Topographical distribution of NADPH-diaphorase activity in the central nervous system of the frog, Rana perezi

Journal of Comparative Neurology

Volumn 367, Issue 1, 1996, Pages 54-69

  Munoz M ^a   Munoz A ^a   Marin O ^a   Alonso, J R ^b   Arevalo R ^b   Porteros, A ^b   Gonzalez A ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

amphibians; catecholamines; evolution; histochemistry; nitric oxide synthase

Indexed keywords

CATECHOLAMINE; ENDOTHELIUM DERIVED RELAXING FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; ARTICLE; CATECHOLAMINE BLOOD LEVEL; CELL POPULATION; CENTRAL NERVOUS SYSTEM; ENZYME ACTIVITY; EVOLUTION; FROG; HISTOCHEMISTRY; LOCUS CERULEUS; NONHUMAN; PRIORITY JOURNAL; SOMATOSENSORY SYSTEM;

EID: 0029915002     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960325)367:1<54::AID-CNE5>3.3.CO;2-N     Document Type: Article

References (140)

1. Agarwala, S., J.I. May, J K. Moore, and H.M. Petry (1992a) Immunohistochemical organization of the ventral lateral gemculate nucleus in the ground squirrel. J. Comp Neurol 318.255-266
2. Agarwala, S., A.E. Günlùk, J I. May, and H.M. Petry (1992b) Immunohistochemical organization of the ventral lateral geniculate nucleus in the tree shrew. J Comp Neurol. 318:267-276.
3. Alonso, J.R., F. Sánchez, R. Arévalo, J. Carretero, R. Vazquez, and J. Aijón (1992) Partial coexistence of NADPH-diaphorase and somatostatin in the rat hypothalamic paraventricular nucleus Neurosci. Lett. 148:101-104.
4. Alonso, J.R., R Arévalo, A. Porteros, J.G. Briñón, J. Lara, and J Aijón (1993) Calbindin D-28K and NADPH-diaphorase activity are localized in different populations of periglomerular cells in the rat olfactory bulb. J. Chem. Neuroanat. 6 1-6.
5. Alonso, J.R-, R. Arévalo, J.G. Briñón, E. García-Ojeda, A. Porteros, and J. Aijón (1996) NADPH-diaphorase staining in the central nervous system. Neurosci. Protocols (in press).
6. Anderson, C.A. (1992) NADPH diaphorase-positive neurons in the rat spinal cord include a subpopulation of autonomic preganglionic neurons. Neurosci. Lett. 139:280-284.
7. Arévalo, R., F. Sánchez, J.R. Alonso, J. Carretero, R. Vázquez, and J. Aijón (1992) NADPH-diaphorase activity in the hypothalamic magnocellular neurosecretory nuclei of the rat. Brain Res. Bull 28:599-603.
8. Arévalo, R., J R. Alonso, J.G. Briñón, A. Porteros, and J. Aijón (1993) NADPH-diaphorase histochemical technique in the teleost brain. Zool. Jb Anat. 123:403-409.
9. Arévalo, R., J.R. Alonso, E García-Ojeda, J.G. Briñón, C. Crespo, and J. Aijón (1995) NADPH-diaphorase in the Central Nervous System of the tench (Tinca tinca L., 1758). J. Comp. Neurol. 352:398-420.
10. Blottner, D., and H.G. Baumgarten (1992) Nitric oxyde synthase (NOS)-containing sympathoadrenal cholinergic neurons of the rat IML-cell column: Evidence from histochemistry, immunohistochemistry and retrograde labeling. J. Comp. Neurol. 316:45-55.
11. Bredt, D.S , D.E. Glatt, H.P.M.M. Fotuhi, T.M. Dawson, and S.H. Snyder (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations in the mammalian CNS together with NADPH diaphorase Neuron 7:615-624.
12. Bredt, D.S., and S.H. Snyder (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl Acad. Sci. U.S.A. 86.9030-9033.
13. Bredt, D.S., and S.H. Snyder (1990) Isolation of nitric oxide synthase, a calmodulin requiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 87:682-685.
14. Bredt, D.S., and S.H. Snyder (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
15. Brüne, B., and E G. Lapetina (1989) Activation of a cytosolic ADP-ribosyltransferase by nitric oxide-generating agents. J. Biol. Chem. 264:8455-8458.
