Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Uveal vascular bed in health and disease: uveal vascular bed anatomy. Paper 1 of 2

Eye volume 37, pages 2590–2616 (2023)Cite this article

Subjects

Abstract

The uveal vascular bed is the largest vascular system in the eye and has a role in supplying almost every tissue in the eyeball. This makes it the most important ocular vascular system. This is an up-to-date review of the literature of the entire uveal vascular bed in health based on detailed anatomy of the posterior ciliary arteries (PCAs), anterior ciliary arteries, cilioretinal arteries, and vortex veins. Although postmortem injection cast preparations gave us useful information on the morphology of the choroidal vascular bed; in vivo studies showed that they misled us for centuries about the in vivo situation. According to the postmortem cast studies, the uveal vascular bed has no segmental distribution, the uveal vessels anastomose freely with one another, there are inter-arterial and arteriovenous anastomoses in the choroid, and the choriocapillaris form a freely communicating and an uninterrupted vascular bed in the entire choroid.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3: Fluorescein fundus angiogram of a normal human eye, showing the sites of entry of the SPCAs and their course in the choroid.
Fig. 4
Fig. 5
Fig. 6: Fluorescein fundus angiogram during retinal arteriovenous phase, of right eye of rhesus monkey after cutting the medial PCA.
Fig. 7
Fig. 8
Fig. 9: Fluorescein fundus angiograms of a rhesus monkey eye at the posterior pole.
Fig. 10
Fig. 11
Fig. 12
Fig. 13: Schematic representation of blood supply of the optic nerve.
Fig. 14
Fig. 15
Fig. 16: Fluorescein fundus angiogram of right eye of a monkey (after experimental central retinal artery occlusion) at 70 mm.
Fig. 17: A three-dimensional schematic representation of the choriocapillaris pattern.
Fig. 18: Diagrammatic representation of watershed zones between the four various vortex veins in rhesus monkeys.
Fig. 19: A magnified view of cast of choriocapillaris.
Fig. 20: Microphotograph of a flat preparation of the human choriocapillaris. (Reproduced by kind courtesy of Torczynski and Tso).
Fig. 21: Drawing of the neoprene cast of Schlemm’s canal and diagrammatic representation of incomplete arterial circle close to the canal.
Fig. 22: Diagrammatic representation of ACAs running along the borders of the four recti muscles, and also of episcleral, intramuscular and major arterial circles.
Fig. 23
Fig. 24
Fig. 25: It shows fluorescein fundus angiograms of four eyes showing various positions of the watershed zone between LPCA and MPCA.
Fig. 26: Diagrammatic representation of some of the locations of the watershed zone (shaded area) between the medial and lateral PCAs in human eyes.
Fig. 27

Similar content being viewed by others

References

  1. Ramon Y Cajal S Recollections of My Life. Santiago Ramon Y Cajal. Translated by EH Craigie from the third Spanish edition (1923) 1937; p. 564-65. Philadelphia: American Philosophical Society.

  2. Hayreh SS. Blood supply of the optic nerve. In: Shaffer RN, Glaucoma Research Conference. Am J Ophthalmol. 1966;61:564.

    Google Scholar 

  3. Hayreh SS. Blood supply of the optic nerve head and its Competing interestsrole in optic atrophy, glaucoma and oedema of the optic disc. Br J Ophthalmol. 1969;53:721–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Duke-Elder S, Wybar KC System of Ophthalmology, Vol. 2: The anatomy of the visual system. 1961; p. 345, 351, London: Kimpton 358,69.

  5. Hayreh SS, Dass R. The ophthalmic Artery: I. Origin and intra-cranial and intra-canalicular course. Br J Ophthalmol. 1962;46:65–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hayreh SS. The ophthalmic artery III. Branches. Br J Ophthalmol. 1962;46:212–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Meyer F. Zur Anatomie der Orbitalarterien. Morphol Jahrüch. 1887;12:414–58.

