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Origin and Function of Nitrergic Nerves in the Human Eye: Morphological Aspects

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Nitric Oxide in the Eye

Abstract

Signals transmitted by the ocular part of the autonomic nervous system regulate important auxiliary systems that are necessary to maintain the basic function of the eye, the perception of light. A considerable number of physiological and morphological studies during the past few years have provided strong evidence that numerous ocular autonomic nerves contain the neuronal isoform of nitric oxide synthase (NOS), the enzyme that synthesizes nitric oxide (NO), and likely use NO as a neurotransmitter. In the eye, such nitrergic nerves are involved in regulating the blood supply to the various intraocular tissues and appear to take part in accommodation and the circulation of aqueous humor.

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References

  • Alder VA, Cringle SJ, Constable IJ (1983) The retinal oxygen profile in cats. Invest Ophthalmol Vis Sci 24:30–36

    PubMed  CAS  Google Scholar 

  • Alm A (1992) Ocular circulation. In: Hart WMJ (ed) Adler’s physiology of the eye. Mosby-Year Book, St. Louis, pp 198–227

    Google Scholar 

  • Alm A, Bill A (1970) Blood flow and oxygen extraction in the cat uvea at normal and high intraocular pressures. Acta Physiol Scand 80:19–28

    Article  PubMed  CAS  Google Scholar 

  • Alm A, Bill A (1972) The oxygen supply to the retina. II. Effects of high intraocular pressure and of increased arterial carbon dioxide tension on uveal and retinal blood flow in cats: a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Acta Physiol Scand 84:306–319

    Article  PubMed  CAS  Google Scholar 

  • Alm A, Bill A (1973) Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus):a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res 15:15–29

    Article  PubMed  CAS  Google Scholar 

  • Ashton N (1952) Anatomical study of Schlemm’s canal and aqueous veins by means of neoprene casts. II. Aqueous veins. Br J Ophthalmol 36:265

    Article  PubMed  CAS  Google Scholar 

  • Bates TE, Loesch A, Burnstock G, Clark JB (1996) Mitochondrial nitric oxide synthase: a ubiquitous regulator of oxidative phosphorylation? Biochem Biophys Res Commun 218:40–44

    Article  PubMed  CAS  Google Scholar 

  • Beesley JE (1995) Histochemical methods for detecting nitric oxide synthase. Histochem J 27:757–769

    PubMed  CAS  Google Scholar 

  • Bergua A (1995) Nitrergische Reaktivtät in den Endothelzellen der menschlichen uvealen Gefässe. Klin Monatsbl Augenheilkd 206:115–121

    Article  PubMed  CAS  Google Scholar 

  • Bergua A (1996) NADPH-diaphorase-positive innervation of the central retinal artery of the human optic nerve. Exp Eye Res 63(Suppl):S.142

    Google Scholar 

  • Bergua A, Jünnemann A, Naumann GOH (1993) NADPH-D reactive choroidal ganglion cells in the human eye. Klin Monatsbl Augenheilkd 203:77–82

    Article  PubMed  CAS  Google Scholar 

  • Bergua A, Neuhuber WL, Naumann GOH (1994) Visualization of human choroidal ganglion cells with the supravital fluorescent dye 4-(4-diethylaminostyryl)-N-methylpyrid-ium iodide. Ophthalmic Res 26:290–295

    Article  PubMed  CAS  Google Scholar 

  • Bergua A, Neuhuber WL, Mayer B (1995) Comparative anatomy of nitrinergic innervation in avian choroid. Invest Ophthalmol Vis Sci 36:S121 (ARVO abstracts)

    Google Scholar 

  • Bergua A, Mayer B, Neuhuber WL (1996) Nitrergic and VIPergic neurons in the choroid and ciliary ganglion of the duck Anis carina. Anat Embryol (Berl) 193:239–248

    Article  CAS  Google Scholar 

  • Bill A (1967) Effects of atropine and pilocarpine on aqueous humor dynamics in cynomol-gus monkeys (Macaca irus). Exp Eye Res 6:120–125

    Article  PubMed  CAS  Google Scholar 

  • Bill A (1968) Capillary permeability to and extravascular dynamics of myoglobin, albumin and gammaglobulin in the uvea. Acta Physiol Scand 73:204–219

    Article  PubMed  CAS  Google Scholar 

  • Bill A (1985) Some aspects of the ocular circulation: Friedenwald lecture. Invest Ophthalmol Vis Sci 26:410–424

    PubMed  CAS  Google Scholar 

  • Bill A (1991) The 1990 Endre Balazs lecture: effects of some neuropeptides on the uvea. Exp Eye Res 53:3–11

    Article  CAS  Google Scholar 

  • Bill A, Törnquist P, Alm A (1980) The permeability of the ocular vessels. Trans Ophthalmol Soc UK 100:332–336

    PubMed  CAS  Google Scholar 

  • Bito LZ, Miranda OC (1987) On the evolution of visual accommodation, the non-accommodating eye and presbyopia. In: De Vincentiis M (ed) The fundamental aging processes of the eye. Fondazione “Giorgio Ronchi” LX,Tipographia Baccini & Chiappi, Florence, pp 58–97

    Google Scholar 

  • Bito LZ, Miranda OC (1989) Accommodation and presbyopia. In: Reinecke RD (ed) Ophthalmology annual. Lippincott-Raven, New York, pp 103–127

    Google Scholar 

  • Blottner D, Grozdanovic Z, Gossrau R (1995) Histochemistry of nitric oxide synthase in the nervous system. Histochem J 27:785–811

