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

Journal of Comparative Neurology

Volumn 368, Issue 1, 1996, Pages 45-56

  Hermanson, Ola ^a   Blomqvist, Anders ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

c fos; immediate early gene; immunohistochemistry; Kolliker Fuse nucleus; pain

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; GENE EXPRESSION; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NOCICEPTION; NONHUMAN; ONCOGENE C FOS; PAIN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY;

ANIMALS; BRACHIAL PLEXUS; FORMALDEHYDE; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; NOCICEPTORS; PAIN; PHYSICAL STIMULATION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 0029962379     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960422)368:1<45::AID-CNE4>3.0.CO;2-K     Document Type: Article

References (81)

1. Bandler, R., and A. Depaulis (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In A. Depaulis and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York: Plenum Press, pp. 175-198.
2. Berk, M.L., and J.A. Finkelstein (1981) Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6:1601-1624.
3. Berkley, K.J., and S.L. Scofield (1990) Relays from the spinal cord and solitary nucleus through the parabrachial nucleus to the forebrain in the cat. Brain Res. 529:333-338.
4. Bernard, J.F., and J.M. Besson (1990) The spino(trigemmo)pontoamygdaloid pathway: Electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63:473-490.
5. 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.
6. 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.
7. 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.
8. Blomqvist. A., W. Ma, and K.J. Berkley (1989) Spinal input to the parabrachial nucleus in the cat. Brain Res. 480:29-36.
9. 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.
10. 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.
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. 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.
13. 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.
14. 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.
15. Chiang. C.Y., J.W. Hu, and B.J. Sessle (1994) Parabrachial area and nucleus raphe magnus-induced modulation of nociceptive and nonnociceptive trigeminal subnucleus caudalis neurons activated by cutaneous or deep inputs. J. Neurophysiol. 71:2430-2445.
16. 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.
17. Dallel, R., P. Raboisson, P. Clavelou, M. Saade, and A. Woda (1995) Evidence for a peripheral origin of the tonic nociceptive response to subcutaneous formalin. Pain 62:11-16.
18. Ding, Y.-Q., B.-Z. Qin, J.-S. Li, and N. Mizuno (1994) Induction of c-fos-like protein in the spinoparabrachial tract-neurons locating within the sacral parasympathetic nucleus in the rat. Brain Res. 659:283-286.
19. 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.
20. Finley, J.C.W., J.L. Maderdrut, and P. Petrusz (1981) The immunocytochemical localization of enkephalin in the central nervous system of the rat. J. Comp. Neurol. 198:541-565.
21. Fleischmann, A., and G. Urea (1988) Different endogenous analgesia systems are activated by noxious stimulation of different body regions. Brain Res. 455:49-57.
22. Friauf, E. (1992) Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur. J. Neurosci. 4:798-812.
23. 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.
24. Fulwiler, C.E., and C.B. Saper (1985) Cholecystokinin-immunoreactive innervation of the ventromedial hypothalamus in the rat: Possible substrate for autonomic regulation of feeding. Neurosci. Lett. 53:289-296.
25. 5 spinothalamic tract neurons in the primate. Brain Res. 409:19-30.
26. Haws, C.M., A.M. Williamson, and H.L. Fields (1989) Putative nociceptive modulatory neurons in the dorsolateral pontomesencephalic reticular formation. Brain Res. 483:272-282.
27. Hayashi, H., and T. Tabata (1990) Pulpal and cutaneous inputs to somatosensory neurons in the parabrachial area of the cat. Brain Res. 511:177-179.
28. 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.
