Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-21T05:32:37.271Z Has data issue: false hasContentIssue false

NADPH-diaphorase reactivity in ciliary ganglion neurons: A comparison of distributions in the pigeon, cat, and monkey

Published online by Cambridge University Press:  02 June 2009

Wensi Sun
Affiliation:
Department of Anatomy, University of Mississippi Medical Center, Jackson
Jonathan T. Erichsen
Affiliation:
Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook
Paul J. May
Affiliation:
Department of Anatomy, University of Mississippi Medical Center, Jackson Department of Ophthalmology, University of Mississippi Medical Center, Jackson

Abstract

Ciliary ganglia from the pigeon, cat, and monkey were investigated for the presence of NADPH-diaphorase reactivity by use of a standard histochemical method. In the pigeon, where the ganglion is known to control lens and pupil function, and the choroidal vasculature, about one-third of the ganglion cells were densely stained and most other somata were lightly stained. In some cases, preganglionic terminals with a cap-like morphology were also darkly stained. The pattern of NADPH-diaphorase staining in mammals was very different from that seen in pigeons. In both mammalian species, where the ganglion is known to control lens and pupil function, a small number (less than 2%) of the ganglion cells were shown to be densely NADPH-diaphorase positive, revealing their neuronal processes. The presence of NADPH-diaphorase positive cells in pigeon, cat, and monkey ciliary ganglia suggests that nitric oxide may be used for intercellular communication in this ganglion, or in light of the known importance of nitric oxide in vascular control, some of these positive neurons may participate in the control of choroidal vasodilation.

