Descending control of persistent pain: Inhibitory or facilitatory?

Brain Research Reviews

Volumn 46, Issue 3, 2004, Pages 295-309

  Vanegas, Horacio ^a,b,c   Schaible, Hans Georg ^b  

^a INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c Institut fuer Physiologie   (Germany)

Author keywords

Chronic pain; Formalin; Hyperalgesia; Inflammation; Neuropathy; Pain modulation

Indexed keywords

1 (2,3 DIHYDRO 1 METHYL 2 OXO 5 PHENYL 1H 1,4 BENZODIAZEPIN 3 YL) 3 (3 METHYLPHENYL)UREA; 2 [[1 (7 CHLORO 4 QUINOLINYL) 5 (2,6 DIMETHOXYPHENYL) 3 PYRAZOLYL]CARBONYLAMINO] 2 ADAMANTANECARBOXYLIC ACID; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 6,7 DINITRO 2,3 QUINOXALINEDIONE; AMPRENAVIR; ATIPAMEZOLE; CLONIDINE; DEXMEDETOMIDINE; DIZOCILPINE; FORMALDEHYDE; FREUND ADJUVANT; IDAZOXAN; LIDOCAINE; N METHYL DEXTRO ASPARTIC ACID; N(G) NITROARGININE METHYL ESTER; OPIATE AGONIST;

FACILITATION; HYPERALGESIA; INFLAMMATION; INHIBITION (PSYCHOLOGY); LONG TERM POTENTIATION; MEDULLA OBLONGATA; NERVE STIMULATION; NEUROPATHIC PAIN; NEUROPATHY; NOCICEPTION; NONHUMAN; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSITIVITY ANALYSIS; SENSITIZATION; SPINAL CORD DORSAL HORN;

ANIMALS; EFFERENT PATHWAYS; HUMANS; MEDULLA OBLONGATA; MODELS, NEUROLOGICAL; NEURAL INHIBITION; PAIN, INTRACTABLE; PERIPHERAL NERVOUS SYSTEM DISEASES; POSTERIOR HORN CELLS; RETICULAR FORMATION; SYNAPTIC TRANSMISSION;

EID: 9644279795     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2004.07.004     Document Type: Review

References (80)

