Intraspinal rewiring of the corticospinal tract requires target-derived brain-derived neurotrophic factor and compensates lost function after brain injury

Brain

Volumn 135, Issue 4, 2012, Pages 1253-1267

  Ueno, Masaki ^a,b   Hayano, Yasufumi ^a,b   Nakagawa, Hiroshi ^a,b   Yamashita, Toshihide ^a,b  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

BDNF; cortical injury; corticospinal tract; functional recovery; plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; PROTEIN KINASE C GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CERVICAL SPINAL CORD; CONTROLLED STUDY; DENERVATION; ELECTROPHYSIOLOGY; FORELIMB; GENE SILENCING; INTERNEURON; MALE; MOTONEURON; MOTOR PERFORMANCE; MOUSE; NERVE CELL NETWORK; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RECOVERY ROOM; SENSORIMOTOR CORTEX; SPINAL CORD NERVE CELL;

EID: 84860146771     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws053     Document Type: Article

References (51)

1. Baird AL, Meldrum A, Dunnett SB. The staircase test of skilled reaching in mice. Brain Res Bull 2001; 54: 243-50. (Pubitemid 32223931)
2. Balkowiec A, Katz DM. Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J Neurosci 2000; 20: 7417-23.
3. Bareyre FM, Haudenschild B, Schwab ME. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J Neurosci 2002; 22: 7097-110. (Pubitemid 35379165)
4. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 2004; 7: 269-77. (Pubitemid 38280451)
5. Benowitz LI, Carmichael ST. Promoting axonal rewiring to improve outcome after stroke. Neurobiol Dis 2009; 37: 259-66.
6. Biernaskie J, Chernenko G, Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci 2004; 24: 1245-54. (Pubitemid 38177031)
7. Biernaskie J, Szymanska A, Windle V, Corbett D. Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur J Neurosci 2005; 21: 989-99. (Pubitemid 40461052)
8. Brus-Ramer M, Carmel JB, Chakrabarty S, Martin JH. Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. J Neurosci 2007; 27: 13793-801. (Pubitemid 350278261)
9. Brus-Ramer M, Carmel JB, Martin JH. Motor cortex bilateral motor representation depends on subcortical and interhemispheric interactions. J Neurosci 2009; 29: 6196-206.
10. Calautti C, Leroy F, Guincestre JY, Marie RM, Baron JC. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport 2001; 12: 3883-6. (Pubitemid 33152417)
11. Carmel JB, Berrol LJ, Brus-Ramer M, Martin JH. Chronic electrical stimulation of the intact corticospinal system after unilateral injury restores skilled locomotor control and promotes spinal axon outgrowth. J Neurosci 2010; 30: 10918-26.
12. Carmichael ST, Chesselet MF. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J Neurosci 2002; 22: 6062-70. (Pubitemid 35387649)
13. Chen P, Goldberg DE, Kolb B, Lanser M, Benowitz LI. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc Natl Acad Sci USA 2002; 99: 9031-6. (Pubitemid 34693678)
14. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 2010; 70: 271-88.
15. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, et al. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 2008; 14: 69-74.
16. Cramer SC, Crafton KR. Somatotopy and movement representation sites following cortical stroke. Exp Brain Res 2006; 168: 25-32. (Pubitemid 41752808)
17. Feydy A, Carlier R, Roby-Brami A, Bussel B, Cazalis F, Pierot L, et al. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 2002; 33: 1610-7. (Pubitemid 34619967)
18. Hioki H, Kuramoto E, Konno M, Kameda H, Takahashi Y, Nakano T, et al. High-level transgene expression in neurons by lentivirus with Tet-Off system. Neurosci Res 2009; 63: 149-54.
19. Isa T, Ohki Y, Alstermark B, Pettersson LG, Sasaki S. Direct and indirect cortico-motoneuronal pathways and control of hand/arm movements. Physiology (Bethesda) 2007; 22: 145-52.
20. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA 2002; 99: 14518-23. (Pubitemid 35257703)
21. Lee JK, Kim JE, Sivula M, Strittmatter SM. Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J Neurosci 2004; 24: 6209-17. (Pubitemid 38891112)
22. Lee S, Ueno M, Yamashita T. Axonal remodeling for motor recovery after traumatic brain injury requires downregulation of gammaaminobutyric acid signaling. Cell Death Dis 2011; 2: e133.
23. Lenzlinger PM, Shimizu S, Marklund N, Thompson HJ, Schwab ME, Saatman KE, et al. Delayed inhibition of Nogo-A does not alter injury-induced axonal sprouting but enhances recovery of cognitive function following experimental traumatic brain injury in rats. Neuroscience 2005; 134: 1047-56. (Pubitemid 41133405)
