Nervous system reorganization following injury

Contrary to the classical view of a pre-determined wiring pattern, there is considerable evidence that cortical representation of body parts is continuously modulated in response to activity, behavior and skill acquisition. Both animal and human studies showed that following injury of the peripheral nervous system such as nerve injury or amputation, the somatosensory cortex that responded to the deafferented body parts become responsive to neighboring body parts. Similarly, there is expansion of the motor representation of the stump area following amputation. Reorganization of the sensory and motor systems following peripheral injury occurs in multiple levels including the spinal cord, brainstem, thalamus and cortex. In early-blind subjects, the occipital cortex plays an important role in Braille reading, suggesting that there is cross-modal plasticity. Functional recovery frequently occurs following a CNS injury such as stroke. Motor recovery from stroke may be associated with the adjacent cortical areas taking over the function of the damaged areas or utilization of alternative motor pathways. The ipsilateral motor pathway may mediate motor recovery in patients who undergo hemispherectomy early in life and in children with hemiplegic cerebral palsy, but it remains to be determined if it plays a significant role in the recovery of adult stroke. One of the challenges in stroke recovery is to identify which of the many neuroimaging and neurophysiological changes demonstrated are important in mediating recovery. The mechanism of plasticity probably differs depending on the time frame. Rapid changes in motor representations within minutes are likely due to unmasking of latent synapses involving modulation of GABAergic inhibition. Changes over a longer time likely involve other additional mechanisms such as long-term potentiation, axonal regeneration and sprouting. While cross-modal plasticity appears to be useful in enhancing the perceptions of compensatory sensory modalities, the functional significance of motor reorganization following peripheral injury remains unclear and some forms of sensory reorganization may even be associated with deleterious consequences like phantom pain. An understanding of the mechanism of plasticity will help to develop treatment programs to improve functional outcome.

[1]  Ralph B. D'Agostino,et al.  Time Course of Functional Recovery After Stroke: The Framingham Study , 1989 .

[2]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[3]  H. Freund,et al.  Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation , 2004, Experimental Brain Research.

[4]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M Hallett,et al.  Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm , 1992, Neurology.

[6]  C Muchnik,et al.  Central auditory skills in blind and sighted subjects. , 1991, Scandinavian audiology.

[7]  P. M. Rossini,et al.  Short-term brain ‘plasticity’ in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia , 1994, Brain Research.

[8]  V E Amassian,et al.  A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. , 1990, Electroencephalography and clinical neurophysiology.

[9]  M. Kotila,et al.  The Profile Of Recovery From Stroke And Factors Influencing Outcome , 1984, Stroke.

[10]  J. Rauschecker,et al.  Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  M. Nicolelis,et al.  Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information , 1993, Nature.

[13]  M. Hallett,et al.  Cortical motor representation of the ipsilateral hand and arm , 2004, Experimental Brain Research.

[14]  M. Hallett,et al.  Plasticity of the Human Motor Cortex , 1993 .

[15]  M. Hallett,et al.  Modulation of motor cortical outputs to the reading hand of braille readers , 1993, Annals of neurology.

[16]  H. Tsuji,et al.  Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation , 1996, Neuroscience Letters.

[17]  G. Bernardi,et al.  Cerebral plasticity after stroke as revealed by ipsilateral responses to magnetic stimulation. , 1996, Neuroreport.

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

[19]  J. Metzler,et al.  Functional changes in cat somatic sensory-motor cortex during short-term reversible epidural blocks , 1979, Brain Research.

[20]  P. Delwaide,et al.  Can motor recovery in stroke patients be predicted by early transcranial magnetic stimulation? , 1996, Stroke.

[21]  M. Hallett,et al.  Functional relevance of cross-modal plasticity in blind humans , 1997, Nature.

[22]  Daniel B Hier,et al.  Infarct topography and hemiparesis profiles with cerebral convexity infarction: the Stroke Data Bank. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[23]  B. Steinhoff,et al.  Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study , 1996, Annals of neurology.

[24]  S. Wise,et al.  The Acquisition of Motor Behavior in Vertebrates , 1996 .

