Advertisement

Neurophysiological Approaches to Understanding Motor Control in DCD: Current Trends and Future Directions

  • Christian HydeEmail author
  • Ian Fuelscher
  • Jacqueline Williams
Motor Disorders (P Wilson, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Motor Disorders

Abstract

Purpose of Review

To provide an account of neurophysiological approaches to understanding motor control in DCD, with a specific focus on emerging techniques such as non-invasive brain stimulation (NIBS) and fNIRS. We also provide an update on evidence from more traditional neurophysiological approaches to understanding atypical motor skills such as EEG.

Recent Findings

With reference to NIBS data from DCD and congenital motor disorders, we present evidence that compromised excitatory and inhibitory neurophysiology within motor circuitry may provide a biomarker for atypical motor development. Further, we draw parallels between work reviewed here and neuroimaging evidence reviewed elsewhere, highlighting converging lines of evidence implicating motor and executive systems in DCD.

Summary

Neurophysiological approaches to understanding DCD have the potential to play an important role in clarifying its underlying mechanisms. Given promising findings emerging from other pediatric motor disorders, we argue that continued work into the viability of NIBS in diagnosis and treatment of DCD is warranted.

Keywords

Developmental coordination disorder (DCD) Non-invasive brain stimulation (NIBS) Transcranial magnetic stimulation (TMS) Functional near-infrared spectroscopy (fNIRS) Electroencephalogram (EEG) 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Association, A.P. Diagnostic and statistical manual of mental disorders (DSM-5®). 2013. American Psychiatric Pub.Google Scholar
  2. 2.
    Biotteau M, Chaix Y, Blais M, Tallet J, Péran P, Albaret JM. Neural signature of DCD: a critical review of MRI neuroimaging studies. Front Neurol. 2016;7.Google Scholar
  3. 3.
    Brown-Lum M, Zwicker JG. Brain imaging increases our understanding of developmental coordination disorder: a review of literature and future directions. Curr Dev Disord Rep. 2015;2(2):131–40.Google Scholar
  4. 4.
    Fuelscher I, Caeyenberghs K, Enticott PG, Williams J, Lum J, Hyde C. Differential activation of brain areas in children with developmental coordination disorder during tasks of manual dexterity: an ALE meta-analysis. Neurosci Biobehav Rev. 2018;86:77–84.Google Scholar
  5. 5.
    Gomez A, Sirigu A. Developmental coordination disorder: core sensori-motor deficits, neurobiology and etiology. Neuropsychologia. 2015;79(Pt B):272–87.Google Scholar
  6. 6.
    Reynolds JE, Thornton AL, Elliott C, Williams J, Lay BS, Licari MK. A systematic review of mirror neuron system function in developmental coordination disorder: imitation, motor imagery, and neuroimaging evidence. Res Dev Disabil. 2015;47:234–83.Google Scholar
  7. 7.
    Wilson PH, Smits-Engelsman B, Caeyenberghs K, Steenbergen B, Sugden D, Clark J, et al. Cognitive and neuroimaging findings in developmental coordination disorder: new insights from a systematic review of recent research. Dev Med Child Neurol. 2017;59:1117–29.Google Scholar
  8. 8.
    Allen CH, Kluger BM, Buard I. Safety of transcranial magnetic stimulation in children: a systematic review of the literature. Pediatr Neurol. 2017;68:3–17.Google Scholar
  9. 9.
    Liew S-L, et al. Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery. Front Hum Neurosci. 2014;8:378.Google Scholar
  10. 10.
    Chung SW, Hill AT, Rogasch NC, Hoy KE, Fitzgerald PB. Use of theta-burst stimulation in changing excitability of motor cortex: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2016;63:43–64.Google Scholar
  11. 11.
    Ilić TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol. 2002;545(1):153–67.Google Scholar
  12. 12.
    Beck S, Hallett M. Surround inhibition in the motor system. Exp Brain Res. 2011;210(2):165–72.Google Scholar
  13. 13.
    Ismail FY, Fatemi A, Johnston MV. Cerebral plasticity: windows of opportunity in the developing brain. Eur J Paediatr Neurol. 2017;21(1):23–48.Google Scholar
