BACKGROUND: Attention-deficit hyperactivity disorder (ADHD) is linked to the presence of motor deficiencies, including balance deficits. The cerebellum serves as an integrative structure for balance control and is also involved in cognition, including timing and anticipatory regulation. Cerebellar development may be delayed in children and adolescents with ADHD, and inconsistent reaction time is commonly seen in ADHD. We hypothesized that dynamic balance deficits would be present in children with ADHD and they would correlate with attention and cerebellar functions. METHODS: Sixty-two children with ADHD and no other neurological conditions and 62 typically developing (TD) children were examined with five trials of the Phyaction Balance Board, an electronic balancing platform. Cerebellar clinical symptoms were evaluated using an international ataxia rating scale. Conners' Continuous Performance Test was used to evaluate patterns of reaction. RESULTS: Children with ADHD had poorer performance on balancing tasks, compared to TD children (P<0.001). They exhibited significantly greater sway amplitudes than TD children (P<0.001) in all of the five balancing trials. The effect size of the difference between the groups increased continuously from the first to the last trial. Balance score in both groups was related to the variation in the reaction time, including reaction time standard error (r =0.25; P=0.0409, respectively, r =0.31; P=0.0131) and Variability of Standard Error (r =0.28; P=0.0252, respectively, r =0.41; P<0.001). The burden of cerebellar symptoms was strongly related to balance performance in both groups (r =0.50, P<0.001; r =0.49, P=0.001). CONCLUSION: This study showed that ADHD may be associated with poor dynamic balance control. Furthermore, we showed that maintaining balance correlates with neuropsychological measures of consistency of reaction time. Balance deficits and impaired cognitive functioning could reflect a common cerebellar dysfunction in ADHD children.

Department of Child Psychiatry 2nd Faculty of Medicine Motol University Hospital

Department of Neurology

Department of Psychiatry Charles University Prague Czech Republic

Department of Psychiatry Harvard Medical School Boston MA USA

Department of Statistics

Zobrazit více v PubMed

Landgren MM, Pettersson RR, Kjellman BB, Gillberg CC. ADHD, DAMP and other neurodevelopmental/psychiatric disorders in 6-year-old children: epidemiology and co-morbidity. Dev Med Child Neurol. 1996;38(10):891–906. PubMed

Udal AH, Malt UF, Lövdahl H, Gjaerum B, Pripp AH, Groholt B. Motor function may differentiate attention deficit hyperactivity disorder from early onset bipolar disorder. Behav Brain Funct. 2009;5(1):47. PubMed PMC

Gustafsson P, Svedin CG, Ericsson I, Lindén C, Karlsson MK, Thernlund G. Reliability and validity of the assessment of neurological soft-signs in children with and without attention-deficit-hyperactivity disorder. Dev Med Child Neurol. 2010;52(4):364–370. PubMed

Ferrin M, Vance A. Examination of neurological subtle signs in ADHD as a clinical tool for the diagnosis and their relationship to spatial working memory. J Child Psychol Psychiatry. 2011;53(4):390–400. PubMed

Konicarova J, Bob P, Raboch J. Persisting primitive reflexes in medication-naïve girls with attention-deficit and hyperactivity disorder. Neuropsychiatr Dis Treat. 2013;9:1457–1461. PubMed PMC

Buderath P, Gärtner K, Frings M, et al. Postural and gait performance in children with attention deficit/hyperactivity disorder. Gait Posture. 2009;29(2):249–254. PubMed

Konicarova J, Bob P, Raboch J. Balance deficits and ADHD symptoms in medication-naïve school-aged boys. Neuropsychiatr Dis Treat. 2014;10:85–88. PubMed PMC

Jacobi-Polishook T, Shorer Z, Melzer I. The effect of methylphenidate on postural stability under single and dual task conditions in children with attention deficit hyperactivity disorder – a double blind randomized control trial. J Neurol Sci. 2009;280(1–2):15–21. PubMed

Ghanizadeh A. Predictors of postural stability in children with ADHD. J Atten Disord. 2011;15(7):604–610. PubMed

Goetz M, Schwabova J, Hlavka Z, et al. Cerebellar symptoms are associated with omission errors and variability of response time in children with ADHD. J Atten Disord. 2017;21(3):190–199. PubMed

Mao H-Y, Kuo L-C, Yang A-L, Su C-T. Research in developmental disabilities balance in children with attention deficit hyperactivity disorder-combined type. Res Dev Disabil. 2014;35(6):1252–1258. PubMed

