Descending facilitatory pathways from the RVM initiate and maintain bilateral hyperalgesia after muscle insult

Pain

Volumn 136, Issue 3, 2008, Pages 331-339

  Tillu, D V ^a,b   Gebhart, G F ^a,b   Sluka, K A ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Facilitation; Gigantocellularis; Pain; Raphe magnus

Indexed keywords

ROPIVACAINE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; BRAIN REGION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; GASTROCNEMIUS MUSCLE; HYPERALGESIA; MALE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; EFFERENT PATHWAYS; HYPERALGESIA; LONG-TERM POTENTIATION; MALE; MEDULLA OBLONGATA; MUSCLE, SKELETAL; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 43549104452     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2007.07.011     Document Type: Article

References (54)

1. Abols I.A., and Basbaum A.I. Afferent connections of the rostral medulla of the cat: a neural substrate for midbrain-medullary interactions in the modulation of pain. J Comp Neurol 201 (1981) 285-297
2. Antal M., Petko M., Polgar E., Heizmann C.W., and StormMathisen J. Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience 73 (1996) 509-518
3. Basbaum A.I., Ralston D.D., and Ralston H.J.I. Bulbospinal projections in the primate: a light and electron microscopic study of a pain modulating system. J Comp Neurol 250 (1986) 311-323
4. Burgess S.E., Gardell L.R., Ossipov M.H., Malan T.P., Vanderah T.W., Lai J., et al. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 22 (2002) 5129-5136
5. Cameron A.A., Khan I.A., Westlund K.N., and Willis W.D. The efferent projections of the periaqueductal gray in the rat: a Phaseoleus vulgaris-leucoagglutinin study. II. Descending projections. J Comp Neurol 351 (1995) 585-601
6. Coutinho S.V., Urban M.O., and Gebhart G.F. Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 78 (1998) 59-69
7. Fields H.L., and Basbaum A.I. Central nervous system mechanisms of pain modulation. In: Wall P.D., and Melzack R. (Eds). Textbook of pain (1999), Churchill Livingstone, New York 243-257
8. Gopalkrishnan P., and Sluka K.A. Effect of varying frequency, intensity and pulse duration of TENS on primary hyperalgesia in inflamed rats. Arch Phys Med Rehabil 81 (2000) 984-990
9. Gran J.T. The epidemiology of chronic generalized musculoskeletal pain. Best Practice Res Clinical Rheumatol 17 (2003) 547-561
10. Granges G., and Littlejohn G. Pressure pain threshold and pain-free subjects, in patients with chronic regional pain syndromes, and in patients with fibromyalgia syndrome. Arthritis Rheum 36 (1993) 641-646
11. Graven-Nielsen T., Aspegren K.S., Henriksson K.G., Bengtsson M., Sorensen J., Johnson A., et al. Ketamine reduces muscle pain, temporal summation, and referred pain in fibromyalgia patients. Pain 85 (2000) 483-491
12. Guan Y., Terayama R., Dubner R., and Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther 300 (2002) 513-520
13. Hoeger-Bement M.K., and Sluka K.A. Phosphorylation of CREB and mechanical hyperalgesia is reversed by blockade of the cAMP pathway in a time-dependent manner after repeated intramuscular acid injections. J Neurosci 23 (2003) 5437-5445
14. Hurley R.W., and Hammond D.L. The analgesic effects of supraspinal mu and delta opioid receptor agonists are potentiated during persistent inflammation. J Neurosci 20 (2000) 1249-1259
15. Jones S.L., and Light A.R. Termination patterns of serotoninergic medullary raphespinal fibers in the rat lumbar spinal cord: an anterograde immunohistochemical study. J Comp Neurol 297 (1990) 267-282
16. Julien N., Goffaux P., Arsenault P., and Marchand S. Widespread pain in fibromyalgia is related to a deficit of endogenous pain inhibition. Pain 114 (2005) 295-302
17. Kalra A., Urban M.O., and Sluka K.A. Blockade of opioid receptors in rostral ventral medulla prevents antihyperalgesia produced by transcutaneous electrical nerve stimulation (TENS). J Pharmacol Exp Ther 298 (2001) 257-263
18. Keay K.A., and Bandler R. Deep and superficial noxious stimulation increases Fos-like immunoreactivity in different regions of the midbrain periaqueductal gray of the rat. Neurosci Lett 154 (1993) 23-26
19. Kehl L.J., Trempe T.M., and Hargreaves K.M. A new animal model for assessing mechanisms and management of muscle hyperalgesia. Pain 85 (2000) 333-343
20. Kosek E., and Hansson P. Modulatory influence on somatosensory perception from vibration and heterotopic noxious conditioning stimulation (HNCS) in fibromyalgia patients and healthy subjects. Pain 70 (1997) 41-51
21. Kovelowski C.J., Ossipov M.H., Sun H., Lai J., Malan T.P., and Porreca F. Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain 87 (2000) 265-273
22. Lautenbacher S., and Rollman G.B. Possible deficiencies of pain modulation in fibromyalgia. Clin J Pain 13 (1997) 189-196
23. Matsuyama K., Ohta Y., and Mori S. Ascending and descending projections of the nucleus reticularis gigantocellularis in the cat demonstrated by the anterograde neural tracer, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 460 (1988) 124-141
24. Miranda A., Peles S., Rudolph C., Shaker R., and Sengupta J.N. Altered visceral sensation in response to somatic pain in the rat. Gastroenterology 126 (2004) 1082-1089