    PubMed  CAS  Google Scholar 

  • Boeke J (1933) Innervationsstudien. III. Die Nervenversorgung des M. ciliaris und des sphincter iridis bei Säugern und Vögeln. Z Mikrosk Anat Forsch 33:233–275

    Google Scholar 

  • Bredt DS, Hwang PM, Snyder SH (1992) Localization of nitric oxide indicating a neuronal role for nitric oxide. Nature 347:768–770

    Article  Google Scholar 

  • Bryson JM, Wolter JR, O’Keefe NT (1966) Ganglion cells in the human ciliary body. Arch Ophthalmol 75:57–60

    PubMed  CAS  Google Scholar 

  • Butler JM, Ruskell GL, Cole DF, Unger WG, Zhang SQ, Blank MA, McGregor GP, Bloom SR (1984) Effects of VIIth (facial) nerve degeneration on vasoactive intestinal polypeptide and substance P levels in ocular and orbital tissues of the rabbit. Exp Eye Res 39:523–532

    Article  PubMed  CAS  Google Scholar 

  • Campbell FW, Robson JG, Westheimer G (1959) Fluctuations in accommodation under steady viewing conditions. J Physiol (Lond) 145:579–594

    CAS  Google Scholar 

  • Castro-Correira J (1967) Studies on the innervation of the uveal tract. Ophthalmologica 154:497–520

    Article  Google Scholar 

  • Chakravarthy U, Stitt AW, McNally J, Bailie JR, Hoey EM, Duprex P (1994) Nitric oxide synthase activity and expression in retinal capillary endothelial cells and pericytes. Curr Eye Res 14:285–294

    Article  Google Scholar 

  • Chin NB, Ishikawa S, Lappin H, Davidowitz J, Breinin GM (1968) Accommodation in monkeys induced by midbrain stimulation. Invest Ophthalmol Vis Sci 7:386–396

    CAS  Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi PM, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801

    Article  PubMed  CAS  Google Scholar 

  • De Stefano ME, Luzzatto AC, Mugnaini E (1993) Neuronal ultrastructure and somatostatin immunolocalization in the ciliary ganglion of chicken and quail. J Neurocytol 22:868–892

    Article  PubMed  Google Scholar 

  • Deussen A, Sonntag M, Vogel R (1993) L-Arginine-derived nitric oxide: a major determinant of uveal blood flow. Exp Eye Res 57:129–134

    Article  PubMed  CAS  Google Scholar 

  • Ding YQ, Takada M, Kaneko T, Mizuno M (1995) Colocalization of vasoactive intestinal polypeptide and nitric oxide in penis-innervating neurons in the major pelvic ganglion of the rat. Neuroreport 22:129–131

    CAS  Google Scholar 

  • Donati G, Pournaras CJ, Munoz J-L, Poitry S, Poitry-Yamate CL, Tsacopoulos M (1995) Nitric oxide controls arteriolar tone in the retina of the miniature pig. Invest Ophthalmol Vis Sci 36:2228–2237

    PubMed  CAS  Google Scholar 

  • Dryer SE, Chiapinelli VA (1985) Properties of choroid and ciliary neurons in the avian ciliary ganglion and evidence for substance P as a neurotransmitter. J Neurosci 5:2654–2661

    PubMed  CAS  Google Scholar 

  • Duke-Elder S (1958) System of ophthalmology. Vol. I. The eye in evolution. Mosby, St. Louis

    Google Scholar 

  • Ehinger B, Sundler F, Uddman R (1983) Functional morphology in two parasympathetic ganglia: the ciliary and the pterygopalatine. In: Elfvin L-G (ed) Autonomic ganglia. Wiley, New York, pp 97–123

    Google Scholar 

  • Elsas T, Edvinsson L, Sundler F, Uddman R (1994) Neuronal pathways to the rat conjunctiva revealed by retrograde tracing and immunocytochemistry. Exp Eye Res 58:117–126

    Article  PubMed  CAS  Google Scholar 

  • Feeney L, Hogan MJ (1961) Electron microscopy of the human choroid. II. The choroidal nerves. Am J Ophthalmol 51:1072–1083

    PubMed  CAS  Google Scholar 

  • Fine BS, Yanoff M, Stone RA (1981) A clinicopathologic study of four cases of primary open-angle glaucoma compared to normal eyes. Am J Ophthalmol 91:88–105

    PubMed  CAS  Google Scholar 

  • Fischer F (1933) Entwicklungsgeschichtliche und anatomische Studien über den Skleral-sporn im menschlichen Auge. Graefes Arch Ophthalmol 133:318–358

    Article  Google Scholar 

  • Fitzgerald MEC, Reiner A (1993) NADPH-diaphorase positive neurons and fibers in the ciliary ganglion and choroid of the pigeon. Soc Neurosci Abstr 19:1202 (abstract)

    Google Scholar 

  • Flügel C, Bárány EH, Lütjen-Drecoll E (1990) Histochemical differences within the ciliary muscle and its function in accommodation. Exp Eye Res 50:219–226

    Article  PubMed  Google Scholar 

  • Flügel C, Tamm E, Lütjen-Drecoll E (1991) Different cell populations in bovine trabecular meshwork: an ultrastructural and immunohistochemical study. Exp Eye Res 52:681–690

    Article  PubMed  Google Scholar 

  • Flügel C, Tamm ER, Mayer B, Lütjen-Drecoll E (1994) Species differences in choroidal vasodilative innervation: evidence for specific intrinsic nitrergic and VIP-positive neurons in the human eye. Invest Ophthalmol Vis Sci 35:592–599

