Pharmacologic evidence for the modulation of nociception by noradrenergic neurons

Progress in Brain Research

Volumn 77, Issue C, 1988, Pages 357-370

  Proudfit, Herbert K ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINOCICEPTIVE AGENT; METHYSERGIDE; NORADRENALIN; PHENTOLAMINE; PROPRANOLOL; YOHIMBINE;

BEHAVIOR; BRAIN STEM; LOCUS CERULEUS; PSYCHOLOGICAL ASPECT; RAPHE NUCLEUS; SHORT SURVEY;

EID: 0023723395     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/S0079-6123(08)62802-2     Document Type: Article

References (114)

1. Abols, I.A., Basbaum, A.I., Afferent connections of the rostral medulla of the cat. J. Comp. Neurol. 201 (1981), 285–297.
2. Barbaro, N.M., Hammond, D.L., Fields, H.L., Effects of intrathecally administered methysergide and yohimbine on microstimulation-produced antinociception in the rat. Brain Res. 343 (1985), 223–229.
3. Behbehani, M.N., Pomeroy, S.L., Mack, C.E., Interaction between central gray and nucleus raphe magnus: role of norepinephrine. Brain Res. Bull. 6 (1981), 361–364.
4. Belcher, G., Ryall, R.W., Schaffner, R., The differential effects of 5-hydroxytryptamine, noradrenaline, and raphe stimulation of nociceptive and non-nociceptive dorsal horn interneurons in the cat. Brain Res. 151 (1978), 307–332.
5. Berthelsen, S., Pettinger, W.A., A functional basis for classification of α-adrenergic receptors. Life Sci. 21 (1977), 595–606.
6. Bowker, R.M., Westlund, K.N., Sullivan, M.C., Wilber, J.F., Coulter, J.D., Descending serotonergic, peptidergic and cholinergic pathways from the raphe nuclei: a multiple transmitter complex. Brain Res. 288 (1983), 33–48.
7. Bragin, E.O., Durinyan, R.A., A study of the catecholamine systems of the lateral reticular nucleus and the serotonergic systems of the raphe magnus in various types of analgesia. Pain 17 (1983), 225–234.
8. Calvillo, O., Ghignone, M., Presynaptic effect of clonidine on unmyelinated afferent fibers in the spinal cord of the cat. Neurosci. Lett. 64 (1986), 335–339.
9. Carlsson, A., Falck, B., Fuxe, K., Hillarp, N.A., Cellular localization of monoamines in the spinal cord. Acta Physiol. Scand. 60 (1964), 112–119.
10. Clarke, F.M., Fitzgerald, L.F., Proudfit, H.K., Alterations in the activity of dorsal horn neurons produced by electrical stimulation of neurons in the ventrolateral pontine tegmentum. Soc. Neurosci. Abstr., 13, 1987, 303.
11. Commissiong, J.W., Evidence that the noradrenergic projection decussates at the spinal level. Brain Res. 212 (1981), 145–151.
12. Commissiong, J.W., Hellström, S.O., Neff, N.H., A new projection from locus coeruleus to the spinal ventral columns: histochemical and biochemical evidence. Brain Res. 148 (1978), 207–213.
13. Dahlstró, Um, Fuxe, K., Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand.(Supplement 232), 1965, 1–55.
14. Dashwood, M.R., Gilbey, M.P., Spyer, K.M., The localization of adrenoceptors and opiate receptors in regions of the cat central nervous system involved in cardiovascular control. Neuroscience 15 (1985), 537–551.
15. Dong, X., Shen, E., Origin of monoaminergic innervation of the nucleus raphe magnus - a combined monoamine histochemistry and fluorescent retrograde tracing study in the rat. Scientia Sinica 6 (1986), 599–608.
16. Engberg, I., Ryall, R.W., The inhibitory actions of noradrenaline and other monoamines on spinal neurons. J. Physiol. (Lond.) 185 (1966), 298–322.
17. Fleetwood-Walker, S.M., Coote, J.H., The contribution of brain stem catecholamine cell groups to the innervation of the sympathetic lateral cell column. Brain Res. 205 (1981), 141–155.