Type
Short Communications
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bohme, G.A., Bon, C., Stutzmann, J.-M., Doble, A. & Blanchard, J.-C. (1991). Possible involvement of nitric oxide in long-term potentiation. European Journal of Pharmacology 199, 379381.CrossRefGoogle ScholarPubMed
Bredt, D.S., Hwang, P.M. & Snyder, S.H. (1990). Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347, 768770.Google Scholar
Bredt, D.S. & Snyder, S.H. (1992). Nitric oxide, a novel neuronal messenger. Neuron 8, 311.CrossRefGoogle ScholarPubMed
Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. & Snyder, S.H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences of the U.S.A. 88, 77977801.CrossRefGoogle ScholarPubMed
Erichsen, J.T., Karten, H.J., Eldred, W.D. & Brecha, N.C. (1982). Localization of substance P-like and enkephalin-like immunoreactivity within preganglionic terminals of the avian ciliary ganglion: Light and electron microscopy. Journal of Neuroscience 2, 9941003.CrossRefGoogle ScholarPubMed
Fitzgerald, M.E.C., Vana, B.A. & Reiner, A. (1990). Control of choroidal blood flow by the nucleus of Edinger-Westphal: A laser-Doppler study. Investigative Ophthalmology and Visual Science 31, 24832492.Google ScholarPubMed
Fitzgerald, M.E.C. & Reiner, A. (1993). NADPH-diaphorase positive neurons and fibers in the ciliary ganglion and choroid of the pigeon. Society for Neuroscience Abstracts 19, 1202.Google Scholar
Gray, D.B., Scranton, V. & Pilar, G. (1993). Somatostatin inhibits transmitter release via nitric oxide and cGMP-dependent kinase in choroid nerve terminals. Society for Neuroscience Abstracts 19, 1177.Google Scholar
Grimes, P. & Von Sallmann, L. (1960). Comparative anatomy of the ciliary nerve. Archives of Ophthalmology 64, 111121.CrossRefGoogle Scholar
Grozdanovic, A., Baumgarten, H.G. & Bruning, G. (1992). Histochemistry of NADPH-diaphorase, a marker for neuronal nitric oxide synthase, in the peripheral autonomic nervous system of the mouse. Neuroscience 48, 225235.CrossRefGoogle ScholarPubMed
Hess, A. (1965). Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. Journal of Cell Biology 25, 119.CrossRefGoogle ScholarPubMed
Hope, B.T., Michael, G.J., Knigge, K.M. & Vincent, S.R. (1991). Neuronal NADPH-diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences of the U.S.A. 88, 28112814.CrossRefGoogle ScholarPubMed
Hope, B.T. & Vincent, S.R. (1989). Histochemical characterization of neuronal NADPH-diaphorase. Journal of Histochemistry and Cytochemistry 37, 653661.Google Scholar
Ignarro, L.J., Bush, P.A., Buga, C.M., Wood, K.S., Fukuto, J.M. & Rajfer, J. (1990). Nitric oxide and cyclic GMP formation upon electrical field stimulation cause relaxation of corpus cavernosum smooth muscle. Biochemical and Biophysical Research Communications 170, 843850.CrossRefGoogle ScholarPubMed
Khurana, G. & Bennett, M.R. (1993). Nitric oxide and arachidonic acid modulation of calcium currents in postganglionic neurons of avian cultured ciliary ganglia. British Journal of Pharmacology 109, 480485.CrossRefGoogle ScholarPubMed
Kuchiiwa, S., Kuchuwa, T. & Suzuki, T. (1989). Comparative anatomy of the accessory ciliary ganglion in mammals. Anatomy and Embryology 180, 199205.CrossRefGoogle ScholarPubMed
Mann, R.M., Riva, C.E., Cranstoun, S.D., Stone, R.A. & Barnes, G.E. (1993). Nitric oxide and choroidal blood flow (chbf) regulation. Investigative Ophthalmology and Visual Science 34, 1394.Google Scholar
May, P.J. & Warren, S. (1993). Ultrastructure of the macaque ciliary ganglion. Journal of Neurocytology 22, 10731095.CrossRefGoogle ScholarPubMed
O'Dell, T.J., Hawkins, R.D., Kandel, E.R. & Arancia, O. (1991). Tests of the roles of two diffusible substances in LTP: Evidence for nitric oxide as a possible early retrograde messenger. Proceedings of the National Academy of Science of the U.S.A. 88, 1128511289.CrossRefGoogle ScholarPubMed
Reiner, A., Karten, H.J., Gamlin, P.D.R. & Erichsen, J.T. (1983). Parasympathetic control of ocular function: Functional subdivisions and connections of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6, 140145.Google Scholar
Reiner, A., Erichsen, J.T., Cabot, J.B., Evinger, C., Fitzgerald, M.E.C. & Karten, H.J. (1991). Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion. Visual Neuroscience 6, 451472.Google Scholar
Scott, T.R.D. & Bennett, M.R. (1993 a). The effects of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. British Journal of Pharmacology 110, 461469.CrossRefGoogle ScholarPubMed
Scott, T.R.D. & Bennett, M.R. (1993 b). The effect of nitric oxide on the efficacy of synaptic transmission through the chick ciliary ganglion. British Journal of Pharmacology 110, 627632.CrossRefGoogle ScholarPubMed
Shibuki, K. & Okada, D. (1991). Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 394, 326328.Google Scholar
Stanforth, D.A., Zhang, J. & Rao, N.A. (1993). Distribution of NADPH-diaphorase in ocular tissues. Investigative Ophthalmology and Visual Science 34, 1282.Google Scholar
Sun, W., May, P.J. & Erichsen, J.T. (1993). NADPH-diaphorase positive neurons in the ciliary ganglion. Society for Neuroscience Abstracts 19, 347.Google Scholar
Toda, N. & Okamura, T. (1990). Possible role of nitric oxide in transmitting information from vasodilator nerve to cerebroarterial muscle. Biochemical and Biophysical Research Communications 170, 308313.Google Scholar
Warwick, R. (1954). The ocular parasympathetic nerve supply and its mesencephalic sources. Journal of Anatomy 88, 7193.Google Scholar
Yamamoto, R., Bredt, D.S., Snyder, S.H. & Stone, R.A. (1993). The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54, 189200.CrossRefGoogle ScholarPubMed