Comparison of the effects of nucleus tractus solitarius and ventral medial medulla lesions on illness-induced and subcutaneous formalin-induced hyperalgesias

Brain Research

Volumn 748, Issue 1-2, 1997, Pages 143-150

  Wiertelak, E P ^a   Roemer, B ^a   Maier, S F ^b   Watkins, L R ^b  

^a MACALESTER COLLEGE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

endotoxin; formalin; hyperalgesia; lipopolysaccharide; nucleus raphe magnus; nucleus reticularis paragigantocellularis; nucleus tractus solitarius; pain facilitation; rat; spinal cord

Indexed keywords

FORMALDEHYDE; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; HISTOLOGY; HYPERALGESIA; MALE; MEDULLA OBLONGATA; NONHUMAN; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; SOLITARY TRACT NUCLEUS; TAIL FLICK TEST;

ANIMALS; FORMALDEHYDE; HYPERALGESIA; INJECTIONS, INTRAPERITONEAL; INJECTIONS, SUBCUTANEOUS; LIPOPOLYSACCHARIDES; MALE; MEDULLA OBLONGATA; PAIN; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS;

EID: 0031049046     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)01289-9     Document Type: Article

References (68)

1. Aicher, S.A. and Randich, A., Antinociception and cardiovascular responses produced by electrical stimulation in the nucleus tractus solitarius, nucleus reticularis ventralis, and the caudal medulla, Pain, 42 (1990) 103-119.
2. Akil, H. and Mayer, D.J., Antagonism of stimulation produced analgesia by p-CPA, a serotonin synthesis inhibitor, Brain Res., 44 (1972) 692-697.
3. Amodel, N. and Paxinos, G., Unilateral knife cuts produce ipsilateral suppression of responsiveness to pain in the formalin test, Brain Res., 193 (1980) 85-94.
4. Auerbach, S., Fornal, C. and Jacobs, B.J., Response of serotonin-containing neurons in nucleus raphe magnus to morphine, noxious stimuli and periaqueductal gray stimulation in freely moving cats, Exp. Neurol., 88 (1985) 609-628.
5. Banna, N.R., Saade, N.B., Atweh, S.F. and Suhayl, J.J., Prolonged discharge of wide-dynamic range spinal neurons evoked by formaldehyde injected in their cutaneous receptive fields, Exp. Neurol., 93 (1986) 275-278.
6. Beitz, A.J., The nuclei of origin of brain stem enkephalin and substance P projections to the rodent nucleus raphe magnus, Neuroscience, 7 (1982) 2753-2768.
7. Beitz, A.J., The sites of origin brain stem neurotensin and serotonin projections to the rodent nucleus raphe magnus, J. Neurosci., 2 (1982) 829-842.
8. Catelli, J.M. and Sved, A.F., Lesions of the AV3V region attenuate sympathetic activation but not the hypertension elicited by destruction of the nucleus tractus solitarius, Brain Res., 439 (1988) 330-336.
9. Ceccatelli, S., Dagerlind, A. and Hökfelt, T., The effect of capsaicin on central nervous systems studied with c-fos histochemistry. In: Genazzani, Nappi, Petraglia and Martignoni (Eds.), Stress and Related Disorders - from Adaptation to Dysfunction, Parthenon, Carnforth, 1991, pp. 157-163.
10. Cervero, F. and Wolstencroft, J.H., A positive feedback loop between spinal cord nociceptive pathways and antinociceptive areas of the cat's brain stem, Pain, 20 (1984) 125-138.
11. 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, 52 (1993) 259-285.
12. Dickenson, A.H. and Sullivan, A.F., 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.
13. Du, H.J. and Zhou, S.Y., Involvement of solitary tract nucleus in control of nociceptive transmission in cat spinal cord neurons, Pain, 40 (1990) 323-331.
