Corticospinal tract development and its plasticity after perinatal injury

Neuroscience and Biobehavioral Reviews

Volumn 31, Issue 8, 2007, Pages 1136-1149

  Eyre, J A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Corticospinal; Development; Human; Plasticity

Indexed keywords

BRAIN DAMAGE; CEREBRAL PALSY; CORTICOSPINAL TRACT DEVELOPMENT; HEMIPLEGIA; HEMISPHERE; HUMAN; LONG TERM MEMORY; MEMORY DISORDER; MOTOR CORTEX; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR CORTEX; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; HUMANS; NEURONAL PLASTICITY; PRENATAL INJURIES; PYRAMIDAL TRACTS;

EID: 36349000576     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2007.05.011     Document Type: Review

References (96)

1. Armand J., Olivier E., Edgley S.A., and Lemon R.N. Postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the Macaque monkey. Journal of Neuroscience 17 (1997) 251-266
2. Balbi P., Trojano L., Ragno M., Perretti A., and Santoro L. Patterns of motor control reorganization in a patient with mirror movements. Clinical Neurophysiology 111 (2000) 318-325
3. Barth T.M., and Stanfield B.B. The recovery of forelimb placing behaviour in rats with neonatal unilateral cortical damage involves the remaining hemisphere. Journal of Neuroscience 10 (1990) 3449-3459
4. Bates C., and Killackey H. The emergence of a discretely distributed pattern of corticospinal projectoin neurons. Developmental Brain Research 13 (1984) 265-273
5. Benecke R., Meyer B.U., and Freund H.J. Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation. Experimental Brain Research 83 (1991) 419-426
6. Bouza H., Dubowitz L., Rutherford M., and Pennock J. Prediction of outcome in children with congenital hemiplegia: a magnetic resonance imaging study. Neuropediatrics 25 (1994) 60-66
7. Cao Y., Vikingstad E.M., Huttenlocher P.R., Towle V.L., and Levin D.N. Functional magnetic resonance studies of the reorganisation of human sensorimotor area after unilateral brain injury in the perinatal period. Proceedings of the National Academy of Sciences 91 (1994) 9612-9616
8. Carr L., Harrison L., Evans A., and Stephens J. Patterns of central motor reorganisation in hemiplegic cerebral palsy. Brain 116 (1993) 1223-1247
9. Chu D., Huttenlocher P., Levin D., and Towle V. Reorganization of the hand somatosensory cortex following perinatal unilateral brain injury. Neuropediatrics 31 (2000) 63-69
10. Clowry G., Davies B., Upile N., Gibson C., and Bradley P. Spinal cord plasticity in response to unilateral inhibition of the rat motor cortex during development: changes to gene expression, muscle afferents and the ipsilateral corticospinal projection. European Journal of Neuroscience 20 (2004) 2555-2566
11. Culham J., and Valyear K. Human parietal cortex in action. Current Opinion in Neurobiology 16 (2006) 205-212
12. Curfs M.H.J.M., Gribnan A.A.M., and Dederen P.J.W.C. Selective elimination of transient corticospinal projections in the rat cervical spinal grey matter. Brain Research Developmental Brain Research 78 (1994) 182-190
13. Curfs M.H.J.M., Gribnan A.A.M., Dederen P.J.W.C., and Bergervoet-Vernooij H.W.M. Transient functional connections between the developing corticospinal tract and cervical spianl interneurone as demonstrated by c-fos immunohistochemistry. Developmental Brain Research 87 (1995) 214-219
14. Curfs M.H.J.M., Gribnan A.A.M., and Dederen P.J.W.C. Direct cortico-motoneuronal synaptic contacts are present in the adult rat cervical spinal cord and are first established at postnatal day 7. Neuroscience Letters 205 (1996) 123-126
15. Davies, B., 2001. Activity Dependent Development of Corticospinal and Segmental Inputs to Interneurones and Motoneurones [B Med Sci]. University of Newcastle, Newcastle upon Tyne.
