Reversal of spinal cord non-opiate analgesia by conditioned anti- analgesia in the rat

Pain

Volumn 71, Issue 3, 1997, Pages 237-247

  Watkins, L R ^a   McGorry, M ^a   Schwartz, B ^a   Sisk, D ^a   Wiertelak, E P ^a   Maier, S F ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

5HT2 receptor; 5HT3 receptor; GABA(A) receptor; GABA(B) receptor; Gamma amino butyric acid (GABA); Pain facilitation; Serotonin (5HT)

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; ARECAIDINE; BACLOFEN; BUSPIRONE; DELTA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; NALTREXONE; PHENYLBIGUANIDE; SEROTONIN; SEROTONIN 1 RECEPTOR; SEROTONIN 2 RECEPTOR; SEROTONIN 3 RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; DOSE RESPONSE; EPIDURAL DRUG ADMINISTRATION; GABAERGIC SYSTEM; INFLAMMATION; INTRAMUSCULAR DRUG ADMINISTRATION; MALE; NONHUMAN; PAIN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM;

EID: 0030835810     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-3959(97)03375-7     Document Type: Article

References (82)

1. Akil, H. and Mayer, D.J., Antagonism of stimulation produced analgesia by p-CPA, a serotonin synthesis inhibitor, Brain Res., 44 (1972) 692–697.
2. Alhaider, A.A., Lei, S.Z. and Wilcox, G.L., Spinal 5HT3 receptor-mediated antinociception: possible release of GABA, J. Neurosci., 11 (1991) 1881–1888.
3. Baber, N.S., Dourish, C.T. and Hill, D.R., The role of CCK, caerulein, and CCK antagonists in nociception, Pain, 39 (1989) 307–328.
4. Barbaro, N.M., Hammond, D.L. and Fields, H.L., Effects of intrathecally administered methysergide and yohimbine on microstimulation-produced antinociception in the rat, Brain Res., 343 (1985) 223–229.
5. Bohlhalter, S., Weinmann, O., Mohler, H. and Fritschy, J.M., Laminar compartmentalization of GABA-A receptor subtypes in the spinal cord: an immunohistochemical study, J. Neurosci., 16 (1996) 283–297.
6. Bourgoin, S., Pohl, M., Benoliel, J.J., Mauborgne, A., Collin, E., Hamon, M. and Cesselin, F., GABA, through GABA-A receptors, inhibits the potassium-stimulated release of calcitonin gene-related peptide – but not that of substance P-like material from rat spinal cord slices, Brain Res., 583 (1992) 344–348.
7. Bowery, N.G., Hudson, A.L. and Price, G.W., GABA-A and GABA-B receptor site distribution in the rat central nervous system, Neuroscience, 20 (1987) 365–383.
8. Coderre, T.J., Katz, J., Vaccarino, A.L. and Melzack, R., Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence, Pain, 377 (1993) 259–285.
9. Crisp, T., Stafinsky, J.L., Hess, J.E. and Uram, M., Spinal beta-endorphin analgesia involves an interaction with local monoaminergic systems, Eur. J. Pharmacol., 160 (1989) 211–217.
10. Crisp, T., Stafinsky, J.L., Spanos, L.J., Uram, M., Perni, V.C. and Donepudi, H.B., Analgesic effects of serotonin and receptor-selective serotonin agonists in the rat spinal cord, Gen. Pharmacol., 22 (1991a) 247–251.
11. Crisp, T., Stafinsky, J.L., Uram, M., Perni, V.C., Weaver, M.F. and Spanos, L.J., Serotonin contributes to the spinal antinociceptive effects of morphine, Pharmacol. Biochem. Behav., 39 (1991b) 591–595.
12. D'Amour, G.E. and Smith, D.L., A method for determining loss of pain sensation, J. Pharmacol. Exp. Ther., 72 (1941) 74–79.