14. Ericsson, A., Kovacs, K.J. and Sawchenko, P.E., A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons, J. Neurosci., 14 (1994) 897-913.
15. Esteves, F., Lima, D. and Coimbra, A., Structural types of spinal cord marginal (lamina I) neurons projecting to the nucleus of the tractus solitarius in the rat, Somatosens. Mot. Res., 10 (1993) 203-216.
16. Guyenet, P.G. and Young, B.S., Projections of nucleus paragiganto-cellularis lateralis to locus coeruleus and other structures in rat, Brain Res., 406 (1987) 171-184.
17. Hart, B.L., Biological basis of the behavior of sick animals, Neurosci. Biobehav. Rev., 12 (1988) 123-137.
18. Houpt, T.A., Philopena, J.M., Wessel, T.C., Joh, T.H. and Smith, G.P., Increased c-fos expression in nucleus of the solitary tract correlated with conditioned taste aversion to sucrose in rats, Neurosci. Lett., 172 (1994) 1-5.
19. Kehl, L.J., Gogas, K.R., Lichtblau, L., Pollock, C.H., Mayes, M., Basbaum, A.I. and Wilcox, G.L., The NMDA antagonist MK801 reduces noxious stimulus-evoked Fos expression in the spinal cord dorsal horn. In: Bond, Charlton and Woolf (Eds.), Proc. VIth World Congres on Pain. Pain Research and Clinical Management, Vol. 4, Elsevier, Amsterdam, 1991, pp. 307-311.
20. Lewis, J.W., Baldrighi, G. and Akil, H., A possible interface between autonomie function and pain control: opioid analgesia and the nucleus tractus solitarius, Brain Res., 424 (1987) 65-70.
21. Lu, G.W., Meng, Z., Luo, L. and Yamakami, Y., The projection linkage between the spinal dorsal horn neurons and both the solitary tract and dorsal column nuclei, Sci. China (B), 34 (1991) 171-183.
22. Maier, S.F., Watkins, L.R. and Fleshner, M., Psychoneuroimmunology: the interface between behavior, brain, and immunity, Am. Psychol., 49 (1994) 1004-1018.
23. Maier, S.F., Wiertelak, E.P., Martin, D. and Watkins, L.R., Interleukin-1 mediates behavioral hyperalgesia produced by lithium chloride and endotoxin, Brain Res., 623 (1993) 321-324.
24. Maier, S.F., Wiertelak, E.P. and Watkins, L.R., Endogenous antianalgesia: effects of ventromedial medulla and dorsal raphe lesions, Pain, Suppl. 7 (1993) 457.
25. Matthies, B.K. and Franklin, K.B., Formalin pain is expressed in decerebrate rats but not attenuated by morphine, Pain, 51 (1992) 199-206.
26. Menétrey, D. and Basbaum, A.I., The distribution of substance P-, enkephalin-, and dynorphin-immunoreactive neurons in the medulla of the rat and their contribution to bulbospinal pathways, Neuroscience, 23 (1987) 173-187.
27. Menétrey, D. and Basbaum, A.I., Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation, J. Comp. Neurol., 255 (1987) 439-450.
28. Minson, J., Pilowshky, P., Llewellyn-Smith, I., Kaneko, T., Kapoor, V. and Chalmers, J., Glutamate in spinally projecting neurons of the rostral ventral medulla, Brain Res., 555 (1991) 326-331.
29. Morgan, M.M., Sohn, J.H., Lohof, A.M., Ben-Eliyahu, S. and Liebeskind, J.C., Characterization of stimulation-produced analgesia from the nucleus tractus solitarius in the rat, Brain Res., 486 (1989) 175-180.
30. Mtui, E.P., Anwar, M., Gomez, R., Reis, D.J. and Ruggiero, D.A., Projections from the nucleus tractus solitarius to the spinal cord, J. Comp. Neurol., 337 (1993) 231-252.
31. Murray, C.W., Cowan, A. and Larson, A.A., Neurokinin and NMDA antagonists (but not a kainic acid antagonist) are antinociceptive in the mouse formalin model, Pain, 44 (1991) 179-185.
