Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea

Neuroscience

Volumn 72, Issue 1, 1996, Pages 243-254

  Meng, I D ^a   Bereiter, D A ^a,b  

^a RHODE ISLAND HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

cornea; immediate early genes; nociception; spinal trigeminal nucleus

Indexed keywords

ALLYL ISOTHIOCYANATE; CALCITONIN GENE RELATED PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA; IMMEDIATE EARLY GENE; IMMUNOCYTOCHEMISTRY; MALE; NOCICEPTION; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; THERMAL EXPOSURE; TRIGEMINAL NUCLEUS;

EID: 0029990390     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(95)00541-2     Document Type: Article

References (77)

1. Abbadie C., Honore P. and Besson J.-M. (1994) Intense cold noxious stimulation of the rat hindpaw induces c-fos expression in lumbar spinal cord neurons. Neuroscience 59, 457-468.
2. Anton F., Herdegen T., Peppel P. and Leah J. D. (1991) c-Fos-like immunoreactivity in rat brainstem neurons following noxious chemical stimulation of the nasal mucosa. Neuroscience 41, 629-641.
3. 3H]GABA. J. auton. Nerv. Syst. 50, 109-122.
4. Belmonte C., Gallar J., Pozo M. A. and Rebollo I. (1991) Excitation by irritant chemical substances of sensory afferent units in the cat's cornea. J. Physiol. 437, 709-725.
5. Belmonte C. and Giraldez F. (1981) Responses of cat corneal sensory receptors to mechanical and thermal stimulation. J. Physiol. 321, 355-368.
6. Bereiter D. A., Bereiter D. F. and Hathaway C. B. (1996) The NMDA receptor antagonist MK-801 reduces Fos-like immunoreactivity in central trigeminal neurons and blocks select endocrine and autonomie responses to corneal stimulation in the rat. Pain (in press).
7. Bereiter D. A., Hathaway C. B. and Benetti A. P. (1994) Caudal portions of the spinal trigeminal complex are necessary for autonomie responses and display Fos-like immunoreactivity after corneal stimulation in the cat. Brain Res. 657, 73-82.
8. Bereiter D. A. and Tonnessen B. H. (1995) Morphine and somatostatin interact to reduce Fos-LI within trigeminal subnucleus caudalis after corneal stimulation in the rat. Soc. Neurosci. Abstr. 21, 1640.
9. Beuerman R. W., Snow A., Thompson H. and Stern M. (1992) Action potential response of the corneal nerves to irritants. Lens Eye Toxicol. Res. 9, 193-210.
10. Beuerman R. W. and Tanelian D. L. (1979) Corneal pain evoked by thermal stimulation. Pain 7, 1-14.
11. Bullitt E. (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. comp. Neurol. 296, 517-530.
12. Bullitt E., Lee C. L., Light A. R. and Willcockson H. (1992) The effect of stimulus duration on noxious-stimulus induced c-fos expression in the rodent spinal cord. Brain Res. 580, 172-179.
13. Burstein R., Cliffer K. D. and Giesler G. J. (1990) Cells of origin of the spinohypothalamic tract in the rat. J. comp. Neurol. 291, 329-344.
14. Chan R. K. W. and Sawchenko P. E. (1994) Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J. comp. Neurol. 348, 433-460.
15. 2 stimulation of the cornea: a comparison between human sensation and nerve activity in polymodal nociceptive afferents of the cat. Eur. J. Neurosci. 7, 1154-1163.
16. Coimbra F. and Coimbra A. (1994) Dental noxious input reaches the subnucleus caudalis of the trigeminal complex in the rat, as shown by c-fos expression upon thermal or mechanical stimulation. Neurosci. Lett. 173, 201-204.
17. Davis K. D. and Dostrovsky J. O. (1988) Responses of feline trigeminal spinal tract nucleus neurons to stimulation of the middle meningeal artery and sagittal sinus. J. Neurophysiol. 59, 648-666.