    Google Scholar 

  8. Sudakevitch T. The variations in the system of the trunks of the posterior ciliary arteries. Br J Ophthalmol. 1947;31:738–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Leber T Die Circulations- und Ernährungsverhältnisse des Auges. Graefe-Saemisch Handbuch der Gesamten Augenheilkunde, 2nd ed. 1903 vol 2. p. 33-35 Leipzig: Wilhelm Engelmann, 43-6.

  10. Ducournau D. Les arteres ciliaires posterieures courtes para-optiques. Une entite anatomo-clinique. [Short para-optic posterior ciliary arteries. An anatomo-clinical entity. Bull Soc Ophtalmol Fr. 1982;82:1527.

    CAS  PubMed  Google Scholar 

  11. Hayreh SS. The Long posterior ciliary arteries. Graefes Arch Clin Exp Ophthalmol. 1974;192:197–213.

    Article  CAS  Google Scholar 

  12. Siam AL, El-Mamoun TA, Ali MH. A restudy of the surgical anatomy of the posterior aspect of the globe: an essential topography for exact macular buckling. Retina 2011;31:1405–11.

    Article  PubMed  Google Scholar 

  13. Ducournau D La systématisation vasculaire de la choroide. [Vascularization of the choroid]. Annee Ther Clin Ophtalmol. 1979:17–22.

  14. Wedel C, Ruysch F. Epistola anatomica, problematica ad Fredericum Ruyschium. De oculorum tunicis. Amstelaedami: Janssonio-Waesbergios; 1737.

    Google Scholar 

  15. Wybar KC. Vascular anatomy of the choroid in relation to selective localization of ocular disease. Br J Ophthalmol. 1954;38:513–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Shimizu K, Ujiie K. Structure of ocular vessels. 54. New York: Igaku-Shoin; 1978. p. 70–9. 108-24

    Google Scholar 

  17. Hogan MJ, Alvarado JA, Weddell JE. Histology of the human eye: an atlas and textbook. 50. Philadelphia: Saunders; 1971. p. 189. 326, 372.

    Google Scholar 

  18. Hayreh SS, Baines JA. Occlusion of the posterior ciliary artery. I. Effects on choroidal circulation. Br J Ophthalmol. 1972;56:719–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hayreh SS. Segmental nature of the choroidal vasculature. Br J Ophthalmol. 1975;59:631–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ring HG, Fujino T. Observations on the anatomy and pathology of the choroidal vasculature. Arch Ophthalmol. 1967;78:431–44.

    Article  CAS  PubMed  Google Scholar 

  21. Uyama M, Ohkuma H, Itotagawa S, Koshibu A, Uraguchi K, Miki K. [Pathology of choroidal circulatory disturbance. Part 1. Angioarchitecture of the choroid, observation on plastic cast preparation (author’s transl)]. Nihon Ganka Gakkai Zasshi. 1980;84:1893–909.

    CAS  PubMed  Google Scholar 

  22. Olver JM. Functional anatomy of the choroidal circulation: methyl methacrylate casting of human choroid. Eye 1990;4:262–72.

    Article  PubMed  Google Scholar 

  23. MacFaul PA. Ciliary artery involvement in giant cell arteritis. Br J Ophthalmol. 1967;51:505–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hayreh SS. Anterior ischaemic optic neuropathy. II. Fundus on ophthalmoscopy and fluorescein angiography. Br J Ophthalmol. 1974;58:964–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hayreh SS, Scott WE. Fluorescein iris angiography. II. Disturbances in iris circulation following strabismus operation on the various recti. Arch Ophthalmol. 1978;96:1390–1400.

    Article  CAS  PubMed  Google Scholar 

  26. Hayreh SS. Blood supply of the optic nerve head and its role in optic atrophy, glaucoma, and oedema of the optic disc. Br J Ophthalmol. 1969;53:721–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hayreh SS. The blood supply of the optic nerve head and the evaluation of it: myth and reality. Prog Retin Eye Res. 2001;20:563–93.