32. Ohkubo, T., Shibata, M., Takahashi, H. and Inoki, R., Roles of substance P and somatostatin on transmission of nociceptive information induced by formalin in spinal cord, J. Pharmacol. Exp. Ther., 252 (1990) 1261-1268.
33. Palkovits, M., Mezey, E., Eskay, R.L. and Brownstein, M.J., Innervation of the nucleus of the solitary tract and the dorsal vagal nucleus by thyrotropin-releasing hormone-containing raphe neurons, Brain Res., 373 (1986) 246-251.
34. Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, Academic Press, New York, 1986.
35. Porro, C.A. and Cavazzuti, M., Functional correlates of acute prolonged pain in the rat central nervous system: 2-DG studies. In: Gonzalez-Lima, Finkenstadt and Scheich (Eds.), Advances in Metabolic Mapping Techniques for Brain Imaging of Behavioral and Learning Function, Kluwer Academic, London, 1992, pp. 319-342.
36. Porro, C.A. and Cavazzuti, M., Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model, Prog. Neurobiol., 41 (1993) 565-607.
37. Powley, T.L., Prechtle, J.C., Fox, E.A. and Berthoud, H.-R., Anatomical considerations for surgery of the rat abdominal vagus: distribution, paraganglia and regeneration, J. Auton. Nerv. Syst., 9 (1983) 79-97.
38. Przybylski, J. and Trzebski, A., Effect of bilateral lesions of the solitary tract nucleus on arterial blood pressure in spontaneously hypertensive rats of Okamoto strain, Acta Physiol. Pol., 27 (1976) 205-214.
39. Puig, S., Rivot, J.P. and Besson, J.M., Effect of subcutaneous administration of the chemical algogen formalin, on 5-HT metabolism in the nucleus raphe magnus and the medullary dorsal horn: a voltammetric study in freely moving rats, Brain Res., 365 (1992) 112-124.
40. Ran, K., Randich, A. and Gebhart, G.F., Vagal afferent modulation of a nociceptive reflex in rats: involvement of spinal opioid and monoamine receptors, Brain Res., 446 (1988) 285-294.
41. Ritter, S., Ritter, R.C. and Barnes, C.D., Neuroanatomy and Physiology of Abdominal Vagal Afferents, CRC Press, Ann Arbor, MI, 1992.
42. Sakurada, T., Katsumata, K., Yogo, H., Tan-No, K., Skaurada, S. and Kisara, K., Antinociception induced by CP96,345, a non-peptide NK-1 receptor antagonist, in the mouse formalin and capsaicin tests, Neurosci. Lett., 151 (1993) 142-145.
43. Schafe, G.E., Seeley, R.J. and Bernstein, I.L., Forebrain contribution to the induction of a cellular correlate of conditioned taste aversion in the nucleus of the solitary tract, J. Neurosci., 15 (1995) 6789-6796.
44. Shima, K., Nakahama, H., Yamamoto, M., Aya, K. and Inase, M., Effects of morphine on two types of nucleus raphe dorsalis neurons in awake cats, Pain, 29 (1989) 375-386.
45. Sim, L.J. and Joseph, S.A., Efferent projections of the nucleus raphe magnus, Brain Res. Bull., 28 (1992) 679-682.
46. Smullin, D.H., Skilling, S.R. and Larson, A.A., Interactions between substance P, calcitonin gene-related peptide, taurine, and excitatory amino acids in the spinal cord, Pain, 42 (1990) 93-101.
47. Sved, A.F., Peripheral pressor systems in hypertension caused by nucleus tractus solitarius lesions, Hypertension, 8 (1986) 742-747.
48. Tasker, R.A.R., Choinière, M., Libman, S.M. and Melzack, R., Analgesia produced by injection of lidocaine into the lateral hypothalamus, Pain, 31 (1987) 237-248.
49. Urban, M.O. and Smith, D.J., Role of neurotensin in the nucleus raphe magnus in opioid-induced antinociception from the periaqueductal gray, J. Pharmacol Exp. Ther., 265 (1993) 580-586.
