Locomotion after spinal cord injury depends on constitutive activity in serotonin receptors

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 2975-2984

  Fouad, K ^a   Rank, M M ^a   Vavrek, R ^a   Murray, K C ^a   Sanelli, L ^a   Bennett, D J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

6 CHLORO 5 METHYL 1 [[2 [(2 METHYL 3 PYRIDYL)OXY] 5 PYRIDYL]CARBAMOYL]INDOLINE; SEROTONIN 2 RECEPTOR;

ANIMAL TISSUE; ARTICLE; FEMALE; LOCOMOTION; MOTONEURON; MUSCLE TONE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD HEMISECTION; SPINAL CORD INJURY;

AMINOPYRIDINES; ANIMALS; CORDOTOMY; ELECTROMYOGRAPHY; FEMALE; GAIT DISORDERS, NEUROLOGIC; HINDLIMB; INDOLES; INJECTIONS, SPINAL; LOCOMOTION; MUSCLE HYPOTONIA; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN, 5-HT2; RECOVERY OF FUNCTION; SEROTONIN; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SEROTONIN RECEPTOR AGONISTS; SPINAL CORD INJURIES; TAIL;

EID: 78650895143     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00499.2010     Document Type: Article

References (62)

1. Ballermann M, Fouad K. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur J Neurosci 23: 1988-1996, 2006.
2. Barbeau H, Fung J, Leroux A, Ladouceur M. A review of the adaptability and recovery of locomotion after spinal cord injury. Prog Brain Res 137: 9-25, 2002.
3. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412: 84-95, 1987.
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 7: 269-277, 2004.
5. Barriere G, Leblond H, Provencher J, Rossignol S. Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. J Neurosci 28: 3976-3987, 2008.
6. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12: 1-21, 1995.
7. Bennett DJ, Sanelli L, Cooke C, Harvey PJ, Gorassini MA. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91: 2247-2258, 2004.
8. Butt SJ, Harris-Warrick RM, Kiehn O. Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22: 9961-9971, 2002.
9. Carlsson A, Magnusson T, Rosengren E. 5-Hydroxytryptamine of the spinal cord normally and after transection. Experientia 19: 359, 1963.
10. Chanrion B, Mannoury la Cour C, Gavarini S, Seimandi M, Vincent L, Pujol JF, Bockaert J, Marin P, Millan MJ. Inverse agonist and neutral antagonist actions of antidepressants at recombinant and native 5- hydroxytryptamine2C receptors: Differential modulation of cell surface expression and signal transduction. Mol Pharmacol 73: 748-757, 2008.
11. Chau C, Barbeau H, Rossignol S. Effects of intrathecal alpha1- and alpha2- noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J Neurophysiol 79: 2941-2963, 1998.
12. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, Qi J, Edgerton VR, Sofroniew MV. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 14: 69-74, 2008.
13. Cowley KC, Schmidt BJ. A comparison of motor patterns induced by N-methyl-D-aspartate, acetylcholine and serotonin in the in vitro neonatal rat spinal cord. Neurosci Lett 171: 147-150, 1994.
14. Cowley KC, Zaporozhets E, Schmidt BJ. Propriospinal neurons are sufficient for bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord. J Physiol 586: 1623-1635, 2008.
15. De Deurwaerdere P, Navailles S, Berg KA, Clarke WP, Spampinato U. Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 24: 3235-3241, 2004.
16. de Leon RD, Hodgson JA, Roy RR, Edgerton VR. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol 79: 1329-1340, 1998.
17. Fouad K, Pedersen V, Schwab ME, Brosamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 11: 1766-1770, 2001.
18. Gerasimenko Y, Musienko P, Bogacheva I, Moshonkina T, Savochin A, Lavrov I, Roy RR, Edgerton VR. Propriospinal bypass of the serotonergic system that can facilitate stepping. J Neurosci 29: 5681-5689, 2009.