1. F.V. Abbott, Y. Hong, and K.B.J. Franklin The effect of lesions of the dorsolateral funiculus on formalin pain and morphine analgesia: a dose-response analysis Pain 65 1996 17 23
2. D. Bian, M.H. Ossipov, C. Zhong, T.P. Malan, and F. Porreca Tactile allodynia, but not thermal hyperalgesia, of the hindlimb is blocked by spinal transection in rats with nerve injury Neurosci. Lett. 241 1998 79 82
3. 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
4. A.A. Calejesan, M.H.-C. Ch'ang, and M. Zhuo Spinal serotonergic receptors mediate facilitation of a nociceptive reflex by subcutaneous formalin injection into the hindpaw in rats Brain Res. 798 1998 46 54
5. F. Cervero, H. Schaible, and R.F. Schmidt Tonic descending inhibition of spinal cord neurones driven by joint afferents in normal cats and in cats with an inflamed knee joint Exp. Brain Res. 83 1991 675 678
6. Z.-F. Cheng, H.L. Fields, and M.M. Heinricher Morphine microinjected into the periaqueductal gray has differential effects on 3 classes of medullary neurons Brain Res. 375 1986 57 65
7. 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
8. A.H. Dickenson, and A.F. Sullivan Subcutaneous formalin-induced activity of dorsal horn neurones in the rat: differential response to an intrathecal opiate administered pre- or post-formalin Pain 30 1987 349 360
9. H.L. Fields, and A.I. Basbaum Central nervous system mechanisms of pain modulation P.D. Wall R. Melzack Textbook of Pain 1999 Churchill Livingstone London 309 329
10. H.L. Fields, J. Bry, I. Hentall, and G. Zorman The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat J. Neurosci. 3 1983 2545 2552
11. H.L. Fields, H. Vanegas, I.D. Hentall, and G. Zorman Evidence that disinhibition of brain stem neurones contributes to morphine analgesia Nature (Lond.) 306 1983 684 686
12. H.L. Fields, M.M. Heinricher, and P. Mason Neurotransmitters in nociceptive modulatory circuits Annu. Rev. Neurosci. 14 1991 219 245
13. L.R. Gardell, T.W. Vanderah, S.E. Gardell, R. Wang, M.H. Osipov, J. Lai, and F. Porreca Enhanced evoked neurotransmitter release in experimental neuropathy requires descending facilitation J. Neurosci. 23 2003 8370 8379
14. A.-K. Gilbert, and K.B.J. Franklin GABAergic modulation of descending inhibitory systems from the rostral ventromedial medulla (RVM). Dose-response analysis of nociception and neurological deficits Pain 90 2001 25 36
15. 2-Adrenoceptor antagonists enhance reponses of dorsal horn neurones to formalin induced inflammation Eur. J. Pharmacol. 347 1998 201 204
16. 3 receptors in the anesthetized rat Pain 89 2000 81 88
17. Y. Guan, R. Terayama, R. Dubner, and K. Ren Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation J. Pharmacol. Exp. Ther. 300 2002 513 520
18. Y. Guan, W. Guo, S.-P. Zou, R. Dubner, and K. Ren Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry Pain 104 2003 401 413
19. I. Harasawa, H.L. Fields, and I.D. Meng Delta opioid receptor mediated actions in the rostral ventromedial medulla on tail flick latency and nociceptive modulatory neurons Pain 85 2000 255 262
20. M.M. Heinricher, and H.J. Kaplan GABA-mediated inhibition in rostral ventromedial medulla: role in nociceptive modulation in the lightly anesthetized rat Pain 47 1991 105 113
21. M.M. Heinricher, and S. McGaraughty Analysis of excitatory amino acid transmission within the rostral ventromedial medulla: implications for circuitry Pain 75 1998 247 255
22. M.M. Heinricher, and V. Tortorici Interference with GABA transmission in the rostral ventromedial medulla: disinhibition of off-cells as a central mechanism in nociceptive modulation Neuroscience 63 1994 533 546
23. M.M. Heinricher, M.M. Morgan, and H.L. Fields Direct and indirect actions of morphine on medullary neurons that modulate nociception Neuroscience 48 1992 533 543
24. M.M. Heinricher, W. Kincaid, and M.J. Neubert Neural substrate for analgesic and hyperalgesic actions of neurotensin within the rostral ventromedial medulla (RVM) Abstr.-Soc. Neurosci. 27 2001 (Progr. No. 161.167)
25. M.M. Heinricher, S. McGaraughty, and V. Tortorici Circuitry underlying anti-opioid actions of cholecystokinin within the rostral ventromedial medulla J. Neurophysiol. 85 2001 280 286
26. N. Hernandez, and H. Vanegas Encoding of noxious stimulus intensity by putative pain modulating neurons in the rostral ventromedial medulla and by simultaneously recorded nociceptive neurons in the spinal dorsal horn of rats Pain 91 2001 307 315
27. N. Hernandez, Y. Lopez, and H. Vanegas Medullary on- and off-cell responses precede both segmental and thalamic responses to tail heating Pain 39 1989 221 230
