Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord.
The failure of injured axons to regenerate following spinal cord injury deprives brain neurons of their normal sources of activation. These injuries also result in the reorganization of affected areas of the central nervous system that is thought to drive both the ensuing recovery of function and the formation of maladaptive neuronal circuitry. Better understanding of the physiological consequences of novel synaptic connections produced by injury and the mechanisms that control their formation are important to the development of new successful strategies for the treatment of patients with spinal cord injuries. Here we discuss the anatomical, physiological and behavioral changes that take place in response to injury-induced plasticity after damage to the dorsal column pathway in rats and monkeys. Complete section of the dorsal columns of the spinal cord at a high cervical level in monkeys and rats interrupts the ascending axon branches of low threshold mechanoreceptor afferents subserving the forelimb and the rest of the lower body. Such lesions render the corresponding part of the somatotopic representation of primary somatosensory cortex totally unresponsive to tactile stimuli. There are also behavioral consequences of the sensory loss, including an impaired use of the hand/forelimb in manipulating small objects. In monkeys, if some of the afferents from the hand remain intact after dorsal column lesions, these remaining afferents extensively reactivate portions of somatosensory cortex formerly representing the hand. This functional reorganization develops over a postoperative period of 1 month, during which hand use rapidly improves. These recoveries appear to be mediated, at least in part, by the sprouting of preserved afferents within the cuneate nucleus of the dorsal column-trigeminal complex. In rats, such functional collateral sprouting has been promoted by the post-lesion digestion of the perineuronal net in the cuneate nucleus. Thus, this and other therapeutic strategies have the potential of enhancing sensorimotor recoveries after spinal cord injuries in humans.
Kaas
Jon H
JH
Department of Psychology, Vanderbilt University, Nashville, TN 37203, USA. jon.h.kaas@vanderbilt.edu
Qi
Hui-Xin
HX
Burish
Mark J
MJ
Gharbawie
Omar A
OA
Onifer
Stephen M
SM
Massey
James M
JM
D000344:Afferent Pathways / Q000293:injuries; D000818:Animals; D001921:Brain / Q000473:pathology*; D006801:Humans; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D051381:Rats; D013119:Spinal Cord Injuries / Q000473:pathology* / Q000503:physiopathology*
Neurol India. 2002 Sep;50(3):310-2
12391459
Neuroscience. 1990;34(2):391-401
2333149
J Neurosci Res. 2003 Feb 1;71(3):427-44
12526031
J Neurosci. 1999 Mar 1;19(5):1885-94
10024372
J Neurosci. 2006 Apr 19;26(16):4406-14
16624960
J Neurophysiol. 1996 Oct;76(4):2675-90
8899637
Cell Tissue Res. 2001 Oct;306(1):15-26
11683176
Brain. 2007 Apr;130(Pt 4):926-39
17255150
J Comp Neurol. 2006 Oct 1;498(4):552-65
16874805
J Neurotrauma. 2004 Jul;21(7):932-43
15307905
J Neurosci. 2006 Jul 12;26(28):7405-15
16837588
Annu Rev Neurosci. 1993;16:565-95
7681638
Exp Brain Res. 1998 Aug;121(3):300-10
9746136
Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):17066-71
12477938
Behav Brain Res. 1991 Jan 31;42(1):77-91
2029348
Neuroreport. 1996 Jul 29;7(11):1725-9
8905652
Somatosens Mot Res. 1998;15(2):157-63
9730116
