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Defining the neuroanatomic basis of motor coordination in children and its relationship with symptoms of attention-deficit/hyperactivity disorder

Published online by Cambridge University Press:  10 June 2016

P. Shaw*
Affiliation:
Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Bethesda, MD, USA
D. Weingart
Affiliation:
Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Bethesda, MD, USA
T. Bonner
Affiliation:
Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Bethesda, MD, USA
B. Watson
Affiliation:
Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Bethesda, MD, USA
M. T. M. Park
Affiliation:
Schulich School of Medicine and Dentistry, Western University, London, Canada Cerebral Imaging Centre, Douglas Mental Health University Institute, Montreal, QC, Canada
W. Sharp
Affiliation:
Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Bethesda, MD, USA
J. P. Lerch
Affiliation:
Program in Neurosciences and Mental Health, the Hospital for Sick Children, and Department of Medical Biophysics, The University of Toronto, Toronto, Canada
M. M. Chakravarty
Affiliation:
Cerebral Imaging Centre, Douglas Mental Health University Institute, Montreal, QC, Canada Departments of Psychiatry and Biological and Biomedical Engineering, McGill University, Montreal, QC, Canada
*
*Address for correspondence: P. Shaw, Section on Neurobehavioral Clinical Research, Social and Behavioral Research Branch, National Human Genome Research Institute, Building 31, B1 B37, Bethesda, MD 20892, USA. (Email: [email protected])

Abstract

Background

When children have marked problems with motor coordination, they often have problems with attention and impulse control. Here, we map the neuroanatomic substrate of motor coordination in childhood and ask whether this substrate differs in the presence of concurrent symptoms of attention-deficit/hyperactivity disorder (ADHD).

Method

Participants were 226 children. All completed Diagnostic and Statistical Manual of Mental Disorders, fifth edition (DSM-5)-based assessment of ADHD symptoms and standardized tests of motor coordination skills assessing aiming/catching, manual dexterity and balance. Symptoms of developmental coordination disorder (DCD) were determined using parental questionnaires. Using 3 Tesla magnetic resonance data, four latent neuroanatomic variables (for the cerebral cortex, cerebellum, basal ganglia and thalamus) were extracted and mapped onto each motor coordination skill using partial least squares pathway modeling.

Results

The motor coordination skill of aiming/catching was significantly linked to latent variables for both the cerebral cortex (t = 4.31, p < 0.0001) and the cerebellum (t = 2.31, p = 0.02). This effect was driven by the premotor/motor cortical regions and the superior cerebellar lobules. These links were not moderated by the severity of symptoms of inattention, hyperactivity and impulsivity. In categorical analyses, the DCD group showed atypical reduction in the volumes of these regions. However, the group with DCD alone did not differ significantly from those with DCD and co-morbid ADHD.

