Corticospinal tract diffusion properties and robotic visually guided reaching in children with hemiparetic cerebral palsy

Perinatal stroke is the leading cause of hemiparetic cerebral palsy (CP), resulting in life‐long disability. In this study, we examined the relationship between robotic upper extremity motor impairment and corticospinal tract (CST) diffusion properties. Thirty‐three children with unilateral perinatal ischemic stroke (17 arterial, 16 venous) and hemiparesis were recruited from a population‐based research cohort. Bilateral CSTs were defined using diffusion tensor imaging (DTI) and four diffusion metrics were quantified: fractional anisotropy (FA), mean (MD), radial (RD), and axial (AD) diffusivities. Participants completed a visually guided reaching task using the KINARM robot to define 10 movement parameters including movement time and maximum speed. Twenty‐six typically developing children underwent the same evaluations. Partial correlations assessed the relationship between robotic reaching and CST diffusion parameters. All diffusion properties of the lesioned CST differed from controls in the arterial group, whereas only FA was reduced in the venous group. Non‐lesioned CST diffusion measures were similar between stroke groups and controls. Both stroke groups demonstrated impaired reaching performance. Multiple reaching parameters of the affected limb correlated with lesioned CST diffusion properties. Lower FA and higher MD were associated with greater movement time. Few correlations were observed between non‐lesioned CST diffusion and unaffected limb function though FA was associated with reaction time (R = −0.39, p < .01). Diffusion properties of the lesioned CST are altered after perinatal stroke, the degree of which correlates with specific elements of visually guided reaching performance, suggesting specific relevance of CST structural connectivity to clinical motor function in hemiparetic children.

[1]  Catherine Lebel,et al.  Sensory tractography and robot‐quantified proprioception in hemiparetic children with perinatal stroke , 2017, Human brain mapping.

[2]  S. Miller,et al.  Evidence of activity-dependent withdrawal of corticospinal projections during human development , 2001, Neurology.

[3]  A. Eliasson,et al.  Development of the Assisting Hand Assessment: A Rasch-built Measure intended for Children with Unilateral Upper Limb Impairments , 2003 .

[4]  T. Raju,et al.  Ischemic Perinatal Stroke: Summary of a Workshop Sponsored by the National Institute of Child Health and Human Development and the National Institute of Neurological Disorders and Stroke , 2007, Pediatrics.

[5]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[6]  P. Ciechanski,et al.  Contralesional Corticomotor Neurophysiology in Hemiparetic Children With Perinatal Stroke , 2017, Neurorehabilitation and neural repair.

[7]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[8]  Derek K. Jones,et al.  Diffusion‐tensor MRI: theory, experimental design and data analysis – a technical review , 2002 .

[9]  N. Ward Functional reorganization of the cerebral motor system after stroke , 2004, Current opinion in neurology.

[10]  A. Gordon,et al.  Fingertip forces during object manipulation in children with hemiplegic cerebral palsy. I: Anticipatory scaling , 1999, Developmental medicine and child neurology.

[11]  A. Kirton Modeling developmental plasticity after perinatal stroke: defining central therapeutic targets in cerebral palsy. , 2013, Pediatric neurology.

[12]  Stephen H. Scott,et al.  Robotic Assessment of Sensorimotor Deficits After Traumatic Brain Injury , 2012, Journal of neurologic physical therapy : JNPT.

[13]  J B Carlin,et al.  Reliability of the Melbourne assessment of unilateral upper limb function. , 2001, Developmental medicine and child neurology.

[14]  Taeun Chang,et al.  Symptomatic Neonatal Arterial Ischemic Stroke: The International Pediatric Stroke Study , 2011, Pediatrics.

[15]  P. Wesseling,et al.  Development and malformations of the human pyramidal tract , 2004, Journal of Neurology.

[16]  G. Molenaers,et al.  Upper limb impairments and their impact on activity measures in children with unilateral cerebral palsy. , 2012, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[17]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[18]  Reorganisation of the sensorimotor cortex after early focal brain lesion: a functional MRI study in monozygotic twins , 2001, Neuroreport.

[19]  A. Eliasson,et al.  The Assisting Hand Assessment: current evidence of validity, reliability, and responsiveness to change , 2007, Developmental medicine and child neurology.

[20]  Diane L Damiano,et al.  Tactile sensory abilities in cerebral palsy: deficits in roughness and object discrimination , 2008, Developmental medicine and child neurology.

[21]  K. Haaland,et al.  Functional significance of ipsilesional motor deficits after unilateral stroke. , 2008, Archives of physical medicine and rehabilitation.

[22]  D. Dewey,et al.  Clinical Characteristics, Risk Factors, and Outcomes Associated With Neonatal Hemorrhagic Stroke: A Population-Based Case-Control Study , 2017, JAMA pediatrics.

