Neural correlates of motor dysfunction in children with traumatic brain injury: exploration of compensatory recruitment patterns.

Traumatic brain injury (TBI) is a common form of disability in children. Persistent deficits in motor control have been documented following TBI but there has been less emphasis on changes in functional cerebral activity. In the present study, children with moderate to severe TBI (n = 9) and controls (n = 17) were scanned while performing cyclical movements with their dominant and non-dominant hand and foot according to the easy isodirectional (same direction) and more difficult non-isodirectional (opposite direction) mode. Even though the children with TBI were shown to be less successful on various items of a clinical motor test battery than the control group, performance on the coordination task during scanning was similar between groups, allowing a meaningful interpretation of their brain activation differences. fMRI analysis revealed that the TBI children showed enhanced activity in medial and anterior parietal areas as well as posterior cerebellum as compared with the control group. Brain activation generally increased during the non-isodirectional as compared with the isodirectional mode and additional regions were involved, consistent with their differential degree of difficulty. However, this effect did not interact with group. Overall, the findings indicate that motor impairment in TBI children is associated with changes in functional cerebral activity, i.e. they exhibit compensatory activation reflecting increased recruitment of neural resources for attentional deployment and somatosensory processing.

[1]  Li Yao,et al.  Ipsilateral brain deactivation specific to the nondominant hand during simple finger movements , 2008, Neuroreport.

[2]  S. Swinnen,et al.  Systems Neuroplasticity in the Aging Brain: Recruiting Additional Neural Resources for Successful Motor Performance in Elderly Persons , 2008, The Journal of Neuroscience.

[3]  S. Swinnen,et al.  The missing link between action and cognition , 2007, Progress in Neurobiology.

[4]  H S Levin,et al.  cerebellar atrophy after moderate-to-severe pediatric traumatic brain injury. , 2007, AJNR. American journal of neuroradiology.

[5]  M. Filippi,et al.  Influence of body segment position during in‐phase and antiphase hand and foot movements: A kinematic and functional MRI study , 2007, Human brain mapping.

[6]  E. Park,et al.  Heavy neurofilament accumulation and α-spectrin degradation accompany cerebellar white matter functional deficits following forebrain fluid percussion injury , 2007, Experimental Neurology.

[7]  M. Potts,et al.  Injury severity determines Purkinje cell loss and microglial activation in the cerebellum after cortical contusion injury , 2007, Experimental Neurology.

[8]  N. Ward,et al.  The neural substrates of motor recovery after focal damage to the central nervous system. , 2006, Archives of physical medicine and rehabilitation.

[9]  P. Ellen Grant,et al.  Developmental neural networks in children performing a Categorical N-Back Task , 2006, NeuroImage.

[10]  M. Jongmans,et al.  Rhythmic coordination of hand and foot in children with Developmental Coordination Disorder. , 2006, Child: care, health and development.

[11]  N. Ward Compensatory mechanisms in the aging motor system , 2006, Ageing Research Reviews.

[12]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[13]  E. Park,et al.  Purkinje Cell Vulnerability to Mild and Severe Forebrain Head Trauma , 2006, Journal of neuropathology and experimental neurology.

[14]  L. Cohen,et al.  Neuroimaging Patterns Associated with Motor Control in Traumatic Brain Injury , 2006, Neurorehabilitation and neural repair.

[15]  M. Hallett,et al.  A functional MRI study of automatic movements in patients with Parkinson's disease. , 2005, Brain : a journal of neurology.

[16]  S. Swinnen,et al.  Neural Basis of Aging: The Penetration of Cognition into Action Control , 2005, The Journal of Neuroscience.

[17]  S. Swinnen,et al.  The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour , 2005, The European journal of neuroscience.

[18]  Helen M. Bramlett,et al.  Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat , 2005, Acta Neuropathologica.

[19]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[20]  M. Hallett,et al.  The influence of normal human ageing on automatic movements , 2005, The Journal of physiology.

[21]  Kyla Pennington,et al.  Differential responses in three thalamic nuclei in moderately disabled, severely disabled and vegetative patients after blunt head injury. , 2004, Brain : a journal of neurology.

[22]  Tobias Sommer,et al.  Evidence of Developmental Differences in Implicit Sequence Learning: An fMRI Study of Children and Adults , 2004, Journal of Cognitive Neuroscience.

[23]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

[24]  Sterling C. Johnson,et al.  Neuroimaging correlates of the Halstead Finger Tapping Test several years post-traumatic brain injury , 2004, Brain injury.

[25]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[26]  F Debaere,et al.  Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency , 2004, NeuroImage.

[27]  S. Swinnen,et al.  Two hands, one brain: cognitive neuroscience of bimanual skill , 2004, Trends in Cognitive Sciences.

[28]  J. Kuhtz-Buschbeck,et al.  Sensorimotor recovery in children after traumatic brain injury: analyses of gait, gross motor, and fine motor skills. , 2003, Developmental medicine and child neurology.

[29]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[30]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[31]  S. Cramer,et al.  Motor Cortex Organization After Stroke Is Related to Side of Stroke and Level of Recovery , 2003, Stroke.

[32]  Richard S. J. Frackowiak,et al.  Age-related changes in the neural correlates of motor performance. , 2003, Brain : a journal of neurology.

[33]  P. Brown,et al.  The importance of the dominant hemisphere in the organization of bimanual movements , 2003, Human brain mapping.

[34]  J. Kuhtz-Buschbeck,et al.  Analyses of gait, reaching, and grasping in children after traumatic brain injury. , 2003, Archives of physical medicine and rehabilitation.