    PubMed  Google Scholar 

  • Flügel-Koch C, Kaufman PL, Lütjen-Drecoll E (1994) Association of choroidal ganglion cell plexus with the fovea centralis. Invest Ophthalmol Vis Sci 35:4268–4272

    PubMed  Google Scholar 

  • Flügel-Koch C, May CA, Lütjen-Drecoll E (1996) Presence of a contractile cell network in the human choroid. Ophthalmologica 210:296–302

    Article  PubMed  Google Scholar 

  • Frank RN, Turczyn TJ, Das A (1990) Pericyte coverage of retinal and cerebral arteries. Invest Ophthalmol Vis Sci 31:999–1007

    PubMed  CAS  Google Scholar 

  • Franz V (1934) Vergleichende Anatomie des Wirbeltierauges. In: Bolk L, Göppert E, Kallius E, Lubasch W (eds) Handbuch der vergleichenden Anatomie der Wirbeltiere. Vol. II/2. Urban & Schwarzenberg, Berlin, pp 1–1202

    Google Scholar 

  • Funk R (1991) Ultrastructure of the ciliary process vasculature in cynomolgus monkeys. Exp Eye Res 53:461–469

    Article  PubMed  CAS  Google Scholar 

  • Funk R, Rohen JW (1988) SEM studies of the functional morphology of the ciliary process vasculature in the cynomolgus monkey: reactions after application of epinephrine. Exp Eye Res 47:653–663

    Article  PubMed  CAS  Google Scholar 

  • Funk R, Rohen JW (1990) Scanning electron microscopic study on the vasculature of the human anterior eye segment, especially with respect to the ciliary processes. Exp Eye Res 51:651–661

    Article  PubMed  CAS  Google Scholar 

  • Funk RHW, Rohen JW (1995) Scanning electron microscopic study of episcleral arteriovenous anastomoses in the owl and cynomolgus monkey. Curr Eye Res 15: 321–327

    Article  Google Scholar 

  • Funk RHW, Mayer B, Wörl J (1994) Nitrergic innervation and nitrergic cells in arteriovenous anastomoses. Cell Tissue Res 277:477–484

    Article  PubMed  CAS  Google Scholar 

  • Funk RHW, Gehr J, Rohen JW (1996) Short-term hemodynamic changes in episcleral arteriovenous anastomoses correlate with venous pressure and IOP changes in the albino rabbit. Curr Eye Res 15:87–93

    Article  PubMed  CAS  Google Scholar 

  • Furness JB, Bornstein JC, Trussell DC (1988) Shapes of nerve cells in the myenteric plexus of the guinea-pig small intestine revealed by the intracellular injection of dye. Cell Tissue Res 254:561–571

    Article  PubMed  CAS  Google Scholar 

  • Gaasterland DE, Jocson VL, Sears ML (1970) Channels of aqueous outflow and related blood vessels. II. Episcleral arteriovenous anastomoses in the rhesus monkey eye (Macaca mulatta). Arch Ophthalmol 84:770–775

    PubMed  CAS  Google Scholar 

  • Goh Y, Hotehama Y, Mishima HK (1995) Characterization of ciliary muscle relaxation by various agents in cats. Invest Ophthalmol Vis Sci 36:1188–1192

    PubMed  CAS  Google Scholar 

  • Haefliger IO, Zschauer A, Anderson DR (1994) Relaxation of retinal pericyte contractile tone through the nitric oxid-cyclic guanosine monophosphate pathway. Invest Ophthalmol Vis Sci 35:991–997

    PubMed  CAS  Google Scholar 

  • Hirano N (1941) Nervöse Innervation des Corpus ciliare des Menschen. Graefes Arch Ophthalmol 142:549–559

    Article  Google Scholar 

  • Hope BC, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa T (1962) Fine structure of the human ciliary muscle. Invest Ophthalmol Vis Sci 1:587–608

    CAS  Google Scholar 

  • Iwanoff A (1874) Der Uvealtractus. In: Graefe A, Saemisch T (eds) Handbuch der gesamten Augenheilkunde. Engelmann, Leipzig, pp 265–287

    Google Scholar 

  • Jocson VL, Grant WM (1965) Interconnections of blood vessels and aqueous vessels in human eyes. Arch Ophthalmol 73:707–720

    PubMed  CAS  Google Scholar 

  • Jocson VL, Sears ML (1968) Channels of aqueous outflow and related blood vessels. I. Macaca mulatta (rhesus). Arch Ophthalmol 80:104–114

    PubMed  CAS  Google Scholar 

  • Jocson VL, Sears ML (1969) Channels of aqueous outflow and related blood vessels. II. Cercopithecus ethiops (Ethiopian green or green vervet). Arch Ophthalmol 81:244–253

    PubMed  CAS  Google Scholar 

  • Kaufman PL (1992) Accommodation and presbyopia. In: Hart WMJ (ed) Adler’s physiology of the eye. Mosby-Year Book, St. Louis, pp 391–411

    Google Scholar 

  • Kirch W, Neuhuber W, Tamm ER (1995) Immunohistochemical localization of neuropeptides in the human ciliary ganglion. Brain Res 681:229–234

    Article  PubMed  CAS  Google Scholar 

  • Kirch W, Horneber M, Tamm ER (1996) Characterization of meibomian gland innervation in the cynomolgus monkey (Macaca fascicularis). Anat Embryol (Berl) 193:365–375

