Reduction of spinal sensory transmission by facilitation of 5-HT1B/D receptors in noninjured and spinal cord-injured humans

Journal of Neurophysiology

Volumn 109, Issue 6, 2013, Pages 1485-1493

  D'Amico, Jessica M ^a   Li, Yaqing ^a   Bennett, David J ^a   Gorassini, Monica A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cutaneomuscular; H reflex; Serotonin; Spasticity; Zolmitriptan

Indexed keywords

SEROTONIN 1B RECEPTOR; ZOLMITRIPTAN;

ADULT; ARTICLE; CELL ACTIVATION; CLINICAL ARTICLE; CONTROLLED STUDY; CUTANEOMUSCULAR REFLEX; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; FEMALE; HOFFMANN REFLEX; HUMAN; MALE; MOTONEURON; NERVOUS SYSTEM FUNCTION; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; REFLEX; SENSORY STIMULATION; SENSORY TRANSMISSION; SPINAL CORD INJURY;

ACTION POTENTIALS; ADULT; DOUBLE-BLIND METHOD; FEMALE; H-REFLEX; HUMANS; MALE; MIDDLE AGED; MOTOR NEURONS; MUSCLE SPASTICITY; MUSCLE, SKELETAL; OXAZOLIDINONES; RECEPTOR, SEROTONIN, 5-HT1B; RECEPTOR, SEROTONIN, 5-HT1D; RECEPTORS, ADRENERGIC, ALPHA-2; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SPINAL CORD INJURIES; SYNAPTIC TRANSMISSION; TRYPTAMINES;

EID: 84878514585     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00822.2012     Document Type: Article

References (60)