18. Fleetwood-Walker, S.M., Mitchell, R., Hope, P.J., Molony, V., Iggo, A., An α2receptor mediates the selective inhibition by noradrenaline of nociceptive responses of identified dorsal horn neurones. Brain Res. 334 (1985), 243–254.
19. Fischbach, G.D., Dunlap, K., Mudge, A., Leeman, S., Peptide and amine transmitter effect on embryonic chick sensory neurons in vitro. Adv. Biochem. Psychopharmacol. 28 (1981), 175–188.
20. Fuxe, K., Evidence for the existence of monoamine neurons in the central nervous system. Acta Physiol. Scand.(Supplement 247), 1965, 37–84.
21. Gebhart, G.F., Ossipov, M.H., Characterization of inhibition of the spinal nociceptive tail-flick reflex in the rat from the medullary lateral reticular nucleus. Neuroscience 6 (1986), 701–713.
22. Greenberg, D.A., U'Prichard, D.C., Snyder, S.H., Alpha-noradrenergic receptor binding in mammalian brain: differential labeling of agonists and antagonist states. Life Sci. 19 (1976), 69–76.
23. Greengrass, P., Bremner, R., Binding characteristics of 3H-prazosin to brain α-adrenergic receptors. Eur. J. Pharmacol. 55 (1979), 323–326.
24. Hall, J.G., Duggan, A.W., Morton, C.R., Johnson, S.M., The location of brainstem neurones tonically inhibiting dorsal horn neurones of the cat. Brain Res. 215 (1982), 215–222.
25. Hammond, D.L., Proudfit, H.K., Effects of locus coeruleus lesions on morphine-induced antinociception. Brain Res. 188 (1980), 79–91.
26. Hammond, D.L., Yaksh, T.L., Antagonism of stimulation-produced antinociception by intrathecal administration of methysergide or phentolamine. Brain Res. 298 (1984), 329–337.
27. Hammond, D.L., Levy, R.A., Proudfit, H.K., Hypalgesia following microinjection of noradrenergic antagonists in the nucleus raphe magnus. Pain 9 (1980), 85–101.
28. Hammond, D.L., Levy, R.A., Proudfit, H.K., Hypoalgesia induced by microinjection of a norepinephrine antagonist in the raphe magnus: reversal by intrathecal administration of a serotonin antagonist. Brain Res. 201 (1980), 475–479.
29. Hammond, D.L., Tyce, G.M., Yaksh, T.L., Efflux of 5-hydroxytryptamine and noradrenaline into spinal cord superfusates during stimulation of the rat medulla. J. Physiol. (Lond.) 359 (1985), 151–162.
30. Headley, P.M., Duggan, A.W., Griersmith, B.T., Selective reduction by noradrenaline and 5-hydroxytryptamine of nociceptive responses of cat dorsal horn neurones. Brain Res. 145 (1978), 185–189.
31. Heinricher, M.M., Haws, C.M., Fields, H.L., Opposing actions of norepinephrine and clonidine on single painmodulating neurons in rostral ventromedial medulla. Pain(Supplement 4), 1987, S28.
32. Hodge, C.J. Jr., Apkarian, A.V., Stevens, R., Vogelsang, G., Wisnicki, H.J., Locus coeruleus modulation of dorsal horn unit responses to cutaneous stimulation. Brain Res. 204 (1981), 415–420.
33. Hodge, C.J. Jr., Apkarian, A.V., Owen, M.P., Hanson, B.S., Changes in the effects of stimulation of locus coeruleus and nucleus raphe magnus following dorsal rhizotomy. Brain Res. 288 (1983), 325–329.
34. Hodge, C.J. Jr., Apkarian, A.V., Stevens, R.T., Vogelsang, G.D., Brown, O., Franck, J.I., Dorsolateral pontine inhibition of dorsal horn cell responses to cutaneous stimulation: lack of dependence on catecholaminergic systems in cat. J. Neurophysiol. 50 (1983), 1220–1235.
35. Holz, G.G., Kream, R.M., Dunlap, K., Norepinephrine inhibits field stimulation-evoked release of substance P from chick dorsal root ganglion cells in culture. Soc. Neurosci. Abstr., 11, 1985, 126.