16. Brüning, G. (1993) Localization of NADPH-diaphorase in the brain of the chicken. J. Comp. Neurol. 334:192-208.
17. Brüning, G. (1994) Comparative localization of nitric oxide synthase in the vertebrate spinal cord. Soc. Neurosci. Abstr. 20:1419.
18. Brüning, G., S. Wiese, and B. Mayer (1994) Nitric oxide synthase in the brain of the turtle Pseudemys scripta elegans. J. Comp. Neurol. 348:183-206.
19. Caballero-Bleda, M., B. Fernández, and L. Puelles (1992) The pretectal complex of the rabbit: Distribution of acetylcholinesterase and reduced nicotinamide adenine dinucleotide diaphorase activities. Acta Anat. 144:7-16.
20. Ciani, F., V. Franceschini, and P. del Grande (1988) Histochemical and biochemical study on the acetylcholinesterase and choline acetyltransferase in the brain and spinal cord of the frog, Rana esculenta. J. Hirnforsch. 29:157-163.
21. Conway, K.M , and H. Gainer (1987) Immunocytochemical studies of vasotocin, mesotocin, and neurophysins in the Xenopus hypothalamoneurohypophysial system. J Comp. Neurol. 264:494-508.
22. Crowe, M J., T.J. Brown, J.C Bresnahan, and M.S. Beattie (1994) NADPH diaphorase (NADPH-d) reaction identifies the terminal nerve in the brain of the frog, Xenopus laevis. Soc. Neurosci. Abstr. 20:259.
23. Davis, B.J. (1991) NADPH-diaphorase activity in the olfactory system of the hamster and rat J Comp. Neurol. 314 493-511.
24. Dawson, T M , T.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Snyder (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues Proc. Natl. Acad Sci. U.S.A. 88:7797-7801.
25. Dohrn, C.S., M.A. Mullett, R.H. Price, and A.J. Beitz (1994) Distribution of nitric oxide synthase-immunoreactive interneurons in the spinal trigeminal nucleus. J. Comp. Neurol. 346:449-460.
26. Duman, R.S., R.Z. Terwilliger, and E.J Nestler (1991) Endogenous ADP-ribosylation in brain: Initial characterization of substrate proteins. J. Neurochem. 57-2124-2132.
27. Dun, N.J., S.L. Dun, S.Y. Wu, U. Forstermann, H.H.H.W. Schmidt, and L.F. Tseng (1993) Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54:845-857.
28. Ebbesson, S.O E. (1976) Morphology of the spinal cord. In R. Llinás and W. Precht (eds): Frog Neurobiology. New York: Springer Verlag, pp. 679-706.
29. Egberongbe, Y.I., S.M. Gentleman, P. Falkai, B. Bogerts, J M. Polak, and G. W. Roberts (1994) The distribution of nitric oxide synthase immunoreactivity in the human brain Neuroscience 59:561-578.
30. Eldred, W.D., T.E. Finger, and J. Nolte (1980) Central projections of the frontal organ of Rana pipiens, as demonstrated by the anterograde transport of horseradish peroxidase. Cell. Tissue Res. 211:215-222.
31. Elphick, M.R., V. Riveros-Moreno, S. Moncada, and M. O'Shea (1993a) Identification of Nitrergic Neurones in Invertebrates (Abstract). 3rd Int. Meeting on Biology of Nitric Oxide, Cologne.
32. Elphick, M.R., I C. Green, and M. O'Shea (1993b) Nitric oxide synthesis and action in an invertebrate brain. Brain Res. 619:344-346.
33. Feng, A.S., and W. Lin (1991) Differential innervation patterns of three divisions of the frog auditory midbrain (torus semicircularis). J. Comp. Neurol. 306:613-630.
34. Förstermann, U., H.H. Schmidt, J.S. Pollock, H. Sheng, J.A. Mitchell, T.D. Warner, M. Nakene, and F. Murad (1991) Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem Pharmac. 442.1849-1857.
35. Fujimori, H., and H. Pan-Hou (1991) Effect of nitric oxide on 1-(3H)glutamate binding to rat brain synaptic membranes. Brain Res. 554:355-357.
36. Furchgott, R F., and J.V Zawadzki (1980) The obligatory role of endothelial cells in the relaxion of arterial smooth muscle by acetylcholine. Nature 288:373-376.