Hove MJ, Zeffiro TA, Biederman J, Li Z, Schmahmann J, Valera EM. Postural sway and regional cerebellar volume in adults with attention-deficit/hyperactivity disorder. Neuroimage Clin. 2015;8(C):422–428. PubMed PMC

Shilon Y, Pollak Y, Aran A, Shaked S, Gross-Tsur V. Accidental injuries are more common in children with attention deficit hyperactivity disorder compared with their non-affected siblings. Child Care Health Dev. 2012;38(3):366–370. PubMed

Kang J-H, Lin H-C, Chung S-D. Attention-deficit/hyperactivity disorder increased the risk of injury: a population-based follow-up study. Acta Paediatr. 2013;102(6):640–643. PubMed

Ren Y, Yu L, Yang L, Cheng J, Feng L, Wang Y. Postural control and sensory information integration abilities of boys with two subtypes of attention deficit hyperactivity disorder: a case-control study. Chin Med J. 2014;127(24):4197–4203. PubMed

Winter DA, Patla AE, Frank JS. Assessment of balance control in humans. Med Prog Technol. 1990;16(1–2):31–51. PubMed

Mostofsky SH, Reiss AL, Lockhart P, Denckla MB. Evaluation of cerebellar size in attention-deficit hyperactivity disorder. J Child Neurol. 1998;13(9):434–439. PubMed

Castellanos FX, Lee PP, Sharp W, et al. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA. 2002;288(14):1740–1748. PubMed

Bussing R, Grudnik J, Mason D, Wasiak M, Leonard C. ADHD and conduct disorder: an MRI study in a community sample. World J Biol Psychiatry. 2002;3(4):216–220. PubMed

Hill DE, Yeo RA, Campbell RA, Hart B, Vigil J, Brooks W. Magnetic resonance imaging correlates of attention-deficit/hyperactivity disorder in children. Neuropsychology. 2003;17(3):496–506. PubMed

Bledsoe J, Semrud-Clikeman M, Pliszka SR. A magnetic resonance imaging study of the cerebellar vermis in chronically treated and treatment-naïve children with attention-deficit/hyperactivity disorder combined type. Biol Psychiatry. 2009;65(7):620–624. PubMed PMC

Bledsoe JC, Semrud-Clikeman M, Pliszka SR. Neuroanatomical and neuropsychological correlates of the cerebellum in children with attention-deficit/hyperactivity disorder–combined type. J Am Acad Child Adolesc Psychiatry. 2011;50(6):593–601. PubMed PMC

Koziol LF, Budding D, Andreasen N, et al. Consensus paper: the cerebellum’s role in movement and cognition. Cerebellum. 2014;13(1):151–177. PubMed PMC

Ogg RJ, Zou P, Allen DN, Hutchins SB, Dutkiewicz RM, Mulhern RK. Neural correlates of a clinical continuous performance test. Magn Reson Imaging. 2008;26(4):504–512. PubMed

Tana MG, Montin E, Cerutti S, Bianchi AM. Exploring cortical attentional system by using fMRI during a Continuous Perfomance Test. Comput Intell Neurosci. 2010 PubMed PMC

Gadow KD, Sprafkin JN. Child Symptom Inventory 4: Screening and Norms Manual. Stony Brook, NY: Checkmate Plus; 2002. p. 179.

Ondrejka I, Abali O, Paclt I, et al. A prospective observational study of attention-deficit/hyperactivity disorder in Central and Eastern Europe and Turkey: symptom severity and treatment options in a paediatric population. Int J Psychiatry Clin Pract. 2010;14(2):116–126. PubMed

Goetz M, Yeh CB, Ondrejka I, et al. A 12-month prospective, observational study of treatment regimen and quality of life associated with ADHD in Central and Eastern Europe and eastern Asia. J Atten Disord. 2012;16(1):44–59. PubMed

American Psychological Association . Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: 1994.

Zang Y, Gu B, Qian Q, Wang Y. Objective measurement of the balance dysfunction in attention deficit hyperactivity disorder children. Chin J Clin Rehabil. 2002;6:1372–1374.

Trouillas P, Takayanagi T, Hallett M, et al. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharmacology Committee of the World Federation of Neurology. J Neurol Sci. 1997;145(2):205–211. PubMed

Schmitz-Hübsch T, Tezenas du Montcel S, Baliko L, et al. Reliability and validity of the International Cooperative Ataxia Rating Scale: a study in 156 spinocerebellar ataxia patients. Mov Disord. 2006;21(5):699–704. PubMed

Storey E, Tuck K, Hester R, et al. Inter-rater reliability of the International Cooperative Ataxia Rating Scale (ICARS) Mov Disord. 2004;19(2):190–192. PubMed

Frings M, Gaertner K, Buderath P, et al. Megalographia in children with cerebellar lesions and in children with attention-deficit/hyperactivity disorder. Cerebellum. 2010;9(3):429–432. PubMed

Conners CK. Conners’ Continuous Performance Test (CPT II): Version 5 for Windows: Technical Guide and SoftWare Manual. Toronto, ON: Multi Health Systems; 2004.

