Physiological properties of the lamina I spinoparabrachial neurons in the rat

Journal of Neurophysiology

Volumn 83, Issue 4, 2000, Pages 2239-2259

  Bester, Hervé ^a,c   Chapman, Victoria ^a,b   Besson, Jean Marie ^a   Bernard, Jean François ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; LUMBAR SPINAL CORD; MALE; MECHANICAL STIMULATION; MYELINATED NERVE; NERVE CONDUCTION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; SINGLE UNIT ACTIVITY; SPINAL CORD DORSAL HORN; THERMAL STIMULATION; TRANSCUTANEOUS NERVE STIMULATION;

EID: 0034076537     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.4.2239     Document Type: Article

References (137)

1. ABBADIE, C., HONORÉ, P., FOURNIE-ZALUSKI, M. C., ROQUES, B. P., AND BESSON, J. M. Effects of opioids and non-opioids on c-Fos-like immunoreactivity induced in rat lumbar spinal cord neurons by noxious heat stimulation. Eur. J. Pharmacol. 258: 215-227, 1994.
2. ALDÉN, M., BESSON, J. M., AND BERNARD, J. F. 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: 289-314, 1994.
3. BELLAVANCE, L. L. AND BEITZ, A. J. Altered c-fos expression in the parabrachial nucleus in a rodent model of CFA-induced peripheral inflammation. J. Comp. Neurol. 366: 431-447, 1996.
4. BENOIST, J. M., KAYSER, V., GAUTRON, M., AND GUILBAUD, G. Acute inflammation and hyperalgesia: their consequences on the responses of various neurons of the ventrobasal thalamic complex in rats. CR Acad. Sci. Ser. III Sci. Vie 299: 401-404, 1984.
5. BERNARD, J. F., ALDÉN, M., AND BESSON, J. M. 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, 1993.
6. BERNARD, J. F. AND BESSON, J. M. Convergence d'informations nociceptives sur des neurones parabachio-amygdaliens chez le rat. CR Acad Sci. Ser. III Sci. Vie 307: 841-847, 1988.
7. BERNARD, J. F. AND BESSON, J. M. The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63: 473-490, 1990.
8. BERNARD, J. F., BESTER, H., AND BESSON, J. M. Involvement of the spino-parabrachio-amygdaloid and -hypothalamic pathways in the autonomic and affective emotional aspects of pain. Prog. Brain Res. 107: 243-255, 1996.
9. BERNARD, J. F., DALLEL, R., RABOISSON, P., VILLANUEVA, L., AND LE BARS, D. 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, 1995.
10. BERNARD, J. F., HUANG, G. F., AND BESSON, J. M. The parabrachial area: electrophysiological evidence for an involvement in visceral nociceptive processes. J. Neurophysiol. 71: 1646-1660, 1994.
11. BERNARD, J. F., PESCHANSKI, M., AND BESSON, J. M. A possible spino(trigemino)-ponto-amygdaloid pathway for pain. Neurosci. Lett. 100: 83-88, 1989.
12. BESSON, J. M. AND CHAOUCH, A. Peripheral and spinal mechanisms of nociception. Physiol. Rev. 67: 67-186, 1987.
13. BESTER, H., BESSON, J. M., AND BERNARD, J. F. Organization of efferent projections from the parabrachial area to the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 383: 245-281, 1997a.
14. BESTER, H., CHAPMAN, V., BERNARD J. F., ONTENIENTE B., AND BESSON J. M. Electrophysiological characterisation of superficial laminae nociceptive neurones projecting to the parabrachial area in the rat. Soc. Neurosci. Abstr. 21: 643, 1995a.
15. BESTER, H., MATSUMOTO, N., BESSON, J. M., AND BERNARD, J. F. Further evidence for the involvement of the spinoparabrachial pathway in nociceptive processes: a c-Fos study in the rat. J. Comp. Neurol. 383: 439-458, 1997b.
16. BESTER, H., MENENDEZ, L., BESSON, J. M., AND BERNARD, J. F. Spino(trigemino)-parabrachiohypothalamic pathway. Electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 73: 568-585, 1995b.
17. BLOMQVIST, A., MA, W., AND BERKLEY, K. J. Spinal input to the parabrachial nucleus in the cat. Brain Res. 480: 29-36, 1989.
