Better functional outcome of compression spinal cord injury in mice is associated with enhanced H-reflex responses

Experimental Neurology

Volumn 216, Issue 2, 2009, Pages 365-374

  Lee, Hyun Joon ^a   Jakovcevski, Igor ^a   Radonjic, Nevena ^a,b   Hoelters, Laura ^a   Schachner, Melitta ^a,c,d   Irintchev, Andrey ^a,e  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

C bouton; CHL1; Cholinergic synapses; Glutamatergic synapses; Inhibitory synapses; Monosynaptic Ia afferent reflex; Motoneuron; Motor recovery; Spinal cord injury; Tenascin R

Indexed keywords

CELL ADHESION MOLECULE; CELL PROTEIN; MATRIX PROTEIN; TENASCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEGENERATION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; COMPRESSION; CONTROLLED STUDY; CONVALESCENCE; CORRELATION ANALYSIS; DEPRESSION; EXPERIMENTAL MOUSE; EXTRACELLULAR MATRIX; FEMALE; HOFFMANN REFLEX; MONOSYNAPTIC PATHWAY; MONOSYNAPTIC REFLEX; MOTION; MOTONEURON; MOUSE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; SPINAL CORD INJURY; SPINAL REFLEX; STEM CELL; STIMULATION; WILD TYPE;

EID: 62149148833     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.12.009     Document Type: Article

References (39)

1. Abbruzzese G. The medical management of spasticity. Eur. J. Neurol. 9 Suppl 1 (2002) 30-34 discussion 53-61
2. Apostolova I., Irintchev A., and Schachner M. Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J. Neurosci. 26 (2006) 7849-7859
3. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., and Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7 (2004) 269-277
4. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 12 (1995) 1-21
5. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., and Popovich P.G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma. 23 (2006) 635-659
6. Chen Y., Chen X.Y., Jakeman L.B., Chen L., Stokes B.T., and Wolpaw J.R. Operant conditioning of H-reflex can correct a locomotor abnormality after spinal cord injury in rats. J. Neurosci. 26 (2006) 12537-12543
7. Chen J., Wu J., Apostolova I., Skup M., Irintchev A., Kügler S., and Schachner M. Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. Brain 130 (2007) 954-969
8. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., and Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14 (2008) 69-74
9. Curtis R., Green D., Lindsay R.M., and Wilkin G.P. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J. Neurocytol. 22 (1993) 51-64
10. Davidoff M.S., and Irintchev A.P. Acetylcholinesterase activity and type C synapses in the hypoglossal, facial and spinal-cord motor nuclei of rats. An electron-microscope study. Histochemistry 84 (1986) 515-524
11. Dietz V., and Colombo G. Recovery from spinal cord injury-underlying mechanisms and efficacy of rehabilitation. Acta. Neurochir. Suppl. 89 (2004) 95-100
12. Dietz V., and Sinkjaer T. Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 6 (2007) 725-733
13. Donnelly D.J., and Popovich P.G. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 209 (2008) 378-388
14. Edgerton V.R., Tillakaratne N.J., Bigbee A.J., de Leon R.D., and Roy R.R. Plasticity of the spinal neural circuitry after injury. Annu. Rev. Neurosci. 27 (2004) 145-167
15. Frigon A., and Rossignol S. Functional plasticity following spinal cord lesions. Prog. Brain Res. 157 (2006) 231-260
16. Gozariu M., Roth V., Keime F., Le Bars D., and Willer J.C. An electrophysiological investigation into the monosynaptic H-reflex in the rat. Brain Res. 782 (1998) 343-347
17. Hellström J., Oliveira A.L., Meister B., and Cullheim S. Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J. Comp. Neurol. 460 (2003) 476-486
18. Ho S.M., and Waite P.M. Effects of different anesthetics on the paired-pulse depression of the h reflex in adult rat. Exp. Neurol. 177 (2002) 494-502
19. Hultborn H. Changes in neuronal properties and spinal reflexes during development of spasticity following spinal cord lesions and stroke: studies in animal models and patients. J. Rehabil. Med (2003) 46-55
20. Irintchev A., Rollenhagen A., Troncoso E., Kiss J.Z., and Schachner M. Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb. Cortex 15 (2005) 950-962
21. Irintchev A., Simova O., Eberhardt K.A., Morellini F., and Schachner M. Impacts of lesion severity and tyrosine kinase receptor B deficiency on functional outcome of femoral nerve injury assessed by a novel single-frame motion analysis in mice. Eur. J. Neurosci. 22 (2005) 802-808
22. Jakovcevski I., Wu J., Karl N., Leshchyns'ka I., Sytnyk V., Chen J., Irintchev A., and Schachner M. Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J. Neurosci. 27 (2007) 7222-7233
23. Jiao Y., Sun Z., Lee T., Fusco F.R., Kimble T.D., Meade C.A., Cuthbertson S., and Reiner A. A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections. J. Neurosci. Methods 93 (1999) 149-162
24. Joshi M., and Fehlings M.G. Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: part 2. Quantitative neuroanatomical assessment and analysis of the relationships between axonal tracts, residual tissue, and locomotor recovery. J. Neurotrauma. 19 (2002) 191-203
25. Lee J.K., Emch G.S., Johnson C.S., and Wrathall J.R. Effect of spinal cord injury severity on alterations of the H-reflex. Exp. Neurol. 196 (2005) 430-440
26. Li Y., and Bennett D.J. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J. Neurophysiol. 90 (2003) 857-869
27. Li Y., Gorassini M.A., and Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J. Neurophysiol. 91 (2004) 767-783
28. Little J.W., Ditunno Jr. J.F., Stiens S.A., and Harris R.M. Incomplete spinal cord injury: neuronal mechanisms of motor recovery and hyperreflexia. Arch. Phys. Med. Rehabil. 80 (1999) 587-599
29. Little J.W., Micklesen P., Umlauf R., and Britell C. Lower extremity manifestations of spasticity in chronic spinal cord injury. Am. J. Phys. Med. Rehabil. 68 (1989) 32-36
30. Miles G.B., Hartley R., Todd A.J., and Brownstone R.M. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc. Natl. Acad Sci. U. S. A. 104 (2007) 2448-2453
31. Montag-Sallaz M., Schachner M., and Montag D. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol. Cell Biol. 22 (2002) 7967-7981
32. Pearson K.G. Could enhanced reflex function contribute to improving locomotion after spinal cord repair?. J. Physiol. 533 (2001) 75-81
33. Petruska J.C., Ichiyama R.M., Jindrich D.L., Crown E.D., Tansey K.E., Roy R.R., Edgerton V.R., and Mendell L.M. Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats. J. Neurosci. 27 (2007) 4460-4471
34. Pierrot-Deseilligny E., and Mazevet D. The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol. Clin. 30 (2000) 67-80
35. Raineteau O., Fouad K., Bareyre F.M., and Schwab M.E. Reorganization of descending motor tracts in the rat spinal cord. Eur. J. Neurosci. 16 (2002) 1761-1771
36. Sheean G. The pathophysiology of spasticity. Eur. J. Neurol. 9 Suppl 1 (2002) 3-9 dicussion 53-61
37. Thompson F.J., Reier P.J., Lucas C.C., and Parmer R. Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J. Neurophysiol. 68 (1992) 1473-1486
38. Valero-Cabre A., Fores J., and Navarro X. Reorganization of reflex responses mediated by different afferent sensory fibers after spinal cord transection. J. Neurophysiol. 91 (2004) 2838-2848
39. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., Margolis R.U., Levinson S.R., Shrager P., Montag D., and Schachner M. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19 (1999) 4245-4262