36. Hornung, R., Presek, P., Glossmann, H., Alpha-adrenoceptors in rat brain: direct identification with prazosin. Naunyn-Schmiedeb. Arch. Pharmacol. 308 (1979), 223–230.
37. Howe, J.R., Yaksh, T.L., Changes in sensitivity to intrathecal norepinephrine and serotonin after 6-hydroxydopamine (6-OHDA), and 5,6-dihydroxytryptamine (5,6-DHT) or repeated monoamine administration. J. Pharmacol. Exp. Ther. 220 (1982), 311–321.
38. Howe, J.R., Zieglgänsberger, W., Responses of rat dorsal horn neurons to natural stimulation and to iontophoretically applied norepinephrine. J. Comp. Neurol. 255 (1987), 1–17.
39. Howe, J.R., Wang, J.-Y., Yaksh, T.L., Selective an tagonism of the antinociceptive effect of intrathecally applied alpha-adrenergic agonists by intrathecal prazosin and intrathecal yohimbine. J. Pharmacol. Exp. Ther. 224 (1983), 552–558.
40. Hylden, J.L.K., Wilcox, G.L., Pharmacological characterization of substance P-induced nociception in mice. Modulation by opioid and noradrenergic agonists at the spinal cord level. J. Pharmacol. Exp. Ther. 226 (1983), 398–404.
41. Iggo, A., McMillan, J.A., Mokha, S.S., Modulation of spinal cord multireceptive neurones from locus coeruleus and nucleus raphe magnus in the cat. J. Physiol. 319 (1981), 107–108P.
42. Janss, A.J., Gebhart, G.F., Quantitative characterization and spinal pathway mediating inhibition of spinal nociceptive transmission from the lateral reticular nucleus in the rat. J. Neurophysiol. 59 (1987), 226–247.
43. Janss, A.J., Cox, B.F., Brody, M.J., Gebhart, G.F., Dissociation of antinociceptive from cardiovascular effects of stimulation in the lateral reticular nucleus in the rat. Brain Res. 405 (1987), 140–149.
44. Janss, A.J., Jones, S.L., Gebhart, G.F., Effect of spinal norepinephrine depletion on descending inhibition of the tail flick reflex from the locus coeruleus and lateral reticular nucleus in the rat. Brain Res. 400 (1987), 40–52.
45. Jeftinija, S., Semba, K., Randic, M., Norepinephrine reduces excitability of single cutaneous afferent C-fibers in the cat spinal cord. Brain Res. 219 (1981), 456–463.
46. Jeftinija, S., Semba, K., Randic, M., Norepinephrine reduces excitability of single cutaneous primary afferent C and A fibers in the cat spinal cord. Adv. Pain Res. Ther. 5 (1983), 271–276.
47. Jensen, T.S., Yaksh, T.L., Spinal monoamine and opiate systems partly mediate the antinociceptive effects produced by glutamate at brainstem sites. Brain Res. 321 (1984), 287–298.
48. Jones, B.E., Friedman, L., Atlas of catecholamine perikarya, varicosities and pathways in the brainstem of the cat. J. Comp. Neurol. 215 (1983), 382–396.
49. Jones, S.L., Gebhart, G.F., Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflex in the rat: mediation by spinal α2-adrenoceptors. Brain Res. 364 (1986), 315–330.
50. Jones, S.L., Gebhart, G.F., Quantitative characterization of ceruleospinal inhibition of nociceptive transmission in the rat. J. Neurophysiol. 56 (1986), 1397–1410.
51. Jones, S.L., Gebhart, G.F., Spinal pathways mediating tonic, coeruleospinal, and raphespinal descending inhibition in the rat. J. Neurophysiol. 58 (1987), 138–159.
52. Karoum, F., Commissiong, J.W., Neff, N.H., Wyatt, R.J., Biochemical evidence for uncrossed locus coeruleus projections to the spinal cord. Brain Res. 196 (1980), 237–241.
53. Kuraishi, T., Harada, T., Takagi, H., Noradrenaline regulation of pain-transmission in the spinal cord mediated by α-adrenoceptors. Brain Res. 174 (1979), 333–336.