    Article  CAS  Google Scholar 

  • Klatt P, Heinzel B, John M, Kastner M, Böhme E, Mayer B (1992) Ca2/cahnodulin-dependent cytochrome-c reductase activity of brain nitric oxide synthase. J Biol Chem 267:11374–11378

    PubMed  CAS  Google Scholar 

  • Kobzik L, Bredt DS, Lowenstein CJ, Drazen J, Gaston B, Sugarbaker D, Stamler JS (1993) Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization. Am J Respir Cell Mol Biol 9:371–377

    PubMed  CAS  Google Scholar 

  • Kobzik L, Stringer B, Balligand J-L, Reid MB, Stamler JS (1995) Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationships. Biochem Biophys Res Commun 211:375–381

    Article  PubMed  CAS  Google Scholar 

  • Krause W (1861) Ganglienzellen im Orbiculus ciliaris. In: Krause W (ed) Anatomische Untersuchungen. Hannover, p 91

    Google Scholar 

  • Krümmel H (1938) Die Nerven des menschlichen Ziliarkörpers. Graefes Arch Ophthalmol 138:845–865

    Article  Google Scholar 

  • Kubes P (1992) Nitric oxide modulates epithelial permeability in the feline small intestine. Am J Physiol 262:G1138–G1142

    PubMed  CAS  Google Scholar 

  • Kummer W, Fischer A, Mundel P, Mayer B, Hoba B, Philippin B, Preissler U (1992) Nitric-oxide synthase in VIP-containing vasodilator nerve-fibers in the guinea-pig. Neuroreport 3:653–655

    Article  PubMed  CAS  Google Scholar 

  • Kupfer C (1962) Relationship of ciliary body meridional muscle and corneoscleral trabecular meshwork. Arch Ophthalmol 68:132–136

    Google Scholar 

  • Kurus E (1955) Über ein Ganglienzellsystem der menschlichen Aderhaut. Klin Monatsbl Augenheilkd 127:198–206

    CAS  Google Scholar 

  • Laties AM (1967) Central retinal artery innervation: absence of adrenergic innervation to intraocular branches. Arch Ophthalmol 77:405–409

    PubMed  CAS  Google Scholar 

  • Lauber H (1936a) Der Strahlenkörper (Corpus ciliare). D. Die Nerven des Strahlenkörpers. In: von Möllendorf W (ed) Handbuch der mikroskopischen Anatomie des Menschen. Vol 3: Haut und Sinnesorgane. Part 2: Auge. Springer, Berlin, pp 165–172

    Google Scholar 

  • Lauber H (1936b) Die Aderhaut (Choroidea). In: von Möllendorf W (ed) Handbuch der mikroskopischen Anantomie. Vol 3: Haut und Sinnesorgane. Part 2: Auge. Springer, Berlin, pp 91–133

    Google Scholar 

  • Lin AY-J, Szmydynger-Chodobska J, Rahman MP, Mayer B, Monfils PR, Johanson CE, Lim Y-P, Corsetti S, Chodobski A (1996) Immunohistochemical localization of nitric oxide synthase in rat anterior choroidal artery, stromal blood microvessels, and choroid plexus epithelial cells. Cell Tissue Res 285:411–418

    Article  PubMed  CAS  Google Scholar 

  • Llewellyn-Smith IJ, Song ZM, Costa M, Bredt DS, Snyder SH (1992) Ultrastructural localization of nitric oxide synthase immunoreactivity in guinea pig enteric neurons. Brain Res 577:337–342

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Costa JJ, Goldstein J, Mallo G, Saavedra JP (1995) NADPH-diaphorase distribution in the choroid after continuous illumination. Neuroreport 26:361–364

    Article  Google Scholar 

  • Lou HC, Edvinsson L, MacKenzie ET (1987) The concept of coupling blood flow to brain function: revision required? Ann Neurol 22:289–297

    Article  PubMed  CAS  Google Scholar 

  • Maciewicz R, Phipps BS, Foote WE, Aronin N, DiFiglia M (1983) The distribution of substance P-containing neurons in the cat Edinger-Westphal nucleus: relationship to efferent projection systems. Brain Res 270:217–230

    Article  PubMed  CAS  Google Scholar 

  • Macintosh SR (1974) The innervation of the conjunctiva in monkeys: an electron microscopic and nerve degeneration study. Graefes Arch Klin Exp Ophthalmol 192:105–116

    Article  CAS  Google Scholar 

  • Mann RM, Riva CE, Stone RA, Barnes GE, Cranstoun SD (1995) Nitric oxide and choroidal blood flow regulation. Invest Ophthalmol Vis Sci 36:925–930

    PubMed  CAS  Google Scholar 

  • Matsumoto T, Nakane M, Pollock JS, Kuk JE, Förstermann U (1993) A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61–64

    Article  PubMed  CAS  Google Scholar 

  • May PJ, Warren S (1993) Ultrastructure of the macaque ciliary ganglion. J Neurocytol 22:1073–1095

    Article  PubMed  CAS  Google Scholar 

  • Meighan SS (1956) Blood vessels of the bulbar conjunctiva in man. Br J Ophthalmol 40:513–526

    Article  PubMed  CAS  Google Scholar 

  • Miller AS, Coster DJ, Costa M, Furness JB (1983) Vasoactive intestinal polypeptide immunoreactive nerve fibres in the human eye. Aust J Ophthalmol 11:185–193

    Article  PubMed  CAS  Google Scholar 

  • Morris JL, Gibbins IL, Kadowitz PJ, Herzog H, Kreulen DL, Toda N, Claing A (1995) Roles of peptides and other substances in cotransmission from vascular autonomic and sensory neurons. Can J Physiol Pharmacol 73:521–332