13. Derkach, V., Surprenant, A. and North, R.A., 5-HT3 receptors are membrane ion channels, Nature, 339 (1989) 706–709.
14. Desarmenien, M., Feltz, P., Occhipinti, G., Santagelo, F. and Schlichter, R., Coexistence of GABA-A and GABA-B receptors on A-delta and C primary afferents, Br. J. Pharmacol., 81 (1984) 327–333.
15. Dickenson, A.H., Brewer, C.M. and Hayes, N.A., Effects of topical baclofen on C fibre-evoked neuronal activity in the rat dorsal horn, Neuroscience, 14 (1985) 557–562.
16. Dirig, D.M. and Yaksh, T.L., Intrathecal baclofen and muscimol, but not midazolam, are antinociceptive using the rat formalin model, J. Pharmacol. Exp. Ther., 275 (1995) 217–219.
17. Faris, P.L., Komisaruk, B.R., Watkins, L.R. and Mayer, D.J., Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia, Science, 219 (1983) 310–312.
18. Fujimoto, J.M., Arts, K.S., Rady, J.J. and Tseng, L.F., Spinal dynorphin A (1–17): possible mediator of antianalgesic action, Neuropharmacology, 29 (1990) 609–617.
19. Gillman, M.A. and Lichtigfeld, F.J., The opiate and antiopiate system: evidence for involvement in withdrawal responses, Can. Anaesth. Soc. J., 30 (1983) 564–565.
20. Giordano, J., Analgesic profile of centrally administered 2-methylserotonin against acute pain in rats, Eur. J. Pharmacol., 199 (1991) 233–236.
21. Glaum, S.R. and Anderson, E.G., Identification of 5HT3 binding sites in rat spinal cord synaptosomal membranes, Eur. J. Pharmacol., 156 (1988) 287–290.
22. Glaum, S.R., Proudfit, H.K. and Anderson, E.G., Reversal of the antinociceptive effects of intrathecally administered serotonin in the rat by a selective 5-HT3 receptor antagonist, Neurosci. Lett., 95 (1988) 313–317.
23. Glaum, S.R., Proudfit, H.K. and Anderson, E.G., 5HT3 receptors modulate spinal nociceptive reflexes, Brain Res., 510 (1990) 12–16.
24. Glennon, R.A., Peroutka, S.J. and Dukat, M., Binding characteristics of a quaternary salt of serotonin: 5-HTQ, 2nd IUPHAR Satellite Meeting on Serotonin, Basel, Switzerland, 1990.
25. Gonzalez-Mariscal, G., Gomora, P. and Beyer, C., Participation of opiatergic, GABAergic and serotonergic systems in the expression of copulatory analgesia in male rats, Pharmacol. Biochem. Behav., 49 (1994) 303–307.
26. Grisel, J.E., Watkins, L.R. and Maier, S.F., Spinal mechanisms of associative and non-associative morphine analgesic tolerance, Psychopharmacology, (1996) in press.
27. Hammond, D.L. and Drower, E.J., Effects of intrathecally administered THIP, baclofen and muscimol on nociceptive threshold, Eur. J. Pharmacol., 103 (1984) 121–125.
28. Hammond, D.L. and Washington, J.D., Antagonism of l -baclofen-induced antinociception by CGP 35348 in the spinal cord of the rat, Eur. J. Pharmacol., 234 (1993) 255–262.
29. Hammond, D.L. and Yaksh, T.L., Antagonism of stimulation-produced antinociception by intrathecal administration of methysergide or phentolamine, Brain Res., 298 (1984) 329–337.
30. Han, J.S., Ding, X.Z. and Fan, S.G., Cholecystokinin octapeptide (CCK-8): antagonism to electroacupuncture analgesia and a possible role in electroacupuncture tolerance, Pain, 27 (1986) 101–115.
31. Helfman, C.C., Anderson, G.F. and Barraco, R.A., Presynaptic displacement of serotonin by alpha-methyl-5-hydroxytryptamine in the nucleus solitarius of the rat, Neurosci. Lett., 189 (1995) 65–68.