[23]  Carlo Pierpaoli,et al.  Regional distribution of measurement error in diffusion tensor imaging , 2006, Psychiatry Research: Neuroimaging.

[24]  Nicole Wenderoth,et al.  The Corticospinal Tract: A Biomarker to Categorize Upper Limb Functional Potential in Unilateral Cerebral Palsy , 2016, Front. Pediatr..

[25]  A. Kirton Advancing non-invasive neuromodulation clinical trials in children: Lessons from perinatal stroke. , 2017, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[26]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[27]  N. Hogan,et al.  The effect of robot-assisted therapy and rehabilitative training on motor recovery following stroke. , 1997, Archives of neurology.

[28]  A. Gordon,et al.  Fingertip Forces During Object Manipulation in Children with Hemiplegic Cerebral Palsy. II: Bilateral Coordination. , 2000, Pediatric physical therapy : the official publication of the Section on Pediatrics of the American Physical Therapy Association.

[29]  F. Groenendaal,et al.  Neonatal neuroimaging predicts recruitment of contralesional corticospinal tracts following perinatal brain injury , 2013, Developmental medicine and child neurology.

[30]  P. Ciechanski,et al.  Transcranial direct current stimulation for children with perinatal stroke and hemiparesis , 2017, Neurology.

[31]  Hermano Igo Krebs,et al.  Upper Limb Robotic Therapy for Children with Hemiplegia , 2008, American journal of physical medicine & rehabilitation.

[32]  John H. Martin,et al.  Activity- and use-dependent plasticity of the developing corticospinal system , 2007, Neuroscience & Biobehavioral Reviews.

[33]  S. Scott,et al.  Do children and adolescent ice hockey players with and without a history of concussion differ in robotic testing of sensory, motor and cognitive function? , 2016, Journal of NeuroEngineering and Rehabilitation.

[34]  Correlation of Fractional Anisotropy With Motor Recovery in Patients With Stroke After Postacute Rehabilitation. , 2016, Archives of physical medicine and rehabilitation.

[35]  John W Krakauer,et al.  Robotic therapy for chronic stroke: general recovery of impairment or improved task-specific skill? , 2015, Journal of neurophysiology.

[36]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[37]  A. Kirton,et al.  Life after perinatal stroke. , 2013, Stroke.

[38]  J. Tiffin,et al.  The Purdue pegboard; norms and studies of reliability and validity. , 1948, The Journal of applied psychology.

[39]  A. Eliasson,et al.  The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. , 2006, Developmental medicine and child neurology.

[40]  Michael Erb,et al.  Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. , 2002, Brain : a journal of neurology.

[41]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[42]  H. Krebs,et al.  Robot‐assisted task‐specific training in cerebral palsy , 2009, Developmental medicine and child neurology.

[43]  Adam Kirton,et al.  Kinesthetic deficits after perinatal stroke: robotic measurement in hemiparetic children , 2017, Journal of NeuroEngineering and Rehabilitation.

[44]  Hans Forssberg,et al.  Hand function in relation to brain lesions and corticomotor‐projection pattern in children with unilateral cerebral palsy , 2010, Developmental medicine and child neurology.

[45]  J. Poole,et al.  Functional implications of ipsilesional motor deficits after unilateral stroke. , 2005, Archives of physical medicine and rehabilitation.

[46]  F. Hegazy,et al.  Kinematic characteristics of reaching in children with hemiplegic cerebral palsy: A comparative study , 2017, Brain injury.

[47]  N. Hogan,et al.  Is robot-aided sensorimotor training in stroke rehabilitation a realistic option? , 2001, Current opinion in neurology.

[48]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[49]  J. Dubois,et al.  Diffusion tensor imaging of brain development. , 2006, Seminars in fetal & neonatal medicine.

[50]  Leire Zubiaurre Elorza,et al.  Tractography of the corticospinal tracts in infants with focal perinatal injury: comparison with normal controls and to motor development , 2012, Neuroradiology.

[51]  David L Streiner,et al.  Test-retest reliability, validity, and sensitivity of the Chedoke arm and hand activity inventory: a new measure of upper-limb function for survivors of stroke. , 2005, Archives of physical medicine and rehabilitation.

[52]  J. Eyre,et al.  Corticospinal tract development and its plasticity after perinatal injury , 2007, Neuroscience & Biobehavioral Reviews.

[53]  H. Bourke-Taylor Melbourne Assessment of Unilateral Upper Limb Function: construct validity and correlation with the Pediatric Evaluation of Disability Inventory , 2003, Developmental medicine and child neurology.

[54]  S. Mori,et al.  Quantification of white matter injury following neonatal stroke with serial DTI , 2013, Pediatric Research.

