J, Roiser JP, Grant JE, Bullmore ET, Robbins TW, Sahakian BJ (2009) Atomoxetine modulates right inferior frontal activation during inhibitory control: a pharmacological functional magnetic resonance imaging study. Biol Psychiatry 65:550–555

    Article  PubMed  CAS  Google Scholar 

  • Chein JM, Schneider W (2005) Neuroimaging studies of practice-related change: fMRI and meta-analytic evidence of a domain-general control network for learning. Brain Res Cogn Brain Res 25:607–623

    Article  PubMed  Google Scholar 

  • Crosbie J, Perusse D, Barr CL, Schachar RJ (2008) Validating psychiatric endophenotypes: inhibitory control and attention deficit hyperactivity disorder. Neurosci Biobehav Rev 32:40–55

    Article  PubMed  Google Scholar 

  • Desman C, Petermann F, Hampel P (2008) Deficit in response inhibition in children with attention deficit/hyperactivity disorder (ADHD): impact of motivation? Child Neuropsychol 14:483–503

    Article  PubMed  Google Scholar 

  • Dillo W, Goke A, Prox-Vagedes V, Szycik GR, Roy M, Donnerstag F, Emrich HM, Ohlmeier MD (2010) Neuronal correlates of ADHD in adults with evidence for compensation strategies—a functional MRI study with a Go/No-Go paradigm. Ger Med Sci 8:1–8

    Google Scholar 

  • Dodds CM, Muller U, Clark L, van Loon A, Cools R, Robbins TW (2008) Methylphenidate has differential effects on blood oxygenation level-dependent signal related to cognitive subprocesses of reversal learning. J Neurosci 28:5976–5982

    Article  PubMed  CAS  Google Scholar 

  • Döpfner M, Breuer D, Schurmann S, Metternich TW, Rademacher C, Lehmkuhl G (2004) Effectiveness of an adaptive multimodal treatment in children with attention-deficit hyperactivity disorder—global outcome. Eur Child Adolesc Psychiatry 13(Suppl 1):I117–I129

    PubMed  Google Scholar 

  • Durston S, Mulder M, Casey BJ, Ziermans T, van Engeland H (2006) Activation in ventral prefrontal cortex is sensitive to genetic vulnerability for attention-deficit hyperactivity disorder. Biol Psychiatry 60:1062–1070

    Article  PubMed  CAS  Google Scholar 

  • Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25:1325–1335

    Article  PubMed  Google Scholar 

  • Epstein JN (2009) A pathophysiology of attention deficit/hyperactivity disorder: clues from neuroimaging. In: Rumsey JM, Ernst M (eds) NeuroImaging in developmental clinical neuroscience. Cambridge University Press, Cambridge, pp 113–129

    Chapter  Google Scholar 

  • Fliessback K, Rohe T, Linder NS, Trautner P, Elger CE, Weber B (2010) Retest reliability of reward-related BOLD signals. NeuroImage 50:1168–1176

    Article  Google Scholar 

  • Freyer T, Valerius G, Kuelz AK, Speck O, Glauche V, Hull M, Voderholzer U (2009) Test-retest reliability of event-related functional MRI in a probabilistic reversal learning task. Psychiatry Res 174:40–46

    Article  PubMed  Google Scholar 

  • Freyer T, Klöppel S, Tüscher O, Kordon A, Zurowski B, Kuelz AK, Speck O, Glauche V, Voderholzer U (2011) Frontostriatal activation in patients with obsessive-compulsive disorder before and after cognitive behavioral therapy. Psychol Med 41:207–216

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Holmes AP, Worsley KP (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Map 2:189–210

    Article  Google Scholar 

  • Gerber WD, Gerber-von Müller G, Petermann U, Niederberger U, Siniatchkin M (2011) Effectiveness of a multimodal behavioral summer camp program for attention deficit/hyperactivity disorder. The impact on neuropsychological functioning. Child Neuropsychol [Epub ahead of print]

  • Gerber-von Müller G, Petermann U, Petermann F, Niederberger U, Stephani U, Siniatchkin M, Gerber W-D (2009) Das ADHS-summer camp–Entwicklung und evaluation eines multimodalen programms. Kindheit und Entwicklung 18:162–172

    Article  Google Scholar 

  • Görtz A, Döpfner M, Nowak A, Bonus B, Lehmkuhl G (2002) Ist das Selbsturteil Jugendlicher bei der Diagnostik von Aufmerksamkeitsdefizit-/Hyperaktivitätsstörungen hilfreich? Eine Analyse mit dem Diagnostiksystem DISYPS. Kindheit und Entwicklung 11:82–89

    Article  Google Scholar 

  • Hoezema E, Carmona S, Tremols V, Gispert JD, Guilart M, Fauquet J et al (2010) Enhanced neural activity in frontal and cerebellar circuits after cognitive training in children with attention-deficit/hyperactivity disorder. Hum Brain Map 31:1945–1950

