Cortical Plasticity during Motor Learning and Recovery after Ischemic Stroke

The motor system has the ability to adapt to environmental constraints and injury to itself. This adaptation is often referred to as a form of plasticity allowing for livelong acquisition of new movements and for recovery after stroke. We are not sure whether learning and recovery work via same or similar neural mechanisms. But, all these processes require widespread changes within the matrix of the brain. Here, basic mechanisms of these adaptations on the level of cortical circuitry and networks are reviewed. We focus on the motor cortices because their role in learning and recovery has been investigated more thoroughly than other brain regions.

[1]  Randolph J. Nudo,et al.  Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys , 2006, Experimental Brain Research.

[2]  J. Kleim,et al.  Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning , 2004, The Journal of Neuroscience.

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

[4]  T. Murphy,et al.  Longitudinal in vivo Imaging Reveals Balanced and Branch-Specific Remodeling of Mature Cortical Pyramidal Dendritic Arbors after Stroke , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  K. Molina-Luna,et al.  Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays , 2007, Journal of Neuroscience Methods.

[6]  K. Furie,et al.  Heart disease and stroke statistics--2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. , 2008, Circulation.

[7]  S. Carmichael,et al.  Plasticity of Cortical Projections after Stroke , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[8]  A. Luft,et al.  Protein synthesis inhibition blocks consolidation of an acrobatic motor skill. , 2004, Learning & memory.

[9]  G. Quirk,et al.  The organization of the rat motor cortex: A microstimulation mapping study , 1986, Brain Research Reviews.

[10]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[11]  Karl J. Friston,et al.  Functional reorganization of the brain in recovery from striatocapsular infarction in man , 1992, Annals of neurology.

[12]  R. Nudo,et al.  Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. , 1996, Journal of neurophysiology.

[13]  T. Jones,et al.  Use-dependent growth of pyramidal neurons after neocortical damage , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  P M Rossini,et al.  Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. , 1997, Stroke.

[15]  S. Barbay,et al.  Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. , 2006, Journal of neurophysiology.

[16]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  S. Carmichael,et al.  New Patterns of Intracortical Projections after Focal Cortical Stroke , 2001, Neurobiology of Disease.

[18]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[19]  T. Robinson,et al.  Brain Plasticity and Behavior , 2003, Annual review of psychology.

[20]  G. Teskey,et al.  Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation , 2004, Neuroscience.

[21]  Timothy H Murphy,et al.  Rapid Morphologic Plasticity of Peri-Infarct Dendritic Spines After Focal Ischemic Stroke , 2008, Stroke.

[22]  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.

[23]  Jerry Silver,et al.  Regeneration beyond the glial scar , 2004, Nature Reviews Neuroscience.

[24]  E. Bullmore,et al.  Society for Neuroscience Abstracts , 1997 .

[25]  S. Carmichael Cellular and molecular mechanisms of neural repair after stroke: Making waves , 2006, Annals of neurology.

[26]  Theresa A. Jones,et al.  Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage , 1992, Brain Research.

[27]  Ann M. Stowe,et al.  Extensive Cortical Rewiring after Brain Injury , 2005, The Journal of Neuroscience.

[28]  R J Andrews,et al.  Transhemispheric diaschisis. A review and comment. , 1991, Stroke.

[29]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[30]  Y. Gioanni,et al.  A reappraisal of rat motor cortex organization by intracortical microstimulation , 1985, Brain Research.

[31]  M. Merzenich,et al.  Experience-induced plasticity of cutaneous maps in the primary somatosensory cortex of adult monkeys and rats , 1996, Journal of Physiology-Paris.

[32]  J. Sanes,et al.  Orderly Somatotopy in Primary Motor Cortex: Does It Exist? , 2001, NeuroImage.

[33]  Andreas R. Luft,et al.  Motor learning transiently changes cortical somatotopy , 2008, NeuroImage.

[34]  K. Zilles,et al.  Neuronal Hyperexcitability and Reduction of GABAA-Receptor Expression in the Surround of Cerebral Photothrombosis , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[35]  T. Neumann-Haefelin,et al.  Increased long‐term potentiation in the surround of experimentally induced focal cortical infarction , 1998, Annals of neurology.

[36]  A. Luft,et al.  Motor Skill Learning Depends on Protein Synthesis in Motor Cortex after Training , 2004, The Journal of Neuroscience.

[37]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[38]  Marie-H Monfils,et al.  In Search of the Motor Engram: Motor Map Plasticity as a Mechanism for Encoding Motor Experience , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[39]  H Asanuma,et al.  Neurobiological basis of motor learning in mammals. , 1997, Neuroreport.

[40]  J. Donoghue,et al.  Strengthening of horizontal cortical connections following skill learning , 1998, Nature Neuroscience.

