Common patterns of increased and decreased fos expression in midbrain and pons evoked by noxious deep somatic and noxious visceral manipulations in the rat

Journal of Comparative Neurology

Volumn 366, Issue 3, 1996, Pages 495-515

  Clement, Colin I ^a   Keay, Kevin A ^a   Owler, Brian K ^a   Bandler, Richard ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

arterial pressure; c fos proto oncogene; pain; periaqueductal gray; tectum

Indexed keywords

ACETIC ACID; CARRAGEENAN; FORMALDEHYDE; HALOTHANE; KAOLIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL PRESSURE; ARTICLE; CELL COUNT; CONTROLLED STUDY; GENE EXPRESSION; HEART RATE; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; INHALATIONAL DRUG ADMINISTRATION; MALE; MESENCEPHALON; NOCICEPTIVE STIMULATION; NONHUMAN; ONCOGENE C FOS; PERIAQUEDUCTAL GRAY MATTER; PONS; PRIORITY JOURNAL; RAT; SUPERIOR COLLICULUS;

EID: 0030025475     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19960311)366:3<495::aid-cne9>3.0.co;2-%23     Document Type: Article

References (125)

1. Abrahams, V.C. (1989) The distribution of muscle and cutaneous projections to the dorsal horn of the upper cervical spinal cord of the cat In Cervero, F., G.J. Bennett, and P.M. Headly (eds). Processing of Sensory Information in the Superficial Dorsal Horn. New York: Plenum, pp. 41-56
2. Abrahams, V.C., G. Anstee, F.J.R. Richmond, and P.K. Rose (1979) Neck muscle and trigeminal input to the upper cervical cord and lower medulla in the cat. Can. J. Physiol. Pharmacol. 57:842-851.
3. Abrahams, V.C., F.J. Richmond, and J. Keane (1984) Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: a study using transganghonic transport of horseradish peroxidase J. Comp. Neurol. 230:142-154.
4. Aitkin, L.M., H. Dickhaus, W. Schult, and M. Zimmermann (1978) External nucleus of inferior colliculus, auditory and spinal somatosensory afferents and their interactions J. Comp Neurol. 41:837-847.
5. Aitkin, L M., C.E. Kenyon, and P. Philpott (1981) The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J. Comp. Neurol. 196:25-40.
6. Anton, F . T Herdegen, P Peppel and J D. Leah (1991) C-fos-like immunoreactivity in rat brainstem neurons following noxious chemical stimulation of the nasal mucosa Neurosci. 41:629-641.
7. Antonetty, C.M , and Z. Webster (1975) The organization of the spinotectal projection. An experimental study in the rat J. Comp Neurol. 163:449-466
8. Auroy, P , B. Irthum, and A. Woda (1991) Oral nociceptive activity in the rat superior colliculus. Brain Res. 549:270-284.
9. Bandler, R., P. Carrive, and S. Zhang (1991) Integration of somatic and autonomic reactions within the midbrain penaqueductal gray: Viscerotopic, somatotopic and functional organization. Prog. Brain Res. 87:269-305
10. Bandler, R., and A. Depaulis (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In Depaulis, A., and R Bandler (eds) The Midbrain Periaqueductal Gray Matter New York: Plenum, pp 175-198
11. Bandler, R., and M. Shipley (1994) Columnar organization in midbrain penaqueductal gray: modules for emotional expression? Trends Neurosci 17:379-389.
12. Benus, R F , B. Bohus, J.M. Koolhaas. and G. A. van-Oortmerssen (1991) Heritable variation for aggression as a reflection of individual coping strategies. Experientia 47:1008-1019.
13. Berberich, P., U. Hoheisel, and S. Mense (1988) Effects of a carrageenaninduced myositis on the discharge properties of group III and IV muscle receptors in the cat. J. Neurophysiol. 55:1395-1409.
14. Bernard, J.F., and J.M Besson (1990) The spmo (trigemino) pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63:473-490.
