Vitamin D3 improves respiratory adjustment to fatigue and H-reflex responses in paraplegic adult rats

Neuroscience

Volumn 188, Issue , 2011, Pages 182-192

  Bianco, J ^a,b   Gueye, Y ^b   Marqueste, T ^a   Alluin, O ^a   Risso, J J ^c   Garcia, S ^c   Lavault, M N ^c   Khrestchatisky, M ^b   Feron, F ^b   Decherchi, P ^a  

^a CNRS   (France)

^b Mediterranée University   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Compression; Monosynaptic Ia afferent reflex; Motoneuron recruitment; Phrenic nerve; Spasticity; Vitamin D

Indexed keywords

COLECALCIFEROL; NEUROFIBRIL ANTIBODY; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; UVEDOSE; VITAMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING RATE; CELL COUNT; CONTROLLED STUDY; DRUG ACTIVITY; ELECTROSTIMULATION; FEMALE; IMMUNOHISTOCHEMISTRY; MUSCLE FATIGUE; MUSCLE REFLEX; NERVE FIBER; NONHUMAN; PARAPLEGIA; PRIORITY JOURNAL; RAT; RESPIRATORY FUNCTION; SPINAL CORD; SPINAL CORD COMPRESSION; TIBIALIS ANTERIOR MUSCLE; VITAMIN SUPPLEMENTATION; ANIMAL; DISEASE MODEL; DRUG EFFECT; ELECTROMYOGRAPHY; HOFFMANN REFLEX; LUNG VENTILATION; METABOLISM; NERVE REGENERATION; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CHOLECALCIFEROL; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; FEMALE; H-REFLEX; IMMUNOHISTOCHEMISTRY; MUSCLE FATIGUE; NERVE REGENERATION; PARAPLEGIA; PULMONARY VENTILATION; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; VITAMINS;

EID: 79958718310     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.066     Document Type: Article

References (87)

