Proximal colon distention increases Fos expression in the lumbosacral spinal cord and activates sacral parasympathetic NADPHd-positive neurons in rats

Journal of Comparative Neurology

Volumn 390, Issue 3, 1998, Pages 311-321

  Martínez, Vicente ^a,b   Wang, Lixin ^a   Mayer, Emeran ^a,b   Taché, Yvette ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Immediate early genes; Nitric oxide; Pain; Sacral parasympathetic nucleus; Visceral afferents

Indexed keywords

ONCOPROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLON DILATATION; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; LUMBOSACRAL SPINE; MALE; MICROPHOTOGRAPHY; NOCICEPTION; NONHUMAN; ONCOGENE C FOS; PARASYMPATHETIC NERVE; PRIORITY JOURNAL; RAT;

EID: 2642706693     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980119)390:3<311::AID-CNE1>3.3.CO;2-Z     Document Type: Article

References (62)

1. Abercrombie, M. (1946) Estimation of nuclear population from microtome sections. Anat. Rec. 94:239-247.
2. Azpiroz, F. (1995) Sensitivity of the stomach and small bowel: Human research and clinical relevance. In G.F. Gebhart (ed): Visceral Pain, Progress in Pain Research and Management. Seattle: IASP Press, pp. 391-428.
3. Barquist, E., B. Bonaz, V. Martínez, J. Rivier, M.J. Zinner, and Y. Taché (1996) Neuronal pathways involved in abdominal surgery-induced gastric ileus in rats. Am. J. Physiol. 270:R888-R894.
4. Bennett, G.J., M. Abdelmoumene, H. Hayashi, and R. Dubner (1980) Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase. J. Comp. Neurol. 194:809-827.
5. Berkley, K.J., C.H. Hubscher, and P.D. Wall (1993) Neuronal responses to stimulation of the cervix, uterus, colon, and skin in the rat spinal cord. J. Neurophysiol. 69:545-556.
6. Birder, L.A., J.R. Roppolo, M.J. Iadarola, and W.C. de Groat (1991) Electrical stimulation of visceral afferent pathways in the pelvic nerve increases c-fos in the rat lumbosacral spinal cord. Neurosci. Lett. 129:193-196.
7. Blottner, D., and H.-G. Baumgarten (1992) Nitric oxide synthetase (NOS)-containing sympathoadrenal cholinergic neurons of the rat IML-cell column: Evidence from histochemistry, immunohistochemistry, and retrograde tracing. J. Comp. Neurol. 316:45-55.
8. Bonaz, B., V. Plourde, and Y. Taché (1994) Abdominal surgery induces Fos immunoreactivity in the rat brain. J. Comp. Neurol. 349:212-222.
9. Bouhassira, D., L. Villanueva, Z. Bing, and D. le Bars (1992) Involvement of the subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat. Brain Res. 595:353-357.
10. Bullitt, E. (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in rat. J. Comp. Neurol. 296:517-530.
11. Chapman, V., J. Buritova, P. Honoré, and J.-M. Besson (1995) 7-Nitro-indozalone, a selective inhibitor of neuronal nitric oxide synthase, reduces formalin evoked c-Fos expression in dorsal horn neurons of the rat spinal cord. Brain Res. 697:258-261.
12. Dawson, A.M. (1985) Origin of pain in the irritable bowel syndrome. In N.W. Read (ed): Irritable Bowel Syndrome. Philadelphia: Grune and Stratton, pp. 155-162.
13. Dawson, T.M., D.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Snyder (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88:7797-7801.
14. Dragunow, M., and R. Faull (1989) The use of c-fos as a metabolic marker in neuronal pathways tracing. J. Neurosci. Methods 29:261-265.
15. Dun, N.J., S.L. Dun, U. Forstermann, and L.F. Tseng (1992) Nitric oxide synthase immunoreactivity in rat spinal cord. Neurosci. Lett. 147:217-220.
16. Fu, Q.-G., M.J. Chandler, D.L. McNeill, and R.D. Foreman (1992) Vagal afferent fibers excite upper cervical neurons and inhibit activity of lumbar spinal cord neurons in the rat. Pain 57:91-100.
17. Gebhart, G.F., and J.N. Sengupta (1995) Evaluation of visceral pain. In T.S. Gaginella (ed): Methods in Gastrointestinal Pharmacology. Boca Raton: CRC Press, pp. 359-373.
18. Giamberardino, M.A., R. Valente, P. de Bigontina, and L. Vecchiet (1995) Artificial ureteral calculosis in rats: Behavioral characterization of visceral pain episodes and their relationship with referred lumbar muscle hyperalgesia. Pain 61:459-469.