18. Ebersberger A., Anton F., Tolle T. R. and Zieglgansberger W. (1995) Morphine, 5-HT2 and 5-HT3 receptor antagonists reduce c-fos expression in the trigeminal nuclear complex following noxious chemical stimulation of the rat nasal mucosa. Brain Res. 676, 336-342.
19. Feil K. and Herbert H. (1995) Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kolliker-Fuse nuclei. J. comp. Neurol. 353, 506-528.
20. Gallar J., Pozo M. A., Tuckett R. P. and Belmonte C. (1993) Response of sensory units with unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat's cornea. J. Physiol. 468, 609-622.
21. Gogas K. R., Presley R. W., Levine J. D. and Basbaum A. I. (1991) The antinociceptive action of supraspinal opioids results from an increase in descending inhibitory control: correlation of nociceptive behavior and c-fos expression. Neuroscience 42, 617-628.
22. Hallas B. H. and Jacquin M. F. (1990) Structure-function relationships in rat brain stem subnucleus interpolaris IX. Inputs from subnucleus caudalis. J. Neurophysiol. 64, 28-45.
23. Hathaway C. B., Hu J. W. and Bereiter D. A. (1995) Distribution of Fos-like immunoreactivity in the caudal brain-stem of the rat following noxious chemical stimulation of the temporomandibular joint. J. comp. Neurol. 356, 444-456.
24. Heinz M., Schafer K. and Braun H. A. (1990) Analysis of facial cold receptor activity in the rat. Brain Res. 521, 289-295.
25. Hirata H., Poulos D. A. and Mol J. T. (1984) Differences in thermal responses of cat trigeminal ganglion "cold" receptors under urethane and pentobarbital anesthesia. Brain Res. 292, 387-389.
26. Hughes P. and Dragunow M. (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmac. Rev. 47, 133-178.
27. Hunt S. P., Pini A. and Evan G. (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328, 632-634.
28. Iwata K., Kanda K., Tsuboi Y., Kitajima K. and Sumino R. (1995) Fos induction in the medullary dorsal horn and C1 segment of the spinal cord by acute inflammation in aged rats. Brain Res. 678, 12-39.
29. Jacquin M. F., Chiaia N. L., Haring J. H. and Rhoades R. W. (1990) Intersubnuclear connections within the rat trigeminal brainstem complex. Somatosensory Motor Res. 7, 399-420.
30. Jasmin L., Gogas K. R., Ahlgren S. C., Levine J. D. and Basbaum A. I. (1994) Walking evokes a distinctive pattern of Fos-like immunoreactivity in the caudal brainstem and spinal cord of the rat. Neuroscience 58, 275-286.
31. Jones S. L. and Light A. R. (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. 335, 335-338.
32. Kenshalo D. R. (1960) Comparison of thermal sensitivity of the forehead, lip, conjunctiva and cornea. J. appl. Physiol. 15, 987-991.
33. Kenshalo D. R., Leonard R. B., Chung J. M. and Willis W. D. (1979) Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J. Neurophysiol. 42, 1370-1389.
34. Lee J.-L. and Beitz A. J. (1992) Electroacupuncture modifies the expression of c-fos in the spinal cord induced by noxious stimulation. Brain Res. 577, 80-91.
35. Lele P. P. and Weddell G. (1959) Sensory nerves of the cornea and cutaneous sensibility. Expl Neurol. 1, 334-359.
36. Lima D., Avelino A. and Coimbra A. (1993) Differential activation of c-fos in spinal neurones by distinct classes of noxious stimuli. NeuroReport 4, 747-750.
37. Lu J. and Bereiter D. A. (1995) Acute injection of adrenal steroids reduces cornea-evoked expression of c-fos within the spinal trigeminal nucleus of adrenalectomized rats. Neuroscience 66, 933-941.
38. Lu J., Hathaway C. B. and Bereiter D. A. (1993) Adrenalectomy enhances Fos-like immunoreactivity within the spinal trigeminal nucleus induced by noxious thermal stimulation of the cornea. Neuroscience 54, 809-818.
