Re-establishment of cortical motor output maps and spontaneous functional recovery via spared dorsolaterally projecting corticospinal neurons after dorsal column spinal cord injury in adult mice

Journal of Neuroscience

Volumn 36, Issue 14, 2016, Pages 4080-4092

  Hilton, Brett J ^a   Anenberg, Eitan ^a,b   Harrison, Thomas C ^a,b   Boyd, Jamie D ^a,b   Murphy, Timothy H ^a,b   Tetzlaff, Wolfram ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Corticospinal; Motor cortex; Optogenetics; Plasticity; Recovery; Spinal cord injury

Indexed keywords

ADENO ASSOCIATED VIRUS; ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MOTOR CORTEX; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PYRAMIDAL TRACT; SPINAL CORD INJURY; ANIMAL; BRAIN MAPPING; C57BL MOUSE; CONVALESCENCE; EFFERENT NERVE; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; NERVE CELL PLASTICITY; OPTOGENETICS; PATHOLOGY; SENSORIMOTOR CORTEX;

ANIMALS; BRAIN MAPPING; EFFERENT PATHWAYS; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MICE; MICE, INBRED C57BL; MOTOR CORTEX; NEURONAL PLASTICITY; OPTOGENETICS; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; SENSORIMOTOR CORTEX; SPINAL CORD INJURIES;

EID: 84964052741     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3386-15.2016     Document Type: Article

References (42)