  14. 14.
    Garvey MA, Mall V. Transcranial magnetic stimulation in children. Clin Neurophysiol. 2008;119(5):973–84.Google Scholar
  15. 15.
    Williams J, Hyde C, Spittle A. Developmental coordination disorder and cerebral palsy: is there a continuum? Curr Dev Disord Rep. 2014;1(2):118–24.Google Scholar
  16. 16.
    Pearsall-Jones JG, Piek JP, Levy F. Developmental coordination disorder and cerebral palsy: categories or a continuum? Hum Mov Sci. 2010;29(5):787–98.Google Scholar
  17. 17.
    Kuo HC, Friel KM, Gordon AM. Neurophysiological mechanisms and functional impact of mirror movements in children with unilateral spastic cerebral palsy. Dev Med Child Neurol. 2018;60(2):155–61.Google Scholar
  18. 18.
    Stinear CM, Coxon JP, Byblow WD. Primary motor cortex and movement prevention: where stop meets go. Neurosci Biobehav Rev. 2009;33(5):662–73.Google Scholar
  19. 19.
    Kuo HC, Ferre CL, Carmel JB, Gowatsky JL, Stanford AD, Rowny SB, et al. Using diffusion tensor imaging to identify corticospinal tract projection patterns in children with unilateral spastic cerebral palsy. Dev Med Child Neurol. 2017;59(1):65–71.Google Scholar
  20. 20.
    Carr L, et al. Patterns of central motor reorganization in hemiplegic cerebral palsy. Brain. 1993;116(5):1223–47.Google Scholar
  21. 21.
    Beaulé V, Tremblay S, Théoret H. Interhemispheric control of unilateral movement. Neural Plast. 2012;2012:1–11.Google Scholar
  22. 22.
    Swinnen S, Young DE, Walter CB, Serrien DJ. Control of asymmetrical bimanual movements. Exp Brain Res. 1991;85(1):163–73.Google Scholar
  23. 23.
    Li JY, Espay AJ, Gunraj CA, Pal PK, Cunic DI, Lang AE, et al. Interhemispheric and ipsilateral connections in Parkinson’s disease: relation to mirror movements. Mov Disord. 2007;22(6):813–21.Google Scholar
  24. 24.
    Nadkarni NA, Deshmukh SS. Mirror movements. Ann Indian Acad Neurol. 2012;15(1):13–4.Google Scholar
  25. 25.
    • He JL, Fuelscher I, Enticott PG, Teo WP, Barhoun P, Hyde C. Interhemispheric cortical inhibition is reduced in young adults with developmental coordination disorder. Front Neurol. 2018;9:179. The first study to employ paired-pulse TMS in DCD; this study demonstrated that young adults with DCD show reduced interhemispheric M1 cortical inhibition. Google Scholar
  26. 26.
    Koerte I, et al. Anisotropy of transcallosal motor fibres indicates functional impairment in children with periventricular leukomalacia. Dev Med Child Neurol. 2011;53(2):179–86.Google Scholar
  27. 27.
    Bruininks RH. Bruininks-Oseretsky test of motor proficiency, (BOT-2). Minneapolis, MN: Pearson Assessment; 2005.Google Scholar
  28. 28.
    Blais M, Baly C, Biotteau M, Albaret JM, Chaix Y, Tallet J. Lack of motor inhibition as a marker of learning difficulties of bimanual coordination in teenagers with developmental coordination disorder. Dev Neuropsychol. 2017;42(3):207–19.Google Scholar
  29. 29.
    • Blais M, Amarantini D, Albaret JM, Chaix Y, Tallet J. Atypical inter-hemispheric communication correlates with altered motor inhibition during learning of a new bimanual coordination pattern in developmental coordination disorder. Dev Sci. 2018;21(3):e12563. Using EEG, this study demonstrated that increased mirror movements in DCD were assocaited with lower cortico-cortical coherence between fronto-central regions. Google Scholar
  30. 30.
    Licari M, Larkin D, Miyahara M. The influence of developmental coordination disorder and attention deficits on associated movements in children. Hum Mov Sci. 2006;25(1):90–9.Google Scholar
  31. 31.
    Stinear, C.M. Corticospinal facilitation during motor imagery. In: The neurophysiological foundations of mental and motor imagery. 2010. p. 47–61.Google Scholar
  32. 32.
    Jeannerod M. Motor cognition: what actions tell the self. Oxford: Oxford University Press; 2006.Google Scholar
  33. 33.
    Hardwick RM, Caspers S, Eickhoff SB, Swinnen SP. Neural correlates of action: comparing meta-analyses of imagery, observation, and execution. Neurosci Biobehav Rev. 2018;94:31–44.Google Scholar
  34. 34.
