Unexpected survival of neurons of origin of the pyramidal tract after spinal cord injury

Journal of Neuroscience

Volumn 30, Issue 34, 2010, Pages 11516-11528

  Nielson, Jessica L ^a,b   Sears Kraxberger, Ilse ^a   Strong, Melissa K ^a,b   Wong, Jamie K ^a,b   Willenberg, Rafer ^a,b   Steward, Oswald ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL SURVIVAL; CERVICAL SPINAL CORD; CONTROLLED STUDY; INJURY SEVERITY; MYELINATED NERVE; NERVE CELL; NERVE DEGENERATION; NERVE FIBER; NERVE FIBER DEGENERATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SPINAL CORD INJURY; THORACIC SPINAL CORD;

ANIMALS; CELL SURVIVAL; CERVICAL VERTEBRAE; MALE; NEURONS; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; THORACIC VERTEBRAE; WALLERIAN DEGENERATION;

EID: 77956113769     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1433-10.2010     Document Type: Article

References (74)

1. Anderson KD, Gunawan A, Steward O (2005) Quantitative assessment of forelimb motor function after cervical spinal cord injury in rats: relationship to the corticospinal tract. Exp Neurol 194:161-174.
2. Barron KD, Dentinger MP (1979) Cytologic observations on axotomized feline Betz cells. 1. Qualitative electron microscopic findings. J Neuropathol Exp Neurol 38:128-151.
3. Barron KD, Dentinger MP, Popp AJ, Mankes R (1988) Neurons of layer Vb of rat sensorimotor cortex atrophy but do not die after thoracic cord transection. J Neuropathol Exp Neurol 47:62-74.
4. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
5. Beirowski B, Berek L, Adalbert R, Wagner D, Grumme DS, Addicks K, Ribchester RR, Coleman MP (2004) Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J Neurosci Methods 134:23-35.
6. Beltramino CA, de Olmos JS, Gallyas F, Heimer L, Záborszky L (1993) Silver staining as a tool for neurotoxic assessment. NIDA Res Monogr 136:101-126; discussion 126-132.
7. Benkovic SA, O'Callaghan JP, Miller DB (2004) Sensitive indicators of injury reveal hippocampal damage in C57BL/6J mice treated with kainic acid in the absence of tonic-clonic seizures. Brain Res 1024:59-76.
8. Beresford WA (1965) A discussion on retrograde changes in nerve fibres. Prog Brain Res 14:33-56.
9. Bodian D (1946) Spinal projections of brain-stem in rhesus monkey, deduced from retrograde chromatolysis. Anat Rec 94:512-513.
10. Bonatz H, Röhrig S, Mestres P, Meyer M, Giehl KM (2000) An axotomy model for the induction of death of rat and mouse corticospinal neurons in vivo. J Neurosci Methods 100:105-115.
11. Bresnahan JC, Beattie MS, Stokes BT, Conway KM (1991) Three-dimensional computer-assisted analysis of graded contusion lesions in the spinal cord of the rat. J Neurotrauma 8:91-101.
12. Brodal A, Walberg F (1952) Ascending fibers in pyramidal tract of cat. AMA Arch Neurol Psychiatry 68:755-775.
13. Brodal A, Walberg F (1982) A re-evaluation of the question of ascending fibers in the pyramidal tract. Brain Res 232:271-281.
14. Carlson J, Armstrong B, Switzer RC 3rd, Ellison G (2000) Selective neurotoxic effects of nicotine on axons in fasciculus retroflexus further support evidence that this a weak link in brain across multiple drugs of abuse. Neuropharmacology 39:2792-2798.
15. Carlson J, Noguchi K, Ellison G (2001) Nicotine produces selective degeneration in the medial habenula and fasciculus retroflexus. Brain Res 906:127-134.
16. Coleman M (2005) Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6:889-898.
17. Crawley AP, Jurkiewicz MT, Yim A, Heyn S, Verrier MC, Fehlings MG, Mikulis DJ (2004) Absence of localized grey matter volume changes in the motor cortex following spinal cord injury. Brain Res 1028:19-25.
18. Davison C (1937) Syndrome of the anterior spinal artery of the medulla. AMA Arch Neurol Psychiatry 37:91-107.
19. Deckwerth TL, Johnson EM Jr (1994) Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis). Dev Biol 165:63-72.
20. de Olmos JS, Beltramino CA, de Olmos de Lorenzo S (1994) Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicol Teratol 16:545-561.