19. Haley, J.E., A.H. Dickenseon, and M. Schachter (1992) Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology 31:251-258.
20. Hamilton, M.O., R.E. Papka, D.L. O'Donoghue, A.M. Vaidya, S.J. Williams, C.R.D. Poff, and D.L. McNeill (1995) Spinal projection neurons to the laterodorsal pontine tegmental nucleus: Relationship to preganglionic neurons and nitric oxide synthase. J. Comp. Neurol. 353:1-8.
21. Herdegen, T., K. Kovary, J. Leah, and R. Bravo (1991) Specific temporal and spatial distribution of JUN, FOS and KROX-24 proteins in spinal neurons following noxious transsynpatic stimulation. J. Comp. Neurol. 313:178-191.
22. Hunt, S.P., A. Pini, and G. Evan (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634.
23. Hylden, J.L.K., H. Hayashi, R. Dubner, and G.J. Bennett (1986) Physiology and morphology of the lamina I spinomesenphalic projection. J. Comp. Neurol. 247:505-515.
24. Jänig, W., and M. Koltzenburg (1991) Receptive properties of sacral primary afferent neurons supplying the colon. J. Neurophysiol. 65:1067-1077.
25. Jones, S.L., and A.R. Light (1990) Electrical stimulation in the medullary nucleus raphe magnus inhibits noxious heat-evoked fos protein-like immunoreactivity in the rat lumbar spinal cord. Brain Res. 530:335-338.
26. Lantéri-Minet, M., P. Isnardon, J. De Pommery, and D. Menétrey (1993) Spinal and hindbrain structures involved in visceroception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 55:737-753.
27. Lee, J.-H., G.L. Wilcox, and A.J. Beitz (1992) Nitric oxide mediates Fos expression in the spinal cord induced by mechanical noxious stimulation. Neuroreport 3:841-844.
28. Lee, J.-H., R.H. Price, F.G. Williams, B. Mayer, and A.J. Beitz (1993) Nitric oxide synthase is found in some spinothalamic neurons and in neuronal processes that appose spinal neurons that express Fos induced by noxious stimulation. Brain Res. 608:324-333.
29. Luckensmeyer, G.B., and J.R. Keast (1994) Projections from the prevertebral and major pelvic ganglia to the ileum and large intestine of the male rat. J. Auton. Nerv. Syst. 49:247-259.
30. Maggi, C.A., S. Manzini, and A. Meli (1987) Contribution of neurogenic and myogenic factors in the response of rat proximal colon to distention. Am. J. Physiol. 252:G447-G457.
31. Malmberg, A.B., and T.L. Yaksh (1993) Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain 54:291-300.
32. Martínez, V., L. Wang, and Y. Taché (1994) C-fos expression in specific areas of the central nervous system induced by proximal colon distention in conscious rats. Soc. Neurosci. Abstr. 20:360.
33. Mawe, G.M., J.C. Bresnahan, and M.S. Beattie (1986) A light and electron microscopic analysis of the sacral parasympathetic nucleus after labelling primary afferent and efferent element with HRP. J. Comp. Neurol. 250:33-57.
34. Meller, S.T., and G.F. Gebhart (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52:127-136.
35. Menétrey, D., and J. De Pommery (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceroniception in the rat. Eur. J. Neurosci. 3:249-259.
36. Menétrey, D., A. Gannon, J.D. Levine, and A.I. Basbaum (1989) Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation. J. Comp. Neurol. 285:177-195.
37. Molander, C., and G. Grant (1995). Spinal cord cytoarchitecture. In G. Paxinos (ed): The Rat Nervous System. San Diego: Academic Press, In., pp 39-45.
38. Morgan, J.I., and T. Curran (1991) Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14:421-451.
39. Morgan, C., I. Nadelhaft, and W.C. de Groat (1981) The distribution of visceral primary afferents from the pelvic nerve to the Lissauer's tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus. J. Comp. Neurol. 201:415-440.
40. Morgan, C.W., W.C. de Groat, L.A. Felkins, and S.J. Zhang (1991) Axon collaterals indicate broad intraspinal role for sacral preganglionic neurons. Proc. Natl. Acad. Sci. USA 88:6888-6892.
