Cortical Reorganization Following Bimanual Training and Somatosensory Stimulation in Cervical Spinal Cord Injury: A Case Report

Background and Purpose Deficits in upper-extremity function in individuals with tetraplegia are primarily due to the loss of motor pathways. Detrimental cortical reorganization, however, may create further loss of function. The purpose of this case report is to describe the cortical changes associated with a combination intervention using bimanual massed practice training with somatosensory stimulation. Case Description “BR” was a 22-year-old man with C6 tetraplegia and hand impairment who participated in this training intervention for 3 weeks. Outcomes BR demonstrated improvements in sensory function, strength (the force-generating capacity of muscle), and performance of functional hand skills. Following the training, the cortical motor map of the biceps brachii muscle shifted anteriorly and increased in area and volume. Discussion This is the first documented case in which changes in the size and location of the cortical map were associated with an intervention and improvement in function in an individual with tetraplegia. This case suggests that an intensive training intervention may induce both functional and neurophysiological changes.

[1]  S. Anand,et al.  Transcranial magnetic stimulation: Neurophysiological applications and safety , 2002, Brain and Cognition.

[2]  M. Hammond,et al.  Sensory perception threshold measurement: an evaluation of semiobjective testing devices. , 1987, Archives of physical medicine and rehabilitation.

[3]  N. Davey,et al.  Comparison of input-output patterns in the corticospinal system of normal subjects and incomplete spinal cord injured patients , 1999, Experimental Brain Research.

[4]  T. Matyas,et al.  Can simultaneous bilateral movement involve the undamaged hemisphere in reconstruction of neural networks damaged by stroke? , 2000, Disability and rehabilitation.

[5]  Graham H. Creasey,et al.  International Standards for Neurological and Functional Classification of Spinal Cord Injury. American Spinal Injury Association. , 1997 .

[6]  L G Cohen,et al.  Mechanisms, functional relevance and modulation of plasticity in the human central nervous system. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[7]  Paolo Maria Rossini,et al.  Modulation of Corticospinal Output to Human Hand Muscles Following Deprivation of Sensory Feedback , 1998, NeuroImage.

[8]  J. Liepert,et al.  Motor cortex plasticity during constraint-induced movement therapy in stroke patients , 1998, Neuroscience Letters.

[9]  R. Waters,et al.  International Standards for Neurological and Functional Classification of Spinal Cord Injury , 1997, Spinal Cord.

[10]  H. Ralston,et al.  The terminations of corticospinal tract axons in the macaque monkey , 1985, The Journal of comparative neurology.

[11]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[12]  W. Donovan,et al.  A test of the 1992 International Standards for Neurological and Functional Classification of Spinal Cord Injury , 1998, Spinal Cord.

[13]  R. Thatcher,et al.  Cortical motor reorganization after paraplegia , 1999, Neurology.

[14]  T. S. Miles,et al.  Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects , 2000, Experimental Brain Research.

[15]  E. Field-Fote,et al.  Massed Practice versus Massed Practice with Stimulation: Effects on Upper Extremity Function and Cortical Plasticity in Individuals with Incomplete Cervical Spinal Cord Injury , 2005, Neurorehabilitation and neural repair.

[16]  K. Mills,et al.  Responses in small hand muscles from magnetic stimulation of the human brain. , 1987, The Journal of physiology.

[17]  K. Anderson.  Targeting recovery: priorities of the spinal cord-injured population. , 2004, Journal of neurotrauma.

[18]  L. Cohen,et al.  Increase in hand muscle strength of stroke patients after somatosensory stimulation , 2002, Annals of neurology.

[19]  H. Woldag,et al.  Change of facilitation during voluntary bilateral hand activation after stroke , 2005, Journal of the Neurological Sciences.

[20]  M. Toyokura,et al.  Activation of Pre–Supplementary Motor Area (SMA) and SMA Proper During Unimanual and Bimanual Complex Sequences: An Analysis Using Functional Magnetic Resonance Imaging , 2002, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[21]  A. Luft,et al.  Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. , 2004, JAMA.

[22]  C. Jerosch-Herold.  Assessment of Sensibility after Nerve Injury and Repair: A Systematic Review of Evidence for Validity, Reliability and Responsiveness of Tests , 2005, Journal of hand surgery.

[23]  Relevance of stimulus duration for activation of motor and sensory fibers: implications for the study of H-reflexes and magnetic stimulation. , 1992 .

[24]  Mark Hallett,et al.  Constraint-Induced Therapy in Stroke: Magnetic-Stimulation Motor Maps and Cerebral Activation , 2003, Neurorehabilitation and neural repair.

[25]  S. Wolf,et al.  Intra- and intersubject reliability of abductor pollicis brevis muscle motor map characteristics with transcranial magnetic stimulation. , 2005, Archives of physical medicine and rehabilitation.

[26]  J. Cauraugh.  Coupled rehabilitation protocols and neural plasticity: upper extremity improvements in chronic hemiparesis. , 2004, Restorative neurology and neuroscience.

[27]  T. Lejeune,et al.  Paradoxical effect of digital anaesthesia on force and corticospinal excitability , 2005, Neuroreport.

[28]  Edward Taub,et al.  Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. , 2004, Restorative neurology and neuroscience.