21. Dunkerley GB, Duncan D (1969) A light and electron microscopic study of the normal and the degenerating corticospinal tract in the rat. J Comp Neurol 137:155-183.
22. Feringa ER, Vahlsing HL (1985) Labeled corticospinal neurons one year after spinal cord transection. Neurosci Lett 58:283-286.
23. Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4:369-374.
24. FitzGerald MJT, Gruener G, Mtui E (2007) Clinical neuroanatomy and neuroscience, Ed 5. Philadelphia: Elsevier Saunders.
25. Ganchrow D, Bernstein JJ (1985) Thoracic dorsal funicular lesions affect the bouton patterns on, and diameters of, layer VB pyramidal cell somata in rat hindlimb cortex. J Neurosci Res 14:71-81.
26. Ghosh A, Sydekum E, Haiss F, Peduzzi S, Zörner B, Schneider R, Baltes C, Rudin M, Weber B, Schwab ME (2009) Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J Neurosci 29:12210-12219.
27. Ghosh A, Haiss F, Sydekum E, Schneider R, Gullo M, Wyss MT, Mueggler T, Baltes C, Rudin M, Weber B, Schwab ME (2010) Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat Neurosci 13:97-104.
28. Giehl KM, Tetzlaff W (1996) BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corticospinal neurons in vivo. Eur J Neurosci 8:1167-1175.
29. Gold BG, Griffin JW, Price DL (1992) Somatofugal axonal atrophy precedes development of axonal degeneration in acrylamide neuropathy. Arch Toxicol 66:57-66.
30. Gorgels TG (1990) A quantitative analysis of axon outgrowth, axon loss, and myelination in the rat pyramidal tract. Brain Res Dev Brain Res 54:51-61.
31. Griffin JW, George EB, Hsieh ST, Glass JD (1995) Axonal degeneration and disorders of the axonal cytoskeleton. New York, Oxford: Oxford UP.
32. Hains BC, Black JA, Waxman SG (2003) Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury. J Comp Neurol 462:328-341.
33. Hammond EN, Tetzlaff W, Mestres P, Giehl KM (1999) BDNF, but not NT-3, promotes long-term survival of axotomized adult rat corticospinal neurons in vivo. Neuroreport 10:2671-2675.
34. Holmes G, May WP (1909) On the exact origin of the pyramidal tract in man and other mammals. Brain 32:1-43.
35. Kalil K, Schneider GE (1975) Retrograde cortical and axonal changes following lesions of the pyramidal tract. Brain Res 89:15-27.
36. Klapka N, Hermanns S, Straten G, Masanneck C, Duis S, Hamers FP, Müller D, Zuschratter W, Müller HW (2005) Suppression of fibrous scarring in spinal cord injury of rat promotes long-distance regeneration of corticospinal tract axons, rescue of primary motoneurons in somatosensory cortex and significant functional recovery. Eur J Neurosci 22:3047-3058.
37. Kost SA, Oblinger MM (1993) Immature corticospinal neurons respond to axotomy with changes in tubulin gene expression. Brain Res Bull 30:469-475.
38. Kost-Mikucki SA, Oblinger MM (1991) Changes in glial fibrillary acidic protein mRNA expression after corticospinal axotomy in the adult hamster. J Neurosci Res 28:182-191.
39. Kuypers HGJM (1981) Anatomy of the descending pathways. Baltimore: Williams and Wilkins.
40. Lassek AM (1942) The pyramidal tract: a study of retrograde degeneration in the monkey. Arch Neurol Psychiatr (Chicago) 48:561-567.
41. Lassek AM, Rasmussen GL (1940) A comparative fiber and numerical analysis of the pyramidal tract. J Comp Neurol 72:417-428.
42. Lee BH, Lee KH, Kim UJ, Yoon DH, Sohn JH, Choi SS, Yi IG, Park YG (2004) Injury in the spinal cord may produce cell death in the brain. Brain Res 1020:37-44.
43. Leenen LP, Meek J, Posthuma PR, Nieuwenhuys R (1985) A detailed morphometrical analysis of the pyramidal tract of the rat. Brain Res 359:65-80.
44. Leenen LP, Meek J, Posthuma PR, Nieuwenuys R (1989) Differences in the fiber composition of the pyramidal tract in two- and 14-month-old rats. Neuroscience 28:635-643.
45. Liu CN (1955) Time pattern in retrograde degeneration after trauma of central nervous system of mammals. In: Regeneration in the central nervous system (Windle WF, ed), pp 84-93. Springfield, IL: Thomas.
46. Mason MR, Lieberman AR, Anderson PN (2003) Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. Eur J Neurosci 18:789-802.
