Light microscopic localization of calcitonin gene-related peptide in the normal feline trigeminal system and following retrogasserian rhizotomy

Journal of Comparative Neurology

Volumn 365, Issue 4, 1996, Pages 526-540

  Henry, Michael A ^a   Johnson, Lonnie R ^a   Nousek Goebl, Nancy ^b,d   Westrum, Lesnick E ^b,c  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

deafferentation; neuropeptides; nociception; orofacial pain; primary afferents

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAT; CONTROLLED STUDY; DEAFFERENTATION; FACE PAIN; IMMUNOREACTIVITY; MOTONEURON; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; RHIZOTOMY; STIMULUS RESPONSE; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CATS; CRANIAL NERVES; FUNCTIONAL LATERALITY; IMMUNOHISTOCHEMISTRY; NERVE FIBERS; REFERENCE VALUES; RHIZOTOMY; TIME FACTORS; TRIGEMINAL CAUDAL NUCLEUS; TRIGEMINAL GANGLION; TRIGEMINAL NERVE; TRIGEMINAL NUCLEI; TRIGEMINAL NUCLEUS, SPINAL;

EID: 0030066452     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960219)365:4<526::AID-CNE2>3.0.CO;2-6     Document Type: Article

References (84)

1. Arvidsson, J., and S. Gabel (1981) An HRP study of the central projections of primary trigeminal neurons which innervate tooth pulps in the cat. Brain Res 210.1-16.
2. Arvidsson, U., H Johnson, F. Piehl, S. Cullheim, T. Hökfelt, M Risling, L. Terenius, and B Ulfhake (1990) Peripheral nerve section induces increased levels of calcitonin gene-related peptide (CGRP)-like immunoreactivity in axotomized motoneurons Exp. Brain Res. 79:212-216.
3. Aström, K.E. (1953) On the central course of afferent fibres in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse. Acta Physiol. Scand 29(Suppl 106):209-320.
4. Batten, T F.C., K. Appenteng, and S. Saha (1988) Visualization of CGRP and CHAT-like immunoreactivity in identified trigeminal neurons by combined peroxidase and alkaline phosphatase enzymatic reactions. Brain Res. 447:314-324.
5. Batten, T.F.C., W.K E. Lo, A. Magbool, and P.N. McWilliam (1989) Distribution of calcitonin gene-related peptide-like immunoreactivity in the medulla oblongata of the cat, in relation to choline acetyltransferase-immunoreactive motoneurones and substance P-immunoreactive fibers. J. Chem. Neuroanat. 2:163-176.
6. Bennett-Clarke, C.A., and N.L. Chiaia (1992) Normal development and effects of neonatal infraorbital nerve damage upon the innervation of the trigeminal brainstem complex by primary afferent fibers containing calcitonin gene-related peptide. J. Comp. Neurol. 324:282-294.
7. Brown, P.B. (1987) Workshop summary: Mechanisms of plasticity. In L.M. Pubols and B.J. Sessle (eds): Effects of Injury on Trigeminal and Spinal Somatosensory Systems. New York: Alan R. Lisa, pp. 461-465
8. Carlton, S M., and E.S. Hayes (1989) Dynorphin A(1-8) immunoreactive cell bodies, dendrites and terminals are postsynaptic to calcitonin gene-related peptide primary afferent terminals in the monkey dorsal horn. Brain Res 504:124-128.
9. Carlton, S.M., D.L. McNeill, K. Chung, and R.E Coggeshall (1987) A light and electron microscopic level analysis of calcitonin gene-related peptide (CGRP) in the spinal cord of the primate: An immunohistochemical study. Neurosci. Lett 82.145-150.
10. Chung, K., W.T. Lee, and S.M. Carlton (1988) The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide-labeled terminals in the rat lumbar dorsal horn. Neurosci. Lett. 90:27-32.
11. Coderre, T.J., J. Katz, A.L. Vaccarino, and R. Melzack (1993) Contribution of central neuroplasticity to pathological pain: Review of clinical and experimental evidence. Pain 52:259-285.
12. Colin, S., and L Kruger (1986) Peptidergic nociceptive axon visualization in whole-mount preparations of cornea and tympanic membrane in rat. Brain Res. 398:199-203.
13. Dallel, R., P. Raboisson, P. Auroy, and A. Woda (1988) The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res. 448:7-19.