    Article  PubMed  CAS  Google Scholar 

  • Morris R, Southam E, Gittins SR, Garthwaite J (1993) NADPH-diaphorase staining in autonomic and somatic cranial ganglia of the rat. Neuroreport 4:62–64

    Article  PubMed  CAS  Google Scholar 

  • Morrison JC, Van Buskirk EM (1983) Anterior collateral circulation in the primate eye. Ophthalmology 90:707–715

    PubMed  CAS  Google Scholar 

  • Morrison JC, Van Buskirk EM (1984) Ciliary process microvasculature of the primate eye. Am J Ophthalmol 97:372–384

    PubMed  CAS  Google Scholar 

  • Mulder H, Uddman R, Moller K, Elsas T, Ekblad E, Alumets J, Sundler F (1995) Pituitary adenylate cyclase activating polypeptide is expressed in autonomic neurons. Regul Pept 59:121–128

    Article  PubMed  CAS  Google Scholar 

  • Müller H (1859a) Über Ganglienzellen im Ziliarmuskel des Menschen. Verh Physik Med Ges Würzburg 10:107–110

    Google Scholar 

  • Müller H (1859b) Über glatte Muskelfasern und Nervengeflechte der Choroidea im menschlichen Auge. Verh Physik Med Ges Würzburg 10:107–179

    Google Scholar 

  • Nathanson JA, McKee M (1995a) Identification of an extensive system of nitric oxide-producing cells in the ciliary muscle and outflow pathway of the human eye. Invest Ophthalmol Vis Sci 36:1765–1773

    PubMed  CAS  Google Scholar 

  • Nathanson JA, McKee M (1995b) Alterations of ocular nitric oxide synthase in human glaucoma. Invest Ophthalmol Vis Sci 36:1774–1784

    PubMed  CAS  Google Scholar 

  • Nilsson SFE (1994) PACAP-27 and PACAP-38: vascular effects in the eye and some other tissues in the rabbit. Eur J Pharmacol 253:17–25

    Article  PubMed  CAS  Google Scholar 

  • Nilsson SFE (1996) Nitric oxide as a mediator of parasympathetic vasodilation in ocular and extraocular tissues in the rabbit. Invest Ophthalmol Vis Sci 37:2110–2119

    PubMed  CAS  Google Scholar 

  • Nilsson SFE, Bill A (1984) Vasoactive intestinal polypeptide (VIP): effects in the eye and on regional blood flows. Acta Physiol Scand 121:385–392

    Article  PubMed  CAS  Google Scholar 

  • Nilsson SFE, Linder J, Bill A (1985) Characteristics of uveal vasodilation produced by facial nerve stimulation in monkeys, cats and rabbits. Exp Eye Res 40:841–852

    Article  PubMed  CAS  Google Scholar 

  • Nyborg NCB, Nielsen PJ (1994) Neurogenic nitric oxide accounts for the non-adrenergic non-cholinergic vasodilation in human posterior ciliary arteries. Invest Ophthalmol Vis Sci 34:1287 (ARVO abstracts)

    Google Scholar 

  • Osborne NN, Barnett NL, Herrera AJ (1993) NADPH diaphorase localization and nitric oxide synthetase activity in the retina and anterior uvea of the rabbit eye. Brain Res 610:194–198

    Article  PubMed  CAS  Google Scholar 

  • Palmer RMJ, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–525

    Article  PubMed  CAS  Google Scholar 

  • Parver LM, Auker C, Carpenter DO (1980) Choroidal blood flow as a heat dissipating mechanism in the macula. Am J Ophthalmol 89:641–646

    PubMed  CAS  Google Scholar 

  • Parver LM, Auker CR, Carpenter DO, Doyle T (1982) Choroidal blood flow. II. Reflexive control in the monkey. Arch Ophthalmol 100:1327–1330

    PubMed  CAS  Google Scholar 

  • Parver LM, Auker CR, Carpenter DO (1983) Choroidal blood flow. III. Reflexive control in human eyes. Arch Ophthalmol 101:1604–1606

    PubMed  CAS  Google Scholar 

  • Perez GM, Keyser RB (1986) Cell body counts in human ciliary ganglia. Invest Ophthalmol Vis Sci 27:1428–1431

    PubMed  CAS  Google Scholar 

  • Perez MT, Larsson B, Alm P, Andersson KE, Ehinger B (1995) Localisation of neuronal nitric oxide synthase-immunoreactivity in rat and rabbit retinas. Exp Brain Res 104:207–217

    Article  PubMed  CAS  Google Scholar 

  • Price KJ, Hanson PJ, Whittle BJR (1996) Localization of constitutive isoforms of nitric oxide synthase in the gastric glandular mucosa of rats. Cell Tissue Res 285:157–163

    Article  PubMed  CAS  Google Scholar 

  • Quartu M, Diaz G, Floris A, Lai ML, Priestley JV, Del Fiacco M (1992) Calcitonin gene-related peptide in the human trigeminal sensory system at developmental and adult life stages: immunohistochemistry, neuronal morphometry and coexistence with substance P. J Chem Neuroanat 5:143–157

    Article  PubMed  CAS  Google Scholar 

  • Riva CE, Harino S, Shonat RD, Petrig BL (1991) Flicker evoked increase in optic nerve head blood flow in anesthetized cats. Neurosci Lett 128:291–296

    Article  PubMed  CAS  Google Scholar 

  • Rohen H (1952) Der Ziliarkörper als funktionelles System. Gegenbaur Morphol Jahrb 92:415–440