[35]  H. Levin,et al.  Neuroplasticity following non-penetrating traumatic brain injury , 2003, Brain injury.

[36]  Abraham Z. Snyder,et al.  The Feasibility of a Common Stereotactic Space for Children and Adults in fMRI Studies of Development , 2002, NeuroImage.

[37]  A R McIntosh,et al.  Functional reorganisation of memory after traumatic brain injury: a study with H2150 positron emission tomography , 2002, Journal of neurology, neurosurgery, and psychiatry.

[38]  Hans Forssberg,et al.  Brain Regions Controlling Nonsynergistic versus Synergistic Movement of the Digits: a Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[39]  S. Swinnen Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[40]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[41]  Gabriella Cerri,et al.  Coordination of coupled hand and foot movements during childhood , 2001, Experimental Brain Research.

[42]  Paul Van Hecke,et al.  Brain Areas Involved in Interlimb Coordination: A Distributed Network , 2001, NeuroImage.

[43]  R. Zafonte,et al.  Verbal Recall and Recognition Following Traumatic Brain Injury: A [O-15]-Water Positron Emission Tomography Study , 2001, Journal of clinical and experimental neuropsychology.

[44]  J. Ghajar Traumatic brain injury , 2000, The Lancet.

[45]  H. Forssberg,et al.  Simultaneous movements of upper and lower limbs are coordinated by motor representations that are shared by both limbs: a PET study , 2000, The European journal of neuroscience.

[46]  O. Hikosaka,et al.  What and When: Parallel and Convergent Processing in Motor Control , 2000, The Journal of Neuroscience.

[47]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[48]  Seong-Gi Kim,et al.  Effects of movement predictability on cortical motor activation , 1998, Neuroscience Research.

[49]  A. Cools,et al.  Evidence for lateral premotor and parietal overactivity in Parkinson's disease during sequential and bimanual movements. A PET study. , 1998, Brain : a journal of neurology.

[50]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[51]  A Weindl,et al.  Central motor processing in Huntington's disease. A PET study. , 1997, Brain : a journal of neurology.

[52]  G. Rizzolatti,et al.  Parietal cortex: from sight to action , 1997, Current Opinion in Neurobiology.

[53]  Natalia Dounskaia,et al.  Egocentric and Allocentric Constraints in the Expression of Patterns of Interlimb Coordination , 1997, Journal of Cognitive Neuroscience.

[54]  P A Bandettini,et al.  Relationship between Finger Movement Rate and Functional Magnetic Resonance Signal Change in Human Primary Motor Cortex , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[55]  S. J. Sullivan,et al.  Motor fitness in children and adolescents with traumatic brain injury. , 1996, Archives of physical medicine and rehabilitation.

[56]  C. Svarer,et al.  Rate Dependence of Regional Cerebral Activation during Performance of a Repetitive Motor Task: A PET Study , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[57]  L. Noble,et al.  Cellular response in the cerebellum after midline traumatic brain injury in the rat , 1996, Neuroscience Letters.

[58]  R. Nudo,et al.  Neural Substrates for the Effects of Rehabilitative Training on Motor Recovery After Ischemic Infarct , 1996, Science.

[59]  D. McArthur,et al.  Epidemiologic aspects of brain injury. , 1996, Neurologic clinics.

[60]  L. Pitts,et al.  Purkinje cell vulnerability to mild traumatic brain injury. , 1996, Journal of neurotrauma.

[61]  J. Kelso,et al.  Phase Transitions and Critical Fluctuations in Rhythmic Coordination of Ipsilateral Hand and Foot. , 1995, Journal of motor behavior.

[62]  S. P. Swinnen,et al.  Relative Phase Alterations During Bimanual Skill Acquisition. , 1995, Journal of motor behavior.

[63]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[64]  K. Jaffe,et al.  Motor performance in children after traumatic brain injury. , 1993, Archives of physical medicine and rehabilitation.

[65]  Richard S. J. Frackowiak,et al.  The functional anatomy of motor recovery after stroke in humans: A study with positron emission tomography , 1991, Annals of neurology.

[66]  S. P. Swinnen,et al.  Relative phase destabilization during interlimb coordination: the disruptive role of kinesthetic afferences induced by passive movement , 1990, Experimental Brain Research.

[67]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[68]  J. Kelso Phase transitions and critical behavior in human bimanual coordination. , 1984, The American journal of physiology.

[69]  U. Norrsell Behavioral studies of the somatosensory system. , 1980, Physiological reviews.

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

[71]  A. Kaelin-Lang Enhancing rehabilitation of motor deficits with peripheral nerve stimulation. , 2008, NeuroRehabilitation.

[72]  Andrzej Urbanik,et al.  Brain correlates of right-handedness. , 2007, Acta neurobiologiae experimentalis.

[73]  Stephan P. Swinnen,et al.  Neural Networks Involved in Cyclical Interlimb Coordination as Revealed by Medical Imaging Techniques , 2004 .

[74]  F. Chollet,et al.  The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. , 1997, Brain : a journal of neurology.

[75]  J. M. Ollinger,et al.  Positron Emission Tomography , 2018, Handbook of Small Animal Imaging.

[76]  J E Sniezek,et al.  Incidence of mild and moderate brain injury in the United States, 1991. , 1996, Brain injury.

[77]  J. E. Davis,et al.  Crossing cultural divides: moral conflict and the Cairo population conference. , 1995, Virginia review of sociology.

[78]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[79]  Paul E. Hamburger,et al.  On an automated method , 1966, ACM '66.

[80]  B. Berle,et al.  neural substrates of , 2022 .