Prog Brain Res. 2002;138:167-76
12432769
J Neurosci. 2000 Mar 15;20(6):2275-86
10704503
Science. 1990 Oct 12;250(4978):294-6
2145629
J Neurosci. 2002 Jun 1;22(11):4611-24
12040068
Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10413-20
8248123
J Comp Neurol. 2004 Mar 1;470(2):134-50
14750157
J Neurotrauma. 1995 Apr;12(2):209-22
7629867
J Neurosurg. 1997 Mar;86(3):538-42
9046313
Brain. 1998 Sep;121 ( Pt 9):1603-30
9762952
Behav Brain Res. 1993 Jul 30;56(1):59-76
7691077
J Neurophysiol. 1999 Oct;82(4):1876-82
10515976
Science. 1998 Nov 6;282(5391):1117-21
9804549
Brain Res. 1972 Feb 25;37(2):173-85
5061111
Brain Res Brain Res Rev. 1994 Jan;19(1):128-45
8167657
Exp Neurol. 2003 Jul;182(1):160-8
12821386
FASEB J. 2004 Jan;18(1):194-6
14630702
Acta Neurochir (Wien). 1999;141(8):881-3
10536726
J Neurosci. 1999 Jul 15;19(14):5810-22
10407022
Somatosens Mot Res. 2001;18(2):106-16
11534774
J Neurosci. 2005 Feb 2;25(5):1169-78
15689553
Trends Mol Med. 2006 Oct;12(10):488-96
16962376
Exp Neurol. 2003 Aug;182(2):399-411
12895450
J Neurosci. 2000 Apr 1;20(7):2427-38
10729323
J Hist Neurosci. 1999 Aug;8(2):186-90
11624300
Cell Mol Life Sci. 2000 Feb;57(2):276-89
10766023
Science. 2002 Nov 8;298(5596):1248-51
12424383
Nat Rev Neurosci. 2004 Feb;5(2):146-56
14735117
J Neurosci. 2005 Aug 31;25(35):8066-76
16135764
Brain Res Bull. 2001 Jan 15;54(2):237-42
11275414
J Neurophysiol. 1995 Apr;73(4):1537-46
7643165
Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14703-8
11114177
Brain Behav Evol. 1972;5(4):303-41
4629567
Trends Neurosci. 1998 Dec;21(12):510-5
9881847
J Neurosci. 1990 Sep;10(9):3014-24
1697900
Eur J Neurosci. 2003 Jan;17(1):13-27
12534965
Exp Neurol. 1995 Nov;136(1):32-43
7589332
J Neurosci. 2007 May 16;27(20):5405-13
17507562
Somatosens Mot Res. 1992;9(1):61-73
1595322
Brain. 1968;91(4):803-18
4178703
Nat Med. 2006 Jul;12(7):790-2
16819551
J Neurol Neurosurg Psychiatry. 1976 Jul;39(7):705-10
1069098
Eur J Neurosci. 2004 Mar;19(5):1226-42
15016081
Neurosurgery. 2000 Jan;46(1):85-90; discussion 90-2
10626939
Brain Res Rev. 2007 Apr;54(1):1-18
17222456
Brain Res Brain Res Rev. 1992 Sep-Dec;17(3):283-9
1467812
Physiol Behav. 1992 Jun;51(6):1151-6
1641415
Neuroscience. 2001;108(2):285-98
11734361
Eur J Neurosci. 2003 Jul;18(2):412-22
12887423
J Neurophysiol. 2000 May;83(5):3154-9
10805710
Eur J Neurosci. 2002 Nov;16(9):1761-71
12431229
Curr Opin Neurobiol. 2004 Feb;14(1):118-24
15018947
J Neurosci. 2003 Nov 12;23(32):10321-30
14614091
Proc Natl Acad Sci U S A. 2000 May 9;97(10):5546-50
10779564
J Neurosci. 1997 Mar 15;17(6):1928-39
9045722
J Neurosci. 2000 May 15;20(10):3884-99
10804228
Exp Neurol. 1993 Apr;120(2):264-76
8491282
West J Med. 1981 Sep;135(3):191-200
7340118
Prog Brain Res. 2001;130:64-72
11480289
Exp Neurol. 2005 Mar;192(1):25-38
15698616
J Neurosci. 2002 Apr 1;22(7):2792-803
11923444
Neuroreport. 2000 Apr 7;11(5):1063-7
10790883
J Neurosci. 2006 Oct 18;26(42):10856-67
17050723
Brain. 1970;93(3):505-24
4990230
J Pain Symptom Manage. 2007 Jan;33(1):99-109
17196911
Nature. 1997 Apr 3;386(6624):495-8
9087408
Exp Neurol. 2008 Feb;209(2):426-45
17540369
Nature. 2002 Apr 11;416(6881):636-40
11948352
J Comp Neurol. 2005 Oct 10;491(1):27-45
16127695
Brain. 1986 Oct;109 ( Pt 5):1003-41
3096488
J Neurosci. 1988 Jul;8(7):2350-60
3249230
Exp Neurol. 2007 Jun;205(2):513-24
17451687
Brain Res Brain Res Rev. 2002 Sep;39(2-3):181-215
12423766
J Neurotrauma. 2005 Feb;22(2):226-39
15716629