37. Garthwaite, J. (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system TINS 14:60-68.
38. Garthwaite, J., S.L. Charles, and R. Chess-Williams (1988) Endothelium derived relaxing on activation of NMDA receptors suggest role as intracellular messenger in the brain. Nature 336:385-388.
39. Garthwaite, J., G. Garthwaite, R.M.J. Palmer, and S. Moncada (1989) NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur. J Pharmac 172:413-416.
40. González, A., and W.J.A.J. Smeets (1991) Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J. Comp. Neurol. 303:457-477.
41. Gonzalez, A., and W.J.A.J. Smeets (1992a) Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J. Comp. Neurol. 315:53-73.
42. González, A., and W.J.A.J. Smeets (1992b) Distribution of vasotocin- and mesotocin-like immunoreactivities in the brain of the South African clawed frog Xenopus laevis. J. Chem. Neuroanat. 5:465-479.
43. González, A., and W.J.A.J. Smeets (1994) Catecholamine systems in the CNS of amphibians. In Smeets, W.J.A.J., and Reiner, A. (eds): Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. Cambridge: Cambridge University Press, pp. 77-102.
44. González, A., R. Tuinhof, and W.J.A.J Smeets (1993) Distribution of tyrosine hydroxylase and dopamine immunoreactivities in the brain of the South African clawed toad Xenopus laevis. Anat. Embryol. 187:193-201.
45. González-Herná;ndez, T., B. González-González, B. Mantolán-Sarmiento, R. Méndez-Medina, R. Ferres-Torres, and G. Meyer (1994) Transient NADPH-diaphorase activity in motor nuclei of foetal human brain stem. Neurochemistry 5.758-760.
46. Grozdanovic, Z., H.G. Baumgarten, and G. Bruning (1992) Histochemistry of NADPH-diaphorase, a marker for neuronal nitric oxide synthase, in the peripheral autonomie nervous system of the mouse. Neuroscience 48:225-235.
47. Gruberg, E.R., T.E. Hughes, and H.J. Karten (1994) Synaptic interrelationships between the optic tectum and the ipsilateral nucleus isthmi in Rana pipiens. J. Comp Neurol. 339.353-364.
48. Haley, J.E., G.L. Wilcox, and P.F. Chapman (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8:1-20.
49. Hedlich, A., H.J. Lüth, L. Werner, B. Bär. U. Hanisch, and E. Winkelmann (1990) GABAerge NADPH-diaphorase-positive Martinottizellen im visuellen cortex der rate. J. Hirnforsch. 31:681-687.
50. Holmqvist, B.I., T. Östholm, P. Alm. and P. Ekstrom (1994) Nitric oxide synthase in the brain of a teleost Neurosci. Lett 171:205-208.
51. Hope, B.T., G.J. Michael. K.M. Knigge, and S.R. Vincent (1991) Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 88:2811-2814.
52. Iadecola, C (1992) Does nitric oxide mediate the increase in cerebral blood flow elicited by hypercapnia? Proc. Natl. Acad. Sci. U.S.A. 89:3913-3916
53. Ignarro, L.J., G.M. Buga, K.S. Wood, R.E. Byrns, and G. Chaudhuri (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84:9265-9269.
54. Ignarro, L J. (1990) Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: A unique transduction mechanism for transcellular signaling. Pharmacol. Toxicol. 67:1-7.
55. Ikeda, M., I. Monta, S. Murota, F Sekiguchi, T. Yuasa, and T Miyatake (1993) Cerebellar nitric oxyde synthase activity is reduced in nervous and Purkinje cell degeneration mutants but not in climbing fiber lesioned mice. Neurosci. Lett. 155:148-150.
56. Inagaki, S. S. Shiosaika, K. Takatsuki, M. Sakanaka, H. Takagi, T. Matsuzaki, and M. Tohyama (1981) Distribution of somatostatin in the frog brain, Rana catesbeiana, in relation to localization of catecholamine-containing neuron system. J. Comp. Neurol. 202:89-101.
57. Johnson, M.D., and P.M. Ma (1993) Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J. Comp. Neurol. 332:391-406.
58. Kauffinan, F C . V.M Picker, K.L Sims, and F E. Bloom (1974) Localization of nicotinamide adenine dinucleotide phosphate-dependent dehydrogenases in catecholamine-containing neurons of rat brain. J Histocnem. Cytochem. 22:20-28.