    Article  CAS  PubMed  Google Scholar 

  28. Hayreh SS. The choriocapillaris. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1974;192:165–79.

    Article  CAS  PubMed  Google Scholar 

  29. Wagenmann A. Experimentelle Untersuchungen über den Einfluss der Circulation in den Netzhaut- und Aderhautgefässen auf die Ernährung des Auges, insbesondere der Retina, und über die Folgen der Sehnervendurchschneidung. Albrecht Von Graefes Arch Ophthalmol. 1890;36:1–120.

    Article  Google Scholar 

  30. Bossalino D. Ricerche sperimentali sulle alterazioni dell’occhio consecutive al taglio dei vasi ciliari. Ann di ottalmologia. 1910;39:866–914.

    Google Scholar 

  31. Freeman HM, Hawkins WR, Schepens CL. Anterior segment necrosis. An experimental study. Arch Ophthalmol. 1966;75:644–50.

    Article  CAS  PubMed  Google Scholar 

  32. Hayreh SS. Choroidal circulation in health and in acute vascular occlusion. In: Cant JS, editor. Proceedings, 3rd William Mackenzie Memorial Symposium (1974: Glasgow). St. Louis: Mosby; 1976. p. 157–70.

    Google Scholar 

  33. Hayreh SS, Baines JA. Occlusion of the posterior ciliary artery. II. Chorio-retinal lesions. Br J Ophthalmol. Br J Ophthalmol. 1972;56:736–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Selbach JM, Rohen JW, Steuhl KP, Lütjen-Drecoll E. Angioarchitecture and innervation of the primate anterior episclera. Curr Eye Res. 2005;30:337–44.

    Article  PubMed  Google Scholar 

  35. Zhang HR, Gao J. [Electron microscopy of the angioarchitecture of the human iris and ciliary body]. [Zhonghua Yan Ke Za Zhi] Chinese. J Ophthalmol. 1989;25:148–51.

    CAS  Google Scholar 

  36. Song Y, Song YJ, Ko MK. A study of the vascular network of the iris using flat preparation. Korean J Ophthalmol. 2009;23:296–300.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Takahashi K, Muraoka K, Kishi S, Shimizu K. Watershed zone in the human peripheral choroid. Ophthalmology 1996;103:336–42.

    Article  CAS  PubMed  Google Scholar 

  38. von Haller A. Arteriarum oculi: historia et tabulae arteriarum oculi. Gottingen: Typis Abrami Vandenhoeck; 1754.

    Google Scholar 

  39. Tiedemann F Der antheil des sympathischen nervens an den verrichtungen der sinne. In: Friedrich T, Treviranus GR, editors. Zeitschrift für Physiologie. 1824. 1. p. 237-90. Heidelberg: August Osswald.

  40. Huschke E. Eingeweide und Sinnesorgane. In: von Sömmerring ST, editor. Vom Bau des menschlichen Körpers, bd 5. Leipzig: Voss; 1844. p. 710.

    Google Scholar 

  41. Olver JM, Spalton DJ, McCartney AC. Quantitative morphology of human retrolaminar optic nerve vasculature. Invest Ophthalmol Vis Sci. 1994;35:3858–66.

    CAS  PubMed  Google Scholar 

  42. Onda E, Cioffi GA, Bacon DR, Van Buskirk EM. Microvasculature of the human optic nerve. Am J Ophthalmol. 1995;120:92–102.

    Article  CAS  PubMed  Google Scholar 

  43. Gauntt CD, Williamson TH, Sanders MD. Relationship of the distal optic nerve sheath to the circle of Zinn. Graefes Arch Clin Exp Ophthalmol. 1999;237:642–47.