[25]  C. Caltagirone,et al.  Involvement of the healthy hemisphere in recovery from aphasia and motor deficit in patients with cortical ischemic infarction , 1995, Neurology.

[26]  M. Hallett,et al.  Effects of transcranial magnetic stimulation on ipsilateral muscles , 1991, Neurology.

[27]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[28]  M. Schwab Myelin-associated inhibitors of neurite growth and regeneration in the CNS , 1990, Trends in Neurosciences.

[29]  J R Wolpaw,et al.  Motoneuron plasticity underlying operantly conditioned decrease in primate H-reflex. , 1994, Journal of neurophysiology.

[30]  Yukio Mano,et al.  Central motor reorganization after anastomosis of the musculocutaneous and intercostal nerves following cervical root avulsion , 1995, Annals of neurology.

[31]  J P Malin,et al.  Cortical reorganization in patients with facial palsy , 1997, Annals of neurology.

[32]  M. Merzenich,et al.  Age-dependent capacity for somatosensory cortex reorganization in chronic spinal cats. , 1987, Brain research.

[33]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[34]  R. G. Lee,et al.  Mechanisms Underlying Functional Recovery Following Stroke , 1995, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[35]  鯨井 隆 Corticocortical inhibition in human motor cortex , 1994 .

[36]  J Valls-Solé,et al.  Rapid modulation of human cortical motor outputs following ischaemic nerve block. , 1993, Brain : a journal of neurology.

[37]  N Birbaumer,et al.  Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. , 1994, Neuroreport.

[38]  J. Donoghue,et al.  Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[39]  C. Fisher,et al.  Concerning the Mechanism of Recovery in Stroke Hemiphegia , 1992, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[40]  H. Freund,et al.  Plasticity of the human motor cortex. , 1997, Advances in neurology.

[41]  Roger N Lemon,et al.  Stroke recovery , 1993, Current Biology.

[42]  Can motor recovery in stroke patients be predicted by early cortical magnetic stimulation , 1996 .

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

[44]  E G Jones,et al.  Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  V L Towle,et al.  Functional magnetic resonance studies of the reorganization of the human hand sensorimotor area after unilateral brain injury in the perinatal period. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[47]  S. Hahn Motor Reorganization After Upper Limb Amputation in Man , 1992 .

[48]  J P Donoghue,et al.  Motor Areas of the Cerebral Cortex , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[49]  H. Mushiake,et al.  Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery , 2004, Experimental Brain Research.

[50]  J. Rothwell,et al.  Interaction between intracortical inhibition and facilitation in human motor cortex. , 1996, The Journal of physiology.

[51]  J. Kaas,et al.  Mechanisms of reorganization in sensory systems of primates after peripheral nerve injury. , 1997, Advances in neurology.

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

[53]  E. G. Jones,et al.  Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17 , 1986, Nature.

[54]  M. Merzenich,et al.  Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly. , 1991, Journal of neurophysiology.

[55]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[56]  J. Rauschecker,et al.  Auditory compensation for early blindness in cat cerebral cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[58]  M Hallett,et al.  Effects of phenytoin on cortical excitability in humans , 1997, Neurology.

[59]  R. N. Lemon,et al.  Non-invasive brain stimulation reveals reorganised cortical outputs in amputees , 1990, Neuroscience Letters.

[60]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[61]  E. Roth,et al.  Multivariate analysis of improvement and outcome following stroke rehabilitation. , 1987, Archives of neurology.

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

[63]  R. J. Seitz,et al.  Thalamic metabolism and corticospinal tract integrity determine motor recovery in stroke , 1996, Annals of neurology.

[64]  Walter Paulus,et al.  The effect of lorazepam on the motor cortical excitability in man , 1996, Experimental Brain Research.

[65]  M. Merzenich,et al.  Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. , 1987, Progress in brain research.

[66]  S. Bandinelli,et al.  Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. , 1991, Brain : a journal of neurology.