R Development Core Team . R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.

Castellanos FX, Tannock R. Neuroscience of attention deficit/hyperactivity disorder: the search for endophenotypes. Nat Rev Neurosci. 2002;3(8):617–628. PubMed

Leth-Steensen C, Elbaz ZK, Douglas VI. Mean response times, variability, and skew in the responding of ADHD children: a response time distributional approach. Acta Psychol (Amst) 2000;104(2):167–190. PubMed

Sonuga-Barke EJS, Castellanos FX. Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci Biobehav Rev. 2007;31(7):977–986. PubMed

Fair DA, Nigg JT, Iyer S, et al. Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Front Syst Neurosci. 2013;4(6):80. PubMed PMC

Ghajar J, Ivry RB. The predictive brain state: asynchrony in disorders of attention? Neuroscientist. 2009;15(3):232–242. PubMed PMC

Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2(9):338–347. PubMed

Imamizu H, Kawato M. Brain mechanisms for predictive control by switching internal models: implications for higher-order cognitive functions. Psychol Res. 2009;73(4):527–544. PubMed

Ivanov I, Murrough JW, Bansal R, Hao X, Peterson BS. Cerebellar morphology and the effects of stimulant medications in youths with attention deficit-hyperactivity disorder. Neuropsychopharmacology. 2013;39(3):718–726. PubMed PMC

Berquin PC, Giedd JN, Jacobsen LK, et al. Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology. 1998;50(4):1087–1093. PubMed

Castellanos FXF, Giedd JNJ, Berquin PCP, et al. Quantitative brain magnetic resonance imaging in girls with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry. 2001;58(3):289–295. PubMed

Mackie SS, Shaw PW, Lenroot RR, et al. Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am J Psychiatry. 2007;164(4):647–655. PubMed

Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501. PubMed

Karalunas SL, Huang-Pollock CL, Nigg JT. Decomposing attention-deficit/hyperactivity disorder (ADHD)-related effects in response speed and variability. Neuropsychology. 2012;26(6):684–694. PubMed PMC

Manto M, Bower JM, Conforto AB, et al. Consensus paper: roles of the cerebellum in motor control – the diversity of ideas on cerebellar involvement in movement. Cerebellum. 2011;11(2):457–487. PubMed PMC

Hart H, Radua J, Mataix-Cols D, Rubia K. Meta-analysis of fMRI studies of timing in attention-deficit hyper-activity disorder (ADHD) Neurosci Biobehav Rev. 2012;36(10):2248–2256. PubMed

Akkal D, Dum RP, Strick PL. Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci. 2007;27(40):10659–10673. PubMed PMC

Mostofsky SH, Schafer JG, Abrams MT, et al. fMRI evidence that the neural basis of response inhibition is task-dependent. Brain Res Cogn Brain Res. 2003;17(2):419–430. PubMed

Suskauer SJ, Simmonds DJ, Caffo BS, Denckla MB, Pekar JJ, Mostofsky SH. fMRI of intrasubject variability in ADHD: anomalous premotor activity with prefrontal compensation. J Am Acad Child Adolesc Psychiatry. 2008;47(10):1141–1150. PubMed PMC

Rucklidge JJ. Gender differences in attention-deficit/hyperactivity disorder. Psychiatr Clin North Am. 2010;33(2):357–373. PubMed

Ghezzo A, Guerini FR, Bolognesi E, et al. Neuropsycological gender differences in healthy individuals and in pediatric neurodevelopmental disorders. A role for SNAP-25. Med Hypotheses. 2009;73(6):978–980. PubMed

Chiappedi M, Togni R, De Bernardi E, et al. Arm trajectories and writing strategy in healthy children. BMC Pediatr. 2012;7(12):173. PubMed PMC

Bonati M, Reale L, Zanetti M, et al. Lombardy ADHD Group A regional ADHD center-based network project for the diagnosis and treatment of children and adolescents with ADHD. J Atten Disord. 2015 Aug 28; Epub. pii: 1087054715599573. PubMed

Clinical Implications of the Perception of Time in Attention Deficit Hyperactivity Disorder (ADHD): A Review