Blockade of opioid receptors in the medullary reticularis nucleus dorsalis, but not the rostral ventromedial medulla, prevents analgesia produced by diffuse noxious inhibitory control in rats with muscle inflammation

Journal of Pain

Volumn 12, Issue 6, 2011, Pages 687-697

  De Resende, Marcos A ^a   Silva, Luis Felipe S ^b   Sato, Karina ^b   Arendt Nielsen, Lars ^c   Sluka, Kathleen A ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF IOWA   (United States)

^c AALBORG UNIVERSITY   (Denmark)

Author keywords

DNIC; inhibition; muscle; opioid; Pain

Indexed keywords

NALOXONE; OPIATE RECEPTOR;

ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; BRAIN STEM; CHRONIC INFLAMMATION; CONTROLLED STUDY; DIFFUSE NOXIOUS INHIBITORY CONTROL; GASTROCNEMIUS MUSCLE; HYPERALGESIA; MALE; MEDULLARY NUCLEUS; MEDULLARY RETICULARIS NUCLEUS DORSALIS; MYALGIA; MYOSITIS; NONHUMAN; RAT; ROSTRAL VENTROMEDIAL MEDULLA; SKIN SENSITIVITY; TEMPERATURE DEPENDENCE;

ANALGESIA; ANIMALS; EFFERENT PATHWAYS; INFLAMMATION; MALE; MEDULLA OBLONGATA; MUSCLE, SKELETAL; NEURAL INHIBITION; PAIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; RETICULAR FORMATION;

EID: 79958118794     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2010.12.009     Document Type: Article

References (64)