[55]  Adam Kirton,et al.  Robotic Quantification of Position Sense in Children With Perinatal Stroke , 2016, Neurorehabilitation and neural repair.

[56]  G. deVeber,et al.  The Pediatric Stroke Outcome Measure: A Validation and Reliability Study , 2012, Stroke.

[57]  S. Rose,et al.  Changes in the integrity of thalamocortical connections are associated with sensorimotor deficits in children with congenital hemiplegia , 2013, Brain Structure and Function.

[58]  Miyabi Tanaka,et al.  Magnetic stimulation of motor cortex in children: maturity of corticospinal pathway and problem of clinical application , 1997, Brain and Development.

[59]  Stephen H. Scott,et al.  Test–retest reliability of KINARM robot sensorimotor and cognitive assessment: in pediatric ice hockey players , 2015, Journal of NeuroEngineering and Rehabilitation.

[60]  Jennifer A. Semrau,et al.  Examining Differences in Patterns of Sensory and Motor Recovery After Stroke With Robotics , 2015, Stroke.

[61]  Bin Chen,et al.  Correction for direction-dependent distortions in diffusion tensor imaging using matched magnetic field maps , 2006, NeuroImage.

[62]  Harold D. Delaney,et al.  Motor deficits after left or right hemisphere damage due to stroke or tumor , 1981, Neuropsychologia.

[63]  A. Kirton,et al.  Presumed perinatal ischemic stroke: Vascular classification predicts outcomes , 2008, Annals of neurology.

[64]  H Forssberg,et al.  IMPAIRED ANTICIPATORY CONTROL OF ISOMETRIC FORCES DURING GRASPING BY CHILDREN WITH CEREBRAL PALSY , 1992, Developmental medicine and child neurology.

[65]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[66]  Stephen E. Rose,et al.  MRI Structural Connectivity, Disruption of Primary Sensorimotor Pathways, and Hand Function in Cerebral Palsy , 2011, Brain Connect..

[67]  Jacques-Donald Tournier,et al.  Diffusion tensor imaging and beyond , 2011, Magnetic resonance in medicine.

[68]  S. Miller,et al.  Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. , 2000, Brain : a journal of neurology.

[69]  J. Menk,et al.  Synergistic effect of combined transcranial direct current stimulation/constraint-induced movement therapy in children and young adults with hemiparesis: study protocol , 2015, BMC Pediatrics.

[70]  A. Gordon,et al.  Impaired force coordination during object release in children with hemiplegic cerebral palsy , 2000, Developmental medicine and child neurology.

[71]  Derek K. Jones,et al.  Estimating the number of fiber orientations in diffusion MRI voxels : a constrained spherical deconvolution study , 2010 .

[72]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[73]  S. Jang,et al.  Changes of the corticospinal tract in the unaffected hemisphere in stroke patients: A diffusion tensor imaging study , 2016, Somatosensory & motor research.

[74]  H. Forssberg,et al.  Advanced Fiber Tracking in Early Acquired Brain Injury Causing Cerebral Palsy , 2015, American Journal of Neuroradiology.

[75]  A. Connelly,et al.  White matter fiber tractography: why we need to move beyond DTI. , 2013, Journal of neurosurgery.

[76]  S. Yoshida,et al.  Quantitative diffusion tensor tractography of the motor and sensory tract in children with cerebral palsy , 2010, Developmental medicine and child neurology.

[77]  Stephen E. Rose,et al.  Diffusion MRI of the neonate brain: acquisition, processing and analysis techniques , 2012, Pediatric Radiology.

[78]  M. Staudt Reorganization of the developing human brain after early lesions , 2007, Developmental medicine and child neurology.

[79]  J. K. Brown,et al.  A NEUROLOGICAL STUDY OF HAND FUNCTION OF HEMIPLEGIC CHILDREN , 1987, Developmental medicine and child neurology.

[80]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[81]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[82]  H. Carlson,et al.  Segmental Diffusion Properties of the Corticospinal Tract and Motor Outcome in Hemiparetic Children With Perinatal Stroke , 2017, Journal of child neurology.

[83]  John H. Martin,et al.  Pathophysiological mechanisms of impaired limb use and repair strategies for motor systems after unilateral injury of the developing brain , 2013, Developmental medicine and child neurology.

[84]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[85]  S. Scott,et al.  The independence of deficits in position sense and visually guided reaching following stroke , 2012, Journal of NeuroEngineering and Rehabilitation.

[86]  Janice I. Glasgow,et al.  Assessment of Upper-Limb Sensorimotor Function of Subacute Stroke Patients Using Visually Guided Reaching , 2010, Neurorehabilitation and neural repair.