Subnuclear localization of FOS-like immunoreactivity in the parabrachial nucleus after orofacial nociceptive stimulation of the awake rat

Journal of Comparative Neurology

Volumn 387, Issue 1, 1997, Pages 114-123

  Hermanson, Ola ^a   Blomqvist, Anders ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Immediate early gene; Kolliker Fuse nucleus; Pain; Somatosensory; Trigeminal dorsal horn

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; HINDLIMB; IMMEDIATE EARLY GENE; LOWER LIP; MALE; NOCICEPTION; NONHUMAN; PAIN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; SENSORY NERVE; SENSORY STIMULATION; SOMATOSENSORY CORTEX; SPINAL CORD DORSAL HORN; TRIGEMINAL NERVE;

AFFERENT PATHWAYS; ANIMALS; CELL NUCLEUS; FACIAL PAIN; HINDLIMB; IMMUNOHISTOCHEMISTRY; MALE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0030986541     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19971013)387:1<114::AID-CNE9>3.0.CO;2-4     Document Type: Article

References (86)

1. Aldén, M., J.-M. Besson, and J.-F. Bernard (1994) Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: A PHA-L study in the rat. J. Comp. Neurol. 341:298-314.
2. Agüero, A., M. Arnedo, M. Gallo, and A. Puerto (1993) The functional relevance of the lateral parabrachial nucleus in lithium chloride-induced aversion learning. Pharmacol. Biochem. Behav. 45:973-978.
3. Bellavance, L.L., and A.J. Beitz (1996) Altered c-fos expression in the parabrachial nucleus in a rodent model of CFA-induced peripheral inflammation. J. Comp. Neurol. 366:431-447.
4. Bernard, J.F., and J.M. Besson (1990) The spino(trigemino)pontoamygdaloid pathway: Electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63:473-490.
5. Bernard, J.F., M. Peschanski, and J.M. Besson (1989) A possible spino(trigemino)-ponto-amygdaloid pathway for pain. Neurosci. Lett. 100: 83-88.
6. Bernard, J.F., G.F. Huang, and J.M. Besson (1990) Effect of noxious somesthetic stimulation on the activity of neurons of the nucleus centralis of the amygdala. Brain Res. 523:347-350.
7. Bernard, J.F., J. Carroué, and J.M. Besson (1991) Efferent projections from the external parabrachial area to the forebrain: A Phaseolus vulgaris leucoagglutinin study in the rat. Neurosci. Lett. 122:257-260.
8. Bernard, J.F., M. Alden, and J.-M. Besson (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: A Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J. Comp. Neurol. 329:201-229.
9. Bernard, J.F., G.F. Huang, and J.M. Besson (1994) The parabrachial area: Electrophysiological evidence for an involvement in visceral nociceptive processes. J. Neurophysiol. 71:1646-1660.
10. Bernard, J.F., R. Dallel, P. Raboisson, L. Villanueva, and D. Le Bars (1995) Organization of the efferent projections from the spinal cervical enlargement to the parabrachial area and periaqueductal gray: A PHA-L study in the rat. J. Comp. Neurol. 353:480-505.
11. Bertrand, F., and A. Hugelin (1971) Respiratory synchronizing function of nucleus parabrachialis medialis: Pneumotaxic mechanisms. J. Neurophysiol. 34:189-207.
12. Blomqvist, A., and K.J. Berkley (1992) Are-examination of the spino-reticulodiencephalic pathway in the cat. Brain Res. 579:17-31.
13. Blomqvist, A., W. Ma, and K.J. Berkley (1989) Spinal input to the parabrachial nucleus in the cat. Brain Res. 480:29-36.
14. Blomqvist, A., O. Hermanson, H. Ericson, and D. Larhammar (1994) Activation of a bulbospinal opioidergic projection by pain stimuli in the awake rat. NeuroReport 5:461-464.
15. Borsook, D., C. Konradi, O. Falkowski, M. Comb, and S.E. Hyman (1994) Molecular mechanisms of stress-induced proenkephalin gene regulation: CREB interacts with the proenkephalin gene in the mouse hypothalamus and is phosphorylated in response to hyperosmolar stress. Mol. Endocrinol. 8:240-248.
16. Burstein, R., R.J. Dado, and G.J. Giesler Jr. (1990) The cells of origin of the spinothalamic tract of the rat: A quantitative reexamination. Brain Res. 511:329-337.