16. Edgley S.A., Eyre J.A., Lemon R.N., and Miller S. Comparison of activation of corticospinal neurones and spinal motoneurones by magnetic and electrical stimulation in the monkey. Brain 120 (1997) 839-853
17. Eyre JA. Developmental aspects of corticospinal projections. In: Eisen A. (Ed). Motor Neuron Diseases (2005), Elsevier, Amsterdam
18. Eyre J., Gibson M., Koh T., and Miller S. Corticospinal transmission excited by electromagnetic stimulation of the brain is impaired in children with spastic hemiparesis but not those with quadriparesis. Journal of Physiology (London) 414 (1989) 9pp
19. Eyre J., Miller S., Clowry G., Conway E., and Watts C. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 123 (2000) 51-64
20. Eyre J., Taylor J., Villagra F., and Miller S. Exuberant ipsilateral corticospinal projections are present in the human newborn and withdrawn during development probably involving an activity-dependent process. Developmental Medicine and Child Neurology 82 (2000) 12
21. Eyre J., Taylor J., Villagra F., Smith M., and Miller S. Evidence of activity-dependent withdrawal of corticospinal projections during human development. Neurology 57 (2001) 1543-1554
22. Eyre J.A., Dobson C., Villagra F., Clowry G.J., Smith M., Kenwrick S., Donnai D., and Miller S. Abnormal corticospinal tract function but no evidence for abnormal axonal guidance in human subjects with L1CAM mutation. Brain 124 (2001) 2393-2406
23. Eyre J.A., Miller S., Clowry G.J., Conway E.A., and Watts C. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 123 (2000) 51-64
24. Eyre J.A., Miller S., and Clowry G.J. The development of the corticospinal tract in humans. In: Pascual-Leone A., Davey G., Rothwell J., and Wasserman E.M. (Eds). Handbook of Transcranial Magnetic Stimulation (2002), Arnold, London 235-249
25. Eyre J., Smith M., Dabydeen L., Clowry G., Petacchi E., Battini R., Guzzetta A., and Cioni G. Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system?. Annals of Neurology PMID (2007) 17444535 [Epub ahead of print]
26. Galea M., and Darian-Smith I. Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cerebral Cortex 4 (1994) 166-194
27. Galea M.P., and Darian-Smith I. Postnatal maturation of the direct corticospinal projections in the macaque monkey. Cerebral Cortex 5 (1995) 518-540
28. Galea M.P., and Darian-Smith I. Corticospinal projection patterns following unilateral section of the cervical spinal cord in the newborn and juvenile macaque monkey. Journal of Comparative Neurology 381 (1997) 282-306
29. Gibson C., Arnott G., and Clowry G. Spinal cord plasticity in response to motor cortex lesions during development in rat. Journal of Physiology 520 (1999) 76P-77P
30. Gibson C.L., Arnott G.A., and Clowry G.C. Plasticity in the rat spinal cord seen in response to lesions to the motor cortex during development but not to lesions in maturity. Experimental Neurology 166 (2000) 422-434
31. Graveline C., Mikulis D., Crawley A., and Hwang P. Regionalized sensorimotor plasticity after hemispherectomy fMRI evaluation. Pediatric Neurology 19 (1998) 337-342
32. Heide G., Witte O., and Ziemann U. Physiology of modulation of motor cortex excitability by low-frequency suprathreshold repetitive transcranial magnetic stimulation. Experimental Brain Research 171 (2006) 26-34
33. Hendricks H., Zwarts M., Plat E., and van Limbeek J. Systematic review for the early prediction of motor and functional outcome after stroke by using motor-evoked potentials. Archives of the Physical Medicine and Rehabilitation 83 (2002) 1303-1308
34. Hendricks H., Pasman J., van Limbeek J., and Zwarts M. Motor evoked potentials in predicting recovery from upper extremity paralysis after acute stroke. Cerebrovascular Diseases 16 (2003) 265-271