39. MacIver M. B. and Tanelian D. L. (1993) Structural and functional specialization of A-δ and C fiber free nerve endings innervating rabbit corneal epithelium. J. Neurosci. 13, 4511-4524.
40. Marfurt C. F. (1981) The central projections of trigeminal primary afferent neurons in the cat as determined by the transganglionic transport of horseradish peroxidase. J. comp. Neurol. 203, 785-798.
41. Marfurt C. F. and Del Toro D. R. (1987) Corneal sensory pathway in the rat: a horseradish peroxidase tracing study. J. comp. Neurol. 261, 450-459.
42. Marfurt C. F. and Echtenkamp S. F. (1988) Central projections and trigeminal ganglion location of corneal afferent neurons in the monkey, Macaca fascicularis. J. comp. Neurol. 272, 370-382.
43. Menetrey. and Basbaum A. I. (1987) Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J. comp. Neurol. 255, 439-450.
44. Menetrey D., Gannon A., Levine J. D. and Basbaum A. I. (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.
45. Meng I. D. and Bereiter D. A. (1993) Differential distribution of Fos-like immunoreactivity in spinal trigeminal nucleus following corneal stimulation. Soc. Neurosci. Abstr. 19, 110.
46. Meng I. D., Bereiter D. F. and Bereiter D. A. (1992) Differential expression of c-fos in trigeminal subnucleus interpolaris after chemical and thermal corneal stimulation in the rat. Soc. Neurosci. Abstr. 18, 497.
47. Meng I. D., Hu J. W., Benetti A. P. and Bereiter D. A. (1995) Differential encoding of corneal input in two distinct regions of the spinal trigeminal nucleus (Vsp) in the rat. Soc. Neurosci. Abstr. 21, 645.
48. Morgan J. I. and Curran T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. A. Rev. Neurosci. 14, 421-451.
49. Mosso J. A. and Kruger L. (1973) Receptor categories represented in spinal trigeminal nucleus caudalis. J. Neurophysiol. 36, 472-488.
50. Murphy A. Z., Ennis M., Shipley M. T. and Behbehani M. M. (1994) Directionally specific changes in arterial pressure induce differential patterns of Fos expression in discrete areas of the rat brainstem: a double-labeling study for Fos and catecholamines. J. comp. Neurol. 349, 36-50.
51. Nagano S., Myers J. A. and Hall R. D. (1975) Representation of the cornea in the brain stem of the rat. Expl Neurol. 49, 653-670.
52. Nishida Y. and Yokota T. (1991) Corneal representation within the trigeminal subnucleus caudalis and adjacent bulbar lateral reticular formation of the cat. J. Physiol. 41, 551-565.
53. Nozaki K., Boccalini P. and Moskowitz M. A. (1992) Expression of c-fos-like immunoreactivity in brainstem after meningeal irritation by blood in the subarchnoid space. Neuroscience 49, 669-680.
54. Panneton W. M. and Burton H. (1981) Corneal and periocular representation within the trigeminal sensory complex in the cat studied with transganglionic transport of horseradish peroxidase. J. comp. Neurol. 199, 327-344.
55. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
56. Phelan K. D. and Falls W. M. (1989) The interstitial system of the spinal trigeminal tract in the rat: anatomical evidence for morphological and functional heterogeneity. Somatosensory Motor Res. 6, 367-399.
57. Pozo M. A. and Cervero F. (1993) Neurons in the rat spinal trigeminal complex driven by corneal nociceptors: receptive-field properties and effects of noxious stimulation of the cornea. J. Neurophysiol. 70, 2370-2378.
58. Pozo M. A., Gallego R., Gallar J. and Belmonte C. (1992) Blockade by calcium antagonists of chemical excitation and sensitization of polymodal nociceptors in the cat's cornea. J. Physiol. 450, 179-189.