18. BROWN, P. B., AND CULBERSON, J. L. Somatotopic organization of hindlimb cutaneous dorsal root projections to cat dorsal horn. J. Neurophysiol. 45: 137-143, 1981.
19. BULLIT, E. Expression of c-fos protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. Neurol. 296: 517-530, 1990.
20. BURITOVA, J., BESSON, J. M., AND BERNARD, J. F. Involvement of the spino-parabrachial pathway in inflammatory nociceptive processes: a c-Fos protein study in the awake rat. J. Comp. Neurol. 397: 10-28, 1998.
21. BURTON, H., CRAIG, A. D., JR., POULOS, D. A., AND MOLT, J. T. Efferent projections from temperature sensitive recording loci within the marginal zone of the nucleus caudalis of the spinal trigeminal complex in the cat. J. Comp. Neurol. 183: 753-778, 1979.
22. BUSHNELL, M. C., DUNCAN, G. H., DUBNER, R., AND HE, L. F. Activity of trigeminothalamic neurons in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. J. Neurophysiol. 52: 170-187, 1984.
23. CECHETTO, D. F., STANDAERT, D. G., AND SAPER C. B. Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat. J. Comp. Neurol. 240: 153-160, 1985.
24. CERVERO, F. AND CONNELL, L. A. Distribution of somatic and visceral primary afferent fibres within the thoracic spinal cord of the cat. J. Comp. Neurol. 230: 88-98, 1984.
25. CERVERO, F., HANDWERKER, H. O., AND LAIRD, J.M.A. Prolonged noxious mechanical stimulation of the rat's tail: responses and encoding properties of dorsal horn neurones. J. Physiol. (Lond.) 404: 419-436, 1988.
26. CHEUNG, S. S. AND MEKJAVIC, I. B. Human temperature regulation during subanesthetic levels of nitrous oxide-induced narcosis. J. Appl. Physiol. 78: 2301-2308, 1995.
27. CHRISTENSEN, B. N. AND PERL, E. R. Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J. Neurophysiol. 33: 293-307, 1970.
28. CHUNG, J. M., KENSHALO, D.R.J., GERHART, K. D., AND WILLIS, W. D. Excitation of primate spinothalamic neurons by cutaneous C-fiber volleys. J. Neurophysiol 42: 1354-1369, 1979.
29. CLEMENT, C. I., KEAY, K. A., OWLER, B. K., AND BANDLER, R. 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, 1996.
30. CRAIG, A. D. Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J. Comp. Neurol. 361: 225-248, 1995.
31. CRAIG, A. D. AND HUNSLEY, S. J. Morphine enhances the activity of thermoreceptive cold-specific lamina-i spinothalamic neurons in the cat. Brain Res. 558: 93-97, 1991.
32. CRAIG, A. D. AND KNIFFKI, K. D. Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. J. Physiol. (Lond.) 365: 197-221, 1985.
33. CRAIG, A. D. AND SERRANO, L. P. Effects of systemic morphine on lamina I spinothalamic tract neurons in the cat. Brain Res. 636: 233-244, 1994.
34. CRAIG, A. D., ZHANG, E. T., AND BLOMQVIST, A. A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey. J. Comp. Neurol. 404: 221-234, 1999.
35. CULBERSON, J. L. AND BROWN, P. B. Projections of hindlimb dorsal roots to lumbosacral spinal cord of cat. J. Neurophysiol. 51: 516-528, 1984.
36. DICKENSON, A. H., LE BARS, D., AND BESSON, J. M. Diffuse inhibitory controls (DNIC). Effects on trigeminal nucleus caudalis neurones in the rat. Brain Res. 200: 293-305, 1980.
37. DOSTROVSKY, J. O. AND CRAIG, A. D. Cooling-specific spinothalamic neurons in the monkey. J. Neurophysiol. 76: 3656-3665, 1996.
38. DOSTROVSKY, J. O. AND HELLON, R. F. The representation of facial temperature in the caudal trigeminal nucleus of the cat. J. Physiol. (Lond.) 277: 29-47, 1978.