41. Morgan, M.M., R.R. Gogas, and A.I. Basbaum (1994) Diffuse noxious inhibitory controls reduce the expression of noxious stimulus-evoked Fos-like immunoreactivity in the superficial and deep laminae of the rat spinal cord. Pain 56:347-352.
42. Nadelhaft, I., and A.M. Booth (1984) The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: A horseradish peroxidase study. J. Comp. Neurol. 226:238-245.
43. Nahin, R.L., A.M. Madsen, and G.J. Giesler Jr. (1983) Anatomical and physiological studies of the gray matter surrounding the spinal cord central canal. J. Comp. Neurol. 220:321-335.
44. Ness, T.J., and G.F. Gebhart (1987) Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat. J. Neurophysiol. 57:1867-1892.
45. Ness, T.J., and G.F. Gebhart (1988a) Characterization of neurons responsive to noxious colorectal distension in the T13-L2 spinal cord of the rat. J. Neurophysiol. 60:1419-1438.
46. Ness, T.J., and G.F. Gebhart (1988b) Colorectal distension as a noxious visceral stimulus: Physiologic and pharmacologic characterization of pseudoaffective reflexes in the rat. Brain Res. 450:153-169.
47. Ness, T.J., and G.F. Gebhart (1990) Visceral pain: A review of experimental studies. Pain 41:167-234.
48. Pascual, J.I., R. Insausti, and L.M. Gonzalo (1989) The pelvic innervation in the rat: Different spinal origin and projections in Sprague-Dawley and Wistar rats. Brain Res. 480:397-402.
49. Presley, R.W., D. Menetrey, J.D. Levine, and A.I. Basbaum (1990) Systemic morphine suppresses noxious stimulus-evoked fos protein-like immunoreactivity in the rat spinal cord. J. Neurosci. 10:323-335.
50. Semos, M.L., and P.M. Headley (1994) The role of nitric oxide in spinal nociceptive reflexes in rats with neurogenic and non-neurogenic peripheral inflammation. Neuropharmacology 33:1487-1497.
51. Sengupta, J.N., and G.F. Gebhart (1994) Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. J. Neurophysiol. 71:2046-2060.
52. Sjöqvist, A., P.M. Hellström, M. Jodal, and O. Lundgren (1984) Neurotransmitters involved in the colonic contraction and vasodilatation elicited by activation of the pelvic nerves in the cat. Gastroenterology 86:1481-1487.
53. Traub, R.J., P. Pechman, M.J. Iadarola, and G.F. Gebhart (1992) Fos-like proteins in the lumbosacral spinal cord following noxious and non-noxious colorectal distention in the rat. Pain 49:393-403.
54. Traub, R.J., T. Herdegen, and G.F. Gebhart (1993) Differential expression of c-fos and c-jun in two regions of the rat spinal cord following noxious colorectal distention. Neurosci. Lett. 160:121-125.
55. Traub, R.J., F. Lim, J.N. Sengupta, S.T. Meller, and G.F. Gebhart (1994) Noxious distention of viscera results in differential c-Fos expression in second order sensory neurons receiving "sympathetic" or "parasympathetic" input. Neurosci. Lett. 180:71-75.
56. Valtschanoff, J.G., R.J. Weinberg, and A. Rustioni (1992) NADPH diaphorase in the spinal cord of rats. J. Comp. Neurol. 321:209-222.
57. Vizzard, M.A., S.L. Erdman, and W.C. de Groat (1993) Localization of NADPH-diaphorase in pelvic afferent and efferent pathways of the rat. Neurosci. Lett. 152:72-76.
58. Vizzard, M.A., S.L. Erdman, V.I. Erickson, R.J. Steward, J.R. Roppolo, and W.C. De Groat (1994) Localization of NADPH diaphorase in the lumbosacral spinal cord and dorsal root ganglia in the cat. J. Comp. Neurol. 339:62-75.
59. Vizzard, M.A., S.L. Erdman, and W.C. de Groat (1995) Increased expression of neuronal nitric oxide synthase (NOS) in visceral neurons after nerve injury. J. Neurosci. 15:4033-4045.
60. Wall, P.D., D.H. Hubscher, and K.J. Berkley (1993) Intraspinal modulation of neuronal responses to uterine and cervix stimulation in rat L1 and L6 dorsal horn. Brain Res. 622:71-78.
61. Zhang, X., V. Verge, Z. Wiesenfeld-Hallin, G. Ju, D. Bredt, S.H. Snyder, and T. Hökfelt (1993) Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J. Comp. Neurol. 335:563-575.
62. Zhang, R.-X., R. Wang, J.-H. Chen, and J.-T. Qiao (1994) Effects of descending inhibitory systems on the c-fos expression in the rat spinal cord during formalin-induced noxious stimulation. Neuroscience 58:299-304.