17. Cechetto, D.F., and C.B. Saper (1987) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J. Comp. Neurol. 262:27-45.
18. Cechetto, D.F., D.G. Standaert, and C.B. Saper (1985) Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat. J. Comp. Neurol. 240:153-160.
19. Chamberlin, N.L., and C.B. Saper (1992) Topographic organization of cardiovascular responses to electrical and glutamate microstimulation of the parabrachial nucleus in the rat. J. Comp. Neurol. 326:245-262.
20. Chamberlin, N.L., and C.B. Saper (1994) Topographic organization of respiratory neurons to glutamate microstimulation of the parabrachial nucleus in the rat. J. Neurosci. 14:6500-6510.
21. Chan, R.K.W., and P.E. Sawchenko (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.
22. Clark, F.M., and H.K. Proudfit (1991) The projection of noradrenergic neurons in the A7 catecholamine cell group to the spinal cord in the rat demonstrated by anterograde tracing combined with immunocytochemistry. Brain Res. 547:279-288.
23. Clement, C.I., K.A. Keay, B.K. Owler, and R. Bandler (1996) Common patterns of increased and decreased Fos expression in midbrain and pons evoked by noxious deep somatic and noxious visceral manipulations in the rat. J. Comp. Neurol. 366:495-515.
24. Coimbra, F., and A. Coimbra (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.
25. Craig, A.D. (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J. Comp. Neurol. 361:225-248.
26. Craig, A.D., M.C. Bushnell, E.-T. Zhang, and A. Blomqvist (1994) A thalamic nucleus specific for pain and temperature sensation. Nature 372:770-773.
27. Feil, K., and H. Herbert (1995) Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kölliker-Fuse nuclei. J. Comp. Neurol. 353:506-528.
28. Floyd, N.S., K.A. Keay, and R. Bandler (1996) Acalbindin immunoreactive deep pain recipient thalamic nucleus in the rat. NeuroReport 7:622-626.
29. Fulwiler, C.E., and C.B. Saper (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res. Rev. 7:229-259.
30. Girardot, M.-N., T.J. Brennan, M.E. Martindale, and R.D. Foreman (1987) Effects of stimulating the subcoeruleus-parabrachial region on the non-noxious and noxious responses of T1-T5 spinothalamic tract neurons in the primate. Brain Res. 409:19-30.
31. Grigson, P.S., A.C. Spector, and R. Norgren (1994) Lesions of the pontine parabrachial nuclei eliminate successive negative contrast effects in rats. Behav. Neurosci. 108:714-723.
32. Hayashi, H., and T. Tabata (1989) Physiological properties of sensory trigeminal neurons projecting to mesencephalic parabrachial area in the cat. J. Neurophysiol. 61:1153-1160.
33. Herbert, H., M.M. Moga, and C.B. Saper (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol. 293:540-580.
34. Herbert, H., and B. Bellintani-Guardia (1995) Morphology and dendritic domains of neurons in the lateral parabrachial nucleus of the rat. J. Comp. Neurol. 354:377-394.
35. Hermanson, O., and A. Blomqvist (1995) Enkephalinergic and catecholaminergic neurons constitute separate populations in the rat Kölliker-Fuse/A7 region. Neurosci. Lett. 190:57-60.
36. Hermanson, O., and A. Blomqvist (1996a) Phosphorylated CREB in the parabrachial nucleus: Relation to preproenkephalin mRNA expression. Soc. Neurosci. Abstr. 22:116.
37. Hermanson, O., and A. Blomqvist (1996b) Subnuclear localization of FOS-like immunoreactivity in the rat parabrachial nucleus after nociceptive stimulation. J. Comp. Neurol. 368:45-56.
38. Hermanson, O., M. Hallbeck, D. Larhammar, and A. Blomqvist (1995) Preprocholecystokinin mRNA expressing neurons in the rat parabrachial nucleus. Soc. Neurosci. Abstr. 21:893.
39. 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.
40. Hylden, J.L.K., H. Hayashi, R. Dubner, and G.J. Bennett (1986) Physiology and morphology of the lamina I spinomesencephalic projection. J. Comp. Neurol. 247:505-515.