1. Annweiler C., Schott A.M., Berrut G., Chauvire V., Le Gall D., Inzitari M., Beauchet O. Vitamin D and ageing: neurological issues. Neuropsychobiology 2010, 62:139-150.
2. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995, 12:1-21.
3. Bennett D.J., Gorassini M., Fouad K., Sanelli L., Han Y., Cheng J. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 1999, 16:69-84.
4. Birge S.J., Haddad J.G. 25-hydroxycholecalciferol stimulation of muscle metabolism. J Clin Invest 1975, 56:1100-1107.
5. Bjugn R., Nyengaard J.R., Rosland J.H. Spinal cord transection-no loss of distal ventral horn neurons. Exp Neurol 1997, 148:179-186.
6. Burke D., Gandevia S.C., McKeon B. Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 1984, 52:435-448.
7. Burke D., Gillies J.D., Lance J.W. The quadriceps stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 1970, 33:216-223.
8. Burne T.H., McGrath J.J., Eyles D.W., Mackay-Sim A. Behavioural characterization of vitamin D receptor knockout mice. Behav Brain Res 2005, 157:299-308.
9. Button D.C., Kalmar J.M., Gardiner K., Marqueste T., Zhong H., Roy R.R., Edgerton V.R., Gardiner P.F. Does elimination of afferent input modify the changes in rat motoneurone properties that occur following chronic spinal cord transection?. J Physiol 2008, 586:529-544.
10. Calancie B., Broton J.G., Klose K.J., Traad M., Difini J., Ayyar D.R. Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol 1993, 89:177-186.
11. Cannell J.J., Hollis B.W., Sorenson M.B., Taft T.N., Anderson J.J. Athletic performance and vitamin D. Med Sci Sports Exerc 2009, 41:1102-1110.
12. Chabas J.F., Alluin O., Rao G., Garcia S., Lavaut M.N., Risso J.J., Legre R., Magalon G., Khrestchatisky M., Marqueste T., Decherchi P., Feron F. Vitamin D2 potentiates axon regeneration. J Neurotrauma 2008, 25:1247-1256.
13. Chang C.W. Evident transsynaptic degeneration of motor neurons after spinal cord injury: a study of neuromuscular jitter by axonal microstimulation. Am J Phys Med Rehabil 1998, 77:118-121.
14. Chen X.Y., Carp J.S., Chen L., Wolpaw J.R. Corticospinal tract transection prevents operantly conditioned H-reflex increase in rats. Exp Brain Res 2002, 144:88-94.
15. Chen X.Y., Feng-Chen K.C., Chen L., Stark D.M., Wolpaw J.R. Short-Term and medium-term effects of spinal cord tract transections on soleus H-reflex in freely moving rats. J Neurotrauma 2001, 18:313-327.
16. Cliffer K.D., Tonra J.R., Carson S.R., Radley H.E., Cavnor C., Lindsay R.M., Bodine S.C., DiStefano P.S. Consistent repeated M- and H-Wave recording in the hind limb of rats. Muscle Nerve 1998, 21:1405-1413.
17. Crisafulli A., Milia R., Vitelli S., Caddeo M., Tocco F., Melis F., Concu A. Hemodynamic responses to metaboreflex activation: insights from spinal cord-injured humans. Eur J Appl Physiol 2009, 106:525-533.
18. Crone C., Johnsen L.L., Biering-Sorensen F., Nielsen J.B. Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 2003, 126:495-507.
19. D'Angelo C.M. The H-reflex in experimental spinal cord trauma. J Neurosurg 1973, 39:209-213.
20. Darques J.L., Jammes Y. Fatigue-induced changes in group IV muscle afferent activity: differences between high- and low-frequency electrically induced fatigues. Brain Res 1997, 750:147-154.
21. Decherchi P., Dousset E. The role played by the afferent metabosensitive fibers in neuromuscular adaptive mechanism. Can J Neurol Sci 2003, 30:1988-1995.
22. Decherchi P., Dousset E., Jammes Y. Respiratory and cardiovascular responses evoked by tibialis anterior muscle afferent fibers in rats. Exp Brain Res 2007, 183:299-312.
23. Delwaide P.J., Figiel C., Richelle C. Influence of the position of the upper limb on the excitability of the reflex arc of the soleus muscle. Electromyogr Clin Neurophysiol 1973, 13:515-523.
24. Diamantopoulos E., Zander Olsen P. Excitability of motor neurones in spinal shock in man. J Neurol Neurosurg Psychiatry 1967, 30:427-431.
25. Dong H.W., Wang L.H., Zhang M., Han J.S. Decreased dynorphin A (1-17) in the spinal cord of spastic rats after the compressive injury. Brain Res Bull 2005, 67:189-195.
26. Eccles J.C., Rall W. Effects induced in a monosynaptic reflex path by its activation. J Neurophysiol 1951, 14:353-376.
27. Eidelberg E., Nguyen L.H., Polich R., Walden J.G. Transsynaptic degeneration of motoneurones caudal to spinal cord lesions. Brain Res Bull 1989, 22:39-45.
28. Eldridge F.L., Millhorn D.E., Kiley J.P., Waldrop T.G. Stimulation by central command of locomotion, respiration and circulation during exercise. Respir Physiol 1985, 59:313-337.
29. Engberg I., Lundberg A., Ryall R.W. Reticulospinal inhibition of transmission in reflex pathways. J Physiol 1968, 194:201-223.