    Google Scholar 

  • Rohen J (1956a) Arteriovenöse Anastomosen im Limbusbereich des Hundes. Graefes Arch Ophthalmol 157:361–367

    Article  CAS  Google Scholar 

  • Rohen JW (1956b) Über den Ansatz der Ciliarmuskulatur im Bereich des Kammerwinkels. Ophthalmologica 131:51–59

    Article  PubMed  CAS  Google Scholar 

  • Rohen JW (1962) Sehorgan. In: Hofer H, Schultz AH, Starck D (eds) Primatologica, handbook of primatology. Vol. II/1. Karger, Basel, pp 6/1–210

    Google Scholar 

  • Rohen JW (1964) Ciliarkörper (Corpus ciliare). In: von Möllendorf W, Bargmann W (eds) Handbuch der mikroskopischen Anatomie des Menschen. Vol 3. Part 4: Haut und Sinnesorgane. Das Auge und seine Hilfsorgane. Springer, Berlin Heidelberg New York, pp 189–237

    Google Scholar 

  • Rohen JW (1982) The evolution of the primate eye in relation to the problem of glaucoma. In: Lütjen-Drecoll E (ed) Basic aspects of glaucoma research. Schattauer, Stuttgart, pp 3–33

    Google Scholar 

  • Rohen JW, Funk RHW (1994) Functional morphology of the episcleral vasculature in the rabbit and canine eye: presence of arteriovenous anastomoses. J Glaucoma 3:51–57

    Article  PubMed  CAS  Google Scholar 

  • Roufail E, Stringer M, Rees S (1995) Nitric oxide synthase immunoreactivity and NADPH diaphorase staining are co-localised in neurons closely associated with the vasculature in rat and human retina. Brain Res 684:36–46

    Article  PubMed  CAS  Google Scholar 

  • Ruskell GL (1965) The orbital distribution of the sphenopalatine ganglion in the rabbit. In: Rohen JW (ed) The structure of the eye. II. Symposium. Schattauer, Stuttgart, pp 355–368

    Google Scholar 

  • Ruskell GL (1970a) The orbital branches of the pterygopalatine ganglion and their relationship with internal carotid nerve branches in primates. J Anat 106:323–339

    PubMed  CAS  Google Scholar 

  • Ruskell GL (1970b) An ocular parasympathetic nerve pathway of facial nerve origin and its influence on intraocular pressure. Exp Eye Res 10:319–330

    Article  PubMed  CAS  Google Scholar 

  • Ruskell GL (1971) Facial parasympathetic innervation of the choroidal blood-vessels in monkeys. Exp Eye Res 12:166–172

    Article  PubMed  CAS  Google Scholar 

  • Ruskell GL, Griffiths T (1979) Peripheral nerve pathway to the ciliary muscle. Exp Eye Res 28:277–284

    Article  PubMed  CAS  Google Scholar 

  • Samuel U, Lütjen-Drecoll E, Tamm ER (1996) Gap junctions are found between iris sphincter smooth muscle cells but not in the ciliary muscle of human and monkey eyes. Exp Eye Res 63:187–192

    Article  PubMed  CAS  Google Scholar 

  • Sanders KM, Ward SM (1992) Nitric oxide as a mediator of nonadrenergic noncholiner-gic neurotransmission. Am J Physiol 262:G379–G392

    PubMed  CAS  Google Scholar 

  • Schmidt HHHW, Walter U (1994) NO at work. Cell 78:919–925

    Article  PubMed  CAS  Google Scholar 

  • Schuman JS, Erickson K, Nathanson JA (1994) Nitrovasodilator effects on intraocular pressure and outflow facility in monkeys. Exp Eye Res 58:99–105

    Article  PubMed  CAS  Google Scholar 

  • Sienkiewicz W, Kaleczyc J, Majewski M, Lakomy M (1995) NADPH-diaphorase-containing cerebrovascular nerve fibres and their possible origin in the pig. J Brain Res 36:353–363

    CAS  Google Scholar 

  • Stjernschantz J, Bill A (1979) Effect of intracranial stimulation of the oculomotor nerve on ocular blood flow in the monkey, cat and rabbit. Invest Ophthalmol Vis Sci 18:99–103

    PubMed  CAS  Google Scholar 

  • Stjernschantz J, Bill A (1980) Vasomotor effects of facial nerve stimulation: noncholiner-gic vasodilation in the eye. Acta Physiol Scand 109:45–50

    Article  PubMed  CAS  Google Scholar 

  • Stöhr P (1957) Handbuch der mikroskopischen Anatomic V Mikroskopische Anatomie des vegetativen Nervensystems. Springer, Berlin Heidelberg

    Google Scholar 

  • Stone RA, Kuwayama Y, Laties AM (1987) Regulatory peptides in the eye. Experientia 43:791–800

    Article  PubMed  CAS  Google Scholar 

  • Su E-N, Alder VA, Yu D-Y, Cringle SJ (1994) Adrenergic and nitrergic neurotransmitters are released by the autonomic system of the pig long posterior ciliary artery. Curr Eye Res 13:907–917

    Article  PubMed  CAS  Google Scholar 

  • Sun W, Erichsen JT, May PJ (1994) NADPH-diaphorase reactivity in ciliary ganglion neurons: a comparison of distributions in the pigeon, cat, and monkey. Vis Neurosci 11:1027–1031

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Fukuuchi Y, Koto A, Naganuma Y, Isozumi K, Matsuoka S, Gotoh J, Shimizu T (1993) Cerebrovascular NADPH diaphorase-containing nerve fibers in the rat. Neurosci Lett 151:1–3