    Article  CAS  PubMed  Google Scholar 

  44. Olver JM, Spalton DJ, McCartney AC. Microvascular study of the retrolaminar optic nerve in man: the possible significance in anterior ischaemic optic neuropathy. Eye 1990;4:7–24.

    Article  PubMed  Google Scholar 

  45. Strek P, Strek W, Nowogrodzka-Zagorska M, Pitynski K. Angiomorphology of the retrobulbar part of the optic nerve. A scanning electron microscopy of vascular casts. Folia Morphol (Warsz). 1996;55:143–50.

    CAS  PubMed  Google Scholar 

  46. Heimann K. The development of the choroid in man. Ophthalmic Res. 1972;3:257–73.

    Article  Google Scholar 

  47. Hayreh SS. Microangioarchitecture of optic papilla [comment]. Jpn J Ophthalmol. 1989;33:519–25.

    CAS  PubMed  Google Scholar 

  48. Hayreh SS. Controversies on submacular choroidal circulation. Ophthalmologica 1981;183:11–9.

    Article  CAS  PubMed  Google Scholar 

  49. Alm A, Bill A. 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. 1973;15:15–29.

    Article  CAS  PubMed  Google Scholar 

  50. Stern WH, Ernest JT. Microsphere occlusion of the choriocapillaris in rhesus monkeys. Am J Ophthalmol. 1974;78:438–48.

    Article  CAS  PubMed  Google Scholar 

  51. Hovius J. Tractatus de circulari humorum motu in oculis. 1716. Lugdunum Batavorum: Langerak.

  52. Eschricht DF. Beobachtungen an dem Seehundsauge. Archiv für Anatomie, Physiologie und Wissenschaftliche Medicin. 1838;1716:575–99.

  53. Passera E. La rete vascolare sanguigna della membrana coriocapillare dell’uomo. Ricerche (fatte nel laboratorio Di Anat Norm della R Univá di Roma). 1896;5-6:133–67.

    Google Scholar 

  54. Winslow J-B. An anatomical exposition of the structure of the human body. Translated from the French original, by G Douglas. 1733; p.77 London: Printed for N. Prevost.

  55. Rohen JW. Morphology of the uveal tract. Int Ophthalmol Clin. 1965;5:581–667.

    Article  CAS  PubMed  Google Scholar 

  56. Ruskell GL. Choroidal vascularization in the rabbit. Am J Ophthalmol. 1961;52:807–15.

    Article  CAS  PubMed  Google Scholar 

  57. Goldor H, Gay AJ. Chorioretinal vascular occlusions with latex microspheres (a long-term study). II. Invest Ophthalmol. 1967;6:51–8.

    CAS  PubMed  Google Scholar 

  58. Dollery CT, Henkind P, Kohner EM, Paterson JW. Effect of raised intraocular pressure on the retinal and choroidal circulation. Invest Ophthalmol. 1968;7:191–98.

    CAS  PubMed  Google Scholar 

  59. Hayreh SS. Vascular pattern of the choriocapillaris. Exp Eye Res. 1974;19:101–4.

    Article  CAS  PubMed  Google Scholar 

  60. Torczynski E, Tso MO. The architecture of the choriocapillaris at the posterior pole. Am J Ophthalmol. 1976;81:428–40.

    Article  CAS  PubMed  Google Scholar 

  61. Loewenstein A. Glomus cells in the human choroid as the basis of arteriovenous anastomoses. Am J Ophthalmol. 1949;32:1651–59.

    Article  CAS  PubMed  Google Scholar 

  62. Lütjen-Drecoll E. Choroidal innervation in primate eyes. Exp Eye Res. 2006;82:357–61.

    Article  PubMed  Google Scholar 

  63. Hayreh SS. The Orbital Vessels of Rhesus Monkeys. Exp Eye Res. 1964;3:16–30.

    Article  CAS  PubMed  Google Scholar 

  64. Ashton N, Smith R. Anatomical study of Schlemm’s canal and aqueous veins by means of neoprene casts. III. Arterial relations of Schlemm’s canal. Br J Ophthalmol. 1953;37:577–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Van Buskirk EM. The ciliary vasculature and its perturbation with drugs and surgery. Trans Am Ophthalmol Soc. 1988;86:794–841.