15. 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. 71:551-569.
16. Bernard, J.F., M. Peschanski, and J.M. Besson (1989) Afferents and efferents of the rat cuneiformis nucleus: an anatomical study with reference to pain transmission. Brain Res. 430:181-185.
17. Besson, J.M., and A, Chaouch (1987) Peripheral and spinal mechanisms of nociception Physiol. Rev. 67:67-186.
18. Blomqvist, A., and A.D. Craig (1991) Organization of spinal and trigeminal input to the PAG. In Depauhs, A, and R. Bandler (eds): The Midbrain Periaqueductal Gray Matter. New York. Plenum, pp. 345-364.
19. Blomqvist, A., and M Wiberg (1985) Some aspects of the anatomy of somatosensory projections to the cat midbrain. In Rowe, M.J., and W D. Willis (eds): Development, Organization and Processing in Somatosensory Pathways. New York: Alan R. Liss, pp. 215-222.
20. Bolser, D.C., S.F. Hobbs, M.J. Chandler, W. Ammons, T.J. Brennan, and R D. Foreman (1991) Convergence of phrenic and cardiopulmonary spinal afferent information on cervical and thoracic spinothalamic tract neurons in the monkey implications for referred pain from the diaphragm and the heart. J. Neurophysiol. 65:1042-1054
21. Bruce, L.L., J.G. McHaffie, and B.E Stein (1987) The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double labelling study with fluorescent dyes J. Comp. NeuroL 202:315-330.
22. Bullit, E. (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. NeuroL 596:517-530.
23. Carrive, P. (1991) Functional organization of PAG neurons controlling regional vascular beds. In Depaulis, A., and R. Bandler (eds): The Midbrain Periaqueductal Gray New York: Plenum, pp. 67-100.
24. Cervero, F., and J.E. Tattersall (1987) Somatic and visceral inputs to the thoracic spinal cord of the cat: marginal zone (lamina I) of the dorsal horn. J. Physiol. 355:383-395.
25. Chan, R.K.W., and P.E. Sawchenko (1994) Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholammergic cell groups induced by cardiovascular challenges in the rat. J. Comp. Neurol. 348:433-460
26. Chase, M.H., S.H. Chandler, and Y. Nakamura (1980) Intracellular determination of membrane potential of trigemmal motoneurons during sleep and wakefulness. J Neurophysiol. 44:349-358.
27. Clement, C.I., K.A. Keay, and R. Bandler (1995) Halothane anesthesiainduced activation of medullary adrenergic and noradrenergic projections to the midbrain penaqueductal gray. Proc. Aust. Neurosci. Soc. 6: 180.
28. Coggeshall, R.E., K.A.P. Hong, L.A. Langford, H.G. Sehaible, and R,F. Schmidt (1983) Discharge characteristics of fine medial articular afferents at rest and during passive movements of the knee joints. Brain Res. 272:183-188.
29. Cooper, L.L., and J.O. Dostrovsky (1985) Projection from the dorsal column nuclei to dorsal meseneephalon. J. Neurophysiol. 53:183-200.
30. Dean, P., I.J. Mitchell, and P. Redgrave (1988a) Contralateral head movements poduced by microinjection of glutamate into superior colliculus: evidence for mediation by multiple output pathways. Neuroscienee 24:491-500.
31. Dean, P., L.J. Mitchell, and P. Redgrave (1988b) Responses resembling defensive behaviour produced by microinjection of glutamate in superior colliculus of rats. Neuroscience 24:501-510.
32. Dean, P., P. Redgrave, and I. Mitchell (1988) Organization of efferent projections from superior colliculus to brainstem in rat: evidence for functional output channnels. Prog. Brain Res. 75:27-36.
33. Dean, P., P. Redgrave, and G.W.M. Westby (1989) Event or emergency ? Two responses systems in the mammalian superior colliculus. Trends Neurosci. 12:137-147.