39. DUBNER, R., KENSHALO, D.R.J., MAIXNER, W., BUSHNELL, M. C., AND OLIVERAS, J. L. The correlation of monkey medullary dorsal horn neuronal activity and the perceived intensity of noxious heat stimuli. J. Neurophysiol. 62: 450-457, 1989.
40. FEIL, K. AND HERBERT, H. Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kolliker-Fuse nuclei. J. Comp. Neurol. 353: 506-528, 1995.
41. FERRINGTON, D. G., SORKIN, L. S., AND WILLIS, W. D. J. Responses of spinothalamic tract cells in the superficial dorsal horn of the primate lumbar spinal cord. J. Physiol. (Lond.) 388: 681-703, 1987.
42. FITZGERALD, M. The course and termination of primary afferent fibres. In: Textbook of Pain, edited by R. Melzack and P. D. Wall. New York: Chuchill Livingston, 1984, p. 34-48.
43. FITZGERALD, M. AND WALL, P. D. The laminar organization of dorsal horn cells responding to peripheral C fibre stimulation. Exp. Brain Res. 41: 36-44, 1980.
44. FLEISCHER, E., HANDWERKER, H. O., AND JOUKHADAR, S. Unmyelinated nociceptive units in 2 skin areas of the rat. Brain Res. 267: 81-92, 1983.
45. GALINDO, A., KRNJEVIC, K., AND SCHWARTZ, S. Patterns of firing in cuneate neurones and some effects of Flaxedil. Exp. Brain Res. 5: 87-101, 1968.
46. GILLMAN, M. A. Analgesic (sub. anesthetic) nitrous oxide interacts with theendogenous opioid system: a review of the evidence. Life Sci. 39: 1209-1221, 1986.
47. GOBEL, S., FALLS, W. M., AND HUMPHREY, E. Morphology and synaptic connections of ultrafine primary axons in lamina I of the spinal dorsal horn: candidates for the terminal axonal arbors of primary neurons with unmyelinated (C) axons. J. Neurosci. 1: 1163-1179, 1981.
48. GOTO, T., MAROTA, J. J., AND CROSBY, G. Nitrous oxide induces preemptive analgesia in the rat that is antagonized by halothane. Anesthesiology 80: 409-416, 1994.
49. GOTO, T., MAROTA, J. J., AND CROSBY, G. Volatile anaesthetics antagonize nitrous oxide and morphine-induced analgesia in the rat. Br. J. Anaesth. 76: 702-706, 1996.
50. GUILBAUD, G., BENOIST, J. M., LEVANTE, A., GAUTRON, M., AND WILLER, J. C. Primary somatosensory cortex in rats with pain-related behaviours due to a peripheral mononeuropathy after moderate ligation of one sciatic nerve: neuronal responsivity to somatic stimulation. Exp. Brain Res. 92: 227-45, 1992.
51. HALPERN, L. M. AND BLACK, R. G. Flaxedil (Gallamine triethiodide). Evidence for a central action. Science 115: 1685-1687, 1967.
52. HAMBA, M., MURO, M., HIRAIDE, T., AND OZAWA, H. Expression of c-fos-like protein in the rat brain after injection of interleukin-1-beta into the gingiva. Brain Res. Bull. 34: 61-68, 1994.
53. HAN, Z. S., ZHANG, E. T., AND CRAIG, A. D. Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat. Neurosci. 1: 218-225, 1998.
54. HANDWERKER, H. O., KILO, S., AND REEH, P. W. Unresponsive afferent nerve fibres in the sural nerve of the rat. J. Physiol. (Lond.) 435: 229-242, 1991.
55. HAYASHI, H. AND TABATA, T. Physiological-properties of sensory trigeminal neurons projecting to mesencephalic parabrachial area in the cat. J. Neurophysiol. 61: 1153-1160, 1989.
56. HAYASHI, H. AND TABATA, T. Pulpal and cutaneous inputs to somatosensory neurons in the parabrachial area of the cat. Brain Res. 511: 177-179, 1990.
57. HAYES, R. L., DUBNER, R., AND HOFFMAN, D. S. Neuronal activity in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. II. Behavioral modulation of responses to thermal and mechanical stimuli. J. Neurophysiol. 46: 428-443, 1981.