1. Anden NE, Haeggendal J, Magnusson T, Rosengren E. The time course of the disappearance of noradrenaline and 5-hydroxytryptamine in the spinal cord after transection. Acta Physiol Scand 62: 115-118, 1964.
2. Antri M, Barthe JY, Mouffle C, Orsal D. Long-lasting recovery of locomotor function in chronic spinal rat following chronic combined pharmacological stimulation of serotonergic receptors with 8-OHDPAT and quipazine. Neurosci Lett 384: 162-7, 2005.
3. Awaad Y, Rizk T, Siddiqui I, Roosen N, Mcintosh K, Waines GM. Complications of intrathecal baclofen pump: prevention and cure. ISRN Neurol 2012: 575168, 2012.
4. Baker LL, Chandler SH. Characterization of postsynaptic potentials evoked by sural nerve stimulation in hindlimb motoneurons from acute and chronic spinal cats. Brain Res 420: 340-350, 1987.
5. Bennett DJ, Li Y, Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86: 1955-1971, 2001a.
6. Bennett DJ, Li Y, Harvey PJ, Gorassini M. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 86: 1972-1982, 2001b.
7. Carlsson A, Magnusson T, Ronsengren E. 5-Hydroxytryptamine of the spinal cord normally and after transection. Experientia 19: 359, 1963.
8. Clarke RW, Eves S, Harris J, Peachey JE, Stuart E. Interactions between cutaneous afferent inputs to a withdrawal reflex in the decerebrated rabbit and their control by descending and segmental systems. Neuroscience 112: 555-571, 2002.
9. Crone C, Nielsen JB. Methodological implications of the post activation depression of the soleus H-reflex in man. Exp Brain Res 78: 28-32, 1989.
10. Curtis DR, Gynther BD, Lacey G, Beattie DT. Baclofen: reduction of presynaptic calcium influx in the cat spinal cord in vivo. Exp Brain Res 113: 520-533, 1997.
11. 1B/D receptor activation in uninjured and spinal cord injured subjects. Soc Neurosci Abstr 552.02, 2012.
12. 1 receptors facilitate muscle spasms in human spinal cord injury. J Neurophysiol (December 5, 2012). doi:10.1152/jn.00821.2012.
13. Davidoff RA. Antispasticity drugs: mechanisms of action. Ann Neurol 17: 107-116, 1985.
14. Di Pasquale E, Lindsay A, Feldman J, Monteau R, Hilaire G. Serotonergic inhibition of phrenic motoneuron activity: an in vitro study in neonatal rat. Neurosci Lett 230: 29-32, 1997.
15. Edwards FR, Harrison PJ, Jack JJ, Kullmann DM. Reduction by baclofen of monosynaptic EPSPs in lumbosacral motoneurones of the anaesthetized cat. J Physiol 416: 539-556, 1989.
16. Engberg I, Lundberg A, Ryall RW. Reticulospinal inhibition of transmission in reflex pathways. J Physiol 194: 201-223, 1968.
17. Gorassini MA, Knash ME, Harvey PJ, Bennett DJ, Yang JF. Role of motoneurons in the generation of muscle spasticity after spinal cord injury. Brain 127: 2247-2258, 2004.
18. Gracies JM, Nance P, Elovic E, McGuire J, Simpson DM. Traditional pharmacological treatments for spasticity. Part II: General and regional treatments. Muscle Nerve Suppl 6: S92-S120, 1997.
19. Heckman CJ, Johnson M, Mottram C, Schuster J. Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist 14: 264-275, 2008.
20. Honda M, Tanabe M, Ono H. Spinal cord injury-specific depression of monosynaptic spinal reflex transmission by L-5-hydroxytryptophan results from loss of the 5-HT uptake system and not 5-HT receptor supersensitivity. Exp Neurol 202: 258-261, 2006.
21. Honda M, Tanabe M, Ono H. Serotonergic depression of spinal monosynaptic transmission is mediated by 5-HT1B receptors. Eur J Pharmacol 482: 155-161, 2003.
22. Jacobs BL, Martin-Cora FJ, Fornal CA. Activity of medullary serotonergic neurons in freely moving animals. Brain Res Rev 40: 45-52, 2002.
23. Jankowska E, Riddell JS, Skoog B, Noga BR. Gating of transmission to motoneurones by stimuli applied in the locus coeruleus and raphe nuclei of the cat. J Physiol 461: 705-722, 1993.
24. Jimenez I, Rudomin P, Enriquez M. Differential effects of (-)-baclofen on Ia and descending monosynaptic EPSPs. Exp Brain Res 85: 103-113, 1991.
25. 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.
26. Kakinohana O, Hefferan MP, Miyanohara A, Nejime T, Marsala S, Juhas S, Juhasova J, Motlik J, Kucharova K, Strnadel J, Platoshyn O, Lazar P, Galik J, Vinay L, Marsala M. Combinational spinal GAD65 gene delivery and systemic GABA-mimetic treatment for modulation of spasticity. PLoS One 7: 1-13, 2012.
27. Kerr JM, Vujnovich LB. The intercept method: a novel method for establishing consistency of M-wave recruitment curves. Electromyogr Clin Neurophysiol 42: 423-432, 2002.
28. Klimstra M, Zehr EP. A sigmoid function is the best fit for the ascending limb of the Hoffman reflex recruitment curve. Exp Brain Res 186: 93-105, 2008.
29. Krach LE. Pharmacotherapy of spasticity: oral medications and intrathecal baclofen. J Child Neurol 16: 31-36, 2001.