28. J.F. Herrero, and F. Cervero Supraspinal influences on the facilitation of rat nociceptive reflexes induced by carrageenan monoarthritis Neurosci. Lett. 209 1996 21 24
29. R.W. Hurley, and D.L. Hammond The analgesic effects of supraspinal μ and δ opioid receptor agonists are potentiated during persistent inflammation J. Neurosci. 20 2000 1249 1259
30. R.W. Hurley, and D.L. Hammond Contribution of endogenous enkephalins to the enhanced analgesic effects of supraspinal μ opioid receptor agonists after inflammatory injury J. Neurosci. 21 2001 2536 2545
31. J.L.K. Hylden, D.A. Thomas, M.J. Iadarola, R.L. Nahin, and R. Dubner Spinal opioid analgesic effects are enhanced in a model of unilateral inflammation/hyperalgesia: possible involvement of noradrenergic mechanisms Eur. J. Pharmacol. 194 1991 135 143
32. S.L. Jones Dipyrone into the nucleus raphe magnus inhibits the rat nociceptive tail-flick reflex Eur. J. Pharmacol. 318 1996 37 40
33. T. Kauppila, V.K. Kontinen, and A. Pertovaara 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 Res. 797 1998 234 242
34. W. Kincaid, M. Xu, C.J. Kim, M.J. Neubert, W.J. Roberts, and M.M. Heinricher Medullary substrate of secondary hyperalgesia produced by mustard oil in lightly anesthetized rats Abstr.-Soc. Neurosci. 27 2001 (Progr. No. 161.165)
35. C.J. Kovelowski, M.H. Ossipov, H. Sun, J. Lai, T.P. Malan, and F. Porreca Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat Pain 87 2000 265 273
36. D. Le Bars, A.H. Dickenson, and J.-M. Besson Diffuse noxious inhibitory controls (DNIC): I. Effects on dorsal horn convergent neurons in the rat Pain 6 1979 283 304
37. 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
38. X.-G. Liu, and J. Sandkühler Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-d-aspartic acid receptor blockage Neurosci. Lett. 191 1995 43 46
39. H. Mansikka, and A. Pertovaara Supraspinal influence on hindlimb withdrawal thresholds and mustard oil-induced secondary allodynia in rats Brain Res. Bull. 42 1997 359 365
40. S. Marinelli, C.W. Vaughan, S.A. Schnell, M.W. Wessendorf, and M.J. Christie Rostral ventromedial medulla neurons that project to the spinal cord express multiple opioid receptor phenotypes J. Neurosci. 22 2002 10847 10855
41. K. Miki, Q.-Q. Zhou, W. Guo, Y. Guan, R. Terayama, R. Dubner, and K. Ren Change in gene expression and neuronal phenotype in brain stem pain modulatory circuitry after inflammation J. Neurophysiol. 87 2002 750 760
42. M.J. Millan Descending control of pain Prog. Neurobiol. 66 2002 355 474
43. R. Monhemius, D.L. Green, M.H.T. Roberts, and J. Azami Periaqueductal grey mediated inhibition of responses to noxious stimulation is dynamically activated in a rat model of neuropathic pain Neurosci. Lett. 298 2001 70 74
44. M.M. Morgan, M.S. Gold, J.C. Liebeskind, and C. Stein Periaqueductal gray stimulation produces a spinally mediated, opioid antinociception for the inflamed hindpaw of the rat Brain Res. 545 1991 17 23
45. M.H. Ossipov, H. Sun, T.P. Malan, J. Lai, and F. Porreca Mediation of spinal nerve injury induced tactile allodynia by descending facilitatory pathways in the dorsolateral funiculus in rats Neurosci. Lett. 290 2000 129 132
46. T. Oyama, M. Ueda, Y. Kuraishi, A. Akaike, and M. Satoh Dual effect of serotonin on formalin-induced nociception in the rat spinal cord Neurosci. Res. 25 1996 129 135
47. Z.Z. Pan, J.T. Williams, and P.B. Osborne Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro J. Physiol. (Lond.) 427 1990 519 532
48. A. Pertovaara, H. Wei, and Hämäläinen Lidocaine in the rostroventromedial medulla and the periaqueductal gray attenuates allodynia in neuropathic rats Neurosci. Lett. 218 1996 127 130
49. A. Pertovaara A neuronal correlate of secondary hyperalgesia in the rat spinal dorsal horn in submodality selective and facilitated by supraspinal influences Exp. Neurol. 149 1998 193 202
50. F. Porreca, M.H. Ossipov, and G.F. Gebhart Chronic pain and medullary descending facilitation Trends Neurosci. 25 2002 319 325
51. 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 μ-opioid receptor J. Neurosci. 21 2001 5281 5288
52. C.A. Porro, and M. Cavazzuti Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model Prog. Neurobiol. 41 1993 565 607
53. M. Randic, M.C. Jiang, and R. Cerne Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord J. Neurosci. 13 1993 5228 5241
54. K. Ren, and R. Dubner Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation J. Neurophysiol. 76 1996 3025 3037