34. Depaulis, A., K.A. Keay, and R. Handler (1994) Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp. Brain Res. 99:75-83.
35. Dickenson, A.H., and A.F. Sullivan (1987a) Peripheral origins and central modulations of subcutaneous formalin-induced activity of rat dorsal horn neurons. Neurosci. Lett. 83:207-211.
36. Dickenson, A.H., and A.F. Sullivan (1987b) Subcutaneous formalin-induced activity of dorsal horn neurons in the rat: differential response to an intrathecal opiate administered pre or post formalin Pain 30:349-360.
37. Dragunow, M., and R. Faull (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29:261-265.
38. Duggan, A.W. (1983) Injury, pain and analgesia. Proc. Aust. Physiol. Pharmacol. Soc. 14:218-240.
39. Durham, D., and T.A. Woolsey (1978) Acute whisker removal reduces neuronal activity in barrels of mouse SmI cortex. J. Comp. Neurol, 178:629-644.
40. Edwards, S B., C.L. Ginsburgh. C.K. Henkel, and B.E. Stein (1979) Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol. 184:300-330.
41. Engel, G.L , and A.H. Schmale (1972) Conservation-withdrawal: a primary regulatory process for organismic homeostasis. CIBA Foundation Symposium 5:57-76.
42. Ennis, M , G. Aston-Jones, and R. Shiekhattar (1992) Activation of locus coeruleus neurons by nucleus paragigantocellularis or noxious sensory stimulation is mediated by intraeoerulear excitatory amino acid neurotransmission. Brain Res. 595:185-195.
43. Faye-Lund, H., and K.K. Osen (1985) Anatomy of the inferior colliculus in rat. Anat. Embryol. 171:1-20.
44. Fields, H.L., and A.I. Basbaum (1978) Brainstem control of spinal paintransmission neurons Ann. Rev. Physiol. 40:217-248.
45. 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.
46. Gebhart, G.F (1986) Modulatory effects of descending systems on spinal dorsal horn neurons. In Yaksh, T.L (eds): Spinal Afferent Processing. New York. Plenum, pp. 391-416.
47. Gieroba, Z.J., and W.W. Blessing (1994) Depressor neurons in caudal medulla demonstrated by Fos expression following activation of cardiopulmonary vagal (Bezold-Jarisch) receptors. Proc. Aust. Neurosci. Soc. 5-189.
48. Giesler, G.J., M. Bjorkeland, Q. Xu, and G. Grant (1988) Organization of the spinocervicothalamic pathway in the rat J. Comp Neurol. 268:223-233.
49. Hammond, D., R. Presley, K.R. Gogas, and A.I. Basbaum (1992) Morphine or U-50488 suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus sohtarius evoked by noxious visceral stimulus in the rat. J. Comp Neurol 315-244-253.
50. Henry, J.P., and P.M. Stephens (1977) Stress Health and the Social Environment: A Sociobiological Approach to Medicine, New York: Springer-Verlag.
51. Herbert, H., and C.B. Saper (1992) Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J. Comp. Neurol 315:34-52.
52. Herdegen, T., K. Kovary, A. Bulp, R. Bravo, M. Zimmermann, and P. Gass (1995) Basal expression of the inducible transcription factors c-jun,jun-B,junD,c-fos, fosB and KEOX-24 in the adult rat brain. J. Comp. Neurol. 354:39-56.
53. Hobbs, S.F , M.J. Chandler, D C. Boiser, and R.D. Foreman (1992) Segmental organization of visceral and somatic input onto C3-T6 spinothalamic tract cells of the monkey. J. Neurophysiol 68:1575-1588.
54. Huerta, M.F., A.J. Frankfurter, and J K Halting (1981) The trigeminocolhcular projection in the cat: Patch-like endings within the intermediate gray. Brain Res. 211:12-15
55. Hunt, S P., A. Pini, and G. Evans (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation Nature 328:632-634.
56. Jones, E. (1985) The Thalamus. New York: Plenum
57. Jones, S., and R. Blair (1995) Noxious heat-evoked fos-like immunoreactivity in the rat medulla, with emphasis on the catecholamine cell groups. J. Comp. Neurol. 354:410-422.