32. Higgins, G.A., Joharchi, N. and Sellers, E.M., Behavioral effects of the 5-hydroxytryptamine-3 receptor agonists l-phenylbiguanide and m-chlorophenylbiguanide in rats, J. Pharmacol. Exp. Ther., 264 (1993) 1440–1449.
33. Hylden, J. and Wilcox, G., Intrathecal morphine in mice: a new technique, Eur. J. Pharmacol., 67 (1980) 313–316.
34. Itoh, S., Katsuura, G. and Maeda, Y., Caerulein and cholecystokinin suppress beta-endorphin-induced analgesia in the rat, Eur. J. Pharmacol., 80 (1982) 421–425.
35. Jones, B.E., Holmes, C.J., Rodriguez-Veiga, E. and Mainville, L., GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the rat, J. Comp. Neurol., 313 (1991) 349–367.
36. Kavaliers, M. and Yang, H.-Y.T., IgG from antiserum against endogenous mammalian FMRF-NH2-related peptides augments morphine and stress-induced analgesia in mice, Peptides, 10 (1989) 741–745.
37. Killian, P., Holmes, B.B., Takemori, A.E., Portoghese, P.S. and Fujimoto, J.M., Cold water swim stress- and delta-2 opioid-induced analgesia are modulated by spinal gamma-aminobutyric acid A receptors, J. Pharmacol. Exp. Ther., 274 (1995) 730–734.
38. Lake, J.R., Hebert, K.M., Payza, K., Deshotel, K.D., Hausam, D.D., Witherspoon, W.E., Arcangeli, K.R. and Malin, D.H., Analog of neuropeptide FF attenuates morphine tolerance, Neurosci. Lett., 146 (1992) 203–206.
39. Li, Y.J., Zhang, Z.H., Chen, J.Y. and Qiao, J.T., Effects of intrathecal naloxone and atropine on the nociceptive suppression induced by norepinephrine and serotonin at the spinal level in rats, Brain Res., 666 (1994) 113–116.
40. Lin, Q., Peng, Y. and Willis, W.D., Glycine and GABAa antagonists reduce the inhibition of primate spinothalamic tract neurons produced by stimulation in periaqueductal gray, Brain Res., 654 (1994) 286–302.
41. Magnuson, D.S.K., Sullivan, A.F., Simonnet, G., Roques, B.P. and Dickenson, A.H., Differential interactions of cholecystokinin and FLFQPQRF-NH2 with mu and delta opioid antinociception in the rat spinal cord, Neuropeptides, 16 (1990) 213–218.
42. Magoul, R., Onteniente, B., Geffard, M. and Calas, A., Anatomical distribution and ultrastructural organization of the GABAergic system in the rat spinal cord. An immunocytochemical study using anti-GABA antibody, Neuroscience, 20 (1987) 1001–1009.
43. Maier, S.F., Wiertelak, E.P. and Watkins, L.R., Endogenous pain facilitory systems: antianalgesia and hyperalgesia, Am. Pain Soc. J., 1 (1992) 191–198.
44. Malcangio, M. and Bowery, N.G., GABA-B but not GABA-A receptor activation inhibits electrically-evoked substance P-like immunoreactivity release from rat spinal cord in vitro, J. Pharmacol. Exp. Ther., 266 (1993) 1490–1496.
45. McGowan, M.K. and Hammond, D.L., Antinociception produced by microinjection of l -glutamate into the ventromedial medulla of the rat: mediation by spinal GABAa receptors, Brain Res., 620 (1993a) 86–96.
46. McGowan, M.K. and Hammond, D.L., Intrathecal GABAb antagonists attenuate the antinociception produced by microinjection of l -glutamate into the ventromedial medulla of the rat, Brain Res., 607 (1993b) 39–46.
47. Meller, S.T., Dykstra, C., Grzybycki, D., Murphy, S. and Gebhart, G.F., The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of rat, Neuropharmacology, 33 (1994) 1471–1478.