59. Kemali, M , and A. De Santis (1983) The extracranial portion of the pineal complex of the frog (frontal organ) is connected to the pineal, the hypothalamus, the brain stem and the retina. Exp. Brain Res. 53:193-196.
60. Kitchener, P.D., and J. Diamond (1993) Distribution and localization of choline acetyltransferase immunoreactivity and NADPH diaphorase reactivity in neurons within the medial septum and diagonal band of Broca in the rat basal forebrain. J. Comp Neurol. 335:1-15.
61. Koh, J., and D.W. Choi (1988) Vulnerability of cultured cortical neurons to damage by excitotoxins: Differential susceptibility of neurons containing NADPH-diaphorase. J. Neurosci. 8.2153-2163.
62. Koh, J , S. Peters, and D.W. Choi (1986) Neurons containing NADPH-diaphorase are selectively resistant to quinolinate toxicity. Science 234:73-76.
63. Kowal, N.W., R.J. Ferrante, M F. Beal, E.P J. Richardson, M.V. Sofroniew, A.C. Cuello, and J.B Martin (1987) Neuropeptide Y, somatostatin and reduced nicotinamide adenine dinucleotide phosphate diaphorase in the human striatum: A combined immunocytochemical and histochemical study. Neuroscience 20:817-828.
64. Kozniewska, E., M Oseka, and T. Stys (1992) Effects of endothelium-derived nitric oxide on cerebral circulation during normoxia and hypoxia in the rat. J. Cereb. Blood Flow Metab. 12:311-317.
65. Kuonen, D.R., M.C. Kemp, and P.J. Roberts (1988) Demonstration and biochemical characterization of rat brain NADPH-dependent diaphorase J. Neurochem. 50:1017-1025.
66. Lá;zár, G., J.L. Maderdrut, S.L. Trasti, Z Liposits, P. Tóth, T. Kozicz, and I. Merchenthaler (1993) Distribution of proneuropeptide Y-derived peptides in the brain of Rana esculenta and Xenopus laevis. J Comp. Neurol. 327:551-571
67. Leight, P.N., J.H. Connick, and T. W. Stone (1990) Distribution of NADPH-diaphorase positive cells in the rat brain. Comp. Biochem. Physiol. 97C 259-264.
68. Levine, R.L. (1980) An autoradiographic study of the retinal projection in Xenopus laevis with comparisons to Rana. J. Comp. Neurol. 189:1-29.
69. Li, Z.S , J B. Burness, H.M. Young, and G. Campbell (1992) Nitric oxide synthase immunoreactivity and NADPH diaphorase enzyme activity in neurons of the gastrointestinal tract of the toad, Bufo marinus. Arch. Histol Cytol. 55:333-350
70. Luebke, J.I., J.M. Weider, R.W, McCarley, and R W. Greene (1992) Distribution of NADPH-diaphorase positive somata in the brainstem of the monitor lizard Varanus exanthematicus. Neurosci. Lett. 148:129-132.
71. Macrae, I.M., D.A. Dawson, J L. Reid, and J McCulloch (1991) Effect of nitric oxide synthase inhibition on cerebral blood flow (CBF) in the conscious rat. Soc. Neurosci. Abstr. 17:475
72. Marín, O , A. Gonzalez, and W.J.A.J. Smeets (1995) Evidence for a mesolimbic pathway in anuran amphibians. A combined tract-tracing/immunohistochemical study. Neurosci. Lett. 190:183-186.
73. Martínez, A , M V. Riveros, J.M. Polak, S. Moncada, and P. Sesma (1994) Nitric oxide (NO) synthase immunoreactivity in the starfish Marthasterias glacialis. Cell Tissue Res. 275:599-603
74. Masino, T., and P. Grobstein (1990) Tectal connectivity in the frog Rana pipiens: Tectotegmental projections and a general analysis of topographic organization. J. Comp. Neurol. 291:103-127.
75. Mitrofanis, J. (1992) NADPH-diaphorase reactivity in the ventral and dorsal lateral geniculate nuclei of rats Visual Neurosci. 9:211-216.
76. Miyagawa, A., H. Okamura, and Y. Ibata (1994) Coexistence of oxytocin and NADPH-diaphorase in magnocellular neurons of the paraventriular and the supraoptic nuclei of the rat hypothalamus Neurosci Lett. 171:13-16.
77. Mizukawa, K , P.L. McGeer, S.R. Vincent, and E.G. McGeer (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J. Comp. Neurol. 279:281-311.