54. Kuraishi, Y., Hirota, N., Sato, Y., Kaneko, S., Satoh, M., Takagi, H., Noradrenergic inhibition of the release of substance P from the primary afferents in the rabbit spinal dorsal horn. Brain Res. 359 (1985), 177–182.
55. Langer, S.Z., Presynaptic receptors and their role in the regulation of transmitter release. Br. J. Pharmacol. 60 (1977), 481–497.
56. Langer, S.Z., Presynaptic regulation of the release of catecholamines. Pharmacol. Rev. 32 (1981), 337–362.
57. Levitt, P., Moore, R.J., Origin and organization of brainstem catecholamine innervation in the rat. J. Comp. Neurol. 186 (1979), 505–528.
58. Light, A.R., 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 (1979), 1171–1232.
59. Margalit, D., Segal, M., A pharmacologic study of analgesia produced by stimulation of the nucleus locus coeruleus. Psychopharmacology 62 (1979), 169–173.
60. McKellar, S., Loewy, A.D., Efferent projections of the A1 catecholamine cell group in the rat: an autoradiographic study. Brain Res. 241 (1982), 11–29.
61. Miller, J.F., Proudfit, H.K., Stimulation-produced analgesia from pontine ventrolateral tegmentum. Soc. Neurosci. Abstr., 10, 1984, 102.
62. Miller, J.F., Proudfit, H.K., Stimulation-produced analgesia from ventrolateral pontine tegmentum is not mediated through the nucleus raphe magnus. Soc. Neurosci. Abstr., 11, 1985, 638.
63. Miller, J.F., Proudfit, H.K., Stimulation-produced analgesia from sites in the ventrolateral pons is mediated by a spinal alpha-2 adrenergic system. Soc. Neurosci. Abstr., 13, 1987, 303.
64. Mokha, S.S., McMillan, J.A., Iggo, A., Descending influences on spinal nociceptive neurons from locus coeruleus: actions, pathway, neurotransmitters, and mechanisms. Adv. Pain Res. Ther. 5 (1983), 387–392.
65. Mokha, S.S., McMillan, J.A., Iggo, A., Descending control of spinal nociceptive transmission. Actions produced on spinal multireceptive neurones from the nuclei locus coeruleus (LC) and raphe magnus. Exp. Brain Res. 58 (1985), 213–226.
66. Mokha, S.S., McMillan, J.A., Iggo, A., Pathways mediating descending control of spinal nociceptive transmission from the nuclei locus coeruleus (LC) and raphe magnus (NRM) in the cat. Exp. Brain Res. 61 (1986), 597–606.
67. Morton, C.R., Johnson, S.M., Duggan, A.W., Lateral reticular regions and the descending control of dorsal horn neurones of the cat: selective inhibition by electrical stimulation. Brain Res. 275 (1983), 13–21.
68. Morton, C.R., Duggan, A.W., Zhao, Z.Q., The effects of lesions of medullary midline and lateral reticular areas on inhibition in the dorsal horn produced by periaqueductal grey stimulation in the cat. Brain Res. 301 (1984), 121–130.
69. North, R.A., Yoshimura, M., The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J. Physiol. (Lond.) 349 (1984), 43–55.
70. Nygren, L.-G., Olson, L., A new major projection from locus coeruleus: the main source of noradrenergic nerve terminals in the ventral and dorsal columns of the spinal cord. Brain Res. 132 (1977), 85–93.
71. Palkovits, M., Jacobowitz, D.M., Topographical atlas of catecholamine and acetylcholinesterase-containing neurons of the rat brain. II. Hindbrain (mesencephalon, rhombencephalon). J. Comp. Neurol. 157 (1974), 29–42.
72. Pang, I.H., Vasko, M.R., Morphine and norepinephrine but not 5-hydroxytryptamine and gamma-amino butyric acid inhibit the potassium-stimulated release of substance P from rat spinal cord slices. Brain Res. 6 (1986), 268–279.
73. Pretel, S., Ruda, M.A., Immunocytochemical investigation of monoaminergic interaction in brain stem raphe nuclei of the cat. Soc. Neurosci. Abstr., 11, 1985, 579.