30. Fernandes de Abreu D.A., Eyles D., Feron F. Vitamin D, a neuro-immunomodulator: implications for neurodegenerative and autoimmune diseases. Psychoneuroendocrinology 2009, 34(Suppl 1):S265-S277.
31. Friedman W.A., Sypert G.W., Munson J.B., Fleshman J.W. Recurrent inhibition in type-identified motoneurons. J Neurophysiol 1981, 46:1349-1359.
32. Frigon A., Rossignol S. Functional plasticity following spinal cord lesions. Prog Brain Res 2006, 157:231-260.
33. Goodwin G.M., McCloskey D.I., Mitchell J.H. Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 1972, 226:173-190.
34. Gozariu M., Roth V., Keime F., Le Bars D., Willer J.C. An electrophysiological investigation into the monosynaptic H-reflex in the rat. Brain Res 1998, 782:343-347.
35. Hasegawa Y., Ono H. Effect of (+/-)-8-hydroxy-2-(di-n-propylamino)tetralin hydrobromide on spinal motor systems in anesthetized intact and spinalized rats. Eur J Pharmacol 1996, 295:211-214.
36. Hasegawa Y., Ono H. Effects of 8-OH-DPAT, a 5-HT1A receptor agonist, and DOI, a 5-HT2A/2C agonist, on monosynaptic transmission in spinalized rats. Brain Res 1996, 738:158-161.
37. Hiersemenzel L.P., Curt A., Dietz V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 2000, 54:1574-1582.
38. Holmes G.M., Van Meter M.J., Beattie M.S., Bresnahan J.C. Serotonergic fiber sprouting to external anal sphincter motoneurons after spinal cord contusion. Exp Neurol 2005, 193:29-42.
39. Horch K.W., Lisney S.J. On the number and nature of regenerating myelinated axons after lesions of cutaneous nerves in the cat. J Physiol 1981, 313:275-286.
40. 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, 41(Suppl):46-55.
41. Hunt C.C. Monosynaptic reflex response of spinal motoneurons to graded afferent stimulation. J Gen Physiol 1955, 38:813-852.
42. Iwamoto G.A., Waldrop T.G., Kaufman M.P., Botterman B.R., Rybicki K.J., Mitchell J.H. Pressor reflex evoked by muscular contraction: contributions by neuraxis levels. J Appl Physiol 1985, 59:459-467.
43. Jimenez O., Marcillo A., Levi A.D. A histopathological analysis of the human cervical spinal cord in patients with acute traumatic central cord syndrome. Spinal Cord 2000, 38:532-537.
44. Kaelan C., Jacobsen P.F., Kakulas B.A. An investigation of possible transynaptic neuronal degeneration in human spinal cord injury. J Neurol Sci 1988, 86:231-237.
45. Kaufman M.P., Hayes S.G. The exercise pressor reflex. Clin Auton Res 2002, 12:429-439.
46. Krogh A., Lindhard J. The regulation of respiration and circulation during the initial stages of muscular work. J Physiol 1913, 47:112-136.
47. Lee H.J., Jakovcevski I., Radonjic N., Hoelters L., Schachner M., Irintchev A. Better functional outcome of compression spinal cord injury in mice is associated with enhanced H-reflex responses. Exp Neurol 2009, 216:365-374.
48. Lee J.K., Emch G.S., Johnson C.S., Wrathall J.R. Effect of spinal cord injury severity on alterations of the H-reflex. Exp Neurol 2005, 196:430-440.
49. Li Y., Bennett D.J. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 2003, 90:857-869.
50. Li Y., Gorassini M.A., Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 2004, 91:767-783.
51. Little J.W., Ditunno J.F., Stiens S.A., Harris R.M. Incomplete spinal cord injury: neuronal mechanisms of motor recovery and hyperreflexia. Arch Phys Med Rehabil 1999, 80:587-599.
52. Little J.W., Micklesen P., Umlauf R., Britell C. Lower extremity manifestations of spasticity in chronic spinal cord injury. Am J Phys Med Rehabil 1989, 68:32-36.
53. Lloyd D.P., Wilson V.J. Reflex depression in rhythmically active monosynaptic reflex pathways. J Gen Physiol 1957, 40:409-426.
54. Magladery J.W., Porter W.E., Park A.M., Teasdall R.D. Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull Johns Hopkins Hosp 1951, 88:499-519.
55. Magladery J.W., Teasdall R.D., Norris A.H. Effect of aging on plantar flexor and superficial abdominal reflexes in man; a clinical and electromyographic study. J Gerontol 1958, 13:282-288.
56. Magladery J.W., Teasdall R.D., Park A.M., Porter W.E. Electrophysiological studies of nerve and reflex activity in normal man. V. Excitation and inhibition of two-neurone reflexes by afferent impulses in the same trunk. Bull Johns Hopkins Hosp 1951, 88:520-537.
57. Malmsten J. Time course of segmental reflex changes after chronic spinal cord hemisection in the rat. Acta Physiol Scand 1983, 119:435-443.
58. Manjarrez E., Rojas-Piloni J.G., Jimenez I., Rudomin P. Modulation of synaptic transmission from segmental afferents by spontaneous activity of dorsal horn spinal neurones in the cat. J Physiol 2000, 529(2):445-460.
59. Misiaszek J.E. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 2003, 28:144-160.
60. Mitchell J.H. Cardiovascular control during exercise: central and reflex neural mechanisms. Am J Cardiol 1985, 55:34D-41D.