55. K. Ren, and R. Dubner Descending modulation in persistent pain: an update Pain 100 2002 1 6
56. J. Sandkühler, and X.-G. Liu Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury Eur. J. Neurosci. 10 1998 2476 2480
57. H.-G. Schaible, V. Neugebauer, F. Cervero, and R.F. Schmidt Changes in tonic descending inhibition of spinal neurons with articular input during the development of acute arthritis in the cat J. Neurophysiol. 66 1991 1021 1032
58. L.C. Stanfa, and A.H. Dickenson Enhanced alpha-2 adrenergic controls and spinal morphine potency in inflammation NeuroReport 5 1994 469 472
59. B. Sung, H.S. Na, Y.I. Kim, Y.W. Yoon, H.C. Han, S.H. Nahm, and S.K. Hong Supraspinal involvement in the production of mechanical allodynia by spinal nerve injury in rats Neurosci. Lett. 246 1998 117 119
60. R. Suzuki, S. Morcuende, M. Webber, S.P. Hunt, and A.H. Dickenson Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways Nat. Neurosci. 5 2002 1319 1326
61. F. Svendsen, A. Tjolsen, and K. Hole LTP of spinal Aβ and C-fibre evoked responses after electrical sciatic nerve stimulation NeuroReport 8 1997 3427 3430
62. 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
63. 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
64. V. Tortorici, and H. Vanegas Putative role of medullary off- and on-cells in the antinociception produced by dipyrone (metamizol) administered systemically or microinjected into PAG Pain 57 1994 197 205
65. V. Tortorici, and H. Vanegas Antinociception induced by systemic or PAG-microinjected lysine-acetylsalicylate in rats. Effects on tail-flick related activity of medullary off- and on-cells Eur. J. Neurosci. 7 1995 1857 1865
66. V. Tortorici, R. Salas, L. Nogueira, and H. Vanegas Modulation of the formalin response by on- and off-cells of the rostral ventromedial medulla Abstr.-Soc. Neurosci. 27 2001 (Progr. No. 161.166)
67. V. Tortorici, R. Salas, D. Vasquez, L. Nogueira, and H. Vanegas Inactivation of RVM on-cells with kynurenate prevents the behavioral response to intraplantar formalin in rats Soc. Neurosci. 2002 Abstr. View./Itin. Plan. CD-ROM 2002 Progr. No. 351.354
68. M. Tsuruoka, and W.D. Willis Bilateral lesions in the area of the nucleus locus coeruleus affect the development of hyperalgesia during carrageenan-induced inflammation Brain Res. 726 1996 233 236
69. M.O. Urban, and G.F. Gebhart Descending nociceptive facilitatory influences modulated by NMDA and neurotensin receptors in the rostral ventromedial medulla significantly contribute to secondary, but not primary thermal hyperalgesia Proc. 9th World Congr. Pain 1999 147
70. M.O. Urban, and G.F. Gebhart Supraspinal contributions to hyperalgesia Proc. Nat. Acad. Sci. U. S. A. 96 1999 7687 7692
71. M.O. Urban, and D.J. Smith Role of neurotensin in the nucleus raphe magnus in opioid-induced antinociception from the periaqueductal gray J. Pharmacol. Exp. Ther. 265 1993 580 586
72. M.O. Urban, M.C. Jiang, and G.F. Gebhart Participation of central descending nociceptive facilitatory systems in secondary hyperalgesia produced by mustard oil Brain Res. 737 1996 83 91
73. M.O. Urban, S.V. Coutinho, and G.F. Gebhart Biphasic modulation of visceral nociception by neurotensin in rat rostral ventromedial medulla J. Pharmacol. Exp. Ther. 290 1999 207 213
74. M.O. Urban, S.V. Coutinho, and G.F. Gebhart Involvement of excitatory amino acid receptors and nitric oxide in the rostral ventromedial medulla in modulating secondary hyperalgesia produced by mustard oil Pain 81 1999 45 55
75. M.O. Urban, P.K. Zahn, and G.F. Gebhart Descending facilitatory influences from the rostral medial medulla mediate secondary, but not primary hyperalgesia in the rat Neuroscience 90 1999 349 352
76. H. Vanegas, N.M. Barbaro, and H.L. Fields Tail-flick related activity in medullospinal neurons Brain Res. 321 1984 135 141
77. H. Wei, and A. Pertovaara MK-801, an NMDA receptor antagonist, in the rostroventral medulla attenuates development of neuropathic symptoms in the rat NeuroReport 10 1999 2933 2937
78. F. Wei, R. Dubner, and K. Ren 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
79. E.P. Wiertelak, L.E. Furness, R. Horan, J. Martinez, S.F. Maier, and L.R. Watkins Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade Brain Res. 649 1994 19 26
80. E.P. Wiertelak, B. Roemer, S.F. Maier, and L.R. Watkins Comparison of the effects of nucleus tractus solitarius and ventral medial medulla lesions on illness-induced and subcutaneous formalin-induced hyperalgesias Brain Res. 748 1997 143 150