25. Morgan M.M., and Fields H.L. Pronounced changes in the activity of nociceptive modulatory neurons in the rostral ventromedial medulla in response to prolonged thermal noxious stimuli. J Neurophysiol 72 (1994) 1161-1170
26. Porreca F., Burgess S.E., Gardell L.R., Vanderah T.W., Malan T.P., Ossipov M.H., et al. Inhibition of neuropathic pain by selective ablation of brainstem medullary cells expressing the mu-opioid receptor. J Neurosci 21 (2001) 5281-5288
27. Porreca F., Ossipov M.H., and Gebhart G.F. Chronic pain and medullary descending facilitation. Trends Neurosci 25 (2002) 319-325
28. Quimby L., Block S., and Gratwich G. Fibromyalgia: generalized pain intolerance and manifold symptom reporting. J Rheumatol 15 (1988) 1264-1270
29. Sim L.J., and Joseph S.A. Efferent projections of the nucleus raphe magnus. Brain Res Bull 28 (1992) 679-682
30. Skyba D.A., King E.W., and Sluka K.A. Effects of NMDA and non-NMDA ionotropic glutamate receptor antagonists on the development and maintenance of hyperalgesia induced by repeated intramuscular injection of acidic saline. Pain 98 (2002) 69-78
31. Skyba D.A., Lisi T.L., and Sluka K.A. Excitatory amino acid concentrations increase in the spinal cord dorsal horn after repeated intramuscular injection of acidic saline. Pain 119 (2005) 142-149
32. Skyba D.A., Radhakrishnan R., and Sluka K.A. Characterization of a method for measuring primary hyperalgesia of deep somatic tissue. J Pain 6 (2005) 41-47
33. Sluka K.A., Kalra A., and Moore S.A. Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24 (2001) 37-46
34. Sluka K.A., Price M.P., Breese N.M., Stucky C.L., Wemmie J.A., and Welsh M.J. Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 106 (2003) 139-229
35. Sorensen J., Graven-Nielsen T., Henriksson K.G., Bengtsson M., and Arendt-Nielsen L. Hyperexcitability in fibromyalgia. J Rheumatol 25 (1998) 152-155
36. Staud R., Carl K.E., Vierck C.J., Price D.D., Robinson M.E., Cannon R.L., et al. Repetitive muscle stimuli result in enhanced wind-up of fibromyalgia patients. Arthritis Rheum 44 (2001) S395
37. Staud R., Robinson M.E., Mauderli A.P., Cannon R.L., Vierck C.J., and Price D.D. Opioids modulate the enhanced temporal summation of second pain of fibromyalgia patients. Arthritis Rheum 46 (2002) S396
38. Staud R., Vierck C.J., Cannon R.L., Mauderli A.P., and Price D.D. Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome. Pain 91 (2001) 165-175
39. Terayama R., Dubner R., and Ren K. The roles of NMDA receptor activation and nucleus reticularis gigantocellularis in the time-dependent changes in descending inhibition after inflammation. Pain 97 (2002) 171-181
40. Tunks E., Crook J., Norman G., and Kalaher S. Tender points in fibromyalgia. Pain 34 (1988) 11-19
41. Urban M.O., and Gebhart G.F. Supraspinal contributions to hyperalgesia. Proc Natl Acad Sci USA 96 (1999) 7687-7692
42. Urban M.O., Zahn P.K., and Gebhart G.F. Descending facilitatory influences from the rostral medial medulla mediate secondary, but not primary hyperalgesia in the rat. Neuroscience 90 (1999) 349-352
43. Vanderah T.W., Suenaga N.M.H., Ossipov M.H., Malan T.P., Lai J., and Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J Neurosci 21 (2001) 279-286
44. Vera-Portocarrero L.P., Xie J.Y., Kowal J., Ossipov M.H., King T., and Porreca F. Descending facilitation from the rostral ventromedial medulla maintains visceral pain in rats with experimental pancreatitis. Gastroenterology 130 (2006) 2155-2164
45. Vera-Portocarrero L.P., Zhang E.T., Ossipov M.H., Xie J.Y., King T., Lai J., et al. Descending facilitation from the rostral ventromedial medulla maintains nerve injury-induced central sensitization. Nerusocience 140 (2006) 1311-1320
46. Vertes R.P., and Kocsis B. Projections of the dorsal raphe nucleus to the brainstem: PHA-L analysis in the rat. J Comp Neurol 340 (1994) 11-26
47. Wei F., Dubner R., and Ren K. Nucleus reticularis gigantocellularis and nucleus raphe magnus in the brain stem exert opposite effects on behavioral hyperalgesia and spinal Fos protein expression after peripheral inflammation. Pain 80 (1999) 127-141
48. Willis W.D., Sluka K.A., Rees H., and Westlund K.N. Cooperative mechanisms of neurotransmitter action in central nervous sensitization. Prog Brain Res 110 (1996) 151-166
49. Yokoyama T., Audette K.M., and Sluka K.A. Pregabalin reduces muscle and cutaneous hyperalgesia in two models of chronic muscle pain in rats. J Pain (2007)
50. Zagon A. Innervation of serotonergic medullary raphe neurons from cells of the rostral ventrolateral medulla in rats. Neuroscience 55 (1993) 849-867
51. Zagon A. Internal connections in the rostral ventromedial medulla of the rat. J Auton Nerv Syst 53 (1995) 43-56
52. Zemlan F.P., Behbehani M.M., and Beckstead R.M. Ascending and descending projections from nucleus reticularis magnocellularis and nucleus reticularis gigantocellularis - an autoradiographic and horseradish peroxidase study in the rat. Brain Res 292 (1984) 207-220
53. Zhuo M., and Gebhart G.F. Characterization of descending inhibition and facilitation from the nucleus reticularis gigantocellularis and nucleus reticularis gigantocellularis pars alpha in the rat. Pain 42 (1990) 337-350
54. Zhuo M., and Gebhart G.F. Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J Neurophysiol 78 (1997) 746-758