    Article  PubMed  CAS  Google Scholar 

  • Szmydynger-Chodobska J, Monfils PR, Lin AY-J, Rahman MP, Johanson CE, Chodobski A (1996) NADPH-diaphorase histochemistry of rat choroid plexus blood vessels and epithelium. Neurosci Lett 208:179–182

    Article  PubMed  CAS  Google Scholar 

  • Talmage EK, Mawe GM (1993) NADPH-diaphorase and VIP are colocalized in neurons of gallbladder ganglia. J Auton Nerv Syst 43:83–90

    Article  PubMed  CAS  Google Scholar 

  • Tamm E, Flügel C, Baur A, Lütjen-Drecoll E (1991a) Cell cultures of human ciliary muscle: growth, ultrastructural and immunocytochemical characteristics. Exp Eye Res 53:375–387

    Article  PubMed  CAS  Google Scholar 

  • Tamm E, Lütjen-Drecoll E, Jungkunz W, Rohen JW (1991b) Posterior attachment of ciliary muscle in young, accommodating old, presbyopic monkeys. Invest Ophthalmol Vis Sci 32:1678–1692

    PubMed  CAS  Google Scholar 

  • Tamm E, Flügel C, Stefani FH, Rohen JW (1992) Contractile cells in the human scleral spur. Exp Eye Res 54:531–543

    Article  PubMed  CAS  Google Scholar 

  • Tamm ER, Lütjen-Drecoll E (1997) Nitrergic nerve cells in the primate ciliary muscle are only present in species with a fovea centralis. Ophthalmologica 211:201–204

    Article  PubMed  CAS  Google Scholar 

  • Tamm ER, Lütjen-Drecoll E (1996a) Functional morphology and origin of nitrergic nerves in the human eye. Exp Eye Res 63(Suppl):S.151

    Article  Google Scholar 

  • Tamm ER, Lütjen-Drecoll E (1996b) Ciliary body. Microsc Res Tech 33:390–439

    Article  PubMed  CAS  Google Scholar 

  • Tamm ER, Flügel-Koch C, Mayer B, Lütjen-Drecoll E (1995a) Nerve cells in the human ciliary muscle: ultrastructural and immunocytochemical characterization. Invest Ophthalmol Vis Sci 36:414–426

    PubMed  CAS  Google Scholar 

  • Tamm ER, Koch TA, Mayer B, Stefani FH, Lütjen-Drecoll E (1995b) Innervation of myofibroblast-like scleral spur cells in human and monkey eyes. Invest Ophthalmol Vis Sci 36:1633–1644

    PubMed  CAS  Google Scholar 

  • Tiffany JM (1995) Physiological functions of the meibomian glands. In: Osborne NN, Chader G (eds) Progress in retinal and eye research. Elsevier Science, Amsterdam, pp 47–74

    Google Scholar 

  • Toda N (1995) Nitroxidergic nerves and hypertension. Hypertens Res 18:19–26

    Article  PubMed  CAS  Google Scholar 

  • Toda N, Ayajiki K, Yoshida K, Kimura H, Okamura T (1993) Impairment by damage of the pterygopalatine ganglion of nitroxidergic vasodilator nerve function in canine cerebral and retinal arteries. Circ Res 72:206–213

    PubMed  CAS  Google Scholar 

  • Toda N, Kitamura Y, Okamura T (1994) Role of nitroxidergic nerve in dog retinal arterioles in vivo and arteries in vitro. Am J Pathol 266:H1985–H1992

    CAS  Google Scholar 

  • Toda N, Toda M, Ayajiki K, Okamura T (1996) Monkey central retinal artery is innervated by nitroxidergic vasodilator nerves. Invest Ophthalmol Vis Sci 37: 2177–2184

    PubMed  CAS  Google Scholar 

  • Toris CB, Pederson JE (1987) Aqueous humor dynamics in experimental iridocyclitis. Invest Ophthalmol Vis Sci 28:477–481

    PubMed  CAS  Google Scholar 

  • Törnquist P, Alm A (1979) Retinal and choroidal contribution to retinal metabolism in vivo: a study in pigs. Acta Physiol Scand 106:351–357

    Article  PubMed  Google Scholar 

  • Törnqvist G (1966) Effect of cervical sympathetic stimulation on accommodation in monkeys: an example of a beta-adrenergic, inhibitory effect. Acta Physiol Scand 67:363–372

    Article  PubMed  Google Scholar 

  • Törnqvist G (1967a) The relative importance of the parasympathetic and sympathetic nervous system for accommodation in monkeys. Invest Ophthalmol Vis Sci 6:612–617

    Google Scholar 

  • Törnqvist G (1967b) Accommodation in monkeys: some pharmacological and physiological aspects. Acta Ophthalmol (Copenh) 45:1–32

    Google Scholar 

  • Tracey WR, Nakane M, Pollock JS, Förstermann U (1993) Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity. Biochem Biophys Res Commun 195:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Tripathi RC, Tripathi BJ (1984) Anatomy of the human eye, orbit, and adnexa. In: Davson H (ed) The eye. Vol 1a: Vegetative physiology and biochemistry. Academic, San Diego, pp 1–268

    Google Scholar 

  • Uddman R, Alumets J, Ehinger B, Hakanson R, Loren I, Sundler F (1980) Vasoactive intestinal peptide nerves in ocular and orbital structures of the cat. Invest Ophthalmol Vis Sci 19:878–885