1. L. Arendt-Nielsen, K.A. Sluka, and H.L. Nie Experimental muscle pain impairs descending inhibition Pain 140 2008 465 471
2. N. Attal, F. Jazat, V. Kayser, and G. Guilbauld Further evidence for "pain-related" behaviours in a model of unilateral peripheral mononeuropathy Pain 41 1990 235 251 (Pubitemid 20179931)
3. N. Attal, V. Kayser, F. Jazat, and G. Guilbaud Behavioural evidence for a bidirectional effect of systemic naloxone in a model of experimental neuropathy in the rat Brain Res 494 1989 276 284 (Pubitemid 19194541)
4. Z. Bing, L. Villanueva, and D. Le Bars Effects of systemic morphine upon A delta- and C-fibre evoked activities of subnucleus reticularis dorsalis neurones in the rat medulla Eur J Pharmacol 164 1989 85 92 (Pubitemid 19123485)
5. D. Bouhassira, D. Chitour, L. Villanueva, and D. Le Bars Morphine and diffuse noxious inhibitory controls in the rat: Effects of lesions of the rostral ventromedial medulla Eur J Pharmacol 232 1993 207 215 (Pubitemid 23080196)
6. D. Bouhassira, D. Chitour, L. Villaneuva, and D. Le Bars The spinal transmission of nociceptive information: Modulation by the caudal medulla Neuroscience 69 1995 931 938
7. D. Bouhassira, D. Le Bars, and L. Villanueva Heterotopic activation of A delta and C fibres triggers inhibition of trigeminal and spinal convergent neurones in the rat J Physiol 389 1987 301 317 (Pubitemid 17115799)
8. D. Bouhassira, L. Villanueva, Z. Bing, and D. Le Bars Involvement of the subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat Brain Res 595 1992 353 357
9. D. Bouhassira, L. Villanueva, and D. Le Bars Effects of systemic morphine on diffuse noxious inhibitory controls: Role of the periaqueductal grey Eur J Pharmacol 216 1992 149 156
10. E.E. Bragdon, K.C. Light, N.L. Costello, A. Sigurdsson, S. Bunting, K. Bhalang, and W. Maixner Group differences in pain modulation: Pain-free women compared to pain-free men and to women with TMD Pain 96 2002 227 237 (Pubitemid 34327868)
11. S.E. Burgess, L.R. Gardell, M.H. Ossipov, T.P. Malan, T.W. Vanderah, J. Lai, and F. Porreca Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain J Neurosci 22 2002 5129 5136 (Pubitemid 37465626)
12. B. Calvino, L. Villanueva, and D. Le Bars The heterotopic effects of visceral pain: Behavioural and electrophysiological approaches in the rat Pain 20 1984 261 271 (Pubitemid 15207394)
13. I. Cattaneo, V. Kayser, and G. Guilbaud Differential effects of specific delta and kappa opioid receptor antagonists on the bidirectional dose-dependent effect of systemic naloxone in arthritic rats, an experimental model of persistent pain Brain Res 623 1993 201 207 (Pubitemid 23275401)
14. T.J. Coderre, and R. Melzack Cutaneous hyperalgesia: Contributions of the peripheral and central nervous systems to the increase in pain sensitivity after injury Brain Res 404 1987 95 106 (Pubitemid 17021884)
15. T.J. Coderre, and R. Melzack Increased pain sensitivity following heat injury involves a central mechanism Behav Brain Res 15 1985 259 262 (Pubitemid 15003213)
16. N. Danziger, M. Gautron, B.D. Le, and D. Bouhassira Activation of diffuse noxious inhibitory controls (DNIC) in rats with an experimental peripheral mononeuropathy Pain 91 2001 287 296 (Pubitemid 32241150)
17. N. Danziger, J. Weil-Fugazza, D. Le Bars, and D. Bouhassira Alteration of descending modulation of nociception during the course of monoarthritis in the Rat J Neurosci 19 1999 2394 2400 (Pubitemid 29133414)
18. N. Danziger, J. Weil-Fugazza, D. Le Bars, and D. Bouhassira Stage-dependent changes in the modulation of spinal nociceptive neuronal activity during the course of inflammation Eur J Neurosci 13 2001 230 240 (Pubitemid 32142467)
19. L.F.S. daSilva, J.M. DeSantana, and K.A. Sluka Activation of NMDA receptors in the brainstem, RVM and Gi mediate hyperalgesia produced by repeated intramuscular injections of acidic saline J Pain 11 2010 378 387
20. R.R. Edwards, R.B. Fillingim, S. Yamauchi, A. Sigurdsson, S. Bunting, S.G. Mohorn, and W. Maixner Effects of gender and acute dental pain on thermal pain responses Clin J Pain 15 1999 233 237 (Pubitemid 29467555)
21. R.R. Edwards, T.J. Ness, and R.B. Fillingim Endogenous opioids, blood pressure, and diffuse noxious inhibitory controls: A preliminary study Percept Mot Skills 99 2004 679 687 (Pubitemid 39621029)