48. Millhorn, D.E., Hokfelt, T., Seroogy, K., Oertel, W., Verhofstad, A.A.J. and Wu, J.-Y., Immunohistochemical evidence for colocalization of gamma-aminobutyric acid and serotonin in neurons of the ventral medulla oblongata projecting to the spinal cord, Brain Res., 410 (1987) 179–185.
49. Murphy, A.Z., Murphy, R.M. and Zemlan, F.P., Role of spinal serotonin-1 receptor subtypes in thermally and mechanically elicited nociceptive reflexes, Psychopharmacology, 108 (1992) 123–130.
50. Pang, I.H. and Vasko, M.R., Morphine and norepinephrine but not 5-hydroxytryptamine and gamma-aminobutyric acid inhibit the potassium-stimulated release of substance P from rat spinal cord slices, Brain Res., 376 (1986) 268–279.
51. Peng, Y.B., Lin, Q. and Willis, W.D., The role of 5-HT3 receptors in periaqueductal gray-induced inhibition of nociceptive dorsal horn neurons in rats, J. Pharmacol. Exp. Ther., 276 (1996) 116–124.
52. Rady, J.J. and Fujimoto, J.M., Dynorphin A(1–17) mediates midazolam antagonism of morphine antinociception in mice, Pharmacol. Biochem. Behav., 46 (1993) 331–339.
53. Reichling, D.B. and Basbaum, A.I., Contribution of brainstem GABAergic circuitry to descending antinociceptive controls. I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus, J. Comp. Neurol., 302 (1990) 370–377.
54. Richardson, B.P. and Engel, G., The pharmacology and function of 5HT3 receptors, Trends Pharmacol. Sci., 7 (1986) 424–428.
55. Roberts, L.A., Beyer, C. and Komisaruk, B.R., Nociceptive responses to altered GABAergic activity at the spinal cord, Life Sci., 39 (1986) 1667–1674.
56. Saruhashi, Y., Young, W., Hassan, A.Z. and Park, R., Excitatory and inhibitory effects of serotonin on spinal axons, Neuroscience, 61 (1994) 645–653.
57. Sawynok, J., Monoamines as mediators of the antinociceptive effect of baclofen, Arch. Pharmacol., 323 (1983) 54–57.
58. Sawynok, J., Kato, N., Kavlicek, V. and LaBella, F.S., Lack of effect of baclofen on substance P and somatostatin release from the spinal cord in vitro, Arch. Pharmacol., 319 (1982) 78–81.
59. Schmauss, C. and Herz, A., Intrathecally administered dynorphin 1–17 modulates morphine-induced antinociception differently in morphine naive and morphine tolerant rats, Eur. J. Pharmacol., 135 (1987) 429–431.
60. Solomon, R.E. and Gebhart, G.F., Mechanisms of effects of intrathecal serotonin on nociception and blood pressure in rats, J. Pharmacol. Exp. Ther., 245 (1988) 905–912.
61. Sorkin, L.S., McAdoo, D.J. and Willis, W.D., Raphe magnus stimulation-induced antinociception in the cat is associated with release of amino acids as well as serotonin in the lumbar dorsal horn, Brain Res., 618 (1993) 95–108.
62. Sullivan, A.F., Hewett, K. and Dickenson, A.H., Differential modulation of alpha 2-adrenergic and opioid spinal antinociception by cholecystokinin and cholecystokinin antagonists in the rat dorsal horn: an electrophysiological study, Brain Res., 662 (1994) 141–147.
63. Todd, A.J. and McKenzie, J., GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord, Neuroscience, 31 (1989) 799–806.
64. Tseng, L.L. and Tang, R., Differential actions of the blockade of spinal opioid, adrenergic, and serotonergic receptors on the tail-flick inhibition induced by morphine microinjected into dorsal raphe and central gray in rats, Neuroscience, 33 (1989) 93–100.
65. Walters, E.T., Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia, and analgesia, Int. Rev. Neurobiol., 36 (1994) 325–327.