78. Moncada, S., R.M J. Palmer, and EA Higgs (1991) Nitric oxide. Physiology, pathophysiology and pharmacology. Am. Soc. Pharmac. Exp. Ther. 43:109-143.
79. Mufson, E.J , D.R. Bradi, and R.G. Carey (1990) Reduced nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry in the hippocampal formation of the new world monkey (Satmiri sciureus). Brain Res. 516:237-247.
80. Muñoz, A., M. Muñoz, A. González, and H.J. ten Donkelaar (1994) Spinothalamic projections in amphibians as revealed with anterograde tracing techniques. Neurosci. Lett. 171:81-84.
81. Muñoz. A., M Muñoz, A González, and H.J. ten Donkelaar (1995) The anuran dorsal column nucleus: organization, immunohistochemical characterization and fiber connections in Rana perezi and Xenopus laevis. J. Comp. Neurol 363:197-220.
82. Munoz, M., A. Muñoz, O Marín, and A. Gonzalez (1994) Primary afferents and second order projections of the trigeminal system in a frog (Rana ridibunda). Eur. J. Morphol. 35:288-292.
83. Nagai, T., P L. McGeer, and E.G. McGeer (1983) Distribution of GABA-T-intensive neurons in the rat forebrain and midbrain. J. Comp. Neurol 218:220-238.
84. Neary, T.J., and W. Wilczynski (1980) Descending inputs to the optic tectum in ranid frogs. Soc, Neurosci. Abst. 6:629.
85. Neary, T.J., and R.G. Northcutt (1983) Nuclear organization of the bullfrog diencephalon. J. Comp. Neurol. 213:262-278.
86. Northcutt, R.G., and M. Ronan (1992) Afferent and efferent connections of the bullfrog medial pallium. Brain Behav. Evol. 40:1-16.
87. Onstott, D., B. Mayer, and A.J. Beitz (1993) Nitric oxide synthase immunoreactive neurons anatomically define a longitudinal dorsolateral column within the midbrain periaqueductal gray of the rat: Analysis using laser confocal microscopy. Brain Res. 610:317-324.
88. Palmer, R.M.J., A.G. Ferrige, and S. Moncada (1987) Nitric oxide release accounts for the biological activity of endothelium derived relaxing factor. Nature 327:524-526.
89. Palmer, R.M.J., D.D Rees, D.S. Ashton, and S. Moncada (1988) L-Arginine is the physiological precursor of the formation of nitric oxide in endothelium dependent relaxation. Biochem, Biophys. Res. Commun. 153:1251-1256.
90. Panzica, G C., R. Arévalo, F. Sánchez, J.R. Alonso, N Aste, P.C. Viglietti, J Aijón, and R. Vázquez (1994) Topographical distribution of reduced nicotinamide adenine dinucleotide phosphate-diaphorase in the brain of the Japanese quail J. Comp. Neurol. 342:97-114
91. Pitzer, M.R., and D. Wirtshafter (1993) The distribution of nitric oxide synthase in the frog brain. Soc. Neurosci. Abstr. 19:161.
92. Porteros, A., J.R. Alonso, R. Arévalo, E. García-Ojeda, C. Crespo, and J Aijón (1994) Histochemical localization of NADPH-diaphorase in the rat accessory olfactory bulb. Chem. Senses 19 413-424.
93. Potter, H.D. (1965) Mesencephalic auditory region of the bullfrog. J. Neurophysiol. 28:1132-1154.
94. Pow, D V. (1992) NADPH-diaphorase (nitric oxide synthase) staining in the rat supraoptic nucleus is activity-dependent: Possible functional implications. J. Neuroendocrinol. 4:377-380.
95. Powers, A.S., and I.S Giusti (1993) Distribution of NADPH-diaphorase-positive neurons in the brains of turtles. Soc. Neurosci. Abstr. 19.89.
96. Radomski, M.W., J.F. Martin, and S. Moncada (1991) Synthesis of nitric oxide by the haemocytes of the american horseshoe crab (Limulus polyphemus) Phil. Trans R. Soc. Lond. B. 334:129-133.
97. Regidor, J., and L. Poch (1988) Histochemical analysis of the lizard cortex An acetylcholinesterase, cytochrome oxidase and NADPH-diaphorase study. In W.K. Schwerdtfeger and W.J.A.J. Smeets (eds): The Forebrain of Reptiles. Basel: Karger, pp. 77-84.