    PubMed  PubMed Central  Google Scholar 

  66. Morrison JC, Van, Buskirk EM. Anterior collateral circulation in the primate eye. Ophthalmology 1983;90:707–15.

    Article  CAS  PubMed  Google Scholar 

  67. Heymann V, George JL, Sirbat D, Rauber G, Raspiller A. Apport artériel au segment antérieur de l’oeil. Etude radio-anatomique d’une série de vingt-cinq globes humains. [Arterial supply to the anterior segment of the eye. Radioanatomical study of a series of 25 human eyes]. J Fr Ophtalmol. 1985;8:697–703.

    CAS  PubMed  Google Scholar 

  68. Johnson MS, Christiansen SP, Rath PP, Watanabe TM, Merten G, Bothun ED, et al. Anterior ciliary circulation from the horizontal rectus muscles. Strabismus 2009;17:45–8.

    Article  PubMed  Google Scholar 

  69. Funk R, Rohen JW. Scanning electron microscopic study on the vasculature of the human anterior eye segment, especially with respect to the ciliary processes. Exp Eye Res. 1990;51:651–61.

    Article  CAS  PubMed  Google Scholar 

  70. Meyer PAR. Patterns of blood flow in episcleral vessels studied by low-dose fluorescein videoangiography. Eye. 1988;2:533–46.

    Article  PubMed  Google Scholar 

  71. Ormerod LD, Fariza E, Webb RH. Dynamics of external ocular blood flow studied by scanning angiographic microscopy. Eye. 1995;9:605–14.

    Article  PubMed  Google Scholar 

  72. Laatikainen L. Perilimbal vasculature in glaucomatous eyes. Acta Ophthalmol Suppl. 1971;111:54–73.

    Google Scholar 

  73. Meyer PA, Watson PG. Low dose fluorescein angiography of the conjunctiva and episclera. Br J Ophthalmol. 1987;71:2–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Talusan ED, Schwartz B. Fluorescein angiography: Demonstration of flow pattern of anterior ciliary arteries. Arch Ophthalmol. 1981;99:1074–80.

    Article  CAS  PubMed  Google Scholar 

  75. Ormerod LD, Fariza E, Hughes GW, Doane MG, Webb RH. Anterior segment fluorescein videoangiography with a scanning angiographic microscope. Ophthalmology 1990;97:745–51.

    Article  CAS  PubMed  Google Scholar 

  76. Nanba K, Schwartz B. Increased diameter of the anterior ciliary artery with increased intraocular pressure. Arch Ophthalmol. 1986;104:1652–5.

    Article  CAS  PubMed  Google Scholar 

  77. Ojima M, Matsuo N. Angioarchitecture of rabbit iris. Acta Med Okayama. 1985;39:47–52.

    CAS  PubMed  Google Scholar 

  78. Raviola G. Effects of paracentesis on the blood-aqueous barrier: an electron microscope study on Macaca mulatta using horseradish peroxidase as a tracer. Invest Ophthalmol. 1974;13:828–58.

    CAS  PubMed  Google Scholar 

  79. Rohen JW, Funk RH. Functional morphology of the episcleral vasculature in rabbits and dogs: presence of arteriovenous anastomoses. J Glaucoma. 1994;3:51–7.

    Article  CAS  PubMed  Google Scholar 

  80. Parodi MB, Bondel E, Saviano S, Da Pozzo S, Bergamini L, Ravalico G. Iris arteriovenous communication: clinical and angiographic features. Int Ophthalmol. 1998;22:1–5.