41. Hyman, S.E., C. Konradi, L. Kobierski, R. Cole, P. Senatus, and D. Green (1994) Pharmacologic regulation of striatal proenkephalin gene expression via transcription factor CREB. Prog. Clin. Biol. Res. 390:155-171.
42. Iwata, K., D.R. Kenshalo Jr., R. Dubner, and R.L. Nahin (1992) Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J. Comp. Neurol. 321:404-420.
43. Jacquin, M.F., K. Semba, M.D. Egger, and R.W. Rhoades (1983) Organization of HRP-labeled trigeminal mandibular primary afferent neurons in the rat. J. Comp. Neurol. 215:397-120.
44. Jones, E.G. (1985) The Thalamus. New York: Plenum Press, 935 pp.
45. Kato, J., S. Wakisaka, M.J. Tabata, Y. Sasaki, and K. Kurisu (1994) Induction of Fos protein in the rat trigeminal nucleus complex during an experimental tooth movement. Arch. Oral Biol. 39:723-726.
46. Klüver, H., and P.C. Bucy (1937) "Psychic blindness" and other symptoms following bilateral temporal lobectomy in Rhesus monkeys. Am. J. Physiol. 119:352-353.
47. Klüver, H., and P.C. Bucy (1939) Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiatry 42:979-1000.
48. Konradi, C., R.L. Cole, D. Green, P. Senatus, J.-C. Leveque, A.E. Pollack, S.J. Grossbard, and S.E. Hyman (1995) Analysis of the proenkephalin second messenger-inducible enhancer in rat striatal cultures. J. Neurochem.. 65:1007-1015.
49. Krukoff, T.L., T.L. Morton, K.H. Harris, and J.H. Jhamandas (1992) Expression of c-fos protein in rat brain elicited by electrical stimulation of the pontine parabrachial nucleus. J. Neurosci. 12:3582-3590.
50. Krukoff, T.L., K.H. Harris, and J.H. Jhamandas (1993) Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris Leucoagglutinin. Brain Res. Bull. 30:163-172.
51. Lantéri-Minet, M., J. Weil-Fugazza, J. de Pommery, and D. Menétrey (1994) Hindbrain structures involved in pain processing as revaled by the expression of c-FOS and other immediate early gene proteins. Neuroscience 58:287-298.
52. Lara, J.P., M.J. Parkes, L. Silva-Carvhalo, P. Izzo, M.S. Dawid-Milner, and K.M. Spyer (1994) Cardiovascular and respiratory effects of stimulation of cell bodies of the parabrachial nuclei in the anaesthetized rat. J. Physiol. (Lond.) 477:321-329.
53. Li, B.-H., and N.B. Rowland (1993) Dexfenfluramine induces Fos-like immunoreactivity in discrete brain regions in rats. Brain Res. Bull. 31:43-48.
54. Light, A.R., M.J. Sedivec, E.J. Casale, and S.L. Jones (1993) Physiological and morphological characteristics of spinal neurons projecting to the parabrachial region of the cat. Somatosens. Mot. Res. 10:309-325.
55. Ma, W., and M. Peschanski (1988) Spinal and trigeminal projections to the parabrachial nucleus in the rat: Electron-microscopic evidence of a spino-ponto-amygdalian somatosensory pathway. Somatosens. Res. 5:247-257.
56. Ma, W., A. Blomqvist, and K.J. Berkley (1989) Spino-diencephalic relays through the parabrachial nucleus in the cat. Brain Res. 480:37-50.
57. 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.
58. Menétrey, D., and A.I. Basbaum (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.
59. 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.
60. Moga, M.M., H. Herbert, K.M. Hurley, Y. Yasui, T.S. Gray, and C.B. Saper (1990) Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat. J. Comp. Neurol. 295:624-661.
61. Murray, E.A., and M. Mishkin (1985) Amygdalectomy impairs crossmodal association in monkeys. Science 228:604-606.
62. Noguchi, K., and M.A. Ruda (1992) Gene regulation in an ascending nociceptive pathway: Inflammation-induced increase in preprotachykinin mRNA in rat lamina I spinal projection neurons. J. Neurosci. 12:2563-2572.
63. Norgren, R., and C.M. Leonard (1973) Ascending central gustatory pathways. J. Comp. Neurol. 150:217-238.
64. Ogawa, H., and T. Hayama (1984) Receptive fields of solitario-parabrachial relay neurons responsive to natural stimulation of the oral cavity in rats. Exp. Brain. Res. 54:359-366.