Conclusions

The superior cerebellar lobules and the premotor/motor cortex emerged as pivotal neural substrates of motor coordination in children. The dimensions of these motor coordination regions did not differ significantly between those who had DCD, with or without co-morbid ADHD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Abdul-Kareem, IA, Stancak, A, Parkes, LM, Sluming, V (2011). Increased gray matter volume of left pars opercularis in male orchestral musicians correlate positively with years of musical performance. Journal of Magnetic Resonance Imaging 33, 2432.Google Scholar
Baer, L, Park, M, Bailey, J, Chakravarty, M, Li, K, Penhune, V (2015). Regional cerebellar volumes are related to early musical training and finger tapping performance. NeuroImage 109, 130139.CrossRefGoogle ScholarPubMed
Brossard-Racine, M, Shevell, M, Snider, L, Bélanger, SA, Majnemer, A (2012). Motor skills of children newly diagnosed with attention deficit hyperactivity disorder prior to and following treatment with stimulant medication. Research in Developmental Disabilities 33, 20802087.Google Scholar
Brown, T, Lalor, A (2009). The Movement Assessment Battery for Children – second edition (MABC-2): a review and critique. Physical and Occupational Therapy in Pediatrics 29, 86103.CrossRefGoogle ScholarPubMed
Brown-Lum, M, Zwicker, JG (2015). Brain imaging increases our understanding of developmental coordination disorder: a review of literature and future directions. Current Developmental Disorders Reports 3, 131.Google Scholar
Chakravarty, MM, Bertrand, G, Hodge, CP, Sadikot, AF, Collins, DL (2006 a). The creation of a brain atlas for image guided neurosurgery using serial histological data. NeuroImage 30, 359376.Google Scholar
Chakravarty, MM, Broadbent, S, Rosa-Neto, P, Lambert, CM, Collins, DL (2009 a). Design, construction, and validation of an MRI-compatible vibrotactile stimulator intended for clinical use. Journal of Neuroscience Methods 184, 129135.Google Scholar
Chakravarty, MM, Rosa-Neto, P, Broadbent, S, Evans, AC, Collins, DL (2009 b). Robust S1, S2, and thalamic activations in individual subjects with vibrotactile stimulation at 1.5 and 3.0 T. Human Brain Mapping 30, 13281337.Google Scholar
Chakravarty, MM, Sadikot, AF, Germann, J, Bertrand, G, Collins, DL (2008). Towards a validation of atlas warping techniques. Medical Image Analysis 12, 713726.Google Scholar
Chakravarty, MM, Sadikot, AF, Mongia, S, Bertrand, G, Collins, DL (2006 b). Towards a multi-modal atlas for neurosurgical planning. Medical Image Computing and Computer-Assisted Intervention: MICCAI 9, 389396.Google Scholar
Chakravarty, MM, Steadman, P, Van, Ee de, MC, Calcott, RD, Gu, V, Shaw, P, Raznahan, A, Collins, DL, Lerch, JP (2013). Performing label-fusion-based segmentation using multiple automatically generated templates. Human Brain Mapping 34, 26352654.Google Scholar
Chow, SM, Hsu, Y, Henderson, SE, Barnett, AL, Lo, SK (2006). The movement ABC: a cross-cultural comparison of preschool children from Hong Kong, Taiwan, and the USA. Adapted Physical Activity Quarterly 23, 31.Google Scholar
Cole, W, Mostofsky, S, Larson, JG, Denckla, M, Mahone, E (2008). Age-related changes in motor subtle signs among girls and boys with ADHD. Neurology 71, 15141520.CrossRefGoogle ScholarPubMed
Collins, DL, Pruessner, JC (2010). Towards accurate, automatic segmentation of the hippocampus and amygdala from MRI by augmenting ANIMAL with a template library and label fusion. NeuroImage 52, 13551366.Google Scholar
Debaere, F, Swinnen, SP, Béatse, E, Sunaert, S, Van, He cke, P, Duysens, J (2001). Brain areas involved in interlimb coordination: a distributed network. NeuroImage 14, 947958.Google Scholar
Di, X, Zhu, S, Jin, H, Wang, P, Ye, Z, Zhou, K, Zhuo, Y, Rao, H (2012). Altered resting brain function and structure in professional badminton players. Brain Connectivity 2, 225233.Google Scholar
Doya, K (1999). What are the computations of the cerebellum, the basal ganglia and the cerebral cortex? Neural Networks 12, 961974.Google Scholar
Doyon, J, Penhune, V, Ungerleider, LG (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41, 252262.CrossRefGoogle ScholarPubMed
Fliers, E, Vermeulen, S, Rijsdijk, FH, Altink, M, Buschgens, C, Rommelse, N, Faraone, S, Sergeant, J, Buitelaar, J, Franke, B (2009). ADHD and poor motor performance from a family genetic perspective. Journal of the American Academy of Child and Adolescent Psychiatry 48, 2534.Google Scholar