58. HERMANSON, O. AND BLOMQVIST, A. Subnuclear localization of FOS-like immunoreactivity in the rat parabrachial nucleus after nociceptive stimulation. J. Comp. Neurol. 368: 45-56, 1996.
59. HOFFMAN, D. S., DUBNER, R., HAYES, R. L., AND MEDLIN, T. P. Neuronal activity in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. I. Responses to innocuous and noxious thermal stimuli. J. Neurophysiol. 46: 409-427, 1981.
60. HUANG, G. F., BESSON, J. M., AND BERNARD, J. F. Morphine depresses the transmission of noxious messages in the spino(trigemino)-ponto-amygdaloid pathway. Eur. J. Pharmacol. 230: 279-284, 1993.
61. HUNT, S. P., PINI, A., AND EVAN, G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328: 632-634, 1987.
62. HYLDEN, J. L., ANTON, F., AND NAHIN, R. L. Spinal lamina I projection neurons in the rat: collateral innervation of parabrachial area and thalamus. Neuroscience 28: 27-37, 1989.
63. HYLDEN, J. L., HAYASHI, H., BENNETT, G. J., AND DUBNER, R. Spinal lamina I neurons projecting to the parabrachial area of the cat midbrain. Brain Res. 336: 195-198, 1985.
64. HYLDEN, J. L., HAYASHI, H., DUBNER, R., AND BENNETT, G. J. Lamina I. spino-mesencephalic neurons in the cat ascend via the dorsolateral funiculi. Somatosens. Res. 4: 31-41, 1986a.
65. HYLDEN, J.L.K., HAYASHI, H. DUBNER, R., AND BENNETT, G. J. Physiology and morphology of the lamina I spinomesencephalic projection. J. Comp. Neurol. 247: 505-515, 1986b.
66. JONG, R., ROBLES, R., AND MORIKAWA, K. I. Gallamine (Flaxedil) and synaptic transmission in the spinal cord. Science 160: 768-769, 1968.
67. KAJANDER, K. C., ALLEN, B. J., ALLARD, B. L., COURTEIX, C., AND SIMONE, D. A. Responses of rat C-fiber nociceptors to noxious cold. Soc. Neurosci. Abstr. 20: 1571, 1994.
68. KENSHALO, D.R.J., LEONARD, R. B., CHUNG, J. M., AND WILLIS, W. D. Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J. Neurophysiol. 42: 1370-1389, 1979.
69. KITAHATA, L. M., GHAZI-SAIDI, K., YAMASHITA, M., KOSAKA, Y., BONIKOS, C., AND TAUB, A. The depressant effect of halothane and sodium thiopental on the spontaneous and evoked activity of dorsal horn cells: lamina specificity, time course and dose dependence. Pharmacol. Exp. Ther. 195: 515-21, 1975.
70. KITAMURA, T., YAMADA, J., SATO, H., AND YAMASHITA, K. Cells of origin of the spinoparabrachial fibers in the rat: a study with fast blue and WGA-HRP. J. Comp. Neurol 328: 449-461, 1993.
71. KRESS, M., KOLTZENBURG, M., REEH, P. W., AND HANDWERKER, H. O. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J. Neurophysiol. 68: 581-595, 1992.
72. KUMAZAWA, T. AND PERL, E. R. Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J. Comp. Neurol. 177: 417-434, 1978.
73. KUMAZAWA, T., PERL, E. R., BURGESS, P. R., AND WHITHORN, D. Ascending projections from marginal zone (lamina I) neurones of the spinal dorsal horn. J. Comp. Neurol. 162: 1-12, 1975.
74. LANTÉRI-MINET, M., ISNARDON, P., DE POMMERY, J., AND MENÉTREY, D. Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 55: 737-753, 1993.
75. LANTÉRI-MINET, M., WEIL-FUGAZZA, J., DE POMMERY, J., AND MENÉTREY, D. Hindbrain structures involved in pain processing as revealed by the expression of c-Fos and other immediate early gene proteins. Neuroscience 58: 287-298, 1994.
76. LE BARS, D. AND CHITOUR, D. Do convergent neurones in the spinal dorsal horn discriminate nociceptive from non-nociceptive information? Pain 17: 1-19, 1983.