    Hetu S, et al. The neural network of motor imagery: an ALE meta-analysis. Neurosci Biobehav Rev. 2013;37(5):930–49.Google Scholar
  35. 35.
    Sharma N, Pomeroy VM, Baron JC. Motor imagery: a backdoor to the motor system after stroke? Stroke. 2006;37(7):1941–52.Google Scholar
  36. 36.
    Grospretre S, Ruffino C, Lebon F. Motor imagery and cortico-spinal excitability: a review. Eur J Sport Sci. 2016;16(3):317–24.Google Scholar
  37. 37.
    Lebon F, Byblow WD, Collet C, Guillot A, Stinear CM. The modulation of motor cortex excitability during motor imagery depends on imagery quality. Eur J Neurosci. 2012;35(2):323–31.Google Scholar
  38. 38.
    Williams J, Pearce AJ, Loporto M, Morris T, Holmes PS. The relationship between corticospinal excitability during motor imagery and motor imagery ability. Behav Brain Res. 2012;226(2):369–75.Google Scholar
  39. 39.
    Craje C, et al. Compromised motor planning and motor imagery in right hemiparetic cerebral palsy. Res Dev Disabil. 2010;31(6):1313–22.Google Scholar
  40. 40.
    Lust JM, Wilson PH, Steenbergen B. Motor imagery difficulties in children with cerebral palsy: a specific or general deficit? Res Dev Disabil. 2016;57:102–11.Google Scholar
  41. 41.
    Mutsaarts M, Steenbergen B, Bekkering H. Impaired motor imagery in right hemiparetic cerebral palsy. Neuropsychologia. 2007;45(4):853–9.Google Scholar
  42. 42.
    Adams IL, et al. Compromised motor control in children with DCD: a deficit in the internal model?-a systematic review. Neurosci Biobehav Rev. 2014;47:225–44.Google Scholar
  43. 43.
    Barhoun P, Fuelscher I, Kothe EJ, He JL, Youssef GJ, Enticott PG, et al. Motor imagery in children with DCD: a systematic and meta-analytic review of hand-rotation task performance. Neurosci Biobehav Rev. 2019;99:282–97.Google Scholar
  44. 44.
    Wilson PH, Thomas PR, Maruff P. Motor imagery training ameliorates motor clumsiness in children. J Child Neurol. 2002;17(7):491–8.Google Scholar
  45. 45.
    Wilson PH, Adams ILJ, Caeyenberghs K, Thomas P, Smits-Engelsman B, Steenbergen B. Motor imagery training enhances motor skill in children with DCD: a replication study. Res Dev Disabil. 2016;57:54–62.Google Scholar
  46. 46.
    Hyde C, Fuelscher I, Williams J, Lum JAG, He J, Barhoun P, et al. Corticospinal excitability during motor imagery is reduced in young adults with developmental coordination disorder. Res Dev Disabil. 2018;72:214–24.Google Scholar
  47. 47.
    Pitcher JB, Schneider LA, Burns NR, Drysdale JL, Higgins RD, Ridding MC, et al. Reduced corticomotor excitability and motor skills development in children born preterm. J Physiol. 2012;590(22):5827–44.Google Scholar
  48. 48.
    Goulardins JB, Rigoli D, Licari M, Piek JP, Hasue RH, Oosterlaan J, et al. Attention deficit hyperactivity disorder and developmental coordination disorder: two separate disorders or do they share a common etiology. Behav Brain Res. 2015;292:484–92.Google Scholar
  49. 49.
    Suppa A, Huang YZ, Funke K, Ridding MC, Cheeran B, di Lazzaro V, et al. Ten years of theta burst stimulation in humans: established knowledge, unknowns and prospects. Brain Stimul. 2016;9(3):323–35.Google Scholar
  50. 50.
    Gillick B, et al. Therapeutic brain stimulation trials in children with cerebral palsy, in Pediatric brain stimulation. Elsevier; 2016. p. 209–236.Google Scholar
  51. 51.
    Saleem GT, et al. Transcranial direct current stimulation in pediatric motor disorders: a systematic review and meta-analysis. Arch Phys Med Rehabil. 2018.Google Scholar
  52. 52.
    Gillick BT, Gordon AM, Feyma T, Krach LE, Carmel J, Rich TL, et al. Non-invasive brain stimulation in children with unilateral cerebral palsy: a protocol and risk mitigation guide. Front Pediatr. 2018;6:56.Google Scholar
  53. 53.
    Barahona-Corrêa JB, Velosa A, Chainho A, Lopes R, Oliveira-Maia AJ. Repetitive transcranial magnetic stimulation for treatment of autism spectrum disorder: a systematic review and meta-analysis. Front Integr Neurosci. 2018;12:27.Google Scholar
  54. 54.
    Rubio B, Boes AD, Laganiere S, Rotenberg A, Jeurissen D, Pascual-Leone A. Noninvasive brain stimulation in pediatric attention-deficit hyperactivity disorder (ADHD) a review. J Child Neurol. 2016;31(6):784–96.Google Scholar
