Development of Multisensory Reweighting Is Impaired for Quiet Stance Control in Children with Developmental Coordination Disorder (DCD)

Background Developmental Coordination Disorder (DCD) is a leading movement disorder in children that commonly involves poor postural control. Multisensory integration deficit, especially the inability to adaptively reweight to changing sensory conditions, has been proposed as a possible mechanism but with insufficient characterization. Empirical quantification of reweighting significantly advances our understanding of its developmental onset and improves the characterization of its difference in children with DCD compared to their typically developing (TD) peers. Methodology/Principal Findings Twenty children with DCD (6.6 to 11.8 years) were tested with a protocol in which visual scene and touch bar simultaneously oscillateded medio-laterally at different frequencies and various amplitudes. Their data were compared to data on TD children (4.2 to 10.8 years) from a previous study. Gains and phases were calculated for medio-lateral responses of the head and center of mass to both sensory stimuli. Gains and phases were simultaneously fitted by linear functions of age for each amplitude condition, segment, modality and group. Fitted gains and phases at two comparison ages (6.6 and 10.8 years) were tested for reweighting within each group and for group differences. Children with DCD reweight touch and vision at a later age (10.8 years) than their TD peers (4.2 years). Children with DCD demonstrate a weak visual reweighting, no advanced multisensory fusion and phase lags larger than those of TD children in response to both touch and vision. Conclusions/Significance Two developmental perspectives, postural body scheme and dorsal stream development, are provided to explain the weak vision reweighting. The lack of multisensory fusion supports the notion that optimal multisensory integration is a slow developmental process and is vulnerable in children with DCD.

[1]  S. Iwaki,et al.  Parietal dysfunction in developmental coordination disorder: a functional MRI study , 2009, Neuroreport.

[2]  Jane E. Clark,et al.  Continuous and Discontinuous Drawing: High Temporal Variability Exists Only in Discontinuous Circling in Young Children , 2008, Journal of motor behavior.

[3]  H. Sigmundsson,et al.  Do ‘clumsy’ children have visual deficits , 2003, Behavioural Brain Research.

[4]  Tim Kiemel,et al.  Development of multisensory reweighting for posture control in children , 2007, Experimental Brain Research.

[5]  A. Tamhane,et al.  Multiple Comparison Procedures , 1989 .

[6]  Murray T. Maybery,et al.  Vision in developmental disorders: Is there a dorsal stream deficit? , 2010, Brain Research Bulletin.

[7]  H. Whiting,et al.  Inter- and intra-sensory modality matching in children with hand-eye co-ordination problems , 1997, Experimental Brain Research.

[8]  Jane E. Clark,et al.  Children with developmental coordination disorder benefit from using vision in combination with touch information for quiet standing. , 2011, Gait & posture.

[9]  M. Mon-Williams,et al.  Visual evoked potentials in children with developmental coordination disorder. , 1996, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[10]  W. Kułak,et al.  The cortical evoked potentials in children with developmental coordination disorder (DCD). , 2005, Roczniki Akademii Medycznej w Bialymstoku.

[11]  R. Geuze Static balance and developmental coordination disorder. , 2003, Human movement science.

[12]  J Whitall,et al.  Auditory-motor coupling of bilateral finger tapping in children with and without DCD compared to adults. , 2008, Human movement science.

[13]  L. Shams,et al.  Crossmodal influences on visual perception. , 2010, Physics of life reviews.

[14]  H. Bülthoff,et al.  Merging the senses into a robust percept , 2004, Trends in Cognitive Sciences.

[15]  Andrej Pázman,et al.  Nonlinear Regression , 2019, Handbook of Regression Analysis With Applications in R.

[16]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[17]  C. Hulme,et al.  Visual, Kinaesthetic and Cross‐modal Judgements of Length by Normal and Clumsy Children , 1982, Developmental medicine and child neurology.

[18]  J. Zwicker,et al.  Brain Activation of Children With Developmental Coordination Disorder is Different Than Peers , 2010, Pediatrics.

[19]  Stephen J. Kim The Use of Vision in Children's Postural Control , 2004 .

[20]  M. Ernst Multisensory Integration: A Late Bloomer , 2008, Current Biology.