[29]  M. Hallett,et al.  Relevance of stimulus duration for activation of motor and sensory fibers: implications for the study of H-reflexes and magnetic stimulation. , 1988, Electroencephalography and clinical neurophysiology.

[30]  Takashi Hanakawa,et al.  Enduring representational plasticity after somatosensory stimulation , 2005, NeuroImage.

[31]  Hatem Alkadhi,et al.  Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. , 2002, Brain : a journal of neurology.

[32]  M Hallett,et al.  Reorganization of corticospinal pathways following spinal cord injury , 1991, Neurology.

[33]  J. Liepert,et al.  Training‐induced changes of motor cortex representations in stroke patients , 2000, Acta neurologica Scandinavica.

[34]  C. Winstein,et al.  Bimanual Training After Stroke: Are Two Hands Better Than One? , 2004, Topics in stroke rehabilitation.

[35]  W. Byblow,et al.  Symmetric facilitation between motor cortices during contraction of ipsilateral hand muscles , 2001, Experimental Brain Research.

[36]  J B Green,et al.  Cortical sensorimotor reorganization after spinal cord injury , 1998, Neurology.

[37]  Arthur F. Gmitro,et al.  Cortical mechanisms for acquisition and performance of bimanual motor sequences , 2003, NeuroImage.

[38]  S. Wolf,et al.  Finger extensor variability in TMS parameters among chronic stroke patients , 2005, Journal of NeuroEngineering and Rehabilitation.

[39]  John Cadwell,et al.  Focal magnetic coil stimulation reveals motor cortical system reorganized in humans after traumatic quadriplegia , 1990, Brain Research.

[40]  V. Dietz,et al.  Differential effect of spinal cord injury and functional impairment on human brain activation. , 2002, Journal of neurotrauma.

[41]  C B Novak,et al.  Development of a new measure of fine sensory function. , 1993, Plastic and reconstructive surgery.

[42]  L. Noreau,et al.  Comparison of three methods to assess muscular strength in individuals with spinal cord injury , 1998, Spinal Cord.

[43]  恵子 紀国谷.  国際生活機能分類(International Classification of Functioning, Disability and Health: ICF)にみた福祉・保健・医療の専門職協働における連携に関する貢献と課題 , 2007 .

[44]  M. Malcolm,et al.  Reliability of motor cortex transcranial magnetic stimulation in four muscle representations , 2006, Clinical Neurophysiology.

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

[46]  Lutz Jäncke,et al.  Bimanual versus unimanual coordination: what makes the difference? , 2004, NeuroImage.

[47]  P H Ellaway,et al.  Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury , 1998, Journal of neurology, neurosurgery, and psychiatry.

[48]  R. Nudo,et al.  Effects of Repetitive Motor Training on Movement Representations in Adult Squirrel Monkeys: Role of Use versus Learning , 2000, Neurobiology of Learning and Memory.

[49]  W. Donovan,et al.  The International Standards Booklet for Neurological and Functional Classification of Spinal Cord Injury , 1994, Paraplegia.

[50]  H. Seelen,et al.  Evaluation of upper extremity motor function tests in tetraplegics , 2002, Spinal Cord.

[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]  Maarten J. IJzerman,et al.  Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics , 2004, Spinal Cord.

[53]  S. Weinstein.  Fifty years of somatosensory research: from the Semmes-Weinstein monofilaments to the Weinstein Enhanced Sensory Test. , 1993, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[54]  G. Lundborg,et al.  A model instrument for the documentation of outcome after nerve repair. , 2000, The Journal of hand surgery.

[55]  N. Sadato,et al.  Role of the Supplementary Motor Area and the Right Premotor Cortex in the Coordination of Bimanual Finger Movements , 1997, The Journal of Neuroscience.

[56]  W. Triggs,et al.  Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation , 1999, Brain Research.

[57]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[58]  Y. Shinoda,et al.  Projection from area 3a to the motor cortex by neurons activated from group I muscle afferents , 1978, Experimental Brain Research.

[59]  J. D. Coulter,et al.  Organization of corticospinal neurons in the cat , 1978, Brain Research.

[60]  S L Wolf,et al.  Conditioning of the spinal stretch reflex: implications for rehabilitation. , 1990, Physical therapy.

[61]  M. T. J. Buñuales,et al.  La clasificación internacional del funcionamiento de la discapacidad y de la salud (CIF) 2001 , 2002 .

[62]  B. Dobkin,et al.  Immediate and Long-Term Changes in Corticomotor Output in Response to Rehabilitation: Correlation with Functional Improvements in Chronic Stroke , 2004, Neurorehabilitation and neural repair.

[63]  J Machetanz,et al.  Reorganization of human motor cortex after hand replantation , 2001, Annals of neurology.

[64]  Gitendra Uswatte,et al.  Constraint-induced movement therapy: bridging from the primate laboratory to the stroke rehabilitation laboratory. , 2003, Journal of rehabilitation medicine.

[65]  S. Wolf,et al.  Repetitive Task Practice: A Critical Review of Constraint-Induced Movement Therapy in Stroke , 2002, The neurologist.

[66]  Mark Hallett,et al.  Mechanisms of Deafferentation-Induced Plasticity in Human Motor Cortex , 1998, The Journal of Neuroscience.