  55. 55.
    Ciechanski P, Zewdie E, Kirton A. Developmental profile of motor cortex transcallosal inhibition in children and adolescents. J Neurophysiol. 2017;118(1):140–8.Google Scholar
  56. 56.
    Cui X, Bray S, Bryant DM, Glover GH, Reiss AL. A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage. 2011;54(4):2808–21.Google Scholar
  57. 57.
    Pinti P, et al. The present and future use of functional near-infrared spectroscopy (fNIRS) for cognitive neuroscience. Annals of the New York Academy of Sciences; 2018.Google Scholar
  58. 58.
    • Caçola P, Getchell N, Srinivasan D, Alexandrakis G, Liu H. Cortical activity in fine-motor tasks in children with developmental coordination disorder: a preliminary fNIRS study. Int J Dev Neurosci. 2018;65:83–90. This was the first study to demonstrate the viability of f NIRS as a measrue of functional neural activity in DCD. Google Scholar
  59. 59.
    Koch JKL, Miguel H, Smiley-Oyen AL. Prefrontal activation during Stroop and Wisconsin card sort tasks in children with developmental coordination disorder: a NIRS study. Exp Brain Res. 2018;1–12.Google Scholar
  60. 60.
    Querne L, Berquin P, Vernier-Hauvette MP, Fall S, Deltour L, Meyer ME, et al. Dysfunction of the attentional brain network in children with developmental coordination disorder: a fMRI study. Brain Res. 2008;1244:89–102.Google Scholar
  61. 61.
    Pangelinan MM, Hatfield BD, Clark JE. Differences in movement-related cortical activation patterns underlying motor performance in children with and without developmental coordination disorder. J Neurophysiol. 2013;109(12):3041–50.Google Scholar
  62. 62.
    Steinbrink J, Villringer A, Kempf F, Haux D, Boden S, Obrig H. Illuminating the BOLD signal: combined fMRI–fNIRS studies. Magn Reson Imaging. 2006;24(4):495–505.Google Scholar
  63. 63.
    Balardin JB, Zimeo Morais GA, Furucho RA, Trambaiolli L, Vanzella P, Biazoli C, et al. Imaging brain function with functional near-infrared spectroscopy in unconstrained environments. Front Hum Neurosci. 2017;11:258.Google Scholar
  64. 64.
    Zwicker JG, Suto M, Harris SR, Vlasakova N, Missiuna C. Developmental coordination disorder is more than a motor problem: children describe the impact of daily struggles on their quality of life. Br J Occup Ther. 2018;81(2):65–73.Google Scholar
  65. 65.
    Cohen MX. Where does EEG come from and what does it mean? Trends Neurosci. 2017;40(4):208–18.Google Scholar
  66. 66.
    Tsai C-L, Pan CY, Chang YK, Wang CH, Tseng KD. Deficits of visuospatial attention with reflexive orienting induced by eye-gazed cues in children with developmental coordination disorder in the lower extremities: an event-related potential study. Res Dev Disabil. 2010;31(3):642–55.Google Scholar
  67. 67.
    Tsai C-L, Pan CY, Cherng RJ, Hsu YW, Chiu HH. Mechanisms of deficit of visuospatial attention shift in children with developmental coordination disorder: a neurophysiological measure of the endogenous Posner paradigm. Brain Cogn. 2009;71(3):246–58.Google Scholar
  68. 68.
    Tsai C-L, Wang C-H, Tseng Y-T. Effects of exercise intervention on event-related potential and task performance indices of attention networks in children with developmental coordination disorder. Brain Cogn. 2012;79(1):12–22.Google Scholar
  69. 69.
    Tsai C-L, Chang YK, Hung TM, Tseng YT, Chen TC. The neurophysiological performance of visuospatial working memory in children with developmental coordination disorder. Dev Med Child Neurol. 2012;54(12):1114–20.Google Scholar
  70. 70.
    Wang CH, Lo YH, Pan CY, Chen FC, Liang WK, Tsai CL. Frontal midline theta as a neurophysiological correlate for deficits of attentional orienting in children with developmental coordination disorder. Psychophysiology. 2015;52(6):801–12.Google Scholar
  71. 71.
    Wang CH, Tseng YT, Liu D, Tsai CL. Neural oscillation reveals deficits in visuospatial working memory in children with developmental coordination disorder. Child Dev. 2017;88(5):1716–26.Google Scholar
  72. 72.
