Ipsilateral Motor Pathways after Stroke: Implications for Non-Invasive Brain Stimulation

In humans the two cerebral hemispheres have essential roles in controlling the upper limb. The purpose of this article is to draw attention to the potential importance of ipsilat-eral descending pathways for functional recovery after stroke, and the use of non-invasive brain stimulation (NBS) protocols of the contralesional primary motor cortex (M1). Conventionally NBS is used to suppress contralesional M1, and to attenuate transcallosal inhibition onto the ipsilesional M1. There has been little consideration of the fact that contralesional M1 suppression may also reduce excitability of ipsilateral descending pathways that may be important for paretic upper limb control for some patients. One such ipsilateral pathway is the cortico-reticulo-propriospinal pathway (CRPP). In this review we outline a neuro-physiological model to explain how contralesional M1 may gain control of the paretic arm via the CRPP. We conclude that the relative importance of the CRPP for motor control in individual patients must be considered before using NBS to suppress contralesional M1. Neurophysiological, neuroimaging, and clinical assessments can assist this decision making and facilitate the translation of NBS into the clinical setting.

[1]  Y. Höller,et al.  Functional brain reorganization after spinal cord injury: Systematic review of animal and human studies , 2013, Brain Research.

[2]  Matthew Petoe,et al.  The PREP algorithm predicts potential for upper limb recovery after stroke. , 2012, Brain : a journal of neurology.

[3]  B. Bussel,et al.  Effects of anodal tDCS on lumbar propriospinal system in healthy subjects , 2012, Clinical Neurophysiology.

[4]  D. Burke,et al.  Enhanced propriospinal excitation from hand muscles to wrist flexors during reach-to-grasp in humans. , 2012, Journal of neurophysiology.

[5]  Heidi Johansen-Berg,et al.  Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke , 2011, Brain : a journal of neurology.

[6]  D. Nowak,et al.  Functional neuromuscular stimulation to improve severe hand dysfunction after stroke: Does inhibitory rTMS enhance therapeutic efficiency? , 2011, Experimental Neurology.

[7]  W. Byblow,et al.  Cathodal transcranial direct current stimulation of the primary motor cortex improves selective muscle activation in the ipsilateral arm. , 2011, Journal of neurophysiology.

[8]  V Achache,et al.  Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects , 2011, The Journal of physiology.

[9]  S. Jang,et al.  Combined study of transcranial magnetic stimulation and diffusion tensor tractography for prediction of motor outcome in patients with corona radiata infarct. , 2011, Journal of rehabilitation medicine.

[10]  Gereon R Fink,et al.  The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. , 2011, Cerebral cortex.

[11]  Steven C Cramer,et al.  Anatomy of Stroke Injury Predicts Gains From Therapy , 2011, Stroke.

[12]  K. Funase,et al.  Increased excitability and reduced intracortical inhibition in the ipsilateral primary motor cortex during a fine-motor manipulation task , 2011, Brain Research.

[13]  K. Funase,et al.  Excitability changes in the ipsilateral primary motor cortex during rhythmic contraction of finger muscles , 2011, Neuroscience Letters.

[14]  C. Stinear,et al.  Prediction of recovery of motor function after stroke , 2010, The Lancet Neurology.

[15]  Min-Kyun Oh,et al.  Effect of Transcranial Direct Current Stimulation on Motor Recovery in Patients with Subacute Stroke , 2010, American journal of physical medicine & rehabilitation.

[16]  S. Cramer Stratifying patients with stroke in trials that target brain repair. , 2010, Stroke.

[17]  S. Jang,et al.  Comparison of TMS and DTT for predicting motor outcome in intracerebral hemorrhage , 2010, Journal of the Neurological Sciences.

[18]  G. Fink,et al.  Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling , 2010, NeuroImage.

[19]  M. Hinder,et al.  The ipsilateral motor cortex contributes to cross‐limb transfer of performance gains after ballistic motor practice , 2010, The Journal of physiology.

[20]  T. Isa,et al.  Compensatory Changes at the Cerebral Cortical Level after Spinal Cord Injury , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[21]  L. Cohen,et al.  Scaling of motor cortical excitability during unimanual force generation , 2009, Cortex.

[22]  T. Isa,et al.  A subcortical oscillatory network contributes to recovery of hand dexterity after spinal cord injury , 2009, Brain : a journal of neurology.

[23]  W. Byblow,et al.  Task-dependent modulation of propriospinal inputs to human shoulder. , 2008, Journal of neurophysiology.

[24]  Pablo Celnik,et al.  Controversy: Noninvasive and invasive cortical stimulation show efficacy in treating stroke patients , 2008, Brain Stimulation.

[25]  J. Rothwell,et al.  Theta burst stimulation induces after‐effects on contralateral primary motor cortex excitability in humans , 2008, The Journal of physiology.

[26]  S. Misawa,et al.  The ipsilateral cortico‐spinal tract is activated after hemiparetic stroke , 2008, European journal of neurology.

[27]  R. Lemon Descending pathways in motor control. , 2008, Annual review of neuroscience.

[28]  Gereon R Fink,et al.  Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. , 2008, Archives of neurology.

[29]  L. Cohen,et al.  Memory formation in the motor cortex ipsilateral to a training hand. , 2008, Cerebral cortex.

[30]  Leonardo G. Cohen,et al.  Mechanisms Underlying Functional Changes in the Primary Motor Cortex Ipsilateral to an Active Hand , 2008, The Journal of Neuroscience.

[31]  G. Fink,et al.  Effects of rTMS on grip force control following subcortical stroke , 2008, Experimental Neurology.

[32]  W. Byblow,et al.  Priming the motor system enhances the effects of upper limb therapy in chronic stroke. , 2008, Brain : a journal of neurology.