58. Jones, S.L., and A.R. Light (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. 530:335-338.
59. Keay, KLA., and R. Bandler (1992) Anatomical evidence for segregated input from the upper cervical spinal cord to functionally distinct regions of the midbrain periaqueductal gray region of the cat. Neurosci. Lett. 339:143-148.
60. Keay, K.A., and R. Bandler (1993) Deep and superficial noxious stimulation increases Fos like immunoreactivity in different regions of the midbrain penaqueductal gray of the rat. Neurosci. Lett. 154.:143-158.
61. Keay, K.A., C.I. Clement, B. Owler, A. Depaulis, and R. Bandler (1994) Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueduetal gray region. Neuroscience 61:727-732.
62. Keay, K.A., P. Dean, and P. Redgrave (1990) N-methyl D-aspartate (NMDA) evoked changes in blood pressure and heart rate from the rat superior colliculus. Exp Brain Res. 50-148-156.
63. Killackey, H.P , and R.S. Erzurumlu (1981) Trigeminal projections to the superior colliculus of the rat. J. Comp. Neurol. 201:221-242.
64. Krukorff, 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.
65. Land, P.W., and D.J. Simons (1985) Metabolic activity m SmI cortical barrels of adult rats is dependent on patterned sensory stimulation of the mystacial vibrissae. Brain Res 341:189-194.
66. Lanteri-Minet, M., P. Isnardon, J. De Pommery, and D. Menetrey (1993) Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and, Krox-24 Proteins. Neurosci. 55:737-753.
67. Lanteri-Minet, M., J. Weil-Fugaza, J. dePommery, and D. Menetrey (1994) Hindbrain structures involved in pain processing as revealed by the expression of c-fos and other immediate early genes. Neurosci 55:287-298.
68. Larson, MA., J.G. McHaffie, and B.E. Stein (1987) Response properties of nociceptive and low-threshold mechanoreceptive neurons in the hamster superior colliculus. J. Neurosci 7:547-564.
69. Lewis, T. (1942) Pain. London: McMillan.
70. Lewis, T., and RD. Kellgren (1939) Observations related to referred pain, viscerosomatic reflexes and other associated phenomena. Clin. Sci. 4:47.
71. Li, Y, and R. Dampney (1993) Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience 61:613-634.
72. Lima, D., and A. Coimbra (1989) Morphological types of spinomesencephalic neurons in the marginal zone (lamina I) of the rat spinal cord as shown after labelling with cholera toxin subunit B. J. Comp. Neurol. 279:327-339
73. Liu, R. (1983) Laminar origins of spinal projection neurons to the periaqueductal of the rat. Brain Res. 264 118-122.
74. Liu, R. (1986) Spinal neuronal collaterals to the intralaminar thalamic nuclei and penaqueductal gray. Brain Res. 365:145-150.
75. Lovick, T.A. (1992) Inhibitory modulation of the cardiovascular defence response by the ventrolateral penaqueductal gray matter in rats. Exp. Brain Res. 89:133-139.
76. Lovick, T.A. (1993) Integrated activity of cardiovascular and pain regulatory systems: role in adaptive behavioural responses. Prog. Neurobiol. 40:631-644.
77. McHaffie, J.G.. C Q. Kao, and B.E. Stein (1989) Nociceptive neurons in rat superior colliculus: Response properties, topography, and functional implications. J. Neurophysiol. 62:510-525
78. Mehler, W.R. (1969) Some neurological species differences- a posteriori. Ann. N Y Acad. Sci. 167:424-468.
79. Meller, S.T., S.J. Lewis, T.J. Ness, M.J. Brody, and G.F. Gebhart (1990) Vagal afferent-mediated inhibition of a nociceptive reflex by intravenous serotonin in the rat. I. Characterisation. Brain Res 524:90-100.