14. Drew, J.P., L.E. Westrum, and R.H. Ho (1986) Mapping of the normal distribution of substance P-like immunoreactivity in the spinal trigeminal nucleus of the cat. Exp. Neurol. 93:168-179
15. Fried, K., M. Risling, U. Arvidsson, and S. Paulie (1990) Nerve growth factor receptor-like immunoreactivity in nerve fibers in the spinal and medullary dorsal horn of the adult monkey and cat: Correlation with calcitonin gene-related peptide-like immunoreactivity. Brain Res. 536:321-326.
16. Fromm, G.H , and B.J. Sessle (1991) Introduction and historical review. In G.H Fromm and B.J. Sessle (eds): Trigeminal Neuralgia, Current Concepts Regarding Pathogenesis and Treatment. Boston: Butterworth-Heinemann, pp. 1-26
17. Gibson, S.J., J.M. Polak, S.R. Bloom, I.M. Sabate, P.M Mulderry, M.A. Ghatei, G.P. McGregor, J F B. Morrison, J.S. Kelly, R M. Evans, and M.G. Rosenfeld (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species J. Neurosci. 4.3101-3111.
18. Graham, S H., F.R. Sharp, and W. Dillon (1988) Intraoral sensation in patients with brainstem lesions: role of the rostral spinal trigeminal nuclei in the pons. Neurology 35:1529-1533.
19. Grothe, C (1993) Biphasic increase of calcitonin gene-related peptide-like immunoreactivity in rat hypoglossal motoneurons after nerve transection. Acta Histochem 94:20-24.
20. Gybels, J M., and W.H. Sweet (1989) The trigeminal nerve. In P L. Gildenberg (ed): Pain and Headache, vol. 11: Neurosurgical Treatment of Persistant Pain, Physiological and Pathological Mechanisms of Human Pain. New York: Karger, pp. 10-69
21. Harmon, P A , K. Chung, R.P. Briner, K.N. Westlund, and S.M Carlton (1988) Calcitonin gene-related peptide (CGRP) in the human spinal cord. A light and electron microscopic analysis. J. Comp. Neurol. 269:371-380.
22. Hayashi, H. (1985) Morphology of termination of small and large myelinated trigeminal primary afferent fibers in the cat. J Comp Neurol. 240:71-89.
23. Henry, M.A., R J. Drangsholt, L E. Westrum, and M. Bothwell (1991) Localization of nerve growth factor receptor immunoreactivity in the trigeminal nucleus of kittens. Exp. Neurol. 113:38-46.
24. Henry, M.A., N.A Nousek-Goebl, and L.E. Westrum (1993a) Light and electron microscopic localization of calcitonin gene-related peptide immunoreactivity in lamina II of the feline trigeminal pars caudalis/medullary dorsal horn: A qualitative study. Synapse 13:99-107.
25. Henry, M.A., L.E. Westrum, M Bothwell, and L.R. Johnson (1993b) Nerve growth factor receptor (p75)-immunoreactivity in the normal adult feline trigeminal system and following retrogasserian rhizotomy J. Comp. Neurol. 335:425-436.
26. Henry, M.A., L.E. Westrum, M. Bothwell, and S. Press (1994) Electron microscopic localization of nerve growth factor receptor (p75)-immunoreactivity in pars caudalis/medullary dorsal horn of the cat. Brain Res. 642:137-145.
27. Hirakawa, M., and M. Kawata (1992) Changes of chemoarchitectural organization of the rat spinal cord following ventral and dorsal root transection. J Comp. Neurol. 320:339-352.
28. Hökfelt, T. (1991) Neuropeptides in perspective: The last ten years. Neuron 7:867-879.
29. Houle, J.D , and P.J. Reier (1989) Regrowth of calcitonin gene-related peptide (CGRP) immunoreactive axons from the chronically injured rat spinal cord into fetal spinal cord tissue transplants Neurosci. Lett. 103:253-258.
30. Itoh, Y., and A. Tessler (1990) Ultrastructural organization of regenerated adult dorsal root axons within transplants of fetal spinal cord. J. Comp. Neurol. 292:396-411.
31. Jacquin, M.F., W.E. Renehan, R D. Mooney, and R.W. Rhoades (1986) Structure-function relationships in rat medullary and cervical dorsal horns I. Trigeminal primary afferents. J. Neurophysiol. 55:1153-1186.