98. Reiner, P.B., and S.R. Vincent (1987) Topographic relations of cholinergic and noradrenergic neurons in the feline pontomesencephalic tegmentum An immunohistochemical study Brain Res. Bull. 19:705-714.
99. Rokoski, R , P.R. Vulliet, and D.B. Glass (1987) Phosphorylation of tyrosine hydroxylase by cyclic GMP-dependent protein kinase. J. Neurochem. 48 040-845.
100. Sagar, SM., and D. Ferreiro (1987) NADPH diaphorase activity in the posterior pituitary: Relation to neuronal function Brain Res. 400:348-352
101. Sajin, B , N. Sestan, and B. Dmitrovic (1992) Compartmentalization of NADPH-diaphorase staining in the developing human striatum. Neurosci. Lett. 140:117-120.
102. Sanchez, F., J.R Alonso, R. Arévalo, E. Blanco, J. Aijón, and R. Vázquez (1994) Coexistence of NADPH-diaphorase with vasopressin and oxytocin in the hypothalamic magnocellular neurosecretory nuclei of the rat. Cell Tissue Res. 276:31-34.
103. Sarrafizadeh, F., T. Braun, and J.C. Houk (1993) Histochemical mapping of NADPH-diaphorase in the turtle brain. Soc. Neurosci. Abstr. 19:996.
104. Sato, T (1990a) Immunohistochemical demonstration of NADPH-diaphorase activity in the pineal organ of the frog (Rana esculenta), but not in the pmea! organ of the rat. Arch. Histol. Cytol. 53:141-146.
105. Sato, T (1990b) A method for the demonstration of NADPH-diaphorase activity in anuran species using unfixed retina wholemounts. Arch. Histol. Cytol. 54:207-211.
106. Scaha, F., and K. Gregory (1970) Retinofugal projections in the frog. Location of the postsynaptic neurons Brain Behav. Evol. 3:16-29.
107. Schmidt, H.H.H.W., and F. Murad (1991) Purification and characterization of a human NO synthase Biochem. Biophys. Res. Commun. 181:1372-1377
108. Schmidt, H.H.H.W., G.D. Gagne, M. Nakane, J.S. Pollock, M.F. Miller, and F Murad (1992) Mapping of nitric oxide synthase in the rat suggest frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneuronal functions for nitrinergic signal transduction. J. Histochem Cytochem. 40.1439-1456.
109. Schober, A.K., K. Brauer, and H. Luppa (1989) Alternate coexistence of NADPH-diaphorase with choline acetyltransferase or somatostatin in the rat neostriatum and basal forebrain. Acta Histochem. Cytochem. 22:669-674.
110. Schober, A,. C.R. Malz, and D.L. Meyer (1993) Enzymehistochemical demonstration of nitric oxide synthase in the diencephalon of the rainbow trout (Oncorhynchus mickiss). Neurosci. Lett. 151:67-70.
111. Schober, A., C.R. Malz, W. Schober, and D.L. Meyer (1994a) NADPH-diaphorase in the central nervous system of the larval lamprey (Lampetra planeri). J. Comp. Neurol. 345:94-104
112. Schober, A., D.L. Meyer, and C.S von Barttheld (1994b) Central projections of the nervous terminalis and the nervous praeopticus in the lungfish brain revealed by nitric oxide synthase J. Comp. Neurol. 349:1-19
113. Schuman, E M., and D.V. Madison (1991) A requirement for the intracellular messenger nitric oxide in long term potentiation. Science 254:1503-1506.
114. Sestan, N., and I. Kostovic (1994) Histochemical localization of nitric oxide synthase in the CNS. TINS 17:105-106
115. Shibuki, K., and D. Okada (1991) Endogenous nitric oxide release required for long term depression in the cerebellum Nature 349:326-328.
116. Smeets, W.J.A.J., and A. González (1990) Are putative dopamine-accumulating cell bodies in the periventricular organ a primitive brain character of non-mammalian vertebrates? Neurosci. Lett. 114.248-252.