22. H. Foo, and F.J. Helmstetter Expression of antinociception in response to a signal for shock is blocked after selective downregulation of mu-opioid receptors in the rostral ventromedial medulla Brain Res Mol Brain Res 76 2000 282 288 (Pubitemid 30179764)
23. M. Granot, I. Weissman-Fogel, Y. Crispel, D. Pud, Y. Granovsky, E. Sprecher, and D. Yarnitsky Determinants of endogenous analgesia magnitude in a diffuse noxious inhibitory control (DNIC) paradigm: Do conditioning stimulus painfulness, gender and personality variables matter? Pain 136 2008 142 149 (Pubitemid 351491376)
24. N. Hernandez, N. Dmitrieva, and H. Vanegas Medullary on-cell activity during tail-flick inhibition produced by heterotopic noxious stimulation Pain 58 1994 393 401 (Pubitemid 24284082)
25. E. Hopkins, M. Spinella, Z.W. Pavlovic, and R.J. Bodnar Alterations in swim stress-induced analgesia and hypothermia following serotonergic or NMDA antagonists in the rostral ventromedial medulla of rats Physiol Behav 64 1998 219 225 (Pubitemid 28458941)
26. R.W. Hurley, and D.L. Hammond The analgesic effects of supraspinal mu and delta opioid receptor agonists are potentiated during persistent inflammation J Neurosci 20 2000 1249 1259 (Pubitemid 30220481)
27. A. Kalra, M.O. Urban, and K.A. Sluka 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 (Pubitemid 32574535)
28. E. Kosek, and P. Hansson Modulatory influence on somatosensory perception from vibration and heterotopic noxious conditioning stimulation (HNCS) in fibromyalgia patients and healthy subjects Pain 70 1997 41 51 (Pubitemid 27128296)
29. E. Kosek, and G. Ordeberg Lack of pressure pain modulation by heterotopic noxious conditioning stimulation in patients with painful osteoarthritis before, but not following, surgical pain relief Pain 88 2000 69 78
30. E. Kraus, B.D. Le, and J.M. Besson Behavioral confirmation of "diffuse noxious inhibitory controls" (DNIC) and evidence for a role of endogenous opiates Brain Res 206 1981 495 499 (Pubitemid 11170234)
31. S. Lautenbacher, and G.B. Rollman Possible deficiencies of pain modulation in fibromyalgia Clin J Pain 13 1997 189 196 (Pubitemid 27524077)
32. D. Le Bars, D. Chitour, E. Kraus, A.H. Dickenson, and J.M. Besson Effect of naloxone upon diffuse noxious inhibitory controls (DNIC) in the rat Brain Res 204 1981 387 402 (Pubitemid 11205709)
33. D. Le Bars, and L. Villanueva Electrophysiological evidence for the activation of descending inhibitory controls by nociceptive afferent pathways Prog Brain Res 77 1988 275 299
34. D. Le Bars, A.H. Dickenson, and J.-M. Besson Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications Pain 6 1979 305 327 (Pubitemid 9205925)
35. A.S. Leffler, P. Hansson, and E. Kosek Somatosensory perception in a remote pain-free area and function of diffuse noxious inhibitory controls (DNIC) in patients suffering from long-term trapezius myalgia Eur J Pain 6 2002 149 159
36. K. Murase, and K. Kawakita Diffuse noxious inhibitory controls in anti-nociception produced by acupuncture and moxibustion on trigeminal caudalis neurons in rats Jpn J Physiol 50 2000 133 140 (Pubitemid 30243416)
37. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates, 6th edition, Academic Press, 2008
38. M.L. Peters, A.J. Schmidt, M.A. Van den Hout, R. Koopmans, and M.E. Sluijter Chronic back pain, acute postoperative pain and the activation of diffuse noxious inhibitory controls (DNIC) Pain 50 1992 177 187
39. M. Pinto, A.R. Castro, F. Tshudy, S.P. Wilson, D. Lima, and I. Tavares Opioids modulate pain facilitation from the dorsal reticular nucleus Mol Cell Neurosci 39 2008 508 518
40. M. Pinto, M. Sousa, D. Lima, and I. Tavares Participation of mu-opioid, GABA(B), and NK1 receptors of major pain control medullary areas in pathways targeting the rat spinal cord: Implications for descending modulation of nociceptive transmission J Comp Neurol 510 2008 175 187
41. F. Porreca, S.E. Burgess, L.R. Gardell, T.W. Vanderah, T.P. Malan, M.H. Ossipov, D.A. Lappi, and J. Lai Inhibition of neuropathic pain by selective ablation of brainstem medullary cells expressing the mu-opioid receptor J Neurosci 21 2001 5281 5288 (Pubitemid 32622953)