    Google Scholar 

  • Huyser C, Veltman DJ, Wolters LH, de Haan E, Boer F (2001) Developmental aspects of error and high-conflict-related brain activity in pediatric obsessive-compulsive disorder: a fMRI study with a Flanker task before and after CBT. J Child Psychol Psychiatry 52:1251–1260

    Article  Google Scholar 

  • Jäncke L, Cheetham M, Baumgartner T (2009) Virtual reality and the role of the prefrontal cortex in adults and children. Front Neurosci 3:52–59

    Article  PubMed  Google Scholar 

  • Kelly AM, Garavan H (2005) Human functional neuroimaging of brain changes associated with practice. Cereb Cortex 15:1089–1102

    Article  PubMed  Google Scholar 

  • Klein C, Wendling K, Huettner P, Ruder H, Peper M (2006) Intra-subject variability in attention-deficit hyperactivity disorder. Biol Psychiatry 60:1088–1097

    Article  PubMed  Google Scholar 

  • Kooistra L, van der Meere JJ, Edwards JD, Kaplan BJ, Crawford S, Goodyear BG (2010) Preliminary fMRI findings on the effects of event rate in adults with ADHD. J Neural Transm 117:655–662

    Article  PubMed  Google Scholar 

  • Kutcher S, Aman M, Brooks SJ, Buitelaar J, van Daalen E, Fegert J, Findling RL, Fisman S, Greenhill LL, Huss M, Kusumakar V, Pine D, Taylor E, Tyano S (2004) International consensus statement on attention-deficit/hyperactivity disorder (ADHD) and disruptive behaviour disorders (DBDs): clinical implications and treatment practice suggestions. Eur Neuropsychopharmacol 14:11–28

    Article  PubMed  CAS  Google Scholar 

  • Langberg JM, Epstein JN, Graham AJ (2008) Organizational-skills interventions in the treatment of ADHD. Expert Rev Neurother 8:1549–1561

    Article  PubMed  Google Scholar 

  • Levesque J, Beauregard M, Mensour B (2006) Effect of neurofeedback training on the neural substrates of selective attention in children with attention-deficit/hyperactivity disorder: a functional magnetic resonance imaging study. Neurosci Lett 394:216–221

    Article  PubMed  CAS  Google Scholar 

  • Loubinoux I, Carel C, Alary F, Boulanouar K, Viallard G, Manelfe C, Rascol O, Celsis P, Chollet F (2001) Within-session and between-session reproducibility of cerebral sensorimotor activation: a test–retest effect evidenced with functional magnetic resonance imaging. J Cereb Blood Flow Metab 21:592–607

    Article  PubMed  CAS  Google Scholar 

  • Melcher T, Falkai P, Gruber O (2008) Functional brain abnormalities in psychiatric disorders: neural mechanisms to detect and resolve cognitive conflict and interference. Brain Res Rev 59:96–124

    Article  PubMed  Google Scholar 

  • Nigg JT, Casey BJ (2005) An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neurosciences. Dev Psychopathol 17:785–806

    PubMed  Google Scholar 

  • Northup J, Fusilier I, Swanson V, Huete J, Bruce T, Freeland J, Gulley V, Edwards S (1999) Further analysis of the separate and interactive effects of methylphenidate and common classroom contingencies. J Appl Behav Anal 32:35–50

    Article  PubMed  CAS  Google Scholar 

  • Passarotti AM, Sweeney JA, Pavuluri MN (2010) Neural correlates of response inhibition in pediatric bipolar disorder and attention deficit hyperactivity disorder. Psychiatry Res 181:36–43

    Article  PubMed  Google Scholar 

  • Pelham WE, Greiner AR, Gnagy EM (1997) Children’s summer treatment program manual. Comprehensive Treatment for Attention Deficit Disorder, Inc., Buffalo

    Google Scholar 

  • Posner MI, Rothbart MK, Sheese BE, Tang Y (2007) The anterior cingulate gyrus and the mechanism of self-regulation. Cogn Affect Behav Neurosci 7:391–395

    Article  PubMed  Google Scholar 

  • Reitman D, Hupp SD, O’Callaghan PM, Gulley V, Northup J (2001) The influence of a token economy and methylphenidate on attentive and disruptive behavior during sports with ADHD-diagnosed children. Behav Modif 25:305–323

    Article  PubMed  CAS  Google Scholar 

  • Rubia K, Overmeyer S, Taylor E, Brammer M, Williams SC, Simmons A, Bullmore ET (1999) Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am J Psychiatry 156:891–896

    PubMed  CAS  Google Scholar 

  • Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E (2005) Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry 162:1067–1075

    Article  PubMed  Google Scholar 

  • Rubia K, Smith AB, Brammer MJ, Taylor E (2007a) Temporal lobe dysfunction in medication-naïve boys with attention-deficit/hyperactivity disorder during attention allocation and its relation to response variability. Biol Psychiatry 62:999–1006