117. Snyder, S.H., and D.S. Bredt (1991) Nitric oxide as a neuronal messenger. Trends Pharmac. Sci. 12:125-128.
118. Snyder, S.H. (1992) Nitric oxide: first in a new class of neurotransmitters? Science 257:494-496.
119. Sternberger, L A. (1979) Immunocytochemistry. New York: John Wiley and Sons.
120. Swanson, L.W. (1982) The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9:321-353.
121. Székely, G., and G. Làzâr (1976) Cellular and synaptic architecture of the optic tectum. In R Llinás and W. Precht (eds): Frog Neurobiology New York: Springer Verlag, pp. 407-434.
122. ten Donkelaar, H.J. (1982) Organization of descending pathways to the spinal cord in amphibians and reptiles. In H.G.J.M. Kuypers and G.F. Martin (eds): Progress in Brain Research, Vol. 57: Descending Pathways to the Spinal Cord. Amsterdam, Elsevier, pp. 25-67.
123. Thomas, E., and A.G.E. Pearse (1964) The solitary active cells: Histochemical demonstration of damage-resistent nerve cells with a TNP-diaphorase reaction. Acta Neuropath. 3:238-249.
124. Tóth, P., G. Csank, and G. Lázár (1985) Morphology of the cells of origin of descending pathways to the spinal cord in Rana esculenta. A tracing study using cobaltic-lysine complex. J. Hirnforsch. 26:365-383.
125. Tuinhof, R., C. Artero, A. Fasolo, M.F Franzoni, H.J ten Donkelaar, P.G.P. Wismans, and E.W. Roubos (1994) Involvement of retinohypothalamic input, suprachiasmatic nucleus, magnocellular nucleus and locus coeruleus in control of melanotrope cells of Xenopus laevis. Neuroscience 61:411-420.
126. Valtschanoff, J.G., R.J. Weinberg, and A. Rustioni (1992) NADPH diaphorase in the spinal cord of rats. J. Comp. Neurol. 321:209-222.
127. Valtschanoff, J G., R.J. Weinberg, and A. Rustioni (1993) Amino acid immunoreactivity in corticospinal terminals. Exp. Brain Res. 93:95-103.
128. Viglietti-Panzica, C. (1986) Immunohistochemical study of the distribution of vasotocin reacting neurons in avian diencephalon. J. Hirnforsch. 27:559-566.
129. Villalba, R.M , R. Martínez-Murillo, I. Blasco, F.J. Alvarez, and J. Rodrigo (1988) C-PON containing neurons in the rat striatum are also positive for NADPH-diaphorase activity: A light microscopic study. Brain Res. 462.359-362.
130. Villar, M J , S. Ceccatelli, M. Rõnnqvist, and T. Hökfelt (1994) Nitric oxide synthase increases in hypothalamic magnocellular neurons after salt loading in the rat: An immunohistochemical and in situ hybridization study. Brain Res. 644:273-281.
131. Vincent, S.R. (1994) Nitric oxide: A radical neurotransmitter in the central nervous system. Prog. Neurobiol. 42.129-160.
132. Vincent, S.R., and D.T. Hope (1992) Neurons that say NO. TINS 15:108-113.
133. Vincent, S R , and H. Kimura (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
134. Vincent, S.R., O. Johansson, T. Hokfelt, L. Skirboll, R.P. Elde, L. Terenius, J. Kimmel, and M. Goldstein (1983a) NADPH-diaphorase: A selective histochemical marker for striatal neurons containing both somatostatin and avian pancreatic polipeptide (APP)-like immunoreactivities. J. Comp. Neurol. 217:252-263.
135. Vincent, S.R., K. Satoh, D.M. Armstrong, and H.G. Fibiger (1983b) NADPH-diaphorase. a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci. Lett. 43:31-36.
136. Vincent, S.R , K. Satoh, D M. Armstrong, P. Panula, W Vale, and H.C. Fibiger (1986) Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience 17:167-182.
137. Wilczynski, W. (1981) Afferents to the midbrain auditory center in the bullfrog Rana catesbeiana. J. Comp. Neurol. 198:421-433.
138. Wilczynski, W., and RG Northcutt (1983) Connections of the bullfrog striatum: Afferent organization. J, Comp. Neurol. 214:321-332.
139. Williams, M.B., X. Li, and R.S. Jope (1991) Modulation of endogenous ADP-ribosylation in brain. Soc. Neurosci. Abstr. 17:96.
140. Young, H.M., J.B. Furness, C Shuttleworth, D.S. Bredt, and S.H. Snyder (1992) Co-localization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guinea-pig intestine. Histochemistry 97:375-378.