24. Li S, Overman JJ, Katsman D, Kozlov SV, Donnelly CJ, Twiss JL, et al. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat Neurosci 2010; 13: 1496-504.
25. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 2010; 13: 1075-1081.
26. Liu Z, Li Y, Qu R, Shen L, Gao Q, Zhang X, et al. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res 2007; 1149: 172-80. (Pubitemid 46659890)
27. Liu Z, Zhang RL, Li Y, Cui Y, Chopp M. Remodeling of the Corticospinal Innervation and Spontaneous Behavioral Recovery After Ischemic Stroke in Adult Mice. Stroke 2009; 40: 2546-2551.
28. Maier IC, Baumann K, Thallmair M, Weinmann O, Scholl J, Schwab ME. Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury. J Neurosci 2008; 28: 9386-403.
29. McKenna JE, Prusky GT, Whishaw IQ. Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: a retrograde carbocyanine dye analysis. J Comp Neurol 2000; 419: 286-96. (Pubitemid 30134140)
30. McNeal DW, Darling WG, Ge J, Stilwell-Morecraft KS, Solon KM, Hynes SM, et al. Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury. J Comp Neurol 2010; 518: 586-621.
31. Metz GA, Whishaw IQ. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 2002; 115: 169-79. (Pubitemid 34461965)
32. Murphy TH, Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 2009; 10: 861-72.
33. Napieralski JA, Butler AK, Chesselet MF. Anatomical and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat. J Comp Neurol 1996; 373: 484-97. (Pubitemid 26336943)
34. Nudo RJ. Mechanisms for recovery of motor function following cortical damage. Curr Opin Neurobiol 2006; 16: 638-44. (Pubitemid 44791925)
35. Omoto S, Ueno M, Mochio S, Takai T, Yamashita T. Genetic deletion of paired immunoglobulin-like receptor B does not promote axonal plasticity or functional recovery after traumatic brain injury. J Neurosci 2010; 30: 13045-52.
36. Omoto S, Ueno M, Mochio S, Yamashita T. Corticospinal tract fibers cross the ephrin-B3-negative part of the midline of the spinal cord after brain injury. Neurosci Res 2011; 69: 187-95.
37. Papadopoulos CM, Tsai SY, Guillen V, Ortega J, Kartje GL, Wolf WA. Motor recovery and axonal plasticity with short-term amphetamine after stroke. Stroke 2009; 40: 294-302.
38. Park JW, Vahidi B, Taylor AM, Rhee SW, Jeon NL. Microfluidic culture platform for neuroscience research. Nat Protoc 2006; 1: 2128-36. (Pubitemid 46773335)
39. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000; 39: 777-87. (Pubitemid 30103682)
40. Starkey ML, Barritt AW, Yip PK, Davies M, Hamers FP, McMahon SB, et al. Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp Neurol 2005; 195: 524-39. (Pubitemid 41297803)
41. Steward O, Zheng B, Ho C, Anderson K, Tessier-Lavigne M. The dorsolateral corticospinal tract in mice: an alternative route for corticospinal input to caudal segments following dorsal column lesions. J Comp Neurol 2004; 472: 463-77. (Pubitemid 38508830)
42. Stoeckel MC, Binkofski F. The role of ipsilateral primary motor cortex in movement control and recovery from brain damage. Exp Neurol 2010; 221: 13-7.
43. Tamura M, Tamura N, Ikeda T, Koyama R, Ikegaya Y, Matsuki N, et al. Influence of brain-derived neurotrophic factor on pathfinding of dentate granule cell axons, the hippocampal mossy fibers. Mol Brain 2009; 2: 2.
44. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2005; 2: 599-605. (Pubitemid 41086851)
45. Thallmair M, Metz GA, Z'Graggen WJ, Raineteau O, Kartje GL, Schwab ME. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1998; 1: 124-31.
46. Ueno M, Yamashita T. Kinematic analyses reveal impaired locomotion following injury of the motor cortex in mice. Exp Neurol 2011; 230: 280-90.
47. Umeda T, Takahashi M, Isa K, Isa T. Formation of descending pathways mediating cortical command to forelimb motoneurons in neonatally hemidecorticated rats. J Neurophysiol 2010; 104: 1707-16.
48. Weidner N, Ner A, Salimi N, Tuszynski MH. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci USA 2001; 98: 3513-8. (Pubitemid 32220876)
49. Yip PK, Wong LF, Sears TA, Yanez-Munoz RJ, McMahon SB. Cortical overexpression of neuronal calcium sensor-1 induces functional plasticity in spinal cord following unilateral pyramidal tract injury in rat. PLoS Biol 2010; 8: e1000399.
50. Yoshihara Y. Visualizing selective neural pathways with WGA transgene: combination of neuroanatomy with gene technology. Neurosci Res 2002; 44: 133-40. (Pubitemid 38365955)
51. Zai L, Ferrari C, Subbaiah S, Havton LA, Coppola G, Strittmatter S, et al. Inosine alters gene expression and axonal projections in neurons contralateral to a cortical infarct and improves skilled use of the impaired limb. J Neurosci 2009; 29: 8187-97.