1. Anenberg E, Arstikaitis P, Niitsu Y, Harrison TC, Boyd JD, Hilton BJ, Tetzlaff W, Murphy TH (2014) Ministrokes in channelrhodopsin-2 transgenic mice reveal widespread deficits in motor output despite maintenance of cortical neuronal excitability. J Neurosci 34:1094-1104. CrossRef Medline
2. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Ehlers MD, Feng G (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54: 205-218. CrossRef Medline
3. Asante CO, Martin JH (2013) Differential joint-specific corticospinal tract projections within the cervical enlargement. PLoS One 8:e74454. CrossRef Medline
4. Ayling OG, Harrison TC, Boyd JD, Goroshkov A, Murphy TH (2009) Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat Methods 6:219-224. CrossRef Medline
5. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7:269-277. CrossRef Medline
6. Bareyre FM, Kerschensteiner M, Misgeld T, Sanes JR (2005) Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat Med 11:1355-1360. CrossRef Medline
7. 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. CrossRef Medline
8. Brown LT (1974) Corticorubral projections in the rat. J Comp Neurol 154: 149-167. CrossRef Medline
9. Brus-Ramer M, Carmel JB, Chakrabarty S, Martin JH (2007) Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. J Neurosci 27:13793-13801. CrossRef Medline
10. Cummings BJ, Engesser-Cesar C, Cadena G, Anderson AJ (2007) Adaptation of a ladder beam walking task to assess locomotor recovery in mice following spinal cord injury. Behav Brain Res 177:232-241. CrossRef Medline
11. Esposito MS, Capelli P, Arber S (2014) Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 508:351-356. CrossRef Medline
12. Fink KL, Strittmatter SM, Cafferty WB (2015) Comprehensive corticospinal labeling with mu-crystallin transgene reveals axon regeneration after spinal cord trauma in ngr1-/-mice. J Neurosci 35:15403-15418. CrossRef Medline
13. Fouad K, Pedersen V, Schwab ME, Brösamle C (2001) Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 11:1766-1770. CrossRef Medline
14. Friedli L, Rosenzweig ES, Barraud Q, Schubert M, Dominici N, Awai L, Nielson JL, Musienko P, Nout-Lomas Y, Zhong H, Zdunowski S, Roy RR, Strand SC, van den Brand R, Havton LA, Beattie MS, Bresnahan JC, Bézard E, Bloch J, Edgerton VR, et al. (2015) Pronounced species divergence in corticospinal tract reorganization and functional recovery after lateralized spinal cord injury favors primates. Sci Transl Med 7:302ra134-302ra134. CrossRef Medline
15. Gensel JC, Tovar CA, Hamers FP, Deibert RJ, Beattie MS, Bresnahan JC (2006) Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 23:36-54. CrossRef Medline
16. 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. CrossRef Medline
17. 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. CrossRef Medline
18. Harrison TC, Ayling OG, MurphyTH (2012) Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography. Neuron 74:397-409. CrossRef Medline
19. Harrison TC, Silasi G, Boyd JD, Murphy TH (2013) Displacement of sensory maps and disorganization of motor cortex after targeted stroke in mice. Stroke 44:2300-2306. CrossRef Medline
20. Hilton BJ, Assinck P, Duncan GJ, Lu D, Lo S, TetzlaffW (2013) Dorsolateral funiculus lesioning of the mouse cervical spinal cord at C4 but not at C6 results in sustained forelimb motor deficits. J Neurotrauma 30:1070-1083. CrossRef Medline
21. Jara JH, Villa SR, Khan NA, Bohn MC, Ozdinler PH (2012) AAV2 mediated retrograde transduction of corticospinal motor neurons reveals initial and selective apical dendrite degeneration in ALS. Neurobiol Dis 47:174-183. CrossRef Medline
22. Jara JH, Genç B, Klessner JL, Özdinler PH (2014) Retrograde labeling, transduction, and genetic targeting allow cellular analysis of corticospinal motor neurons: implications in health and disease. Front Neuroanat 8.
23. Klaw MC, Xu C, Tom VJ (2013) Intraspinal AAV injections immediately rostral to a thoracic spinal cord injury site efficiently transduces neurons in spinal cord and brain. Mol Ther Nucleic Acids 2:e108. CrossRef Medline
24. Krajacic A, Weishaupt N, Girgis J, Tetzlaff W, Fouad K (2010) Traininginduced plasticity in rats with cervical spinal cord injury: effects and side effects. Behav Brain Res 214:323-331. CrossRef Medline
25. Maier IC, Baumann K, Thallmair M, Weinmann O, Scholl J, Schwab ME (2008) Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury. J Neurosci 28:9386-9403. CrossRef Medline
26. Nishimura Y, Isa T (2009) Compensatory changes at the cerebral cortical level after spinal cord injury. The Neuroscientist 15:436-444. CrossRef Medline
27. Nishimura Y, Isa T (2012) Cortical and subcortical compensatory mechanisms after spinal cord injury in monkeys. Exp Neurol 235:152-161. CrossRef Medline
28. Nudo RJ (2006) Mechanisms for recovery of motor function following cortical damage. Curr Opin Neurobiol 16:638-644. CrossRef Medline
29. Oudega M, Perez MA (2012) Corticospinal reorganization after spinal cord injury. J Physiol 590:3647-3663. CrossRef Medline
30. Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263-273. CrossRef Medline
31. Ramer LM, Ramer MS, Bradbury EJ (2014) Restoring function after spinal cord injury: towards clinical translation of experimental strategies. Lancet Neurol 13:1241-1256. CrossRef Medline
32. Rogan SC, Roth BL (2011) Remote control of neuronal signaling. Pharmacol Rev 63:291-315. CrossRef Medline
33. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, Nout YS, Roy RR, Miller DM, Beattie MS, Havton LA, Bresnahan JC, Edgerton VR, TuszynskiMH (2010) Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13:1505-1510. CrossRef Medline
34. Roth EJ, Park T, Pang T, Yarkony GM, Lee MY (1991) Traumatic cervical Brown-Sequard and Brown-Sequard-plus syndromes: the spectrum of presentations and outcomes. Paraplegia 29:582-589. CrossRef Medline
35. Siegel CS, Fink KL, Strittmatter SM, Cafferty WB (2015) Plasticity of intact rubral projections mediates spontaneous recovery of function after corticospinal tract injury. J Neurosci 35:1443-1457. CrossRef Medline
36. Silasi G, Boyd JD, Ledue J, Murphy TH (2013) Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thinskull preparation. Front Neural Circuits 7:123. Medline
37. Steeves JD, Kramer JK, Fawcett JW, Cragg J, Lammertse DP, Blight AR, Marino RJ, Ditunno JF Jr, Coleman WP, Geisler FH, Guest J, Jones L, Burns S, Schubert M, van Hedel HJ, Curt A; EMSCI Study Group (2011) Extent of spontaneous motor recovery after traumatic cervical sensorimotor complete spinal cord injury. Spinal Cord 49:257-265. CrossRef Medline
38. Steward O, Zheng B, Ho C, Anderson K, Tessier-Lavigne M (2004) The dorsolateral corticospinal tract in mice: an alternative route for corticospinal input to caudal segments following dorsal column lesions. J Comp Neurol 472:463-477. CrossRef Medline
39. Vavrek R, Girgis J, Tetzlaff W, Hiebert GW, Fouad K (2006) BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 129:1534-1545. CrossRef Medline
40. Wahl AS, Omlor W, Rubio JC, Chen JL, Zheng H, Schröter A, Gullo M, Weinmann O, Kobayashi K, Helmchen F, Ommer B, Schwab ME (2014) Asynchronous therapy restores motor control by rewiring of the rat corticospinal tract after stroke. Science 344:1250-1255. CrossRef Medline
41. Wang Z, Reynolds A, Kirry A, Nienhaus C, Blackmore MG (2015) Overexpression of sox11 promotes corticospinal tract regeneration after spinal injury while interfering with functional recovery. J Neurosci 35:3139-3145. CrossRef Medline
42. Weidner N, Ner A, Salimi N, Tuszynski MH (2001) Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci U S A 98:3513-3518. CrossRef Medline