80. Menetrey, D., and J. dePommery (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur. J. Neurosci. 3:249-259.
81. Menetrey, 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
82. Mense, S. (1993) Nociception from skeletal muscle in relation to clinical muscle pain. Pain 54:241-289.
83. Morest. D.K., and D.L. Oliver (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J. Comp. Neurol. 222:209-236.
84. Morgan, J.O., and T. Curran (1986) Role of ion influx in the control of c-fos expression. Nature 522:552-550.
85. Murphy, A., and M.T. Shipley (1993) Longitudinal columnar organization of Fos-reactive neurons in the periaqueductal gray following changes in blood pressure. Soc. Neurosci. Abs. (USA) 19:391.5.
86. Neto, F.R. (1978) The depolarising action of 5-HT on mammalian nonmyelinated nerve fibers. Eur. J. Pharmacol. 40:351-356.
87. Owler, B., C.I. Clement, K.A. Keay, and R. Bandler (1994) Deep somatic and visceral noxious stimuli evoke Fos expression in different spinal cord laminae and a common region of the nucleus of the solitary tract. Proc Aust Neurosci. Soc. 5.200
88. Page, I H., and J.W. McCubbin (1953) The variable arterial pressure response to serotonin in laboratory animals and man. Circ. Res. 1:354-362.
89. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Co-ordinates. Sydney Academic Press.
90. Person, R J. (1989) Somatic and vagal afferent convergence on solitary tract neurons in cat: electrophysiological characteristics. Neurosci. 30:283-295.
91. Pigarev, I. (1994) Neurons of visual cortex respond to visceral stimulation during slow wave sleep. Neurosci 62:1237-1243
92. Redgrave, P., S. Telford, S. Wang, J. McHaffie, and B. Stein (1995) Functional anatomy of nociceptive neurones in rat superior colliculus. Prog. Brain Res (in press).
93. Rhoades, R.W., K.D. Mooney, and M.F Jacquin (1983) Complex somatosensory receptive fields of cells in the deep laminae of the hamsters superior colliculus. J. Neurosci. 3:1342-1354.
94. Robards, M.J (1979) Somatic neurons in the brainstem and neocortex projecting to the external nucleus of the inferior coiliculus: an anatomical study in the opossum. J. Comp. Neuro. 184:547-65.
95. Sagar, S.M., F.R. Sharp, and T Curran (1988) Expression of c-fos protein in brain: metabolic mapping at the cellular level Science 240:1328-1331
96. Schaible, H.-G., and R.F. Schmidt (1985) Effects of an experimental arthritis on the sensory properties of fine articular afferent units J. Neurophysiol. 54:1109-1122.
97. Schober, W (1981) Efferente und afférente Verbindungen des nucleus lateralis posterior thalami ('pulvinar') der albinoratte. Z mikrosk. Anat. Forsch. 95.431-446.
98. Schroeder, D.M., and J.A Jane (1971) Projection of dorsal column nuclei and spinal cord to brainstem and thalamus in the tree shrew, Tupaia glis J. Comp. Neurol. 142:309-350.
99. Sheng, M., and M.E. Greenberg (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477-485.
100. Siegel, S. (1956) Non-parametric statistics for the behavioural sciences New York: McGraw-Hill
101. Soja, P.J. (1991) Excitability of facial motorneurons is reduced during the atonia of active sleep. Soc. Neurosci. Abst. 17:644.
102. Stanfa, L C., A F. Sullivan, and A.H. Dickenson (1992) Alterations in neuronal excitability and the potency of spinal mu, delta and kappa opioids after carrageenan- induced inflammation. Pain 50:345-354.
103. Stansfield, C.E , and D.I. Walhs (1985) Properties of visceral primary afferent neurons in the nodose ganglion of the rabbit. J. Neurophysiol 54:245-260.
