Descending facilitatory control of mechanically evoked responses is enhanced in deep dorsal horn neurones following peripheral nerve injury

Brain Research

Volumn 1019, Issue 1-2, 2004, Pages 68-76

  Suzuki, Rie ^a   Rahman, Wahida ^a   Hunt, Stephen P ^a   Dickenson, Anthony H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

5HT3 receptor; Descending facilitation; Neuropathy; Ondansetron; Pain modulation; Pharmacology; Spinal cord

Indexed keywords

ONDANSETRON; SEROTONIN 3 RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; ELECTROSTIMULATION; EVOKED RESPONSE; FACILITATION; HEAT; LOW DRUG DOSE; MALE; MECHANICAL STIMULATION; NERVE CELL; NERVE EXCITABILITY; NERVE FIBER; NERVE LIGATION; NOCICEPTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR BLOCKING; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL NERVE;

ACTION POTENTIALS; ANIMALS; MALE; NEURAL PATHWAYS; ONDANSETRON; PAIN MEASUREMENT; PERIPHERAL NERVES; PHYSICAL STIMULATION; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN, 5-HT3;

EID: 4043065626     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.05.108     Document Type: Article

References (59)

1. Ali Z., Wu G., Kozlov A., Barasi S. The role of 5-HT3 in antinociceptive processing in the rat spinal cord: results from behavioural and electrophysiological studies. Neuroscience Letters. 208:1996;203-207
2. Baranauskas G., Nistri A. Sensitization of pain pathways in the spinal cord: cellular mechanisms. Progress in Neurobiology. 54:1998;349-365
3. Bian D., Ossipov M.H., Zhong C., Malan T.P. Jr., Porreca F. Tactile allodynia, but not thermal hyperalgesia, of the hindlimbs is blocked by spinal transection in rats with nerve injury. Neuroscience Letters. 241:1998;79-82
4. Birder L.A., Perl E.R. Expression of alpha2-adrenergic receptors in rat primary afferent neurones after peripheral nerve injury or inflammation. Journal of Physiology. 515:1999;533-542
5. Bowsher D. Central pain. Pain Reviews. 2:1995;175-186
6. Burgess S., Gardell L., Ossipov M., Malan T. Jr., Vanderah T., Lai J., Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. Journal of Neuroscience. 22:2002;5129-5136
7. Calejesan A., Ch'ang M., Zhuo M. Spinal serotonergic receptors mediate facilitation of a nociceptive reflex by subcutaneous formalin injection into the hindpaw in rats. Brain Research. 798:1998;46-54
8. Chapman V., Suzuki R., Dickenson A.H. Electrophysiological characterization of spinal neuronal response properties in anaesthetized rats after ligation of spinal nerves L5-L6. Journal of Physiology. 507:1998;881-894
9. Cho H., Kim D., Lee N., Kim J.K., Lee K.M., Han K.S., Kang Y.N., Kim K.J. Changes in the alpha 2-adrenergic receptor subtypes gene expression in rat dorsal root ganglion in an experimental model of neuropathic pain. NeuroReport. 8:1997;3119-3122
10. Crisp T., Stafinsky J., Spanos L., Uram M., Perni V., Donepudi H. Analgesic effects of serotonin and receptor-selective serotonin agonists in the rat spinal cord. General Pharmacology. 22:1991;247-251
11. Danziger N., Gautron M., Le Bars D., Bouhassira D. Activation of diffuse noxious inhibitory controls (DNIC) in rats with an experimental peripheral mononeuropathy. Pain. 91:2001;287-296
12. Deegan R. Ondansetron: pharmacology of a specific 5HT3 receptor antagonist. American Journal of the Medical Sciences. 304:1992;373-378
13. Dickenson A., Matthews E., Suzuki R. Central nervous system mechanisms of pain in peripheral neuropathy. Hansson P., Fields H., Hill R., Marchettini P. Neuropathic Pain: Pathophysiology and Treatment. vol. 21:2001;85-106 IASP Press, Seattle
14. Farber L., Stratz T., Bruckle W., Spath M., Pongratz D., Lautenschlager J., Kotter I., Zoller B., Peter H., Neeck G., Alten R., Muller W. Efficacy and tolerability of tropisetron in primary fibromyalgia - a highly selective and competitive 5-HT3 receptor antagonist. Scandinavian Journal of Rheumatology. Supplement. 113:2000;49-54
15. Fields H.L., Heinricher M.M. Anatomy and physiology of a nociceptive modulatory system. Philosophical Transactions of the Royal Society of London. Series B Biological Sciences. 308:1985;361-374