77. LE BARS, D., CHITOUR, D., KRAUS, E., CLOT, A. M., DICKENSON, A. H., AND BESSON, J. M. The effect of systemic morphine upon diffuse noxious inhibitory controls (DNIC) in the rat: evidence for a lifting of certain descending inhibitory controls of dorsal horn convergent neurones. Brain Res. 215: 257-274, 1981.
78. LE BARS, D., DICKENSON, A. H., AND BESSON, J. M. Diffuse inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6: 283-304, 1979a.
79. LE BARS, D., DICKENSON, A. H., AND BESSON, J. M. Diffuse inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6: 305-327, 1979b.
80. LE BARS, D., GUILBAUD, G., CHITOUR, D., AND BESSON, J. M. Does systemic morphine increase descending inhibitory controls of dorsal horn neurones involved in nociception? Brain Res. 202: 223-228, 1980.
81. LEEM, J. W., WILLIS, W. D., AND CHUNG, J. M. Cutaneous sensory receptors in the rat foot. J. Neurophysiol. 69: 1684-1699, 1993a.
82. LEEM, J. W., WILLIS, W. D., WELLER, S. C., AND CHUNG, J. M. Differential activation and classification of cutaneous afferents in the rat. J. Neurophysiol. 70: 2411-2424, 1993b.
83. LIGHT, A. R., CASALE, E., AND SEDIVEC, M. 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: Fine Afferent Nerve Fibers and Pain, edited by R. F. Schmidt, H. G. Schaible, and C. Vahle-Hinz. Weinheim, Germany: VCH, 1987, p. 347-356.
84. LIGHT, A. R. AND PERL, E. R. Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J. Comp. Neurol. 186: 117-131, 1979.
85. LIGHT, A. R., SEDIVEC, M. J., CASALE, E. J., AND JONES, S. L. Physiological and morphological characteristics of spinal neurons projecting to the parabrachial region of the cat. Somatosens. Mot. Res. 10: 309-325, 1993.
86. LIMA, D. AND COIMBRA. A. Morphological types of spinomesencephalic neurons in the marginal zone (lamina I) of the rat spinal cord, as shown after retrograde labelling with cholera toxin subunit B [published erratum appears in J. Comp. Neurol. 286: 542, 1989]. J. Comp. Neurol. 279: 327-339, 1989.
87. LIPSKI, J. Antidromic activation of neurons as an analytic tool in the study of the central nervous-system. J. Neurosci. Methods 4: 1-32, 1981.
88. LONG, R. R. Sensitivity of cutaneous cold fibers to noxious heat: paradoxical cold discharge. J. Neurophysiol. 40: 489-502, 1977.
89. LYNN, B. AND CARPENTER, S. E. Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238: 29-43, 1982.
90. MAIXNER, W., DUBNER, R., BUSHNELL, M. C., KENSHALO, D.R.J., AND OLIVERAS, J. L. Wide-dynamic-range dorsal horn neurons participate in the encoding process by which monkeys perceive the intensity of noxious heat stimuli. Brain Res. 374: 385-388, 1986.
91. MAIXNER, W., DUBNER, R., KENSHALO, D.R.J., BUSHNELL, M. C., AND OLIVERAS, J. L. Responses of monkey medullary dorsal horn neurons during the detection of noxious heat stimuli. J. Neurophysiol. 62: 437-449, 1989.
92. MATSUMOTO, N., BESTER, H., MENENDEZ, L., BESSON, J. M., AND BERNARD, J. F. Changes in the responsiveness of parabrachial neurons in the arthritic rat: an electrophysiological study. J. Neurophysiol. 76: 4113-4126, 1996.
93. MCHAFFIE, J. G., LARSON, M. A., AND STEIN, B. E. Response properties of nociceptive and low-threshold neurons in rat trigeminal pars caudalis. J. Comp. Neurol. 347: 409-425, 1994.
94. MCMAHON, S. B. AND WALL, P. D. A system of rat spinal cord lamina I cells projecting through the contralateral dorsolateral funiculus. J. Comp. Neurol. 214: 217-223, 1983.
95. MCMAHON, S. B. AND WALL, P. D. Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res. 333: 19-26, 1985.
96. MEHLER, W. R., MARTIN, E. F. AND NAUTA, W.J.H. Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain. 83: 718-751, 1960.