61. Moreira-Pfrimer L.D., Pedrosa M.A., Teixeira L., Lazaretti-Castro M. Treatment of vitamin D deficiency increases lower limb muscle strength in institutionalized older people independently of regular physical activity: a randomized double-blind controlled trial. Ann Nutr Metab 2009, 54:291-300.
62. Olsen P.Z., Diamantopoulos E. Excitability of spinal motor neurones in normal subjects and patients with spasticity, Parkinsonian rigidity, and cerebellar hypotonia. J Neurol Neurosurg Psychiatry 1967, 30:325-331.
63. Petersen N., Christensen L.O., Nielsen J. The effect of transcranial magnetic stimulation on the soleus H reflex during human walking. J Physiol 1998, 513(2):599-610.
64. Pierrot-Deseilligny E., Mazevet D. The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 2000, 30:67-80.
65. Powers R.K., Campbell D.L., Rymer W.Z. Stretch reflex dynamics in spastic elbow flexor muscles. Ann Neurol 1989, 25:32-42.
66. Reese N.B., Skinner R.D., Mitchell D., Yates C., Barnes C.N., Kiser T.S., Garcia-Rill E. Restoration of frequency-dependent depression of the H-reflex by passive exercise in spinal rats. Spinal Cord 2006, 44:28-34.
67. Remy-Neris O., Barbeau H., Daniel O., Boiteau F., Bussel B. Effects of intrathecal clonidine injection on spinal reflexes and human locomotion in incomplete paraplegic subjects. Exp Brain Res 1999, 129:433-440.
68. Rowell L.B., O'Leary D.S. Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physiol 1990, 69:407-418.
69. Rudomin P. Presynaptic selection of afferent inflow in the spinal cord. J Physiol Paris 1999, 93:329-347.
70. Sato Y., Iwamoto J., Kanoko T., Satoh K. Low-dose vitamin D prevents muscular atrophy and reduces falls and hip fractures in women after stroke: a randomized controlled trial. Cerebrovasc Dis 2005, 20:187-192.
71. Schmidt B.J., Jordan L.M. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 2000, 53:689-710.
72. Skinner R.D., Houle J.D., Reese N.B., Berry C.L., Garcia-Rill E. Effects of exercise and fetal spinal cord implants on the H-reflex in chronically spinalized adult rats. Brain Res 1996, 729:127-131.
73. Smith J.E., Hall P.V., Campbell R.L., Jones A.R., Aprison M.H. Levels of gamma-aminobutyric acid in the dorsal grey lumbar spinal cord during the development of experimental spinal spasticity. Life Sci 1976, 19:1525-1529.
74. Sorensen O.H., Lund B., Saltin B., Andersen R.B., Hjorth L., Melsen F., Mosekilde L. Myopathy in bone loss of ageing: improvement by treatment with 1 alpha-hydroxycholecalciferol and calcium. Clin Sci (Lond) 1979, 56:157-161.
75. Stewart A., Wong K., Cachat J., Elegante M., Gilder T., Mohnot S., Wu N., Minasyan A., Tuohimaa P., Kalueff A.V. Neurosteroid vitamin D system as a nontraditional drug target in neuropsychopharmacology. Behav Pharmacol 2010, 21:420-426.
76. Taborikova H. Fraction of the motoneurone pool activated in the monosynaptic H-reflexes in man. Nature 1966, 209:206-207.
77. Taylor S., Ashby P., Verrier M. Neurophysiological changes following traumatic spinal lesions in man. J Neurol Neurosurg Psychiatry 1984, 47:1102-1108.
78. Thilmann A.F., Fellows S.J., Garms E. The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity. Brain 1991, 114(1A):233-244.
79. Thompson F.J., Reier P.J., Lucas C.C., Parmer R. Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J Neurophysiol 1992, 68:1473-1486.
80. Tillakaratne N.J., de Leon R.D., Hoang T.X., Roy R.R., Edgerton V.R., Tobin A.J. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J Neurosci 2002, 22:3130-3143.
81. Tillakaratne N.J., Mouria M., Ziv N.B., Roy R.R., Edgerton V.R., Tobin A.J. Increased expression of glutamate decarboxylase (GAD(67)) in feline lumbar spinal cord after complete thoracic spinal cord transection. J Neurosci Res 2000, 60:219-230.
82. Valero-Cabre A., Fores J., Navarro X. Reorganization of reflex responses mediated by different afferent sensory fibers after spinal cord transection. J Neurophysiol 2004, 91:2838-2848.
83. Vanicky I., Urdzikova L., Saganova K., Cizkova D., Galik J. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J Neurotrauma 2001, 18:1399-1407.
84. Wassner S.J., Li J.B., Sperduto A., Norman M.E. Vitamin D deficiency, hypocalcemia, and increased skeletal muscle degradation in rats. J Clin Invest 1983, 72:102-112.
85. Xia R., Rymer W.Z. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord 2005, 43:14-21.
86. Yablon S.A., Stokic D.S. Neurophysiologic evaluation of spastic hypertonia: implications for management of the patient with the intrathecal baclofen pump. Am J Phys Med Rehabil 2004, 83:S10-S18.
87. Zengel J.E., Reid S.A., Sypert G.W., Munson J.B. Presynaptic inhibition, EPSP amplitude, and motor-unit type in triceps surae motoneurons in the cat. J Neurophysiol 1983, 49:922-931.