29. 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.
30. Herdegen, T., J.D. Leah, T. Walker, B. Basler, R. Bravo, and M. Zimmermann (1991) Noxious stimulation induces molecular genetic events in neurons of the central nervous system: Expression of immediate-early gene encoded proteins. In M.R. Bond, J.E. Charlton, and C.J. Woolf (eds): Proceedings of the Sixth World Congress on Pain. New York: Elsevier, pp. 325-330.
31. 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.
32. Hermanson, O., H. Ericson, D. Larhammar, and A. Blomqvist (1992) Expression of FOS-Uke immunoreactivity and preproenkephalin mRNA in the rat parabrachial nucleus after nociceptive mechanical stimulation of the skin. Soc. Neurosci. Abstr. 18:832.
33. Hermanson, O., M. Hallbeck, D. Larhammar, and A. Blomqvist (1995) Preprocholecystokinin mRNA expressing neurons in the rat parabrachial nucleus. Soc. Neurosci. Abstr. 21:893.
34. Hubbard, J.W., R.A. Buchholz, T.K. Keeton, and M.A. Nathan (1987) Parabrachial lesions increase plasma norepinephrine concentration, plasma renin activity and enhance barorefiex sensitivity in the conscious rat. Brain Res. 421:226-234.
35. 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.
36. Jasmin, L., H. Wang, K. Tarczy-Hornoch, J.D. Levine, and A.I. Basbaum (1994) Differential effects of morphine on noxious stimulus-evoked FOS-like immunoreactivity in subpopulations of spinoparabrachial neurons. J. Neurosci. 14:7252-7260.
37. Johnston, H.M., and B.J. Morris (1994) Induction of c-fos gene expression is not responsible for increased proenkephalin mRNA levels in the hippocampal dentate gyms following NMDA stimulation. Mol. Brain Res. 25:147-150.
38. Kobashi, M., H. Ichikawa, T. Sugimoto, and A. Adachi (1993) Response of neurons in the solitary tract nucleus, area postrema and lateral parabrachial nucleus to gastric load of hypertonic saline. Neurosci. Lett. 158:47-50.
39. 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. 22:3582-3590.
40. Lantéri-Minet, M., J. Weil-Fugazza, J. de Pommery, and D. Menétrey (1994) Hindbrain structures involved in pain processing as revealed by the expression of c-Fos and other immediate early gene proteins. Neurosci-ence 58:287-298.
41. 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. (London) 477:321-329.
42. Lee, J.H., and A.J. Beitz (1993) The distribution of brain-stem and spinal cord nuclei associated with different frequencies of electroacupuncture analgesia. Pain 52:11-28.
43. Li, B.-H., A.C. Spector, and N.E. Rowland (1994) Reversal of dexfenfluramine-induced anorexia and c-FOS/c-JUN expression by lesion in the lateral parabrachial nucleus. Brain Res. 640:255-267.
44. Light, A.R., E. Casale, and M. Sedivec (1987) The physiology and anatomy of spinal laminae I and II neurons antidromically activated by stimulation in the parabrachial region of the midbrain and pons. In F.F. Schmidt, G.-H. Schaible, and C. Vahle-Hinz (eds): Fine Afferent Nerve Fibers and Pain. Weinheim: VCH, pp. 347-356.
45. 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. Motor Res. 10:309-325.
46. Lind, R.W., and L.W. Swanson (1984) Evidence for corticotropin releasing factor and leu-enkephalin in the neural projection from the lateral parabrachial nucleus to the median preoptic nucleus: A retrograde transport, immunohistochemical double labeling study in the rat. Brain Res. 321:217-224.
47. Luckman, S.M., R.E.J. Dyball, and G. Leng (1994) Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J. Neurosci. 14:4825-4830.
48. Luo, P., J. Li. and Z. Rao (1990) A morphological analysis of neurons in the lateral parabrachial nucleus: An intracellular horseradish peroxidase study in the rat. Neurosci. Lett. 112:133-136.
49. Ma, W., A. Blomqvist, and K.J. Berkley (1989) Spino-diencephalic relays through the parabrachial nucleus in the cat. Brain Res. 480:37-50.
50. Macedonia, J.M., and C.S. Evans (1993) Variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology 93:177-197.
51. Mehler, W.R., M.E. Feferman, and W.J.H. Nauta (1960) Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain 83:718-750.