59. Presley R. W., Menetrey D., Levine J. D. and Basbaum A. I. (1990) Systemic morphine suppresses noxious stimulus-evoked fos protein-like immunoreactivity in the rat spinal cord. J. Neurosci. 10, 323-335.
60. Rowbotham G. F. (1939) Observations on the effects of trigeminal denervation. Brain 62, 364-380.
61. Rozsa A. J. and Beuerman R. W. (1982) Density and organization of free nerve endings in the corneal epithelium of the rabbit. Pain 14, 105-120.
62. Sandrini G., Alfonsi E., Ruiz L., Pavesi G., Micieli G., Manzoni G. C., Mancia D. and Nappi G. (1991) Impairment of corneal pain perception in cluster headache. Pain 47, 299-304.
63. Standaert D. G., Watson S. J., Houghten R. A. and Saper C. B. (1986) Opioid peptide immunoreactivity in spinal and trigeminal dorsal horn neurons projecting to the parabrachial nucleus in the rat. J. Neurosci. 6, 1220-1226.
64. Strassman A. M., Mineta Y. and Vos B. P. (1994) Distribution of Fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat. J. Neurosci. 14, 3725-3735.
65. Strassman A. M., Potrebic S. and Maciewicz R. J. (1994) Anatomical properties of brainstem trigeminal neurons that respond to electrical stimulation of dural blood vessels. J. comp. Neurol. 346, 349-365.
66. Strassman A. M., Vos B. P., Mineta Y., Naderi S., Borsook D. and Burstein R. (1993) Fos-like immunoreactivity in the superficial medullary dorsal horn induced by noxious and innocuous thermal stimulation of facial skin in the rat. J. Neurophysiol. 70, 1811-1821.
67. Strassman A. M. and Voss B. P. (1993) Somatotopic and laminar organization of Fos-like immunoreactivity in the medullary and cervical dorsal horn induced by noxious facial stimulation in the rat. J. comp. Neurol. 331, 495-516.
68. Sugimoto T., Hara T., Shirai H., Abe T., Ichikawa H. and Sato T. (1994) c-Fos induction in the subnucleus caudalis following noxious mechanical stimulation of the oral mucous membrane. Expl Neurol. 129, 251-256.
69. Tanelian D. L. (1991) Cholinergic activation of a population of corneal afferent nerves. Expl Brain Res. 86, 414-420.
70. Tanelian D. L. and Beuerman R. W. (1984) Responses of rabbit corneal nociceptors to mechanical and thermal stimulation. Expl Neurol. 84, 165-178.
71. Tolle T. R., Herdegen T., Schadrack J., Bravo R., Zimmermann M. and Zieglgansberger W. (1994) Application of morphine prior to noxious stimulation differentially modulates expression of Fos, Jun and Krox-24 proteins in rat spinal cord neurons. Neuroscience 58, 305-321.
72. Whitear M. (1960) An electron microscope study of the cornea in mice, with special reference to the innervation. J. Anat. 94, 387-409.
73. Williams S., Pini A., Evan G. and Hunt S. P. (1989) Molecular events in the spinal cord following sensory stimulation. In Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord (eds Cervero F., Bennett G. J. and Headley P. M.), pp. 273-283. Plenum Press, New York.
74. Winer B. J. (1971) Statistical Principles in Experimental Design. 2nd edn, pp. 514-603. McGraw-Hill, New York.
75. Yokota T., Koyama N., Nishikawa Y., Nishikawa N., Nishida Y., Hasegawa A. and Fujino Y. (1991) Trigeminal nociceptive neurons in the subnucleus reticularis ventralis - I. Response properties and afferent connections. Neurosci. Res. 11, 1-17.
76. Yoshida A., Dostrovsky J. O., Sessle B. J. and Chiang C. Y. (1991) Trigeminal projections to the nucleus submedius of the thalamus in the rat. J. comp. Neurol. 307, 609-625.
77. Zander E. and Weddell G. (1951) Observations on the innervation of the cornea. J. Anat. 85, 68-99.