74. Proudfit, H.K., Effects of raphe magnus and raphe pallidus lesions on morphine-induced analgesia and spinal cord monoamines. Pharmacol. Biochem. Behav. 13 (1980), 705–714.
75. Proudfit, H.K., Reversible inactivation of raphe magnus neurons: effects on nociceptive threshold and morphine-induced antinociception. Brain Res. 201 (1980), 459–464.
76. Proudfit, H.K., Time-course of alterations in morphine-induced analgesia and nociceptive threshold following medullary raphe lesions. Neuroscience 6 (1981), 945–951.
77. Proudfit, H.K., Anderson, E.G., Morphine analgesia: blockade by raphe magnus lesions. Brain Res. 98 (1975), 612–618.
78. Ralston, H.J. III, Ralston, D.D., 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 (1979), 643–684.
79. Reddy, S.V.R., Yaksh, T.L., Spinal noradrenergic terminal system mediates antinociception. Brain Res. 189 (1980), 391–401.
80. Reddy, S.V.R., Maderdrut, J.L., Yaksh, T.L., Spinal cord pharmacology of adrenergic agonist-mediated antinociception. J. Pharmacol. Exp. Ther. 213 (1980), 525–533.
81. Ross, R.A., Reis, D.J., Effects of lesions of locus coeruleus on regional distribution of dopamine-β-hydroxylase activity in rat brain. Brain Res. 73 (1974), 161–166.
82. Saavedra, J.M., Grobecker, H., Zivin, J., Catecholamines in the raphe nuclei of the rat. Brain Res. 114 (1976), 339–345.
83. Sagen, J., Proudfit, H.K., Hypoalgesia induced by blockade of noradrenergic projections to the raphe magnus: reversal by blockade of noradrenergic projections to the spinal cord. Brain Res. 223 (1981), 391–396.
84. Sagen, J., Proudfit, H.K., The role of the A7 catecholamine group in the modulation of pain perception. Soc. Neurosci. Abstr., 9, 1983, 785.
85. Sagen, J., Proudfit, H.K., Effect of intrathecally administered noradrenergic antagonists on nociception in the rat. Brain Res. 310 (1984), 295–301.
86. Sagen, J., Proudfit, H.K., Evidence for pain modulation by pre- and postsynaptic noradrenergic receptors in the medulla oblongata. Brain Res. 331 (1985), 285–293.
87. Sagen, J., Proudfit, H.K., Alterations in nociception following lesions of the A5 catecholamine nucleus. Brain Res. 370 (1986), 93–101.
88. Sagen, J., Proudfit, H.K., Release of endogenous monoamines into spinal cord superfusates following the microinjection of phentolamine into the nucleus raphe magnus. Brain Res. 406 (1987), 246–254.
89. Sagen, J., Winker, M.A., Proudfit, H.K., Hypoalgesia induced by the local injection of phentolamine in the nucleus raphe magnus: blockade by depletion of spinal cord monoamines. Pain 16 (1983), 253–263.
90. Sandberg, D.E., Segal, M., Pharmacological analysis of analgesia and self-stimulation elicited by electrical stimulation of catecholamine nuclei in the rat brain. Brain Res. 152 (1978), 529–542.
91. Satoh, K., Tohyama, K., Yamamoto, K., Sakumoto, T., Shimizu, N., Noradrenaline innervation of the spinal cord studied by the horseradish peroxidase method combined with monoamine oxidase staining. Exp. Brain Res. 30 (1977), 175–186.
92. Schmidt, R.F., Presynaptic inhibition in the vertebrate central nervous system. Ergebn. Physiol. 63 (1971), 20–101.
93. Segal, M., Sandberg, D., Analgesia produced by electrical stimulation of catecholamine nuclei in the rat brain. Brain Res. 123 (1977), 369–372.
94. Seybold, V.S., Elde, R.P., Receptor autoradiography in thoracic spinal cord: correlation of neurotransmitter binding sites with sympathoadrenal neurons. J. Neurosci. 4 (1984), 2533–2542.
95. Starke, K., Regulation of noradrenaline release by presynaptic receptor systems. Rev. Physiol. Biochem. Pharmacol. 77 (1977), 1–124.