    Article  PubMed  Google Scholar 

  • Rubia K, Smith A, Taylor E (2007b) Performance of children with attention deficit hyperactivity disorder (ADHD) on a test battery of impulsiveness. Child Neuropsychol 13:276–304

    Article  PubMed  Google Scholar 

  • Rubia K, Halari R, Cubillo A, Mohammad AM, Brammer M, Taylor E (2009) Methylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naive children with ADHD during a rewarded continuous performance task. Neuropharmacology 57:640–652

    Article  PubMed  CAS  Google Scholar 

  • Sergeant JA, Geurts H, Oosterlaan J (2002) How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder? Behav Brain Res 130:3–28

    Article  PubMed  Google Scholar 

  • Smith AB, Taylor E, Brammer M, Toone B, Rubia K (2006) 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. Am J Psychiatry 163:1044–1051

    Article  PubMed  Google Scholar 

  • Solanto MV, Schulz KP, Fan J, Tang CY, Newcorn JH (2009) Event-related FMRI of inhibitory control in the predominantly inattentive and combined subtypes of ADHD. J Neuroimaging 19:205–212

    Article  PubMed  Google Scholar 

  • Suskauer SJ, Simmonds DJ, Caffo BS, Denckla MB, Pekar JJ, Mostofsky SH (2008) fMRI of intrasubject variability in ADHD: anomalous premotor activity with prefrontal compensation. J Am Acad Child Adolesc Psychiatry 47:1141–1150

    Article  PubMed  Google Scholar 

  • Tamm L, Carlson CL (2007) Task demands interact with the single and combined effects of medication and contingencies on children with ADHD. J Atten Disord 10:372–380

    Article  PubMed  Google Scholar 

  • Tamm L, Menon V, Ringel J, Reiss AL (2004) Event-related FMRI evidence of frontotemporal involvement in aberrant response inhibition and task switching in attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 43:1430–1440

    Article  PubMed  Google Scholar 

  • Toplak ME, Connors L, Shuster J, Knezevic B, Parks S (2008) Review of cognitive, cognitive-behavioral, and neural-based interventions for attention-deficit/hyperactivity disorder (ADHD). Clin Psychol Rev 28:801–823

    Article  PubMed  Google Scholar 

  • Toussaint A, Petermann F, Schmidt S, Petermann U, Gerber-von Müller G, et al. (2011) Effectiveness of behavioral therapy on attention regulation and executive functioning in children and adolescents with ADHD. Zeitschrift Psychiatrie Psychologie und Psychotherapie 59:25–36

    Google Scholar 

  • Uebel H, Albrecht B, Asherson P, Borger NA, Butler L, Chen W, Christiansen H, Heise A, Kuntsi J, Schafer U, Andreou P, Manor I, Marco R, Miranda A, Mulligan A, Oades RD, van der Meere J, Faraone SV, Rothenberger A, Banaschewski T (2010) Performance variability, impulsivity errors and the impact of incentives as gender-independent endophenotypes for ADHD. J Child Psychol Psychiatry 51:210–218

    Article  PubMed  Google Scholar 

  • Vaidya CJ, Austin G, Kirkorian G, Ridlehuber HW, Desmond JE, Glover GH, Gabrieli JD (1998) Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc Natl Acad Sci USA 95:14494–14499

    Article  PubMed  CAS  Google Scholar 

  • Vaurio RG, Simmonds DJ, Mostofsky SH (2009) Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands. Neuropsychologia 47:2389–2396

    Article  PubMed  Google Scholar 

  • Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57:1336–1346

    Article  PubMed  Google Scholar 

  • Wodka EL, Mahone EM, Blankner JG, Larson JC, Fotedar S, Denckla MB, Mostofsky SH (2007) Evidence that response inhibition is a primary deficit in ADHD. J Clin Exp Neuropsychol 29:345–356

    Article  PubMed  Google Scholar 

  • Yoo SS, O’Leary HM, Lee JH, Chen NK, Panych LP, Jolesz FA (2007) Reproducibility of trial-based functional MRI on motor imagery. Int J Neurosci 117:215–227

    Article  PubMed  Google Scholar 

  • Zandbelt BB, Gladwin TE, Raemaekers M, van Buuren M, Neggers SF, Kahn RS, Ramsey NF, Vink M (2008) Within-subject variation in BOLD-fMRI signal changes across repeated measurements: quantification and implications for sample size. NeuroImage 42:196–206

    Article  PubMed  Google Scholar 

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Siniatchkin, M., Glatthaar, N., von Müller, G.G. et al. Behavioural Treatment Increases Activity in the Cognitive Neuronal Networks in Children with Attention Deficit/Hyperactivity Disorder. Brain Topogr 25, 332–344 (2012). https://doi.org/10.1007/s10548-012-0221-6

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