16. Fields H., Rowbotham M. Multiple mechanisms of neuropathic pain: a clinical perspective. Gebhart G., Hammond D., Jensen T. Proceedings of the 7th World Congress on Pain. Progress in Pain Research and Management. vol. 2:1994;437-454 IASP Press, Seattle
17. Fields H., Bry J., Hentall I., Zorman G. The activity of neurones in the rostral medulla of the rat during withdrawal from noxious heat. Journal of Neuroscience. 3:1983;2545-2552
18. Glaum S., Anderson E. Identification of 5HT3 receptor binding sites in rat spinal cord synaptosomal membranes. European Journal of Pharmacology. 156:1988;287-290
19. Glaum S., Proudfit H., Anderson E. 5-HT3 receptors modulate spinal nociceptive reflexes. Brain Research. 510:1988;12-16
20. Green G.M., Lyons L., Dickenson A.H. Alpha2-adrenoceptor antagonists enhance responses of dorsal horn neurones to formalin induced inflammation. European Journal of Pharmacology. 347:1998;201-204
21. Green G., Scarth J., Dickenson A. An excitatory role for 5-HT in spinal inflammatory nociceptive transmission; state-dependent actions via dorsal horn 5-HT3 receptors in the anaesthetized rat. Pain. 89:2000;81-88
22. Guan Y., Terayama R., Dubner R., Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. Journal of Pharmacology and Experimental Therapeutics. 300:2002;513-520
23. Heinricher M., Roychowdhury S. Reflex-related activation of putative pain facilitating neurones in rostral ventromedial medulla requires excitatory amino acid transmission. Neuroscience. 78:1997;1159-1165
24. Kauppila T., Kontinen V.K., Pertovaara A. Influence of spinalization on spinal withdrawal reflex responses varies depending on the submodality of the test stimulus and the experimental pathophysiological condition in the rat. Brain Research. 797:1998;234-242
25. Kidd E., Laporte A., Langlois X., Fattaccini C., Doyen C., Lombard M., Gozlan H., Hamon M. 5HT3 receptors in the rat central nervous system are mainly located on nerve fibres and terminals. Brain Research. 612:1993;289-298
26. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain. 50:1992;355-363
27. Kovelowski C., Ossipov M., Sun H., Lai J., Malan T., Porreca F. Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain. 87:2000;265-273
28. Ma W., Eisenach J.C. Chronic constriction injury of sciatic nerve induces the up-regulation of descending inhibitory noradrenergic innervation to the lumbar dorsal horn of mice. Brain Research. 970:2003;110-118
29. Martin W., Gupta N., Loo C., Rohde D., Basbaum A. Differential effects of neurotoxic destruction of descending noradrenergic pathways on acute and persistent nociceptive processing. Pain. 80:1999;57-65
30. Mason P. Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Annual Review of Neuroscience. 24:2001;737-777
31. McCleane G.J., Suzuki R., Dickenson A.H. Does a single intravenous injection of the 5HT3 receptor antagonist ondansetron have an analgesic effect in neuropathic pain? A double-blinded, placebo-controlled cross-over study. Anesthesia and Analgesia. 97:2003;1474-1478
32. Miki K., Zhou Q.-Q., Guo W., Guan Y., Terayama R., Dubner R., Ren K. Changes in gene expression and neuronal phenotype in brain stem pain modulatory circuitry after inflammation. Journal of Neurophysiology. 87:2002;750-760
33. Miquel M., Emerit M., Nosjean A., Simon A., Rumajogee P., Brisorgueil M., Doucet E., Hamon M., Verge D. Differential subcellular localization of the 5HT3-As receptor subunit in the rat central nervous system. European Journal of Neuroscience. 15:2002;449-457
34. Ossipov M., Sun H., Malan T. Jr., Lai J., Porreca F. Mediation of spinal nerve injury induced tactile allodynia by descending facilitatory pathways in the dorsolateral funiculus in rats. Neuroscience Letters. 290:2000;129-132
35. Ossipov M., Lai J., Malan T. Jr., Vanderah T., Porreca F. Tonic descending facilitation as a mechanism of neuropathic pain. Hansson P., Fields H., Hill R., Marchettini P. Neuropathic Pain: Pathophysiology and Treatment. Progress in Pain Research and Management. vol. 21:2001;107-124 IASP Press, Seattle