52. Menétrey, D., and J. de Pommery (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur. J. Neurosci. 3:249-259.
53. Molander, C., and G. Grant (1985) Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J. Comp. Neurol. 237:476-484.
54. 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.
55. Mraovitch, S., M. Kumada, and D.J. Reis (1982) Role of the nucleus parabrachialis in cardiovascular regulation in cat. Brain Res. 232:57-75.
56. Murphy. A.Z., M. Ennis, M.T. Shipley, and M.M. Behbehani (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.
57. 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.
58. Norgren, R., and C.M. Leonard (1973) Ascending central gustatory path-ways. J. Comp. Neurol. 150:217-238.
59. Nyberg, G., and A. Blomqvist (1985) The somatotopic organization of forelimb cutaneous nerves in the brachial dorsal horn: An anatomical study in the cat. J. Comp. Neurol. 242:28-39.
60. Ohman, L.E., and A.K. Johnson (1986) Lesions in lateral parabrachial nucleus enhance drinking to angiotensin II and isoproterenol. Am. J. Physiol. 251:R504-R509.
61. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. Sydney: Academic Press.
62. Pierson, M., and A. Snyder-Keller (1994) Development of frequency-selective domains in inferior colliculus of normal and neonatally noise-exposed rats. Brain Res. 636:55-67.
63. Rocha, M.J.A., E. Friauf, and H. Herbert (1994) Effects of cardiovascular and osmotic stimuli on c-fos expression in the parabrachial nucleus of anaesthetized rats. Soc. Neurosci. Abstr. 20:298.
64. Saito, H., K. Sakai, and M. Jouvet (1977) Discharge patterns of the nucleus parabrachialis lateralis neurons of the cat during sleeping and waking. Brain Res. 134:59-72.
65. 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.
66. Saper, C.B. (1995) The spinoparabrachial pathway: Shedding new light on an old path. J. Comp. Neurol. 353:477-479.
67. Saper, C.B., and D. Levisohn (1983) Afferent connections of the median preoptic nucleus in the rat: Anatomical evidence for a cardiovascular integrative mechanism in the anteroventral third ventricular (AV3V) region. Brain Res. 288:21-31.
68. Saper, C.B., and A.D. Loewy (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197:291-317.
69. Slugg, R.M., and A.R. Light (1990) Physiology and morphology of nocireceptive and thermoreceptive parabrachial neurons. Soc. Neurosci. Abstr. 16:1144.
70. Slugg, R.M., and A.R. Light (1991) Efferent projections from the lateral parabrachial nucleus as demonstrated by PHA-L. Soc. Neurosci. Abstr. 17:1204.
71. 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.
72. Smith, J.C., D.E. Morrison, H.H. Ellenberger, M.R. Otto, and J.L. Feldman (1989) Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J. Comp. Neurol. 281:69-96.
73. Sonnenberg, J.L., F.J. Rauscher III, J.I. Morgan, and T. Curran (1989) Regulation of proenkephalin by Fos and Jun. Science 46:1622-1625.
74. 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.
75. Swanson, L.W. (1987) The hypothalamus. In A. Björklund, T. Hökfelt, and L.W. Swanson (eds): Handbook of Chemical Neuroanatomy, Vol. 5: Integrated Systems of the CNS, Part I. Amsterdam: Elsevier, pp. 1-124.
76. 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.
77. Ward, D.G. (1988) Stimulation of the parabrachial nuclei with monosodium glutamate increases arterial pressure. Brain Res. 462:383-390.
78. Watts, A.G. (1991) Ether anesthesia differentially affects the content of prepro-corticotropin-releasing hormone, prepro-neurotensin/neuromedin N and prepro-enkephalin mRNAs in the hypothalamic paraventricular nucleus of the rat. Brain Res. 544:353-357.
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 (1987) Somatosensory projection to the mesencephalon: An anatomical study in the monkey. J. Comp. Neurol. 264:92-117.
81. Zäborszky, L., M.C. Beinfeld, M. Palkovits, and L. Heimer (1984) Brainstem projection to the hypothalamic ventromedial nucleus in the rat: A CCK-containing long ascending pathway. Brain Res. 303:225-231.