19. Gimenez y Ribotta M, Privat A. Biological interventions for spinal cord injury. Curr Opin Neurol 11: 647-654, 1998.
20. Girgis J, Merrett D, Kirkland S, Metz GA, Verge V, Fouad K. Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 130: 2993-3003, 2007.
21. Giroux N, Chau C, Barbeau H, Reader TA, Rossignol S. Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats. J Neurophysiol 90: 1027-1045, 2003.
22. Grillner S, Zangger P. On the central generation of locomotion in the low spinal cat. Exp Brain Res 34: 241-261, 1979.
23. Grob M, Guertin PA. Role of Ca(2+) in the pacemaker-like property of spinal motoneurons. Med Sci 23: 64-66, 2007.
24. Guertin PA. Role of NMDA receptor activation in serotonin agonist-induced air-stepping in paraplegic mice. Spinal Cord 42: 185-190, 2004.
25. Gurevich I, Englander MT, Adlersberg M, Siegal NB, Schmauss C. Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J Neurosci 22: 10529-10532, 2002.
26. Herrick-Davis K, Grinde E, Niswender CM. Serotonin 5-HT2C receptor RNA editing alters receptor basal activity: Implications for serotonergic signal transduction. J Neurochem 73: 1711-1717, 1999.
27. Holohean AM, Hackman JC. Mechanisms intrinsic to 5-HT2B receptorinduced potentiation of NMDA receptor responses in frog motoneurons. Br J Pharmacol 143: 351-360, 2004.
28. Hoyer D, Hannon JP, Martin GR. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71: 533-554, 2002.
29. Jacobs BL, Martin-Cora FJ, Fornal CA. Activity of medullary serotonergic neurons in freely moving animals. Brain Res Brain Res Rev 40: 45-52, 2002.
30. Jane JA, Evans JP, Fisher LE. An investigation concerning the restitution of motor function following injury to the spinal cord. J Neurosurg 21: 167-171, 1964.
31. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG. Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57: 183-191, 2008.
32. Kennett GA, Wood MD, Bright F, Cilia J, Piper DC, Gager T, Thomas D, Baxter GS, Forbes IT, Ham P, Blackburn TP. In vitro and in vivo profile of SB 206553, a potent 5-HT2C/5-HT2B receptor antagonist with anxiolytic-like properties. Br J Pharmacol 117: 427-434, 1996.
33. Kennett GA, Wood MD, Bright F, Trail B, Riley G, Holland V, Avenell KY, Stean T, Upton N, Bromidge S, Forbes IT, Brown AM, Middlemiss DN, Blackburn TP. SB 242084, a selective and brain penetrant 5-HT2C receptor antagonist. Neuropharmacology 36: 609-620, 1997.
34. Kiehn O, Kjaerulff O. Spatiotemporal characteristics of 5-HT and dopamineinduced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75: 1472-1482, 1996.
35. Knight AR, Misra A, Quirk K, Benwell K, Revell D, Kennett G, Bickerdike M. Pharmacological characterisation of the agonist radioligand binding site of 5-HT(2A), 5-HT(2B) and 5-HT(2C) receptors. Naunyn Schmiedebergs Arch Pharmacol 370: 114-123, 2004.
36. Kuhn RA, Macht MB. Some manifestations of reflex activity in spinal man with particular reference to the occurrence of extensor spasm. Bull Johns Hopkins Hosp 84: 43-75, 1948.
37. Landry ES, Guertin PA. Differential effects of 5-HT1 and 5-HT2 receptor agonists on hindlimb movements in paraplegic mice. Prog Neuropsychopharmacol Biol Psychiatry 28: 1053-1060, 2004.
38. Li Y, Harvey PJ, Li X, Bennett DJ. Spastic long-lasting reflexes in the chronic spinal rat studied in vitro. J Neurophysiol 91: 2236-2246, 2004.
39. MacLean JN, Cowley KC, Schmidt BJ. NMDA receptor-mediated oscillatory activity in the neonatal rat spinal cord is serotonin dependent. J Neurophysiol 79: 2804-2808, 1998.
40. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ. Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92: 1566-1576, 2004.
41. McEwen ML, Van Hartesveldt C, Stehouwer DJ. L-DOPA and quipazine elicit air-stepping in neonatal rats with spinal cord transections. Behav Neurosci 111: 825-833, 1997.