    Holeckova I, Cepicka L, Mautner P, Stepanek D, Moucek R. Auditory ERPs in children with developmental coordination disorder. Act Nerv Super. 2014;56(1–2):37–44.Google Scholar
  73. 73.
    de Castelnau P, Albaret JM, Chaix Y, Zanone PG. A study of EEG coherence in DCD children during motor synchronization task. Hum Mov Sci. 2008;27(2):230–41.Google Scholar
  74. 74.
    Bosl WJ, Tager-Flusberg H, Nelson CA. EEG analytics for early detection of autism spectrum disorder: a data-driven approach. Sci Rep. 2018;8(1):6828.Google Scholar
  75. 75.
    Grossi E, Olivieri C, Buscema M. Diagnosis of autism through EEG processed by advanced computational algorithms: a pilot study. Comput Methods Prog Biomed. 2017;142:73–9.Google Scholar
  76. 76.
    Reynolds JE, Licari MK, Reid SL, Elliott C, Winsor AM, Bynevelt M, et al. Reduced relative volume in motor and attention regions in developmental coordination disorder: a voxel-based morphometry study. Int J Dev Neurosci. 2017;58:59–64.Google Scholar
  77. 77.
    Williams J, Kashuk SR, Wilson PH, Thorpe G, Egan GF. White matter alterations in adults with probable developmental coordination disorder: an MRI diffusion tensor imaging study. Neuroreport. 2017;28(2):87–92.Google Scholar
  78. 78.
    Geeraert B, Reynolds J, Lebel C. Diffusion imaging perspectives on brain development in childhood and adolescence.Google Scholar
  79. 79.
    Cermak S, et al. Participation in physical activity, fitness, and risk for obesity in children with developmental coordination disorder: a cross-cultural study. Occup Ther Int. 2015;22(4):163–73.Google Scholar
  80. 80.
    Leonard HC, Hill EL. Executive difficulties in developmental coordination disorder: methodological issues and future directions. Curr Dev Disord Rep. 2015;2(2):141–9.Google Scholar
  81. 81.
    Leonard HC, Bernardi M, Hill EL, Henry LA. Executive functioning, motor difficulties, and developmental coordination disorder. Dev Neuropsychol. 2015;40(4):201–15.Google Scholar
  82. 82.
    Langevin LM, MacMaster FP, Crawford S, Lebel C, Dewey D. Common white matter microstructure alterations in pediatric motor and attention disorders. J Pediatr. 2014;164(5):1157–1164 e1.Google Scholar
  83. 83.
    Hyde C, et al. White matter organization in developmental coordination disorder: a pilot study exploring the added value of constrained spherical deconvolution. NeuroImage: Clin. 2018;21:101625.Google Scholar
  84. 84.
    Forkel SJ, Thiebaut de Schotten M, Kawadler JM, Dell'Acqua F, Danek A, Catani M. The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography. Cortex. 2014;56:73–84.Google Scholar
  85. 85.
    Parlatini V, Radua J, Dell’Acqua F, Leslie A, Simmons A, Murphy DG, et al. Functional segregation and integration within fronto-parietal networks. Neuroimage. 2017;146:367–75.Google Scholar
  86. 86.
    de Kieviet JF, Pouwels PJW, Lafeber HN, Vermeulen RJ, van Elburg RM, Oosterlaan J. A crucial role of altered fractional anisotropy in motor problems of very preterm children. Eur J Paediatr Neurol. 2014;18(2):126–33.Google Scholar
  87. 87.
    McLeod KR, Langevin LM, Goodyear BG, Dewey D. Functional connectivity of neural motor networks is disrupted in children with developmental coordination disorder and attention-deficit/hyperactivity disorder. NeuroImage: Clin. 2014;4:566–75.Google Scholar
  88. 88.
    Cantin N, Polatajko HJ, Thach WT, Jaglal S. Developmental coordination disorder: exploration of a cerebellar hypothesis. Hum Mov Sci. 2007;26(3):491–509.Google Scholar
  89. 89.
    Casula EP, Pellicciari MC, Ponzo V, Stampanoni Bassi M, Veniero D, Caltagirone C, et al. Cerebellar theta burst stimulation modulates the neural activity of interconnected parietal and motor areas. Sci Rep. 2016;6:36191.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Christian Hyde
    • 1
    Email author
  • Ian Fuelscher
    • 1
  • Jacqueline Williams
    • 2
  1. 1.Cognitive Neuroscience Unit, School of PsychologyDeakin UniversityBurwoodAustralia
  2. 2.Institute for Health and Sport, College of Sport and Exercise ScienceVictoria UniversityMelbourneAustralia

Personalised recommendations