65. Ogawa, H., T. Hayama, and S. Ito (1982) Convergence of input from tongue and palate to the parabrachial nucleus neurons of rats. Neurosci. Lett. 28:9-14.
66. Ogawa, H., T. Imoto, and T. Hayama (1984) Responsiveness of solitario-parabrachial relay neurons to taste and mechanical stimulation applied to the oral cavity in rats. Exp. Brain. Res. 54:349-358.
67. Panneton, W.M., S.N. Johnson, and N.B. Christensen (1994) Trigeminal projections to the peribrachial region in the muskrat. Neuroscience 58:605-625.
68. Pfaller, K., and J. Arvidsson (1988) Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J. Comp. Neurol. 268:91-108.
69. Reilly, S., P.S. Grigson, and R. Norgren (1993) Parabrachial nucleus lesions and conditioned taste aversion: Evidence supporting an associative deficit. Behav. Neurosci. 107:1005-1017.
70. Sambucetti, L.C., and T. Curran (1986) The Fos protein complex is associated with DNA in isolated nuclei and binds to DNA cellulose. Science 234:1417-1419.
71. Saper, C.B. (1995) The spinoparabrachial pathway: Shedding new light on an old path. J. Comp. Neurol. 353:477-479.
72. Slugg, R.M., and A.R. Light (1994) Spinal cord and trigeminal projections to the pontine parabrachial region in the rat as demonstrated with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 339:49-61.
73. Sonnenberg, J.L., F.J. Rauscher III, J.I. Morgan, and T. Curran (1989) Regulation of proenkephalin by Fos and Jun. Science 246:1622-1625.
74. Strassman, A.M., and B.P. Vos (1993) Somatotopic and laminar organization of Fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J. Comp. Neurol. 331:495-516.
75. Swank, M.W., and I.L. Bernstein (1994) c-FOS induction in response to a conditioned stimulus after single trial taste aversion learning. Brain Res. 636:202-208.
76. Takayama, K., T. Suzuki, and M. Miura (1994) The comparison of effects of various anesthetics on expression of FOS protein in the rat brain. Neurosci. Lett. 176:59-62.
77. Wang, L.G., H.M. Li, and J.S. Li (1994) Formalin induced FOS-like immunoreactive neurons in the trigeminal spinal caudal subnucleus project to contralateral parabrachial nucleus in the rat. Brain Res. 649:62-70.
78. Westlund, K.N., R.M. Bowker, M.G. Ziegler, and J.D. Coulter (1983) Noradrenergic projections to the spinal cord of the rat. Brain Res. 263:15-31.
79. Wiberg, M., and A. Blomqvist (1984) The spinomesencephalic tract in the cat: Its cells of origin and termination pattern as demonstrated by the intraaxonal transport method. Brain Res. 291:1-18.
80. Wiberg, M., J. Westman, and A. Blomqvist (1986) The projection to the mesencephalon from the sensory trigeminal nuclei: An anatomical study in the cat. Brain Res. 399:51-68.
81. Xing, G., L. Zhang, L. Zhang, T. Heynen, T. Yoshikawa, M. Smith, S. Weiss, and S. Detera-Wadleigh (1995) Rat PPAR delta contains a CGG triplet and is prominently expressed in the thalamic nuclei. Biochem. Biophys. Res. Comm. 217:1015-1025.
82. Yamamoto, T., T. Shimura, N. Sakai, and N. Ozaki (1994) Representation of hedonics and quality of taste stimuli in the parabrachial nucleus of the rat. Physiol. Behav. 56:1197-1202.
83. Yasoshima Y., T. Shimura, and T. Yamamoto (1995) Single unit responses of the amygdala after conditioned taste aversion in conscious rats. NeuroReport 6:2424-2428.
84. Young, R.F., V. Tronnier, and P.C. Rinaldi (1992) Chronic stimulation of the Kölliker-Fuse nucleus region for relief of intractable pain in humans. J. Neurosurg. 76:979-985.
85. Zhao, Z.-Q., and A.W. Duggan (1988) Idazoxan blocks the action of noradrenaline but not spinal inhibition from electrical stimulation of the locus coeruleus and nucleus Kolliker-Fuse of the cat. Neuroscience 25:997-1005.
86. Zhuo, H., S.J. Fung, and C.D. Barnes (1993) Opioid action on spinal cord reflexes due to dorsolateral pontine tegmentum stimulation. Neuropharmacology 32:621-631.