42. F. Porreca, M.H. Ossipov, and G.F. Gebhart Chronic pain and medullary descending facilitation Trends Neurosci 25 2002 319 325 (Pubitemid 34667014)
43. R. Radhakrishnan, S.A. Moore, and K.A. Sluka Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats Pain 104 2003 567 577 (Pubitemid 37289056)
44. K.C. Ram, E. Eisenberg, M. Haddad, and D. Pud Oral opioid use alters DNIC but not cold pain perception in patients with chronic pain - new perspective of opioid-induced hyperalgesia Pain 139 2008 431 438
45. M.A. Resende, G.G. Sabino, C.R.M. Candido, L.S.M. Pereira, and J.N. Francischi Transcutaneous electrical stimulation (TENS) effects in experimental inflammatory edema and pain Eur J Pharmacol 504 2004 217 222 (Pubitemid 39488218)
46. G. Sandrini, P. Rossi, I. Milanov, M. Serrao, A.P. Cecchini, and G. Nappi Abnormal modulatory influence of diffuse noxious inhibitory controls in migraine and chronic tension-type headache patients Cephalalgia 26 2006 782 789 (Pubitemid 43882986)
47. M. Serrao, P. Rossi, G. Sandrini, L. Parisi, G.A. Amabile, G. Nappi, and F. Pierelli Effects of diffuse noxious inhibitory controls on temporal summation of the RIII reflex in humans Pain 112 2004 353 360 (Pubitemid 39550736)
48. D.A. Skyba, R. Radhakrishnan, and K.A. Sluka Characterization of a method for measuring primary hyperalgesia of deep somatic tissue J Pain 6 2005 41 47 (Pubitemid 40052000)
49. K.A. Sluka Stimulation of deep somatic tissue with capsaicin produces long-lasting mechanical allodynia and heat hypoalgesia that depends on early activation of the cAMP pathway J Neurosci 22 2002 5687 5693 (Pubitemid 35386490)
50. K.A. Sluka, A. Kalra, and S.A. Moore Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia Muscle Nerve 24 2001 37 46 (Pubitemid 32038025)
51. L.C. Stanfa, and A. Dickenson Spinal opioid systems in inflammation Inflammation Research 44 1995 231 241
52. L.C. Stanfa, A.F. Sullivan, and A.H. Dickenson Alterations in neuronal excitability and the potency of spinal-mu, delta and kappa opioids after carrageenan-induced inflammation Pain 50 1992 345 354
53. R. Terayama, R. Dubner, and K. Ren 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 (Pubitemid 34603320)
54. R. Terayama, Y. Guan, R. Dubner, and K. Ren Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation Neuroreport 11 2000 1915 1919 (Pubitemid 30429135)
55. D.V. Tillu, G.F. Gebhart, and K.A. Sluka Descending facilitatory pathways from the RVM initiate and maintain bilateral hyperalgesia after muscle insult Pain 136 2008 331 339
56. M. Tsuruoka, Y. Hiruma, and W.D. Willis The subnucleus reticularis dorsalis is involved in antinociception produced by a low dose of naloxone during carrageenan-induced inflammation Brain Res 762 1997 264 268 (Pubitemid 27315963)
57. L.P. Vera-Portocarrero, J.Y. Xie, J. Kowal, M.H. Ossipov, T. King, and F. Porreca Descending facilitation from the rostral ventromedial medulla maintains visceral pain in rats with experimental pancreatitis Gastroenterology 130 2006 2155 2164 (Pubitemid 43816956)
58. L. Villanueva, and D. Le Bars The encoding of thermal stimuli applied to the tail of the rat by lowering the excitability of trigeminal convergent neurones Brain Res 330 1985 245 251 (Pubitemid 15107032)
59. L. Villanueva, and D. Le Bars The activation of bulbo-spinal controls by peripheral nociceptive inputs: Diffuse noxious inhibitory controls Biol Res 28 1995 113 125
60. R.Y. Walder, L.A. Rasmussen, J.D. Rainier, A.R. Light, J.A. Wemmie, and K.A. Sluka ASIC1 and ASIC3 play different roles in the development of hyperalgesia after inflammatory muscle injury J Pain 11 2010 210 218
61. P.D. Wall, and C.J. Woolf Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat J Physiol 356 1984 443 458 (Pubitemid 14011558)
62. C.H. Wilder-Smith, D. Schindler, K. Lovblad, S.M. Redmond, and A. Nirkko Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls Gut 53 2004 1595 1601 (Pubitemid 39434102)
63. J.C. Willer, D. Le Bars, and B.T. De Diffuse noxious inhibitory controls in man: Involvement of an opioidergic link Eur J Pharmacol 182 1990 347 355 (Pubitemid 20225728)
64. D. Yarnitsky, Y. Crispel, E. Eisenberg, Y. Granovsky, A. Ben-Nun, E. Sprecher, L.A. Best, and M. Granot Prediction of chronic post-operative pain: Pre-operative DNIC testing identifies patients at risk Pain 138 2008 22 28