104. Stein, B.E., and J.P. Dixon (1978) Superior colliculus cells respond to noxious stimuli. Brain Res. 158:65-73.
105. Steiner, H , and C.E. Gerfen (1994) Tactile sensory input regulates basal and apomorphine-induced immediate - early gene expression in rat barrel cortex J. Comp. Neurol. 344:297-304.
106. Strassman, A.M., and B.P. Voss (1993) Somatotopic and laminar organization of Fos-like imimmoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation, J. Comp. Neurol. 331:495-516.
107. Szczepamak, W.S., and A.R. Moller (1993) Interaction between auditory and somatosensory systems: a study of evoked potentials in the inferior colliculus. Electroencephalo. Clin. Neurophysiol. 88:508-515.
108. Taber, R., D. Greenhouse, J. Rendell, and S. Irwin (1969) Agonist and antagonist interactions of opioids on acetic acid induced abdominal stretching in mice. J. Pharm. Exp. Ther. 169:29-38
109. 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. Letters 176:59-62.
110. Vogt, B., and M. Miller (1983) Cortical connections between rat cingulate cortex and visual, motor and postsubicular cortices J. Comp. Neurol. 276:192-210.
111. Vogt, B . R. Sikes, H. Swadlow, and T. Weyand (1986) Rabbit cingulate cortex: cytoarchitecture, physiological border with visual cortex and afferent cortical connections of visual, motor postsubicular and intracingulate origin. J. Comp. Neurol 248:74-94.
112. Wall, P D (1979) On the relation of injury to pain. Pain 6:253-264.
113. Wallis, D.I., C.E. Stansfield, and H L. Nash (1982) Depolarising responses recorded from nodose ganglion cells of the rabbit evoked by 5-hydroxytryptamine and other substances. Neuropharmacology 21:31-40.
114. Westby, G.W.M., K.A. Keay, P. Redgrave, P. Dean, and M. Bannister (1990) Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp. Brain Res. 81:626-638.
115. Wiberg, M., and A. Blomqvist (1984) The spinomesencephalic tract in the cat: its cells of origin and termination patterns as demonstrated by intra-axonal transport method. Brain Res. 291:1-18.
116. Wiberg, M., J. Westman, and A. Blomqvist (1987) Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J. Comp. Neurol, 254:92-117.
117. Willis, W.D (1984) The raphe spinal system. In Barnes, C.D. (eds): Brainstem Control of Spinal Cord Function. New York: Academic Press, pp. 141-214.
118. Wong - Riley, M.T.T., and C. Welt (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc. Natl. Acad. Sci. USA. 77:2333-2337.
119. Worley, P.F., B.A. Christy, Y. Nakabeppu, R.V. Bhat, A.J. Cole, and J.M. Baraban (1991) Constitutive expression of zif 268 in neocortex is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA 88:5106-5110.
120. Yamuy, J., J.R. Mancillas, F.R. Morales, and M.H. Chase (1993) C-fos expression in the pons and medulla of the cat during carbachol-induced active sleep. J. Neurosci 13:2703-2718.
121. Yezierski, R.P. (1988) Spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat and monkey J. Comp. Neurol. 267:131-146
122. Yezierski, R.P. (1991) Somatosensory input to the periaqueductal gray: a spinal relay to a descending control centre. In Depaulis, A., and R. Bandler (eds): The Midbrain Periaqueductal Gray New York: Plenum, pp. 365-386.
123. Yezierski, R.P., and J.G. Broton (1991) Functional properties of spinomesencephahc cells in the upper cervical spinal cord of the cat Pain 45:187-198.
124. Yezierski, R.P., and C.M. Mendez (1991) Spinal distribution and collateral projections of rat Spinomesencephalic tract cells. Neuroscience 44:113-130.
125. Zittel, T T., R.d. Georgio, N.C. Breeha, C. Sternini, and H.E. Raybould (1993) Abdominal surgery induces c-fos expression in the nucleus of the solitary tract in the rat. Neurosci. Lett. 259:79-82.