97. MENENDEZ, L., BESTER, H., BESSON, J. M., AND BERNARD, J. F. Parabrachial area: electrophysiological evidence for an involvement in cold nociception. J. Neurophysiol. 75: 2099-2116, 1996.
98. MENÉTREY, D., CHAOUCH, A., AND BESSON, J. M. Responses of spinal cord dorsal horn neurones to non-noxious and noxious cutaneous temperature changes in the spinal rat. Pain 6: 265-282, 1979.
99. MENETREY, D. AND DE POMMERY, J. Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur. J. Neurosci. 3: 249-259. 1991.
100. MENETREY, D., CHAOUCH, A., BINDER, D., AND BESSON, J. M. The origin of the spinomesencephalic tract in the rat - an anatomical study using the retrograde transport of horseradish-peroxidase. J. Comp. Neurol. 206: 193-207, 1982.
101. MENETREY, D., DE POMMERY J., THOMASSET, M., AND BAIMBRIDGE, K. G. Calbindin-D28k (Cabp28k)-like immunoreactivity in ascending projections.2. spinal projections to brain-stem and mesencephalic areas. Eur. J. Neurosci. 4: 70-76, 1992.
102. MENETREY, D., GIESLER G. J., AND BESSON J. M. An analysis of response properties of spinal cord dorsal horn neurones to non-noxious and noxious stimuli in the spinal rat. Exp. Brain Res. 27: 15-33, 1977.
103. MENG, I. D., HU, J. W., BENETTI, A. P., AND BEREITER, D. A. Encoding of corneal input in two distinct regions of the spinal trigeminal nucleus in the rat: cutaneous receptive field properties, responses to thermal and chemical stimulation, modulation by diffuse noxious inhibitory controls, and projections to the parabrachial area. J. Neurophysiol. 77: 43-56, 1997.
104. MIZUMURA, K., SUGIURA, Y., AND KUMAZAWA, T. Spinal termination patterns of canine identified A-delta and C spermatic polymodal receptors traced by intracellular labeling with Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 335: 460-468, 1993.
105. MORGAN, M. M., GOGAS, K. R., AND BASBAUM, A. I. 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, 1994.
106. O'CONNOR, T. C. AND ABRAM, S. E. Inhibition of nociception-induced spinal sensitization by anesthetic agents. Anesthesiology 82: 259-266, 1995.
107. PANNETON, W. M. AND BURTON, H. Projections from the paratrigeminal nucleus and the medullary and spinal dorsal horns to the peribrachial area in the cat. Neuroscience 15: 779-797, 1985.
108. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates. Sydney, Australia: Academic, 1986.
109. PERTOVAARA, A., BRAVO, R., AND HERDEGEN, T. Induction and suppression of immediate-early genes in the rat brain by a selective alpha-2-adrenoceptor agonist and antagonist following noxious peripheral stimulation. Neuroscience 54: 117-126, 1993.
110. PRICE, D. D., DUBNER, R., AND HU, J. W. Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J. Neurophysiol. 39: 936-953, 1976.
111. PRICE, D. D., HAYES, R. L., RUDA, M., AND DUBNER, R. Spatial and temporal transformations of input to spinothalamic tract neurons and their relation to somatic sensations. J. Neurophysiol. 41: 933-947, 1978.
112. RANCK, J.B.J. Which elements are evoked in electrical stimulation of mammalian central nervous system: a review. Brain Res. 98: 417-440, 1975.
113. SANDERS, K. H. AND ZIMMERMANN, M. Mechanoreceptors in rat glabrous skin: redevelopment of function after nerve crush. J. Neurophysiol. 55: 644-659, 1986.
114. SAPER C. B. The spinoparabrachial pathway: shedding new light on an old path. J. Comp. Neurol. 353: 477-479, 1995.
115. SLUGG, R. M. AND LIGHT, A. R. Physiology and morphology of nociceptive and thermoreceptive parabrachial neurons. Soc. Neurosci. Abstr. 16: 1144, 1990.
116. SLUGG, R. M. AND LIGHT, A. R. 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, 1994.
117. SMITH, K. J. AND SCHAUF, C. L. Effects of gallamine triethiodide on membrane currents inamphibian and mammalian peripheral nerve. J. Pharmacol. Exp. Ther. 217: 719-726, 1981.