32. Jacquin, M.F., M.C. Beinfeld, N.L. Chiaia, and D.S. Zahm (1992) Cholecystokinin concentrations and peptide immunoreactivity in the intact and deafferented medullary dorsal horn of the rat. J Comp. Neurol. 326:22-43.
33. Johnson, L.R., M.A. Henry, L.E. Westrum, and N.A. Nousek-Goebl (1988) Calcitonin gene-related peptide like immunoreactivity in feline trigeminal nuclei. Soc Neurosci. Abstr. 14:1164.
34. Johnson, L.R., M.A. Henry, C D. Kullas, and L.E. Westrum (1990) Effect of retrogasserian rhizotomy on the localization of calcitonin gene-related peptide and Griffonia simplifolia in feline trigeminal nuclei. Soc. Neurosci. Abstr. 16:222.
35. Jones, M.A., and C.F. Marfurt (1991) Calcitonin gene-related peptide and corneal innervation: A developmental study in the rat. J. Comp. Neurol. 313:132-150.
36. Ju, G., T Hökfelt, E. Brodin, J. Fahrenkrug, J.A. Fischer, P. Frey, R.P. Elde, and J.C. Brown (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin, vasoactive intestinal polypeptide-and cholecystokinin-immunoreactive ganglion cells. Cell Tiss. Res. 247: 417-431.
37. Kerr, F.W.L. (1961) Structural relation of the trigeminal spinal tract to upper cervical roots and the solitary nucleus in the cat. Exp Neurol. 4: 134-148.
38. Kerr, F.W.L. (1963) The divisional organization of afferent fibres of the trigeminal nerve. Brain 86:721-732.
39. Kerr. F W.L. (1972) The potential of cervical primary afferents to sprout in the spinal nucleus of V following long term trigeminal denervation Brain Res. 43:547-560.
40. Kerr, F.W.L. (1975) Neuroplasticity of primary afferents in the neo-natal cat and some results of early deafferentation of the trigeminal spinal nucleus. J. Comp. Neurol. 163:305-328.
41. Kerr, F.W.L., and R. Minn (1962) Facial, vagal and glossopharyngeal nerves in the cat. Arch. Neurol. 6:264-281.
42. Kruger, L., P.W. Mantyh, C. Sternini, N.C. Brecha, and C.R. Mantyh (1988a) Calcitonin gene-related peptide (CGRP) in the rat central nervous system: Patterns of immunoreactivity and receptor binding sites. Brain Res. 463:223-244
43. Kruger, L., C Sternini, N.C. Brecha, and P.W. Mantyh (1988b) Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection. J. Comp. Neurol. 273:149-162.
44. Kuwayama, Y , G. Terenghi, J.M Polak, J.Q. Trojanowski, and R.A. Stone (1987) A quantitative correlation of substance P-, calcitonin gene-related peptide- and cholecystokinin-like immunoreactivity with retrogradely labeled trigeminal ganglion cells innervating the eye. Brain Res. 405:220-266.
45. Matthews, M.A., K.D. Hoffman, and J.D. Stover (1992) Ultrastructural characterization of substance-P-immunoreactive synaptic terminals in the cat's normal and rhizotomized trigeminal subnucleus caudalis Somatosens. Mot. Res. 9:131-156.
46. McNeill, D.L., S.M. Carlton, R.E. Coggeshall, and C.E. Hulsebosch (1990) Denervation-induced intraspinal synaptogenesis of calcitonin gene-related peptide containing primary afferent terminals. J. Comp. Neurol. 296:263-268.
47. Micevych, P.E., and L. Kruger (1992) The status of calcitonin gene-related peptide as an effector peptide. Ann. NY Acad. Sci. 657:379-396
48. Mizuno, N., and S. Nomura (1986) Primary afferent fibers in the glossopharyngeal nerve terminate in the dorsal division of the principal sensory trigeminal nucleus: An HRP study in the cat. Neurosci. Lett. 66:338-340.
49. Nomura, S., and N. Mizuno (1981) Central distribution of afferent and efferent components of the chordi tympani in the cat as revealed by the horseradish peroxidase method. Brain Res. 214:229-237
50. Nomura, S., and N. Mizuno (1983a) Central distribution of afferent fibers in the intermediate nerve: A transganglionic HRP study in the cat. Neurosci. Lett. 41:227-231.