[67]  J. Kalaska,et al.  Chronic paw denervation causes an age-dependent appearance of novel responses from forearm in "paw cortex" of kittens and adult cats. , 1979, Journal of neurophysiology.

[68]  J. Wolpaw,et al.  Operantly conditioned motoneuron plasticity: possible role of sodium channels. , 1995, Journal of neurophysiology.

[69]  B. Day,et al.  Stimulation of the human motor cortex through the scalp , 1991, Experimental physiology.

[70]  E. Taub,et al.  Chronic deafferentation in monkeys differentially affects nociceptive and nonnociceptive pathways distinguished by specific calcium-binding proteins and down-regulates gamma-aminobutyric acid type A receptors at thalamic levels. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. Donoghue,et al.  Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions , 2004, Experimental Brain Research.

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

[73]  C Pantev,et al.  Reorganizational and perceptional changes after amputation. , 1996, Brain : a journal of neurology.

[74]  Á. Pascual-Leone,et al.  Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. , 1993, Brain : a journal of neurology.

[75]  D J Felleman,et al.  Recovery of normal topography in the somatosensory cortex of monkeys after nerve crush and regeneration. , 1983, Science.

[76]  A. Aguayo,et al.  Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. , 1981, Science.

[77]  J. Rauschecker,et al.  Auditory Localization Behaviour in Visually Deprived Cats , 1994, The European journal of neuroscience.

[78]  L M Harrison,et al.  Patterns of central motor reorganization in hemiplegic cerebral palsy. , 1993, Brain : a journal of neurology.

[79]  J C Rothwell,et al.  Intra-operative recording of motor tract potentials at the cervico-medullary junction following scalp electrical and magnetic stimulation of the motor cortex. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[80]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

[81]  P. Manger,et al.  Plasticity of the somatosensory cortical map in macaque monkeys after chronic partial amputation of a digit , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[82]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[83]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[84]  M Hallett,et al.  Physiological analysis of motor reorganization following lower limb amputation. , 1992, Electroencephalography and clinical neurophysiology.

[85]  L Bozzao,et al.  Motor recovery after stroke. Morphological and functional brain alterations. , 1996, Brain : a journal of neurology.

[86]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[87]  B Kirschenbaum,et al.  In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. , 1994, Cerebral cortex.

[88]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  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.

[90]  E. G. Jones,et al.  Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. , 1991, Journal of neurophysiology.

[91]  Jon H. Kaas,et al.  Central reorganization of sensory pathways following peripheral nerve regeneration in fetal monkeys , 1996, Nature.

[92]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  H. Tsuji,et al.  Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. , 1997, The Journal of physiology.

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

[95]  P Ashby,et al.  Ipsilateral fast corticospinal pathways do not account for recovery in stroke , 1992, Annals of neurology.

[96]  J. Donoghue,et al.  Dynamic organization of primary motor cortex output to target muscles in adult rats I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions , 2004, Experimental Brain Research.

[97]  J P Donoghue,et al.  Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[98]  J C Rothwell,et al.  Reorganization of cortical blood flow and transcranial magnetic stimulation maps in human subjects after upper limb amputation. , 1994, Journal of neurophysiology.

[99]  M. Hallett,et al.  Regional cerebral blood flow changes in motor cortical areas after transient anesthesia of the forearm , 1995, Annals of neurology.

[100]  V. Ramachandran,et al.  Perceptual correlates of massive cortical reorganization. , 1992, Neuroreport.

[101]  Fisher Cm,et al.  Concerning the Mechanism of Recovery in Stroke Hemiphegia , 1992 .

[102]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[103]  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.

[104]  R. H. Ray,et al.  Functional reorganization of adult raccoon somatosensory cerebral cortex following neonatal digit amputation , 1981, Brain Research.

[105]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[106]  E. Welker,et al.  Plasticity in the barrel cortex of the adult mouse: Effects of peripheral deprivation on GAD-immunoreactivity , 2004, Experimental Brain Research.

[107]  G. Bertrand,et al.  The position and organization of motor fibers in the internal capsule found during stereotactic surgery. , 1979, Applied neurophysiology.