35. Hertz-Pannier L. Plasticite au cours de la maturation cerebrale: bases physogiques et etude par IRM fontionelle. Journal of Neuroradiology 26 (1999) IS66-IS74
36. Hicks S., and D'Amato C. Motor-sensory and visual behaviour after hemispherectomy in newborn and mature rats. Experimental Neurology 29 (1970) 416-438
37. Hicks S., and D'Amato C. Locating corticospinal neurons by retrograde axonal transport of horseradish peroxidase. Experimental Neurology 56 (1977) 410-420
38. Holloway V., Chong W., Connelly A., Harkness W., and Gadian D. Somatomotor fMRI and the presurgical evaluation of a case of focal epilepsy. Clinical Radiology 54 (1999) 301-303
39. Huttenlocher P.R., and Raichelson R.M. Effects of neonatal hemispherectomy on location and number of corticospinal neurons in the rat. Brain Research Developmental Brain Research 47 (1989) 59-69
40. Jankowska E., and Roberts W.J. Synaptic actions of single interneurones mediating reciprocal 1a inhibition of motoneurones. Journal of Physiology 222 (1972) 623-642
41. Jankowska E., Padel Y., and Tanaka R. Projections of pyramidal cells to alpha motoneurones innervating hind limb muscles in the monkey. Journal of Physiology 249 (1975) 637-667
42. Jankowska E., Padel Y., and Tanaka R. Disynaptic inhibition of spinal motoneurones from the motor cortex of the monkey. Journal of Physiology 258 (1976) 467-487
43. Jansen E.M., and Low W.C. Quantitative analysis of contralateral hemisphere hypertrophy and sensorimotor performance in adult rats following unilateral neonatal ischemic-hypoxic brain injury. Brain Research 708 (1996) 93-99
44. Joosten E., Schuitman R., Vermelis M., and Dederen P. Postnatal development of the ipsilateral corticospinal component in rat spinal cord: a light and electron microscopic anterograde HRP study. Journal of Comparative Neurology 326 (1992) 133-146
45. Kamiyama T., Yoshioka N., and Sakurai M. Synapse elimination in the corticospinal projection during the early postnatal period. Journal of Neurophysiology 95 (2006) 2304-2313
46. Kartje-Tillotson G., Neafsey E.J., and Castro A.J. Electrophysiological and analysis of motor cortical plasticity after cortical lesions in newborn rats. Brain Research 332 (1985) 103-111
47. Kartje-Tillotson G., O' Donoghue D.L., Dauzvardis M.F., and Castro A.J. Pyramidotomy abolishes the abnormal movements evoked by intracortical microstimulation in adult rats that sustained neonatal cortical lesions. Brain Research 415 (1987) 172-177
48. Kennard M. Age and other factors in motor recovery for precentral lesions in monkeys. American Journal of Physiology 115 (1936) 138-146
49. Konstantinidou A., Silos-Santiago I., Flaris N., and Snider W. Development of primary afferent projection in the human spinal cord. Journal of Comparative Neurology 354 (1995) 11-12
50. Kuypers H.G.J.M. Corticospinal connections: postnatal development in the rhesus monkey. Science 138 (1962) 678-680
51. Lacroix S., Havton L., McKay H., Yang H., Brant A., Roberts J., and Tuszynski M. Bilateral corticospinal projections arise from each motor cortex in the macaque monkey: a quantitative study. Journal of Comparative Neurology 473 (2004) 147-161
52. LaMantia A.S., and Rakic P. Axonal over production and elimination in the corpus callosum of the developing rhesus monkey. Journal of Neuroscience 10 (1990) 2156-2175
53. LaMantia A.S., and Rakic P. Axon over production and elimination in the anterior commissure of the developing rhesus monkey. Journal of Comparative Neurology 340 (1994) 328-336
54. Leong S.K. A qualitative electron microscopic investigation of the anomalous corticofugal projections following neonatal lesions in the albino rat. Brain Research 107 (1976) 1-8
55. Lewine J.D., Astur R.S., Davis L.E., Knight J.E., Maclin E.L., and Orrison W.W. Cortical organization in adulthood is modified by neonatal infarct: a case study. Radiology 190 (1994) 93-96