47. Merline M, Kalil K (1990) Cell death of corticospinal neurons is induced by axotomy before but not after innervation of spinal targets. J Comp Neurol 296:506-516.
48. Mikucki SA, Oblinger MM (1991) Corticospinal neurons exhibit a novel pattern of cytoskeletal gene expression after injury. J Neurosci Res 30:213-225.
49. Miller MW (1987) The origin of corticospinal projection neurons in rat. Exp Brain Res 67:339-351.
50. Neumann S, Woolf CJ (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23:83-91.
51. Nissl F (1892) Ueber die Veranderungen der Ganglienzellen am Facialiskern des Kaninchens nach Ausreissung der Nerven. Allgen Z Psychiatr 48:197-198.
52. Pallini R, Fernandez E, Sbriccoli A (1988) Retrograde degeneration of corticospinal axons following transection of the spinal cord in rats. A quantitative study with anterogradely transported horseradish peroxidase. J Neurosurg 68:124-128.
53. Piecharka DM, Kleim JA, Whishaw IQ (2005) Limits on recovery in the corticospinal tract of the rat: partial lesions impair skilled reaching and the topographic representation of the forelimb in motor cortex. Brain Res Bull 66:203-211.
54. Raff MC, Whitmore AV, Finn JT (2002) Axonal self-destruction and neurodegeneration. Science 296:868-871.
55. Ramirez LF, Kalil K (1985) Critical stages for growth in the development of cortical neurons. J Comp Neurol 237:506-518.
56. Ramon y Cajal S (1928) Cajal's degeneration and regeneration of the nervous system. New York, Oxford: Oxford UP.
57. Ranson SW (1914) A note on the degeneration of the fasciculus cerebrospinalis in the albino rat. J Comp Neurol 24:503-507.
58. Rao RS, Krinke G (1983) Changes with age in the number and size of myelinated axons in the rat L4 dorsal spinal root. Acta Anat (Basel) 117: 187-192.
59. Reh T, Kalil K (1981) Development of the pyramidal tract in the hamster. I. A light microscopic study. J Comp Neurol 200:55-67.
60. Rosenbluth (1995) Pathology of demylinated and dysmyelinated axons. New York, Oxford: Oxford UP.
61. Schauwecker PE (2002) Modulation of cell death by mouse genotype: differential vulnerability to excitatory amino acid-induced lesions. Exp Neurol 178:219-235.
62. Schauwecker PE, Ramirez JJ, Steward O (2000) Genetic dissection of the signals that induce synaptic reorganization. Exp Neurol 161:139-152.
63. Schmidlin E, Wannier T, Bloch J, Rouiller EM (2004) 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. Brain Res 1017:172-183.
64. Schmidlin E, Wannier T, Bloch J, Belhaj-Saif A, Wyss AF, Rouiller EM (2005) Reduction of the hand representation in the ipsilateral primary motor cortex following unilateral section of the corticospinal tract at cervical level in monkeys. BMC Neurosci 6:56.
65. Schmued LC, Scallet AC, Slikker W Jr (1995) Domoic acid-induced neuronal degeneration in the primate forebrain revealed by degeneration specific histochemistry. Brain Res 695:64-70.
66. Strong MK, Blanco JE, Anderson KD, Lewandowski G, Steward O (2009) An investigation of the cortical control of forepaw gripping after cervical hemisection injuries in rats. Exp Neurol 217:96-107.
67. Swank RL (1936) The pyramidal tract. An experimental study of the corticospinal tract and other components in the rabbit. AMA Arch Neurol Psychiatry 36:530-541.
68. Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7:628-643.
69. Tseng GF, Prince DA (1996) Structural and functional alterations in rat corticospinal neurons after axotomy. J Neurophysiol 75:248-267.
70. Van Gehuchten A (1903) La degenerescence dite retrograde ou degenerescence wallerienne indirecte. Nevraxe 5:1-108.
71. Waller A (1850) Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc London 140:423-429.
72. Wannier T, Schmidlin E, Bloch J, Rouiller EM (2005) A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. J Neurotrauma 22:703-717.
73. Wiesendanger M (1981) The pyramidal tract. Its structure and function. New York: Plenum.
74. Zimmerman EA, Chambers WW, Liu CN (1964) An experimental study of the anatomical organization of the cortico-bulbar system in the albino rat. J Comp Neurol 123:301-323.