Gillberg, C, Rasmussen, P, Carlström, G, Svenson, B, Waldenström, E (1982). Perceptual, motor and attentional deficits in six-year-old children. Epidemiological aspects. Journal of Child Psychology and Psychiatry, and Allied Disciplines 23, 131144.Google Scholar
Gillberg, IC (1987) Deficits in Attention, Motor Control and Perception. Uppsala University: Uppsala.Google Scholar
Graff-Radford, NR, Eslinger, PJ, Damasio, AR, Yamada, T (1984). Nonhemorrhagic infarction of the thalamus: behavioral, anatomic, and physiologic correlates. Neurology 34, 1423.Google Scholar
Henderson, SE, Sugden, DA, Barnett, AL (2007). Movement Assessment Battery for Children-2: Movement ABC-2: Examiner's Manual. Pearson Assessment: London.Google Scholar
Hutchinson, S, Lee, LH-L, Gaab, N, Schlaug, G (2003). Cerebellar volume of musicians. Cerebral Cortex 13, 943949.Google Scholar
Ingalhalikar, M, Smith, A, Parker, D, Satterthwaite, TD, Elliott, MA, Ruparel, K, Hakonarson, H, Gur, RE, Gur, RC, Verma, R (2014). Sex differences in the structural connectome of the human brain. Proceedings of the National Academy of Sciences of the United States of America 111, 823828.Google Scholar
Kadesjo, B, Gillberg, C (1999). Developmental coordination disorder in Swedish 7-year-old children. Journal of the American Academy of Child and Adolescent Psychiatry 38, 820828.Google Scholar
Kaiser, ML, Schoemaker, MM, Albaret, JM, Geuze, RH (2015). What is the evidence of impaired motor skills and motor control among children with attention deficit hyperactivity disorder (ADHD)? Systematic review of the literature. Research in Developmental Disabilities 36, 338357.Google Scholar
Karussis, D, Leker, R, Abramsky, O (2000). Cognitive dysfunction following thalamic stroke: a study of 16 cases and review of the literature. Journal of the Neurological Sciences 172, 2529.Google Scholar
Kelly, RM, Strick, PL (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. Journal of Neuroscience 23, 84328444.Google Scholar
Kraemer, HC, Yesavage, JA, Taylor, JL, Kupfer, D (2000). How can we learn about developmental processes from cross-sectional studies, or can we? American Journal of Psychiatry 157, 163171.Google Scholar
Kühn, S, Gleich, T, Lorenz, R, Lindenberger, U, Gallinat, J (2014). Playing Super Mario induces structural brain plasticity: gray matter changes resulting from training with a commercial video game. Molecular Psychiatry 19, 265271.Google Scholar
Kühn, S, Romanowski, A, Schilling, C, Banaschewski, T, Barbot, A, Barker, GJ, Brühl, R, Büchel, C, Conrod, PJ, Czech, K, Dalley, JW, Flor, H, Garavan, H, Häke, I, Ittermann, B, Ivanov, N, Mann, K, Lathrop, M, Loth, E, Lüdemann, K, Mallik, C, Martinot, JL, Palafox, C, Poline, JB, Reuter, J, Rietschel, M, Robbins, TW, Smolka, MN, Nees, F, Walaszek, B, Schumann, G, Heinz, A, Gallinat, J; IMAGEN consortium (2012). Manual dexterity correlating with right lobule VI volume in right-handed 14-year-olds. NeuroImage 59, 16151621.CrossRefGoogle ScholarPubMed
Langevin, LM, Macmaster, FP, Crawford, S, Lebel, C, Dewey, D (2014). Common white matter microstructure alterations in pediatric motor and attention disorders. Journal of Pediatrics 164, 11571164.e1.CrossRefGoogle ScholarPubMed
Langevin, LM, Macmaster, FP, Dewey, D (2015). Distinct patterns of cortical thinning in concurrent motor and attention disorders. Developmental Medicine and Child Neurology 57, 257264.Google Scholar
Leh, SE, Chakravarty, MM, Ptito, A (2008). The connectivity of the human pulvinar: a diffusion tensor imaging tractography study. International Journal of Biomedical Imaging 2008, 789539.Google Scholar
Leh, SE, Ptito, A, Chakravarty, MM, Strafella, AP (2007). Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neuroscience Letters 419, 113118.Google Scholar
Lenroot, RK, Giedd, JN (2010). Sex differences in the adolescent brain. Brain and Cognition 72, 4655.Google Scholar
Lubke, GH, Hudziak, JJ, Derks, EM, Van, Bi jsterveldt, TCEM, Boomsma, DI (2009). Maternal ratings of attention problems in ADHD: evidence for the existence of a continuum. Journal of the American Academy of Child and Adolescent Psychiatry 48, 10851093.Google Scholar
Martin, NC, Piek, JP, Hay, D (2006). DCD and ADHD: a genetic study of their shared aetiology. Human Movement Science 25, 110124.Google Scholar
Mayka, MA, Corcos, DM, Leurgans, SE, Vaillancourt, DE (2006). Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. NeuroImage 31, 14531474.Google Scholar