56. Liu C., and Chambers W. An experimental study of the cortico-spinal system in the monkey. The spinal pathways and preterminal distribution of degenerating fibres following discrete lesions of the pre- and postcentral gyri and bulbar pyramid. Journal of Comparative Neurology 123 (1964) 257-284
57. Maegaki Y., Yamamoto T., and Takeshita K. Plasticity of central motor and sensory pathways in a case of unilateral extensive cortical dysplasia. Investigation of magnetic resonance imaging, transcranial magnetic stimulation and short latency somatosensory evoked potentials. Neurology 45 (1995) 2255-2261
58. Martin J. The corticospinal system: from development to motor control. The Neuroscientist 11 (2005) 161-173
59. Martin J.H., and Lee S.J. Activity-dependent competition between developing corticospinal terminations. Neuroreport 10 (1999) 2277-2282
60. Martin J.H., Kably B., and Hacking A. Activity-dependent development of cortical axon terminations in the spinal cord and brain stem. Experimental Brain Research 125 (1999) 184-199
61. McClung J.R., and Castro A.J. An ultrastructional study of ipsilateral corticospinal projections after frontal cortical lesions in newborn rats. Anatomical Record 181 (1975) 417-418
62. McDonough S., Clowry G., Miller S., and Eyre J. Group 1a inhibition and renshaw (recurrent) inhibition are functional in man at birth. Brain Research 899 (2001) 66-81
63. Meng Z., and Martin J. Postnatal development of corticospinal postsynaptic action. Journal of Neurophysiology 90 (2003) 683-692
64. Muller R.A., Rothermel R.D., Behen M.E., Muzik O., Chakraborty P.K., and Chugani H.T. Plasticity of motor organization in children and adults. Neuroreport 8 (1997) 3103-3108
65. Muller R.A., Watson C.E., Muzik O., Chakraborty P.K., and Chugani H.T. Motor organization after early middle cerebral artery stroke: a PET study. Pediatric Neurology 19 (1998) 294-298
66. Nathan P., Smith M., and Deacon P.V. The corticospinal tracts in man. Course and location of fibres at different segmental levels. Brain 113 (1990) 303-324
67. Netz J., Lammers T., and Hömberg V. Reorganization of motor output in the non-affected hemisphere after stroke. Brain 120 (1997) 1579-1586
68. Nezu A., Kimura S., Uehara S., Kobayashi T., Tanaka M., and Saito K. Maturity of corticospinal pathway and problem of clinical application. Brain and Development 19 (1997) 176-180
69. Nirkko A.C., Rosler K.M., Ozdoba C., Heid O., Schroth G., and Hess C.W. Human cortical plasticity. Functional recovery with mirror movements. Neurology 48 (1997) 1090-1093
70. O'Leary D., Schlaggar B., and Stanfield B. The specification of sensory cortex: lessons from cortical transplantation. Experimental Neurology 115 (1992) 121-126
71. O'Sullivan M.C., Eyre J.A., and Miller S. Radiation of the phasic stretch reflex in biceps brachii to muscles of the armin man and its restriction during development. Journal of Physiology (London) 439 (1991) 529-543
72. O'Sullivan M.C., Miller S., Ramesh V., Conway E., Gilfillan K., McDonough S., and Eyre J.A. Abnormal development of biceps brachii phasic stretch reflex and persistence of short latency heteronymous excitatory responses to triceps brachii in spastic cerebral palsy. Brain 121 (1998) 2381-2395
73. Okado N., and Kojima T. Ontogeny of the central nervous system: neurogenesis, fibre connection, synaptogenesis and myelination in the spinal cord. In: Prechtl H. (Ed). Continuity of Neural Functions from Prenatal Life to Postnatal Life (1984), McKeith Press, London 31-45
74. Oudega M., Varon S., and Hagg T. Distribution of corticospinal motor neurons in the postnatal rat: quantitative evidence for massive collateral elimination and modest cell death. Journal of Comparative Neurology 347 (1994) 115-126