[33]  G. Fink,et al.  Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging , 2008, Annals of neurology.

[34]  H. Onoe,et al.  Time-Dependent Central Compensatory Mechanisms of Finger Dexterity After Spinal Cord Injury , 2007, Science.

[35]  Eric J. Perreault,et al.  Side of lesion influences bilateral activation in chronic, post-stroke hemiparesis , 2007, Clinical Neurophysiology.

[36]  E. Pierrot-Deseilligny,et al.  Task‐related changes in propriospinal excitation from hand muscles to human flexor carpi radialis motoneurones , 2007, The Journal of physiology.

[37]  Marc H Schieber,et al.  Bilateral Spike-Triggered Average Effects in Arm and Shoulder Muscles from the Monkey Pontomedullary Reticular Formation , 2007, The Journal of Neuroscience.

[38]  Alan J Thompson,et al.  The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke , 2007, The European journal of neuroscience.

[39]  W. Byblow,et al.  Functional potential in chronic stroke patients depends on corticospinal tract integrity. , 2006, Brain : a journal of neurology.

[40]  B. Alstermark,et al.  Properties of propriospinal neurons in the C3-C4 segments mediating disynaptic pyramidal excitation to forelimb motoneurons in the macaque monkey. , 2006, Journal of neurophysiology.

[41]  Christian Gerloff,et al.  The Role of Multiple Contralesional Motor Areas for Complex Hand Movements after Internal Capsular Lesion , 2006, The Journal of Neuroscience.

[42]  M Davare,et al.  Role of the ipsilateral primary motor cortex in controlling the timing of hand muscle recruitment. , 2006, Cerebral cortex.

[43]  Richard S. J. Frackowiak,et al.  Motor system activation after subcortical stroke depends on corticospinal system integrity. , 2006, Brain : a journal of neurology.

[44]  Adam G. Davidson,et al.  Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging , 2006, Experimental Brain Research.

[45]  Ichiro Watanabe,et al.  Repetitive Transcranial Magnetic Stimulation of Contralesional Primary Motor Cortex Improves Hand Function After Stroke , 2005, Stroke.

[46]  Sergio P. Rigonatti,et al.  Transcranial direct current stimulation of the unaffected hemisphere in stroke patients , 2005, Neuroreport.

[47]  David Burke,et al.  The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders , 2005 .

[48]  Sergio P. Rigonatti,et al.  A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients , 2005, Neurology.

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

[50]  W. Byblow,et al.  The Contribution of Cervical Propriospinal Premotoneurons in Recovering Hemiparetic Stroke Patients , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[51]  J. Bloch,et al.  Progressive plastic changes in the hand representation of the primary motor cortex parallel incomplete recovery from a unilateral section of the corticospinal tract at cervical level in monkeys , 2004, Brain Research.

[52]  Adam G Davidson,et al.  Motor outputs from the primate reticular formation to shoulder muscles as revealed by stimulus-triggered averaging. , 2004, Journal of neurophysiology.

[53]  Winston D. Byblow,et al.  Proposed cortical and sub-cortical contributions to the long-latency stretch reflex in the forearm , 2004, Experimental Brain Research.

[54]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[55]  Richard S. J. Frackowiak,et al.  Neural correlates of outcome after stroke: a cross-sectional fMRI study. , 2003, Brain : a journal of neurology.

[56]  Sabine Meunier,et al.  Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. , 2003, Brain : a journal of neurology.

[57]  Christian Gerloff,et al.  Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? , 2003, Clinical Neurophysiology.

[58]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  P. Rossini,et al.  Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. , 2002, Brain : a journal of neurology.

[60]  G. Abbruzzese,et al.  Motor recovery following stroke: a transcranial magnetic stimulation study , 2000, Clinical Neurophysiology.

[61]  M Hallett,et al.  Changes in motor cortex excitability during ipsilateral hand muscle activation in humans , 2000, Clinical Neurophysiology.

[62]  M Hallett,et al.  Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract , 1998, The Journal of physiology.

[63]  V. Hömberg,et al.  Reorganization of motor output in the non-affected hemisphere after stroke. , 1997, Brain : a journal of neurology.

[64]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[65]  R N Lemon,et al.  Contralateral and ipsilateral EMG responses to transcranial magnetic stimulation during recovery of arm and hand function after stroke. , 1996, Electroencephalography and clinical neurophysiology.

[66]  B. Alstermark,et al.  Motoneuronal projection pattern of single C3-C4 propriospinal neurones. , 1996, Canadian journal of physiology and pharmacology.

[67]  W. Fries,et al.  Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. , 1993, Brain : a journal of neurology.

[68]  H. Kuypers,et al.  Cells of origin of cortical projections to dorsal column nuclei, spinal cord and bulbar medial reticular formation in the rhesus monkey , 1976, Neuroscience Letters.

[69]  Alvaro Pascual-Leone,et al.  rTMS combined with motor learning training in healthy subjects. , 2006, Restorative neurology and neuroscience.

[70]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[71]  M. Hallett,et al.  Excitability of the ipsilateral motor cortex during phasic voluntary hand movement , 2002, Experimental Brain Research.

[72]  H. Kuypers,et al.  THE DESCENDING PATHWAYS TO THE SPINAL CORD, THEIR ANATOMY AND FUNCTION. , 1964, Progress in brain research.

[73]  A JOURNAL OF NEUROLOGY REVIEW ARTICLE , 2022 .

[74]  S. Edgley,et al.  Newcastle University E-prints Citation for Item: Publisher's Copyright Statement: Changes in Descending Motor Pathway Connectivity after Corticospinal Tract Lesion in Macaque Monkey , 2022 .