[21]  Frans C. T. van der Helm,et al.  An adaptive model of sensory integration in a dynamic environment applied to human stance control , 2001, Biological Cybernetics.

[22]  David C. Burr,et al.  Young Children Do Not Integrate Visual and Haptic Form Information , 2008, Current Biology.

[23]  Ron Dumont,et al.  Woodcock-Johnson III Tests Of Cognitive Abilities , 2014 .

[24]  M. Denckla,et al.  Revised Neurological Examination for Subtle Signs (1985). , 1985, Psychopharmacology bulletin.

[25]  J. H. Killebrew,et al.  Influence of visual motion on tactile motion perception. , 2006, Journal of neurophysiology.

[26]  Visual–proprioceptive mapping in children with developmental coordination disorder , 1999, Developmental medicine and child neurology.

[27]  H. Whiting,et al.  Inter‐ and intrasensory modality matching in children with hand‐eye coordination problems: exploring the developmental lag hypothesis , 1997, Developmental medicine and child neurology.

[28]  R. Peterka Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[29]  D. De Clercq,et al.  Sensory contributions to balance in boys with developmental coordination disorder. , 2008, Adapted physical activity quarterly : APAQ.

[30]  George Adelman,et al.  Encyclopedia of neuroscience , 2004 .

[31]  B. McKenzie,et al.  Information processing deficits associated with developmental coordination disorder: a meta-analysis of research findings. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[32]  L. Rowell,et al.  Exercise : regulation and integration of multiple systems , 1996 .

[33]  F. Horak,et al.  Postural Orientation and Equilibrium , 2011 .

[34]  C. Spence,et al.  Multisensory contributions to the perception of motion , 2003, Neuropsychologia.

[35]  J. Massion Postural control system , 1994, Current Opinion in Neurobiology.

[36]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[37]  Beatrice de Gelder,et al.  Audiovisual speech integration in pervasive developmental disorder: evidence from event-related potentials. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[38]  J. Atkinson,et al.  Normal and anomalous development of visual motion processing: motion coherence and ‘dorsal-stream vulnerability’ , 2003, Neuropsychologia.

[39]  Robert J. Peterka,et al.  Comparison of human and humanoid robot control of upright stance , 2009, Journal of Physiology-Paris.

[40]  Motohide Miyahara,et al.  Developmental dyspraxia and developmental coordination disorder , 1995, Neuropsychology Review.

[41]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[42]  Denckla Mb,et al.  Revised Neurological Examination for Subtle Signs (1985). , 1985 .

[43]  M. Ernst,et al.  Optimal integration of shape information from vision and touch , 2007, Experimental Brain Research.

[44]  Brigitte Röder,et al.  Semantic confusion regarding the development of multisensory integration: a practical solution , 2010, The European journal of neuroscience.

[45]  S. Mostofsky,et al.  Toward a Narrower, More Pragmatic View of Developmental Dyspraxia , 2010, Journal of child neurology.

[46]  Nobu Shirai,et al.  How do infants utilize radial optic flow for their motor actions?: A review of behavioral and neural studies , 2010 .

[47]  Renaud Ronsse,et al.  Multisensory Integration in Dynamical Behaviors: Maximum Likelihood Estimation across Bimanual Skill Learning , 2009, The Journal of Neuroscience.

[48]  T. Kiemel,et al.  Multisensory reweighting of vision and touch is intact in healthy and fall-prone older adults , 2006, Experimental Brain Research.

[49]  Kelvin S. Oie,et al.  Multisensory fusion: simultaneous re-weighting of vision and touch for the control of human posture. , 2002, Brain research. Cognitive brain research.

[50]  Andrea Facoetti,et al.  Multisensory Spatial Attention Deficits Are Predictive of Phonological Decoding Skills in Developmental Dyslexia , 2010, Journal of Cognitive Neuroscience.

[51]  J. Atkinson,et al.  Form and motion coherence processing in dyspraxia: evidence of a global spatial processing deficit , 2002, Neuroreport.

[52]  F O Black,et al.  Age-related changes in human posture control: sensory organization tests. , 1990, Journal of vestibular research : equilibrium & orientation.