66. Watkins, L.R., Kinscheck, I.B., Kaufman, E., Frenk, H., Miller, J. and Mayer, D.J., Cholecystokinin antagonists selectively potentiate analgesia induced by endogenous opiates, Brain Res., 327 (1985a) 181–190.
67. Watkins, L.R., Kinscheck, I.B. and Mayer, D.J., Potentiation of morphine analgesia and apparent reversal of morphine tolerance by proglumide, Science, 244 (1985b) 395–396.
68. Watkins, L.R., Suberg, S.N., Thurston, C.L. and Culhane, E.S., Role of spinal cord neuropeptides on pain sensitivity and analgesia: thyrotropin-releasing hormone and vasopressin, Brain Res., 362 (1985c) 308–317.
69. Watkins, L.R. and Mayer, D.J., Multiple endogenous opiate and nonopiate analgesia systems: evidence of their existence and clinical implications, Ann. N.Y. Acad. Sci., 467 (1987) 273–299.
70. Watkins, L.R., Wiertelak, E.P., Grisel, J., Silbert, L. and Maier, S.F., Parallel activation of multiple spinal opiate systems appears to mediate `non-opiate' stress-induced analgesia, Brain Res., 594 (1992) 99–108.
71. Watkins, L.R., Maier, S.F. and Goehler, L.E., Immune activation: the role of proinflammatory cytokines in inflammation, illness responses, and pathological pain states, Pain, (1995) in press.
72. Wiertelak, E.P., Maier, S.F. and Watkins, L.R., Cholecystokinin antianalgesia: safety cues abolish morphine analgesia, Science, 256 (1992a) 830–833.
73. Wiertelak, E.P., Watkins, L.R. and Maier, S.F., Conditioned inhibition of analgesia, Anim. Learn. Behav., 20 (1992b) 339–349.
74. Wiertelak, E.P., Smith, K.P., Furness, L., Mooney-Heiberger, K., Mayr, T., Maier, S.F. and Watkins, L.R., Acute and conditioned hyperalgesic responses to illness, Pain, 56 (1994a) 227–234.
75. Wiertelak, E.P., Yang, H.-Y.T., Mooney-Heiberger, K., Maier, S.F. and Watkins, L.R., The nature of conditioned anti-analgesia: spinal cord opiate and anti-opiate neurochemistry, Brain Res., 634 (1994b) 214–226.
76. 3H]5-HT from spinal cord synaptosomes of rat, Neuropharmacology, 31 (1992) 725–733.
77. Xu, W., Cui, X. and Han, J.S., Spinal serotonin 1A and 1C/2 receptors mediate supraspinal mu opioid-induced analgesia, Neuroreport, 5 (1994) 2665–2668.
78. Yang, H.-Y.T., Fratta, W., Majane, E.A. and Costa, E., Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine, Proc. Natl. Acad. Sci. USA, 82 (1985) 7757–7761.
79. Yang, S.W., Zhang, Z.H., Wang, R., Xie, Y.F., Quao, J.T. and Dafny, N., Norepinephrine and serotonin-induced antinociception are blocked by naloxone with different dosages, Brain Res. Bull., 35 (1994) 113–117.
80. Yang, S.W., Chen, J.Y., Zhang, Z.H., Xie, Y.F., Qiao, J.T. and Dafny, N., Adenosine and opiate-like substances mediate antinociception at the spinal cord, Brain Res., 673 (1995) 170–174.
81. Zemlan, F.P., Behbehani, M.M. and Murphy, R.M., Serotonin receptor subtypes and the modulation of pain transmission. In: H.L. Fields and J.-M. Besson (Eds.), Progress in Brain Research, 77, Elsevier, Amsterdam, 1988, pp. 349–355.
82. Zemlan, F.P., Murphy, A.Z. and Behehani, M.M., 5HT1A receptors mediate the effect of the bulbospinal serotonin system on spinal dorsal horn nociceptive neurons, Pharmacology., 48 (1994) 1–10.