    PubMed  CAS  Google Scholar 

  • Ueno M, Naumann GOH (1989) Uveal damage in secondary glaucoma. Graefes Arch Clin Exp Ophthalmol 227:380–383

    Article  PubMed  CAS  Google Scholar 

  • Unger WG (1989) Mediation of the ocular response to injury and irritation: peptides versus prostaglandins. In: Bito LZ, Stjernschantz J (eds) The ocular effects of prostaglandins and other eicosanoids: proceedings in clinical and biological research. Vol 312. Liss, New York, pp 293–328

    Google Scholar 

  • Van Alphen GWHM, Robinette SL, Macri FJ (1962) Drug effects on ciliary muscle and choroid preparations in vitro. Arch Ophthalmol 68:81–93

    Google Scholar 

  • Van der Werf F (1993) Innervation of the lacrimal gland in the cynomolgus monkey: a retrograde tracing and immunohistochemical study. In: van der Werf F (ed) Autonomic and sensory innervation of some orbital structures in the primate. Thesis, Universiteit van Amsterdam, Amsterdam, pp 51–70

    Google Scholar 

  • Van der Zypen E (1967) Licht-und elektronenmikroskopische Untersuchungen über den Bau und die Innervation des Ziliarmuskels bei Mensch und Affe (Cercopithecus ethiops). Graefes Arch Klin Exp Ophthalmol 174:143–168

    Article  Google Scholar 

  • Wang I, Kondo M, Bill A (1995) Vascular responses to flickering light in the retina in cats and monkeys: effect of L-NAME. Acta Physiol Scand 153:39A

    Google Scholar 

  • Wang ZY, Alm P, Hakanson R (1995) Distribution and effects of pituitary adenylate cyclase activating polypeptide in the rabbit eye. Neuroscience 69:297–308

    Article  PubMed  CAS  Google Scholar 

  • Warwick R (1954) The ocular parasympathetic nerve supply and its mesencephalic sources. J Anat 88:195–203

    Google Scholar 

  • Wiedenmann B, Franke WW (1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38000 characteristic of presynaptic vesicles. Cell 41:1017–1028

    Article  PubMed  CAS  Google Scholar 

  • Wiederholt M, Sturm A, Lepple-Wienhues A (1994) Relaxation of trabecular meshwork and ciliary muscle by release of nitric oxide. Invest Ophthalmol Vis Sci 35:2515–2520

    PubMed  CAS  Google Scholar 

  • Wiederholt M, Bielka S, Schweig F, Lütjen-Drecoll E, Lepple-Wienhues A (1996) Regulation of outflow rate and resistance in the perfused anterior segment of the bovine eye. Exp Eye Res 61:223–234

    Article  Google Scholar 

  • Wiencke AK, Nilsson H, Nielsen PJ, Nyborg NCB (1994) Nonadrenergic noncholinergic vasodilation in bovine ciliary artery involves CGRP and neurogenic nitric oxide. Invest Ophthalmol Vis Sci 35:3268–3277

    PubMed  CAS  Google Scholar 

  • Wilcox LM, Keough EM, Connolly RJ, Hote CE (1980) The contribution of blood flow by the anterior ciliary arteries to the anterior segment in the primate eye. Exp Eye Res 30:167–174

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson KD, Lee K, Deshapande S, Duerksen-Hughes P, Boss JM, Pohl J (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246:670–673

    Article  PubMed  CAS  Google Scholar 

  • Wizemann A, Wizemann V (1980) Untersuchungen zur ambulanten und perioperativen Augendrucksenkung mit organischen Nitraten. Klin Monatsbl Augenheilkd 177:292–295

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto R, Bredt DS, Snyder SH, Stone RA (1993) The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54:189–200

    Article  PubMed  CAS  Google Scholar 

  • Ye X, Laties AM, Stone RA (1990) Peptidergic innervation of the retinal vasculature and the optic nerve head. Invest Ophthalmol Vis Sci 31:1731–1737

    PubMed  CAS  Google Scholar 

  • Yoshida K, Okamura T, Kimura H, Bredt DS, Snyder SH, Toda N (1993) Nitric oxide syn-thase-immunoreactive nerve fibers in dog cerebral and peripheral arteries. Brain Res 629:67–72

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Okamura T, Toda N (1994) Histological and functional studies on the nitrox-idergic nerve innervating monkey cerebral, mesenteric and temporal arteries. Jpn J Pharmacol 65:351–359

    Article  PubMed  CAS  Google Scholar 

  • Zagvazdin YS, Fitzgerald MEC, Sancesario G, Reiner A (1996) Neural nitric oxide mediates Edinger-Westphal nucleus evoked increase in choroidal blood flow in the pigeon. Invest Ophthalmol Vis Sci 37:666–672

    PubMed  CAS  Google Scholar 

  • Zhang YL, Tan CK, Wong WC (1994a) Localisation of substance P-like immunoreactiv-ity in the ciliary ganglia of monkey (Macaca fascicularis)and cat: a light-and electron-microscopic study. Cell Tissue Res 276:163–171

    Article  PubMed  CAS  Google Scholar 

  • Zhang YL, Tan CK, Wong WC (1994b) The ciliary ganglion of the monkey: a light and electron microscope study. J Anat 184:251–260

    PubMed  Google Scholar 

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Tamm, E.R., Lütjen-Drecoll, E. (2000). Origin and Function of Nitrergic Nerves in the Human Eye: Morphological Aspects. In: Kashii, S., Akaike, A., Honda, Y. (eds) Nitric Oxide in the Eye. Springer, Tokyo. https://doi.org/10.1007/978-4-431-67949-3_3

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