36. Oyama T., Ueda M., Kuraishi Y., Akaike A., Satoh M. Dual effect of serotonin on formalin-induced nociception in the rat spinal cord. Neuroscience Research. 25:1996;129-135
37. Pertovaara A., Wei H., Hamalainen M. Lidocaine in the rostroventromedial medulla and the peraqueductal gray attenuates allodynia in neuropathic rats. Neuroscience Letters. 218:1996;127-130
38. Pertovaara A., Keski-Vakkuri U., Kalmari J., Wei H., Panula P. Response properties of neurons in the rostroventromedial medulla of neuropathic rats: attempted modulation of responses by [1DMe]NPYF, a neuropeptide FF analogue. Neuroscience. 105:2001;457-468
39. Porreca F., Burgess S., Gardell L., Vanderah T., Malan T. Jr., Ossipov M., Lappi D., Lai J. Inhibition of neuropathic pain by selective ablation of brainstem medullary cells expressing the mu-opioid receptor. Journal of Neuroscience. 21:2001;5281-5288
40. Porreca F., Ossipov M., Gebhart G. Chronic pain and medullary descending facilitation. Trends in Neurosciences. 25:2002;319-325
41. Ren K., Dubner R. Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. Journal of Neurophysiology. 76:1996;3025-3037
42. Sindrup S., Jensen T. Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action. Pain. 83:1999;389-400
43. Sung B., Na H.S., Kim Y.I., Yoon Y.W., Han H.C., Nahm S.H., Hong S.K. Supraspinal involvement in the production of mechanical allodynia by spinal nerve injury in rats. Neuroscience Letters. 246:1998;117-119
44. Suzuki R., Dickenson A. Neuropathic pain: nerves bursting with excitement... NeuroReport. 11:2000;R17-R21
45. Suzuki R., Chapman V., Dickenson A. The effectiveness of spinal and systemic morphine on rat dorsal horn neuronal responses in the spinal nerve ligation model of neuropathic pain. Pain. 80:1999;215-228
46. Suzuki R., Kontinen V., Matthews E., Dickenson A. Enlargement of receptive field size to low intensity mechanical stimulation in the rat spinal nerve ligation model of neuropathy. Experimental Neurology. 163:2000;408-413
47. Suzuki R., Morcuende S., Webber M., Hunt S., Dickenson A. Superficial NK1 expressing neurones control spinal excitability by activation of descending pathways. Nature Neuroscience. 5:2002;1319-1326
48. Suzuki R., Green G., Millan M., Dickenson A. Electrophysiologic characterization of the antinociceptive actions of S18616, a novel and potent alpha2-adrenoceptor agonist, after acute and persistent pain states. Journal of Pain. 3:2002;234-243
49. Tecott L., Maricq A., Julius D. Nervous system distribution of the serotonin 5HT3 receptor mRNA. Proceedings of the National Academy of Sciences of the United States of America. 90:1993;1430-1434
50. Terayama R., Guan Y., Dubner R., Ren K. Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation. Neuroreport. 11:2000;1915-1919
51. Tsuruoka M., Willis W. Descending modulation from the region of the locus coeruleus on nociceptive sensitivity in a rat model of inflammatory hyperalgesia. Brain Research. 743:1996;86-92
52. Urban M., Gebhart G. Supraspinal contributions to hyperalgesia. Proceedings of the National Academy of Sciences of the United States of America. 95:1999;2630-2635
53. Wei F., Dubner R., Ren K. Laminar-selective noradrenergic and serotoninergic modulation includes spinoparabrachial cells after inflammation. Neuroreport. 10:1999;1757-1761
54. Zeitz K., Guy N., Malmberg A., Dirajlal S., Martin W., Sun L., Bonhaus D., Stucky C., Julius D., Basbaum A. The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. Journal of Neuroscience. 22:2002;1010-1019
55. Zhuo M., Gebhart G.F. Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Pain. 42:1990;337-350
56. Zhuo M., Gebhart G.F. Spinal cholinergic and monoaminergic receptors mediate descending inhibition from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Research. 535:1990;67-78
57. Zhuo M., Gebhart G.F. Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Research. 550:1991;35-48
58. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 16:1983;109-110
59. Zimmermann M. Pathobiology of neuropathic pain. European Journal of Pharmacology. 429:2001;23-37