30. Lazorthes Y, Sallerin-Caute B, Verdie JC, Bastide R, Carillo JP. Chronic intrathecal baclofen administration for control of severe spasticity. J Neurosurg 72: 393-402, 1990.
31. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857-869, 2003.
32. Li Y, Gorassini MA, Bennett DJ. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91: 767-783, 2004a.
33. Li Y, Li X, Harvey PJ, Bennett DJ. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92: 2694-2703, 2004b.
34. Lundbye-Jensen J, Nielsen JB. Central nervous adaptations following 1 wk of wrist and hand immobilization. J Appl Physiol 105: 139-151, 2008.
35. Manuel NA, Wallis DI, Crick H. Ketanserin-sensitive depressant actions of 5-HT receptor agonists in the neonatal rat spinal cord. Br J Pharmacol 116: 2647-2654, 1995.
36. Martin GR. Pre-clinical pharmacology of zolmitriptan (Zomig; formerly 311C90), a centrally and peripherally acting 5HT1B/1D agonist for migraine. Cephalalgia 17, Suppl 18: 4-14, 1997.
37. Martin GR, Robertson AD, MacLennan SJ, Prentice DJ, Barrett VJ, Buckingham J, Honey AC, Giles H, Moncada S. Receptor specificity and trigemino-vascular inhibitory actions of a novel 5HT1B/D receptor partial agonist, 311C90 (zolmitriptan). Br J Pharmacol 121: 157-164, 1997.
38. Meleger AL. Muscle relaxants and antispasticity agents. Phys Med Rehabil Clin N Am 17: 401-413, 2006.
39. Meythaler JM, Roper JF, Brunner RC. Cyproheptadine for intrathecal baclofen withdrawal. Arch Phys Med Rehabil 84: 638-642, 2003.
40. Miles TS, Turker KS, Le TH. Ia reflexes and EPSPs in human soleus motor neurones. Exp Brain Res 77: 628-636, 1989.
41. Millan MJ. Descending control of pain. Prog Neurobiol 66: 355-474, 2002.
42. Misiaszek JE. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28: 144-160, 2003.
43. Mohammed I, Hussain A. Intrathecal baclofen withdrawal syndrome-a life threatening complication of baclofen pump: a case report. BMC Clin Pharmacol 4: 6, 2004.
44. Murray KC, Nakae A, Stephens MJ, Rank M, D'Amico JM, Harvey PJ, Li X, Harris RL, 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 5HT2C receptors. Nat Med 16: 694-700, 2010.
45. 1F receptors. J Neurophysiol 106: 925-943, 2011.
46. Nielsen JF, Hansen HJ, Sunde N, Christensen JJ. Evidence of tolerance to baclofen in treatment of severe spasticity with intrathecal baclofen. Clin Neurol Neurosurg 104: 142-145, 2002.
47. Norton JA, Bennett DJ, Knash ME, Murray KC, Gorassini MA. Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man. Brain 131: 1478-1491, 2008.
48. Peterlin BL, Rapoport AM. Clinical pharmacology of the serotonin receptor agonist, zolmitriptan. Expert Opin Drug Metab Toxicol 3: 899-911, 2007.
49. Proietti-Cecchini A, Afra J, Schoenen J. Intensity dependence of the cortical auditory evoked potentials as a surrogate marker of central nervous system serotonin transmission in man: demonstration of a central effect for the 5HT1B/D agonist zolmitriptan (311C90, Zomig). Cephalalgia 17: 849-854, 1997.
50. Rank MM, Murray KC, Stephens MJ, D'Amico J, Gorassini MA, Bennett DJ. Adrenergic receptors modulate motoneuron excitability, sensory synaptic transmission and muscle spasms after chronic spinal cord injury. J Neurophysiol 105: 410-422, 2011.
51. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
52. Rosche J. Treatment of spasticity. Spinal Cord 40: 261-262, 2002.
53. Singer JH, Bellingham MC, Berger AJ. Presynaptic inhibition of glutamatergic synaptic transmission to rat motoneurons by serotonin. J Neurophysiol 76: 799-807, 1996.
54. Stempien L, Tsai T. Intrathecal baclofen pump use for spasticity: a clinical survey. Am J Phys Med Rehabil 79: 536-541, 2000.
55. Vinay LR, Bos R, Boulenguez P, Bras H, Brocard C, Buttigieg G, Haase S, Liabeuf K, Sadlaoud K. Activation of 5-HT2A receptors reduces spasticity after spinal cord injury via PKC-dependent up-regulation of KCC2 function. Soc Neurosci Abstr 182.07, 2012.
56. Visser WH, Klein KB, Cox RC, Jones D, Ferrari MD. 311C90, a new central and peripherally acting 5-HT1D receptor agonist in the acute oral treatment of migraine: a double-blind, placebo-controlled, dose-range finding study. Neurology 46: 522-526, 1996.
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. Werhahn KJ, Forderreuther S, Straube A. Effects of the serotonin 5HT1B/1D receptor agonist zolmitriptan in motor cortical excitability in humans. Neurology 51: 896-898, 1998.
59. Yoshimura M, Furue H. Mechanisms for the anti-nociceptive actions of the descending noradrenergic and serotonergic systems in the spinal cord. J Pharmacol Sci 101: 107-117, 2006.
60. Zehr EP. Considerations for the use of the Hoffman reflex in exercise studies. Eur J Appl Physiol 86: 455-468, 2002.