42. Mejia-Gervacio S, Hounsgaard J, Diaz-Munoz M. Roles of ryanodine and inositol triphosphate receptors in regulation of plateau potentials in turtle spinal motoneurons. Neuroscience 123: 123-130, 2004.
43. Mestre C, Pelissier T, Fialip J, Wilcox G, Eschalier A. A method to perform direct transcutaneous intrathecal injection in rats. J Pharmacol Toxicol Methods 32: 197-200, 1994.
44. Murray K, Nakae A, Stephens MJ, Rank M, D'Amico J, Harvey P, Li X, Harris L, Ballou EW, Anelli R, Heckman CJ, Mashimo T, Vavrek R, Sanelli L, Gorassini MA, Bennett DJ, Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med 16: 694-700, 2010.
45. Musienko P, Gerasimenko Y, Van Den Brand R, Roy R, Zhong H, Edgerton V, and Courtine G. Monoaminergic modulation of locomotion facilitated by epidural stimulation (ES) in spinal rats. Soc Neurosci Abstr 573.2, 2008.
46. Niswender CM, Copeland SC, Herrick-Davis K, Emeson RB, Sanders- Bush E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J Biol Chem 274: 9472-9478, 1999.
47. Perrier JF, Mejia-Gervacio S, Hounsgaard J. Facilitation of plateau potentials in turtle motoneurones by a pathway dependent on calcium and calmodulin. J Physiol 528: 107-113, 2000.
48. Ribotta MG, Provencher J, Feraboli-Lohnherr D, Rossignol S, Privat A, Orsal D. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J Neurosci 20: 5144-5152, 2000.
49. Rossignol S. Plasticity of connections underlying locomotor recovery after central and/or peripheral lesions in the adult mammals. Philos Trans R Soc Lond B Biol Sci 361: 1647-1671, 2006.
50. Seifert R, Wenzel-Seifert K. Constitutive activity of G-protein-coupled receptors: Cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366: 381-416, 2002.
51. Shay BL, Sawchuk M, Machacek DW, Hochman S. Serotonin 5-HT2 receptors induce a long-lasting facilitation of spinal reflexes independent of ionotropic receptor activity. J Neurophysiol 94: 2867-2877, 2005.
52. Thomas SL, Gorassini MA. Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J Neurophysiol 94: 2844-2855, 2005.
53. Tillakaratne NJ, de Leon RD, Hoang TX, Roy RR, Edgerton VR, Tobin AJ. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J Neurosci 22: 3130-3143, 2002.
54. Turrigiano G, Abbott LF, Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264: 974-977, 1994. (Pubitemid 24196170)
55. Vavrek R, Girgis J, Tetzlaff W, Hiebert GW, Fouad K. BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 129: 1534-1545, 2006.
56. Viala D, Buser P. Methods of obtaining locomotor rhythms in the spinal rabbit by pharmacological treatments (DOPA, 5-HTP, D-amphetamine). Brain Res 35: 151-165, 1971.
57. Wainberg M, Barbeau H, Gauthier S. The effects of cyproheptadine on locomotion and on spasticity in patients with spinal cord injuries. J Neurol Neurosurg Psychiatry 53: 754-763, 1990.
58. 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 98: 3513-3518, 2001.
59. Weiner DM, Burstein ES, Nash N, Croston GE, Currier EA, Vanover KE, Harvey SC, Donohue E, Hansen HC, Andersson CM, Spalding TA, Gibson DF, Krebs-Thomson K, Powell SB, Geyer MA, Hacksell U, Brann MR. 5- hydroxytryptamine2A receptor inverse agonists as antipsychotics. J Pharmacol Exp Ther 299: 268-276, 2001.
60. Westphal RS, Sanders-Bush E. Reciprocal binding properties of 5-hydroxytryptamine type 2C receptor agonists and inverse agonists. Mol Pharmacol 46: 937-942, 1994.
61. Wirz M, Zemon DH, Rupp R, Scheel A, Colombo G, Dietz V, Hornby TG. Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: A multicenter trial. Arch Phys Med Rehabil 86: 672-680, 2005.
62. Yoshio R, Taniguchi T, Itoh H, Muramatsu I. Affinity of serotonin receptor antagonists and agonists to recombinant and native alpha1- adrenoceptor subtypes. Jpn J Pharmacol 86: 189-195, 2001.