50. Urban, M.O. and Smith, D.J., Localization of the antinociceptive and antianalgesic effects of neurotensin within the rostral ventromedial medulla, Neurosci. Lett., 174 (1994) 21-25.
51. Vaccarino, A.L. and Melzack, R., Analgesia produced by injection of lidocaine into the anterior cingulum bundle of the rat, Pain, 39 (1989) 213-219.
52. Vaccarino, A.L. and Melzack, R., Temporal processes of formalin pain: differential role of the cingulum bundle, fornix pathway and medial bulboreticular formation, Pain, 49 (1992) 257-271.
53. Van Bockstaele, E.J. and Aston-Jones, G., Collateralized projections from neurons in the rostral medulla to the nucleus locus coeruleus, the nucleus of the solitary tract and the periaqueductal gray, Neuroscience, 49 (1992) 653-668.
54. Voege-Sipahi, J., Ramsaroop, N.K. and Cox, V.C., The differential effects of lateral midbrain lesions on the two phases of formalin pain, NeuroReport, 3 (1992) 587-590.
55. Walters, E.T., Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia, and analgesia, Int. Rev. Neurobiol., 36 (1994) 325-427.
56. Wan, W., Janz, L., Vriend, C.Y., Sorensen, C.M., Greenberg, A.H. and Nance, D.M., Differential induction of c-fos immunoreactivity in hypothalamus and brain stem nuclei following central and peripheral administration of endotoxin, Brain Res. Bull., 32 (1993) 581-587.
57. Wan, W., Wetmore, L., Sorensen, C.M., Greenberg, A.H. and Nance, D.M., Neural and biochemical mediators of endotoxin and stress-induced c-fos expression in the rat brain, Brain Res. Bull., 34 (1994) 7-14.
58. Watkins, L.R., Goehler, L.E. and Maier, S.F., Immune activation: the role of proinflammatory cytokines in inflammation, illness responses and pathological pain states, Pain, 63 (1995) 289-302.
59. Watkins, L.R., Goehler, L.E., Relton, J.K., Brewer, M.T. and Maier, S.F., Immune-to-brain communication: systemic tumor necrosis factor-α (TNF-α) produces behavioral hyperalgesia via vagal afferents, Brain Res., 692 (1995) 244-250.
60. Watkins, L.R., Maier, S.F. and Goehler, L.E., Minireview: Cytokine-to-brain communication: a review and analysis of alternative mechanisms, Life Sci., 57 (1995) 1011-1026.
61. Watkins, L.R., Wiertelak, E.P., Furness, L.E. and Maier, S.F., Illness-induced hyperalgesia is mediated by spinal neuropeptides and excitatory amino acids, Brain Res., 664 (1994) 17-24.
62. Watkins, L.R., Wiertelak, E.P., Goehler, L.E., Mooney-Heiberger, K., Martinez, J., Furness, L., Smith, K.P. and Maier, S.F., Neurocircuitry of illness-induced hyperalgesia, Brain Res., 639 (1994) 283-299.
63. Watkins, L.R., Wiertelak, E.P., Goehler, L.E., Smith, K.P., Martin, D. and Maier, S.F., Characterization of cytokine-induced hyperalgesia, Brain Res., 654 (1994) 15-26.
64. Wiertelak, E.P., Furness, L.E., Horan, R., Martinez, J., Maier, S.F. and Watkins, L.R., Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade, Brain Res., 649 (1994) 19-26.
65. Wiertelak, E.P., Furness, L.E., Watkins, L.R. and Maier, S.F., Illness-induced hyperalgesia is mediated by a spinal NMDA-nitric oxide cascade, Brain Res., 664 (1994) 9-16.
66. Wiertelak, E.P., Maier, S.F. and Watkins, L.R., Learning to activate CCK anti-analgesia: light cues abolish morphine analgesia, Science, 256 (1992) 330-333.
67. 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 (1994) 227-234.
68. Young, E.G., Watkins, L.R. and Mayer, D.J., Comparison of the effects of ventral medullary lesions on systemic and microinjection morphine analgesia, Brain Res., 290 (1984) 119-129.