Mcleod, KR, Langevin, LM, Goodyear, BG, Dewey, D (2014). Functional connectivity of neural motor networks is disrupted in children with developmental coordination disorder and attention-deficit/hyperactivity disorder. NeuroImage: Clinical 4, 566575.Google Scholar
Mostofsky, SH, Newschaffer, CJ, Denckla, MB (2003). Overflow movements predict impaired response inhibition in children with ADHD. Perceptual and Motor Skills 97, 13151331.Google Scholar
Mostofsky, SH, Rimrodt, SL, Schafer, JG, Boyce, A, Goldberg, MC, Pekar, JJ, Denckla, MB (2006). Atypical motor and sensory cortex activation in attention-deficit/hyperactivity disorder: a functional magnetic resonance imaging study of simple sequential finger tapping. Biological Psychiatry 59, 4856.CrossRefGoogle ScholarPubMed
Pangelinan, MM, Zhang, G, Vanmeter, JW, Clark, JE, Hatfield, BD, Haufler, AJ (2011). Beyond age and gender: relationships between cortical and subcortical brain volume and cognitive–motor abilities in school-age children. NeuroImage 54, 30933100.Google Scholar
Paola, M, Caltagirone, C, Petrosini, L (2013). Prolonged rock climbing activity induces structural changes in cerebellum and parietal lobe. Human Brain Mapping 34, 27072714.Google Scholar
Park, IS, Lee, KJ, Han, JW, Lee, NJ, Lee, WT, Park, KA (2009). Experience-dependent plasticity of cerebellar vermis in basketball players. Cerebellum 8, 334339.Google Scholar
Park, IS, Lee, KJ, Han, JW, Lee, NJ, Lee, WT, Park, KA (2011). Basketball training increases striatum volume. Human Movement Science 30, 5662.Google Scholar
Park, IS, Lee, NJ, Kim, T-Y, Park, J-H, Won, Y-M, Jung, Y-J, Yoon, J-H (2012). Volumetric analysis of cerebellum in short-track speed skating players. Cerebellum 11, 925930.Google Scholar
Park, MTM, Pipitone, J, Baer, LH, Winterburn, JL, Shah, Y, Chavez, S, Schira, MM, Lobaugh, NJ, Lerch, JP, Voineskos, AN, Chakravarty MM (2014). Derivation of high-resolution MRI atlases of the human cerebellum at 3T and segmentation using multiple automatically generated templates. NeuroImage 95, 217231.Google Scholar
Paus, T (2001). Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nature Reviews Neuroscience 2, 417424.Google Scholar
Petersen, SE, Posner, MI (2012). The attention system of the human brain: 20 years after. Annual Review of Neuroscience 35, 7389.CrossRefGoogle ScholarPubMed
Picard, N, Strick, PL (1996). Motor areas of the medial wall: a review of their location and functional activation. Cerebral Cortex 6, 342353.CrossRefGoogle Scholar
Polderman, TJC, Derks, EM, Hudziak, JJ, Verhulst, FC, Posthuma, D, Boomsma, DI (2007). Across the continuum of attention skills: a twin study of the SWAN ADHD rating scale. Journal of Child Psychology and Psychiatry, and Allied Disciplines 48, 10801087.Google Scholar
Reich, W (2000). Diagnostic Interview for Children and Adolescents (DICA). Journal of the American Academy of Child and Adolescent Psychiatry 39, 5966.Google Scholar
Ruff, RM, Parker, SB (1993). Gender- and age-specific changes in motor speed and eye–hand coordination in adults: normative values for the finger tapping and grooved pegboard tests. Perceptual and Motor Skills 76, 12191230.Google Scholar
Sanchez, G (2013). PLS path modeling with R. Trowchez Editions: Berkeley, CA (http://www.gastonsanchez.com/PLSPathModelingwithR.pdf). Accessed March 2016.Google Scholar
Stoodley, CJ, Schmahmann, JD (2010). Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46, 831844.CrossRefGoogle ScholarPubMed
Tenenhaus, M, Vinzi, VE, Chatelin, Y-M, Lauro, C (2005). PLS path modeling. Computational Statistics and Data Analysis 48, 159205.Google Scholar
Toyokura, M, Muro, I, Komiya, T, Obara, M (1999). Relation of bimanual coordination to activation in the sensorimotor cortex and supplementary motor area: analysis using functional magnetic resonance imaging. Brain Research Bulletin 48, 211217.Google Scholar
Watson, NV, Kimura, D (1991). Nontrivial sex differences in throwing and intercepting: relation to psychometrically-defined spatial functions. Personality and Individual Differences 12, 375385.Google Scholar
Wilson, BN, Crawford, SG, Green, D, Roberts, G, Aylott, A, Kaplan, BJ (2009). Psychometric properties of the revised Developmental Coordination Disorder Questionnaire. Physical and Occupational Therapy in Pediatrics 29, 182202.Google Scholar
Zhuang, J, Laconte, S, Peltier, S, Zhang, K, Hu, X (2005). Connectivity exploration with structural equation modeling: an fMRI study of bimanual motor coordination. NeuroImage 25, 462470.Google Scholar
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