96. Stevens, R.T., Hodge, C.J., Apkarian, A.V., Kölliker-Fuse nucleus: the principal source of pontine catecholaminergic cells projecting to the lumbar spinal cord of cat. Brain Res. 239 (1982), 589–594.
97. Swanson, L.W., Hartman, B.K., The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-β-hydroxylase as a marker. J. Comp. Neurol. 163 (1975), 467–506.
98. Takagi, H., Yamamoto, K., Shiosaka, S., Senba, E., Takutsuki, K., Inagaki, S., Sakanaka, M., Toyama, M., Morphological study of noradrenaline innervation in the caudal raphe nuclei with special reference to fine structure. J. Comp. Neurol. 203 (1981), 15–22.
99. Taube, H.D., Starke, K., Borowski, E., Presynaptic receptor systems on the noradrenergic neurones of rat brain. Naunyn-Schmiedeb. Arch. Pharmacol. 299 (1977), 123–141.
100. Todd, A.J., Millar, J., Receptive fields and responses to iontophoretically applied noradrenaline and 5-hydroxytryptamine of units recorded in laminae I-III of cat dorsal horn. Brain Res. 288 (1983), 159–167.
101. Unnerstall, J.R., Kopajtic, T.A., Kuhar, M.J., Distribution of α2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res. Rev. 7 (1984), 69–101.
102. Versteeg, D.H.G., Van der Gugten, J., De Jong, W., Palkovits, M., Regional concentrations of noradrenaline and dopamine in rat brain. Brain Res. 113 (1976), 563–574.
103. Wessendorf, M.W., Anderson, E.G., Single unit studies of identified bulbospinal serotonergic units. Brain Res. 279 (1983), 93–103.
104. Wessendorf, M.W., Proudfit, H.K., Anderson, E.G., The identification of serotonergic neurons in the nucleus raphe magnus by conduction velocity. Brain Res. 214 (1981), 168–173.
105. Westlund, K.N., Coulter, J.D., Descending projections of the locus coeruleus and subcoeruleus/medial parabrachial nuclei in monkey: axonal transport studies and dopamine-β-hydroxylase. Brain Res. Rev. 2 (1980), 235–264.
106. Westlund, K.N., Bowker, R.M., Ziegler, M.G., Coulter, J.D., Origins of spinal noradrenergic pathways demonstrated by retrograde transport of antibody to dopamine-β-hydroxylase. Neurosci. Lett. 25 (1981), 243–249.
107. Westlund, K.N., Bowker, R.M., Ziegler, M.G., Coulter, J.D., Descending noradrenergic projections and their spinal terminations. Kuypers, H.G.J.M., Martin, G.F., (eds.) Descending Pathways to the Spinal Cord, Progress in Brain Research, 57, 1982, Elsevier, Amsterdam, 219–238.
108. Westlund, K.N., Bowker, R.M., Ziegler, M.G., Coulter, J.D., Noradrenergic projections to the spinal cord in the rat. Brain Res. 263 (1983), 15–31.
109. Westlund, K.N., Bowker, R.M., Ziegler, M.G., Coulter, J.D., Origins and terminations of descending noradrenergic projections to the spinal cord of monkey. Brain Res. 292 (1984), 1–16.
110. Willcockson, W.S., Gerhart, K.D., Cargill, C.L., Willis, W.D., Effects of biogenic amines on raphe-spinal tract cells. J. Pharmacol. Exp. Ther. 225 (1983), 637–645.
111. Willcockson, W.S., Chung, J.M., Hori, Y., Lee, K.H., Willis, W.D., Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J. Neurosci. 4 (1984), 732–740.
112. Yaksh, T.L., Pharmacology of spinal adrenergic systems which modulate spinal nociceptive processing. Pharmacol. Biochem. Behav. 22 (1985), 845–858.
113. Yaksh, T.L., Go, V.L.W., Physiology and pharmacology of the release of substance P from spinal primary afferents. Soc. Neurosci. Abstr., 11, 1985, 121.
114. Young, W.S. III, Kuhar, M.J., Noradrenergic α1 and α2 receptors: light microscopic and autoradiographic localization. Proc. Natl. Acad. Sci. USA 77 (1980), 1696–1700.