[41]  Norton W. Milgram,et al.  Post-activation potentiation in the neocortex. IV. Multiple sessions required for induction of long-term potentiation in the chronic preparation , 1995, Brain Research.

[42]  Gary F. Egan,et al.  Evolution of Brain Activation with Good and Poor Motor Recovery after Stroke , 2006, Neurorehabilitation and neural repair.

[43]  J. Kleim,et al.  Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization , 2001, Behavioural Brain Research.

[44]  R. Nudo,et al.  3.21 – Neurophysiology of Motor Skill Learning , 2008 .

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

[46]  A. Maude REVIEW AND COMMENTARY , 2006 .

[47]  K. Uğurbil,et al.  Analysis of fMRI and finger tracking training in subjects with chronic stroke. , 2002, Brain : a journal of neurology.

[48]  J. Larson,et al.  Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. , 1985, Behavioral and neural biology.

[49]  S. Barbay,et al.  Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. , 2003, Journal of neurophysiology.

[50]  Alan J Thompson,et al.  The influence of time after stroke on brain activations during a motor task , 2004, Annals of neurology.

[51]  R. Krishnan RELEARNING TOWARD MOTOR RECOVERY IN STROKE, SPINAL CORD INJURY, AND CEREBRAL PALSY: A COGNITIVE NEURAL SYSTEMS PERSPECTIVE , 2006, The International journal of neuroscience.

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

[53]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[54]  Ling Wang,et al.  Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain , 2011, Proceedings of the National Academy of Sciences.

[55]  D. Corbett,et al.  Efficacy of Rehabilitative Experience Declines with Time after Focal Ischemic Brain Injury , 2004, The Journal of Neuroscience.

[56]  R. Nudo,et al.  Role of adaptive plasticity in recovery of function after damage to motor cortex , 2001, Muscle & nerve.

[57]  G. Teskey,et al.  Induction of long‐term depression is associated with decreased dendritic length and spine density in layers III and V of sensorimotor neocortex , 2004, Synapse.

[58]  S. Carmichael,et al.  Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex , 2005, Experimental Neurology.

[59]  S. Cramer,et al.  Brain Function Early after Stroke in Relation to Subsequent Recovery , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[60]  Jeff Biernaskie,et al.  Enriched Rehabilitative Training Promotes Improved Forelimb Motor Function and Enhanced Dendritic Growth after Focal Ischemic Injury , 2001, The Journal of Neuroscience.

[61]  Michael W. Salter,et al.  Src kinases: a hub for NMDA receptor regulation , 2004, Nature Reviews Neuroscience.

[62]  J. Donoghue,et al.  Plasticity of the synaptic modification range. , 2007, Journal of neurophysiology.

[63]  J. Kleim,et al.  Functional reorganization of the rat motor cortex following motor skill learning. , 1998, Journal of neurophysiology.

[64]  Jin Li,et al.  A New Hierarchical ID-Based Cryptosystem and CCA-Secure PKE , 2006, EUC Workshops.

[65]  S. Cramer,et al.  Activity in the Peri-Infarct Rim in Relation to Recovery From Stroke , 2006, Stroke.

[66]  A Keller,et al.  Intrinsic synaptic organization of the motor cortex. , 1993, Cerebral cortex.

[67]  J. Kleim,et al.  Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination , 1996, Brain Research.

[68]  E. M. Rouiller,et al.  Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys , 1999, Experimental Brain Research.

[69]  J. Kleim,et al.  Long-term potentiation induces expanded movement representations and dendritic hypertrophy in layer V of rat sensorimotor neocortex. , 2004, Cerebral cortex.

[70]  S. Barbay,et al.  Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. , 2008, Journal of neurophysiology.

[71]  S. Thomas Carmichael,et al.  Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke , 2006, Neurobiology of Disease.

[72]  Andreas R. Luft,et al.  Speed of motor re-learning after experimental stroke depends on prior skill , 2007, Experimental Brain Research.

[73]  M. Tuszynski,et al.  Lesions of the Basal Forebrain Cholinergic System Impair Task Acquisition and Abolish Cortical Plasticity Associated with Motor Skill Learning , 2003, Neuron.

[74]  S. Carmichael,et al.  Tissue Microenvironments within Functional Cortical Subdivisions Adjacent to Focal Stroke , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[75]  J. P. Miller,et al.  Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. , 2006, JAMA.

[76]  W. Greenough,et al.  Reach training selectively alters dendritic branching in subpopulations of layer II–III pyramids in rat motor-somatosensory forelimb cortex , 1989, Neuropsychologia.

[77]  Carlos Portera-Cailliau,et al.  Absence of Large-Scale Dendritic Plasticity of Layer 5 Pyramidal Neurons in Peri-Infarct Cortex , 2011, The Journal of Neuroscience.

[78]  J. Donoghue,et al.  Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. , 1994, Journal of neurophysiology.