75. Passingham R.E., Perry R.E., and Wilkinson F. The long term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 106 (1983) 675-705
76. Payne B., and Lomber S. Reconstructing functional systems after lesions of the cerebral cortex. Nature Reviews Neuroscience 2 (2001) 911-919
77. Plassman B., and Gandevia S. High voltage stimulation over human spinal cord: sources of latency variation. Journal of Neurology Neurosurgery and Psychiatry 52 (1989) 213-217
78. Porter R., and Hoare J. The time course of minimal corticomotoneuronal excitatory post synaptic potentials in lumbar motoneurones of the monkey. Journal of Neurophysiology 32 (1969) 443-451
79. Quartarone A., Bagnato S., Rizzo V., Morgante F., Sant'angelo A., Battaglia F., Messina C., Siebner H., and Girlanda P. Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Experimental Brain Research 161 (2005) 114-124
80. Reinoso B.S., and Castro A.J. A study of corticospinal remodelling using retrograde fluorescent tracers in rats. Experimental Brain Research 74 (1989) 387-394
81. Rouiller E.M., Liang P., Moret V., and Wiesendanger M. Trajectory of redirected corticospinal axons after unilateral lesion of the sensorimotor cortex in neonatal rat; a phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Experimental Neurology 114 (1991) 53-65
82. Salimi I., and Martin J. Rescuing transient corticospinal terminations and promoting growth with corticospinal stimulation in kittens. Journal of Neuroscience 24 (2004) 4952-4961
83. Scales D.A., and Collins G.H. Cerebral degeneration with hypertrophy of the contralateral pyramid. Archives of Neurology 26 (1972) 186-190
84. Schreyer D., and Jones E. Growth and target finding by axons of the corticospinal tract in prenatal and postnatal rats. Neuroscience 7 (1982) 1387-1853
85. Stanfield B.B., and O'Leary D.D. The transient corticospinal projection from the occipital cortex during postnatal development of the rat. Journal of Comparative Neurology 238 (1985) 236-248
86. Stanfield B.B., O'Leary D.D.M., and Fricks C. Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298 (1982) 371-373
87. Staudt M., Gerloff C., Grodd W., Holthausen H., Niemann G., and Krägeloh-Mann I. Reorganization in congenital hemiparesis acquired at different gestational ages. Annals of Neurology 56 (2004) 854-863
88. Szelenyi A., Bueno de Camargo A., and Deletis V. Neurophysiological evaluation of the corticospinal tract by D-wave recording in young children. Childs Nervous System 19 (2003) 30-34
89. Terashima T. Anatomy, development and lesion induced plasticity of rodent corticospinal tract. Neuroscience Research 22 (1995) 139-161
90. Thickbroom G., Byrnes M., Archer S., Nagarajan L., and Mastaglia F. Differences in sensory and motor cortical organization following brain injury early in life. Annals of Neurology 49 (2001) 320-327
91. Uematsu J., Ono K., Yamano T., and Shimanda M. Development of corticospinal tract fibres and their plasticity II. Neonatal unilateral cortical damage and subsequent development of the corticospinal tract in mice. Brain and Development 18 (1996) 173-178
92. Verhaart J. On thick and thin fibres in the pyramidal tracts. Acta Psychiatrica et Neurologica 22 (1947) 271-281
93. Verhaart J. Hypertrophy of the pes pedunculi and pyramid as a result of degeneration of the contralateral corticofugal fibre tracts. Journal of Comparative Neurology 92 (1950) 1-15
94. Wiesel T., and Hubel D. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. Journal of Neurophysiology 28 (1965) 1029-1040
95. Wieser H., Henke K., Zumsteg D., Taub E., Yonekawa Y., and Buck A. Activation of the left motor cortex during left leg movements after right central resection. Journal of Neurology Neurosurgery and Psychiatry 67 (1999) 487-491
96. Wu C., and Hunter D. Amblyopia: diagnostic and therapeutic options. American Journal of Ophthalmology 141 (2006) 175-184