118. SONNER, J., LI, J., AND EGER, E. I., II Desflurane and nitrous oxide, but not nonimmobilizers, affect nociceptive responses. Anesth. Analg. 86: 629-634, 1998.
119. SUGIURA, Y., HOSOYA, Y., ITO, R., AND KOHNO, K. Ultrastructural features of functionally identified primary afferent neurons with C (unmyelinated) fibers of the guinea-pig - classification of dorsal-root ganglion-cell type with reference to sensory modality. J. Comp. Neurol. 276: 265-278, 1988.
120. SUGIURA, Y., LEE, C., AND PERL, E. Central projections of identified, unmyelinated (C) afferent-fibers innervating mammalian skin. Science 234: 358-361, 1986.
121. SUGIURA, Y., TERUI, N., AND HOSOYA, Y. Difference in distribution of central terminals between visceral and somatic unmyelinated (C) primary afferent-fibers. J. Neurophysiol. 62: 834-840, 1989.
122. SUGIURA, Y., TERUI, N., HOSOYA, Y., TONOSAKI, Y., NISHIYAMA, K., AND HONDA, T. Quantitative-analysis of central terminal projections of visceral and somatic unmyelinated (C) primary afferent-fibers in the guinea-pig. J. Comp. Neurol. 332: 315-325, 1993.
123. SWETT, J. E. AND WOOLF, C. J. The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J. Comp. Neurol. 231: 66-77, 1985.
124. SWETT, J. E., MCMAHON, S. B., AND WALL, P. D. Long ascending projections to the midbrain from cells of lamina I and nucleus of the dorsolateral funiculus of the rat spinal cord. J. Comp. Neurol. 238: 401-416, 1985.
125. VILLANUEVA, L., CADDEN, S. W., AND LE BARS, D. Diffuse noxious inhibitory controls (DNIC) - evidence for post-synaptic inhibition of trigeminal nucleus caudalis convergent neurons. Brain Res. 321: 165-168, 1984.
126. VILLANUEVA, L. AND LE BARS, D. Indirect effects of intrathecal morphine upon diffuse noxious inhibitory controls (DNICs) in the rat. Pain 26: 233-243, 1986.
127. WALL, P. D. The laminar organization of dorsal horn and effects of descending impulses. J. Physiol. (Lond.) 188: 403-23, 1967.
128. WIBERG, M. AND BLOMQVIST, A. 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, 1984.
129. WIBERG, M., WESTMAN, J., AND BLOMQVIST, A. Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J. Comp. Neurol. 264:92-117, 1987.
130. WILLER, J. C., BERGERET, S., GAUDY, J. H., AND DAUTHIER, C. Failure of naloxone to reverse the nitrous oxide-induced depression of a brain stem reflex: an electrophysiologic and double-blind study in humans. Anesthesiology 63: 467-472, 1985.
131. WOOLF, C. J. AND FITZGERALD, M. The properties of neurones recorded in the superficial dorsal horn of the rat spinal cord. J. Comp. Neurol. 221: 313-328, 1983.
132. WOOLF, C. J. AND FITZGERALD, M. Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord. J. Comp. Neurol. 251: 517-531, 1986.
133. WOOLF, C. J., SHORTLAND, P., AND SIVILOTTI, L. G. Sensitization of high mechanothreshold superficial dorsal horn and flexor motor neurones following chemosensitive primary afferent activation. Pain 58: 141-155, 1994.
134. YAMADA, J. AND KITAMURA, T. Spinal cord cells innervating the bilateral parabrachial nuclei in the rat. A retrograde fluorescent double-labeling study. Neurosci. Res. 15: 273-280, 1992.
135. ZHANG, E. T. AND CRAIG, A. D. Morphology and distribution of spinothalamic lamina I neurons in the monkey. J. Neurosci. 17: 3274-3284, 1997.
136. ZHANG, E. T., HAN Z. S., AND CRAIG, A. D. Morphological class of spinothalamic lamina I neurons in the cat. J. Comp. Neurol. 367: 537-549, 1996.
137. ZIMMERMANN, M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110, 1983.