51. Nomura, S., and N. Mizuno (1983b) Central distribution of efferent and afferent components of the cervical branches of the vagus nerve. Anat. Embryol. (Berl.) 166;1-16.
52. Nomura, S., and N. Mizuno (1984) Central distribution of primary afferent fibers in the Arnold's nerve (the auricular branch of the vagus nerve): A transganglionic HRP study in the cat. Brain Res 292:199-205.
53. Peterfreund, R.A., and W. W. Vale (1986) Local anesthetics inhibit veratridine-induced secretion of calcitonin gene-related peptide (CGRP) from cultured rat trigeminal ganglion cells. Brain Res. 380:159-161.
54. Piehl, F., U. Arvidsson, H. Johnson, A. Dagerlind, T. Hokfelt, L. Terenius, and B Ulfhake (1992) Reappearance of calcitonin gene-related peptide-like immunoreactivity in the dorsal horn in the long-term dorsal root transected rat. Brain Res. 585:400-404.
55. Priestley, J.V., P. Somogyi, and A.C. Cuello (1982) Immunocytochemical localization of substance P in the spinal trigeminal nucleus of the rat: A light and electron microscopy study. J. Comp. Neurol. 211.31-49.
56. Quartu, M., G. Diaz, A Floris, M.L. Lai, J V. Priestley, and M. Del Fiacco (1992a) Calcitonin gene-related peptide in the human trigeminal sensory system at developmental and adult life stages: Immunohistochemistry, neuronal morphology and coexistence with substance P. J. Chem. Neuroanat 5:143-157.
57. Quartu, M., G. Diaz, M.L. Lai, and M Del Fiacco (1992b) Immunohistochemical localization of putative peptide neurotransmitters in the human trigeminal sensory system. Ann. NY Acad. Sci. 657.469-472
58. Ralston, H J. III, and D.D. Ralston (1979) The distribution of dorsal root axons in laminae I, II and III of the macaque spinal cord: A quantitative electron microscope study. J. Comp. Neurol. 184:643-684.
59. Rosenfeld, M.G , J.J. Mermod, S.G Amara, L W Swanson, P.E. Sawchenko, J. Rivier, W.W. Vale, and R.M. Evans (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature (Lond.) 304:129-135.
60. Sessle, B.J. (1987) The neurobiology of facial and dental pain: Present knowledge, future directions. J. Dent. Res. 66:962-981.
61. Sessle, B J (1991) Physiology of the trigeminal system In G.H. Fromm and B.J. Sessle (eds): Trigeminal Neuralgia, Current Concepts Regarding Pathogenesis and Treatment. Boston: Butterworth-Heinemann, pp. 71-104.
62. Shigenaga, Y., T. Nishimori, E Suemune, Y.C. Chen, I.D Nasution, H. Sato, T. Okamoto, M. Sera, K. Tabuchi, K. Kagawa, and M. Hosoi (1984) Laminar-related projection of primary trigeminal fibers in the caudal medulla demonstrated by transganglionic transport of horseradish peroxidase Brain Res. 309:341-345.
63. Shigenaga, Y., I.C. Chen, S. Suemune, T. Nishimori, I.D. Nasution, A. Yoshida, H. Sato, T. Okamoto, M. Sera, and M. Hosoi (1986a) Oral and facial representation within the medullary and upper cervical dorsal horns in the cat. J Comp. Neurol. 243:388-408.
64. Shigenaga, Y., S. Suemune, M. Nishimura, T Nishimon, H. Sato, H. Ishidori, A. Yoshida, K. Tsuru, Y. Tsuiki, Y. Dateoka, I.D. Nasution, and M Hosoi (1986b) Topographic representation of lower and upper teeth within the trigeminal sensory nuclei of adult cats as demonstrated by the transganglionic transport of horseradish peroxidase. J. Comp. Neurol. 251:299-316.
65. Silverman, J D., and L Kruger (1987) An interpretation of dental innervation based upon the pattern of calcitonin gene-related peptide (CGRP)-immunoreactive thin sensory axons. Somatosens. Res. 5:157-175
66. Silverman, J D., and L. Kruger (1989) Calcitonin-gene-related-peptide-immunoreactivity innervation of the rat head with emphasis on specialized sensory structures. J. Comp. Neurol. 280:303-330.