[53]  Jenn-Yeu Chen,et al.  Standing balance of children with developmental coordination disorder under altered sensory conditions. , 2007, Human movement science.

[54]  Manabu Honda,et al.  Tactile–visual integration in the posterior parietal cortex: A functional magnetic resonance imaging study , 2008, Brain Research Bulletin.

[55]  Michael Wolfe,et al.  J+ = J , 1994, ACM SIGPLAN Notices.

[56]  Vincent Hayward,et al.  Motion Aftereffects Transfer between Touch and Vision , 2009, Current Biology.

[57]  Mark Mon-Williams,et al.  Eye movements, prematurity and developmental co-ordination disorder , 1998, Vision Research.

[58]  Peterka Rj,et al.  AGE-RELATED CHANGES IN HUMAN POSTURE CONTROL: SENSORY ORGANIZATION TESTS , 1990 .

[59]  Colin R Grove,et al.  Impaired re-weighting of sensory feedback for maintenance of postural control in children with developmental coordination disorder. , 2007, Human movement science.

[60]  Gereon R. Fink,et al.  Human medial intraparietal cortex subserves visuomotor coordinate transformation , 2004, NeuroImage.

[61]  G. Essick,et al.  Tactile motion activates the human middle temporal/V5 (MT/V5) complex , 2002, The European journal of neuroscience.

[62]  A. Kuo An optimal state estimation model of sensory integration in human postural balance , 2005, Journal of neural engineering.

[63]  S. Keele,et al.  Timing and Force Control Deficits in Clumsy Children , 1991, Journal of Cognitive Neuroscience.

[64]  Christine Assaiante,et al.  An ontogenetic model for the sensorimotor organization of balance control in humans , 1995 .

[65]  J. P. Pick,et al.  KINAESTHETIC SENSITIVITY AND MOTOR PERFORMANCE OF CHILDREN WITH DEVELOPMENTAL CO‐ORDINATION DISORDER , 1995, Developmental medicine and child neurology.

[66]  Pete R. Jones,et al.  Development of Cue Integration in Human Navigation , 2008, Current Biology.

[67]  H. Keselman,et al.  Multiple Comparison Procedures , 2005 .

[68]  A. Ho,et al.  Speech and oro-motor function in children with developmental coordination disorder: a pilot study. , 2010, Human movement science.

[69]  David N. Lee,et al.  Visual proprioceptive control of standing in human infants , 1974 .

[70]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[71]  R. Geuze,et al.  INCONSISTENCY AND ADAPTATION IN TIMING OF CLUMSY CHILDREN , 1987 .

[72]  Tim Kiemel,et al.  Multisensory fusion and the stochastic structure of postural sway , 2002, Biological Cybernetics.

[73]  E. Mammen The Bootstrap and Edgeworth Expansion , 1997 .

[74]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[75]  S. Astill,et al.  Developmental sequences of two-handed catching: How do children with and without developmental coordination disorder differ? , 2007, Physiotherapy theory and practice.

[76]  Mark Mon-Williams,et al.  Postural control and co-ordination disorders: The swinging room revisited , 1998 .

[77]  M. Turvey,et al.  Common effects of touch and vision on postural parameters , 1997, Experimental Brain Research.

[78]  M. Schoemaker,et al.  Clinical and research diagnostic criteria for developmental coordination disorder: a review and discussion. , 2001, Human movement science.

[79]  B. Smits-Engelsman,et al.  Fine motor deficiencies in children diagnosed as DCD based on poor grapho-motor ability. , 2001, Human movement science.

[80]  R. Peterka,et al.  Role of somatosensory and vestibular cues in attenuating visually induced human postural sway , 2004, Experimental Brain Research.

[81]  L. Miller,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Review Article Clinical Field Related to Sensory Integration Description of the Disorder , 2022 .

[82]  B. McKenzie,et al.  Cross-Modal Transfer of Sequential Visual and Haptic Shape Information by Clumsy Children , 1993, Perception.

[83]  J. Duysens,et al.  Children with developmental coordination disorder are equally able to generate force but show more variability than typically developing children. , 2008, Human movement science.

[84]  Tim Kiemel,et al.  Modeling the Dynamics of Sensory Reweighting , 2006, Biological Cybernetics.