Dynamic balance in children with attention-deficit hyperactivity disorder and its relationship with cognitive functions and cerebellum

Michal Goetz, Jaroslava Paulasova Schwabova, Zdenek Hlavka, Radek Ptacek, Craig Bh Surman, Michal Goetz, Jaroslava Paulasova Schwabova, Zdenek Hlavka, Radek Ptacek, Craig Bh Surman

Abstract

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.

Keywords: attention-deficit hyperactivity disorder; balance; cerebellum; reaction time.

Conflict of interest statement

Disclosure Dr Goetz serves as a speaker for Eli Lilly CR. Dr Surman reports that since the last year, he has been a consultant to Ironshore, Rhodes, and Shire; has presented educational lectures for Neos, Graduate Medical Education Continuing Medical Education (CME), and Massachusetts General Hospital (MGH) Academy; and has received research support from Neurocentria, Pamlab, and Shire. He also reports receiving royalties for Fast Minds: How to Thrive If You Have ADHD (Or Think You Might) and ADHD in Adults: A Practical Guide to Evaluation and Management. Dr Schwabova, Dr Hlavka, and Dr Ptacek report no conflicts of interest in this work.

Figures

Figure 1
Figure 1
Laterolateral balance measures. Notes:aThe sum of the area, which is defined by the path of a point oscillating from the imaginary center and a line bisecting the center. Higher number means worse performance. bTrial on the balance platform. Significance code: ***P<0.001. Abbreviations: ADHD, Attention-deficit hyperactivity disorder; TD, typically developing.

References

    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. Konicarova J, Bob P, Raboch J. Balance deficits and ADHD symptoms in medication-naïve school-aged boys. Neuropsychiatr Dis Treat. 2014;10:85–88.
    1. 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.
    1. Ghanizadeh A. Predictors of postural stability in children with ADHD. J Atten Disord. 2011;15(7):604–610.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. Winter DA, Patla AE, Frank JS. Assessment of balance control in humans. Med Prog Technol. 1990;16(1–2):31–51.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. Koziol LF, Budding D, Andreasen N, et al. Consensus paper: the cerebellum’s role in movement and cognition. Cerebellum. 2014;13(1):151–177.
    1. 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.
    1. Tana MG, Montin E, Cerutti S, Bianchi AM. Exploring cortical attentional system by using fMRI during a Continuous Perfomance Test. Comput Intell Neurosci. 2010
    1. Gadow KD, Sprafkin JN. Child Symptom Inventory 4: Screening and Norms Manual. Stony Brook, NY: Checkmate Plus; 2002. p. 179.
    1. 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.
    1. 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.
    1. American Psychological Association . Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: 1994.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. Conners CK. Conners’ Continuous Performance Test (CPT II): Version 5 for Windows: Technical Guide and SoftWare Manual. Toronto, ON: Multi Health Systems; 2004.
    1. R Development Core Team . R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
    1. Castellanos FX, Tannock R. Neuroscience of attention deficit/hyperactivity disorder: the search for endophenotypes. Nat Rev Neurosci. 2002;3(8):617–628.
    1. 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.
    1. 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.
    1. 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.
    1. Ghajar J, Ivry RB. The predictive brain state: asynchrony in disorders of attention? Neuroscientist. 2009;15(3):232–242.
    1. Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2(9):338–347.
    1. 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.
    1. 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.
    1. Berquin PC, Giedd JN, Jacobsen LK, et al. Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology. 1998;50(4):1087–1093.
    1. 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.
    1. 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.
    1. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. 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.
    1. Rucklidge JJ. Gender differences in attention-deficit/hyperactivity disorder. Psychiatr Clin North Am. 2010;33(2):357–373.
    1. 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.
    1. Chiappedi M, Togni R, De Bernardi E, et al. Arm trajectories and writing strategy in healthy children. BMC Pediatr. 2012;7(12):173.
    1. 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.

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