67. Sjöqvist, O. (1938) Studies on pain conduction in trigeminal nerve; contribution to surgical treatment of facial pain. Acta Psychiatr. Neurol. (Scand.) 17(Suppl.):1-133.
68. Skofitsch, G., and D M. Jacobowitz (1985) Calcitonin gene-related peptide: detailed immunohistochemical distribution in the central nervous system Peptides 6:721-745.
69. Stover, J.D., C.A. Schwab, and M.A. Matthews (1992) Selective deafferentation of convergent inputs to trigeminal subnucleus caudalis: Effects on calcitonin gene-related peptide distribution. Somatosens. Mot. Res. 9:107-130.
70. Streit, W.J., F.L. Dumoulin, G. Raivich, and G.W. Kreutzberg (1989) Calcitonin gene-related peptide increases in rat facial motoneurons after peripheral nerve transaction. Neurosci. Lett. 101:143-148.
71. Taquet, H., J.J. Plachot, M. Pohl, E. Collin, J.J. Benoliel, S. Bourgoin, A. Mauborgne, J.C. Meunier, F. Cesselin, and M. Hamon (1992) Increased calcitonin gene-related peptide- and cholecystokinin-like immunoreactivities in spinal motoneurones after dorsal rhizotomy. J. Neural Transm. 88:127-141.
72. Tashiro, T , O. Takahashi, T. Satoda, R. Matsushima, M. Uemura-Sumi, and N. Mizuno (1991) Distribution of axons showing calcitonin gene-related peptide and/or substance P-like immunoreactivity in the sensory trigeminal nuclei of the cat. Neurosci. Res. 11:119-133.
73. Tessler, A., E. Gazer, R. Artymyshyn, M. Murray, and M.E. Goldberger (1980) Recovery of substance P in the cat spinal cord after unilateral lumbosacral deafferentation. Brain Res. 191.459-470.
74. Tessler, A., B.T. Himes, R. Artymyshyn, M. Murray, and M E. Goldberger (1981) Spinal neurons mediate return of substance P following deafferentation of cat spinal cord. Brain Res. 230:263-281
75. Torvik, A (1956) Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. An experimental study in the rat. J. Comp. Neurol. 106:51-142.
76. Traub, R.J., A. Solodkin, and M.A. Ruda (1989) Calcitonin gene-related peptide immunoreactivity in the cat lumbosacral spinal cord and the effects of multiple dorsal rhizotomies. J. Comp. Neurol. 257:225-237.
77. Traub, R.J., B. Allen, A. Humphrey, and M.A. Ruda (1990) Analysis of calcitomn gene-related peptide-like immunoreactivity in the cat dorsal spinal cord and dorsal root ganglia provides evidence for a multisegmental projection of nociceptive C-fiber primary afferents. J. Comp. Neurol. 302:562-574
78. Unger, J. W., and W. Lange (1991) Immunohistochemical mapping of neurophysins and calcitonin gene-related peptide in the human brain-stem and spinal cord. J. Chem. Neuroanat. 4:299-309.
79. Wang, X.H., P.G lannuzzelli, and E.H. Murphy (1993) Calcitomn gene-related peptide increases following axotomy of trochlear motoneurons. Exp. Neurol. 123:157-166.
80. Westrum, L.E , and M.A. Henry (1991) Contralateral degeneration in the cat spinal trigeminal nucleus following unilateral retrogasserian trigeminal rhizotomy. Neurosci. Lett. 121:143-146
81. Westrum, L.E., and M.A. Henry (1993) Unilateral retrogasserian rhizotomy causes contralateral degeneration in spinal trigeminal nuclei of cats. An ultrastructural study. Exp. Brain Res 93:28-36.
82. Westrum, L.E., R.C. Canfield, and T A. O'Connor (1981) Each canine tooth projects to all brainstem trigeminal nuclei in cat. Exp. Neurol. 74:787-799.
83. Woolf, C. J (1989) Afferent induced alterations of receptive field properties. In F. Cervero, G.J. Bennett, and P.M. Headley (eds): Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord. New York: Plenum Press, pp. 443-162.
84. Young, R F., and K.M. Perryman (1986) Neuronal responses in rostral trigeminal brain-stem nuclei of macaque monkeys after chronic trigemi-nal tractotomy. J Neurosurg. 65:508-516.