    Article  CAS  PubMed  Google Scholar 

  81. Raviola G, Butler JM. Unidirectional transport mechanism of horseradish peroxidase in the vessels of the iris. Invest Ophthalmol Vis Sci. 1984;25:827–36.

    CAS  PubMed  Google Scholar 

  82. Bill A. The blood-aqueous barrier. Trans Ophthalmol Soc U K 1986;105:149–55.

    PubMed  Google Scholar 

  83. Hayreh SS, Scott WE. Fluorescein Iris Angiography. I. Normal Pattern. Arch Ophthalmol. 1978;96:1383–9.

    Article  CAS  PubMed  Google Scholar 

  84. Virdi PS, Hayreh SS. Normal fluorescein iris angiographic pattern in subhuman primates. Invest Ophthalmol Vis Sci. 1983;24:790–3.

    CAS  PubMed  Google Scholar 

  85. Iovino C, Peiretti E, Braghiroli M, Tatti F, et al. Imaging of iris vasculature: current limitations and future perspective. Eye (Lond). 2022;36:930–40.

    Article  PubMed  Google Scholar 

  86. Chignell AH, Easty DL. Iris fluorescein photography following retinal detachment and in certain ocular ischaemic disorders. Trans Ophthalmol Soc U K 1971;91:243–59.

    CAS  PubMed  Google Scholar 

  87. Ishikawa T. Fine structure of retinal vessels in man and the macaque monkey. Invest Ophthalmol. 1963;2:1–15.

    CAS  PubMed  Google Scholar 

  88. Amalric P. The angiography of the anterior segment of the eye. In: Shimizu K, editor. Proceedings of the International Symposium of Fluorescein Angiography, Tokyo, 1972. Tokyo: Igaku Shoin Ltd; 1974. p. 281–318.

    Google Scholar 

  89. Vannas A. Fluorescein angiography of the vessels of the iris in pseudoexfoliation of the lens capsule, capsular glaucoma and some other forms of glaucoma. Acta Ophthalmol Suppl. 1969;105:1–75.

    CAS  PubMed  Google Scholar 

  90. Kottow M, Metzler D, P H Iris angiographic findings in retinal vein occlusion. In: Cant JS, editor. Vision and circulation. 1976. p. 251–4 London: Kimpton.

  91. Kottow M Iris angiography in vascular diseases of the fundus. In: DeLaey JJ, editor. Proceedings of the International Symposium on Fluorescein Angiography. 1976. Vol. 9. p. 465-71. Documenta Ophthalmologica Proceedings Servies. The Hague: W. Junk.

  92. Shiose Y, Oguri M. Electron microscopic studies on the blood-retinal barrier and the blood-aqueous barrier. Jpn J Ophthalmol. 1970;14:73–87.

    Google Scholar 

  93. Shakib M, Cunha-Vaz JG. Studies on the permeability of the blood-retinal barrier. IV. Junctional complexes of the retinal vessels and their role in the permeability of the blood-retinal barrier. Exp Eye Res. 1966;5:229–34.

    Article  CAS  PubMed  Google Scholar 

  94. Szalay J, Nunziata B, Henkind P. Permeability of iridial blood vessels. Exp Eye Res. 1975;21:531–43.

    Article  CAS  PubMed  Google Scholar 

  95. Satoh K, Takaku Y, Ohtsuki K, Mizuno K. Effects of aging on fluorescein leakage in the iris and angle in normal subjects. Jpn J Ophthalmol. 1999;43:166–70.

    Article  CAS  PubMed  Google Scholar 

  96. Van Nerom PR, Rosenthal AR, Jacobson DR, Pieper I, Schwartz H, Greider BW. Iris angiography and aqueous photofluorometry in normal subjects. Arch Ophthalmol. 1981;99:489–93.

    Article  PubMed  Google Scholar 

  97. Cunha-Vaz J. The blood-ocular barriers. Surv Ophthalmol. 1979;23:279–96.

    Article  CAS  PubMed  Google Scholar 

  98. Morrison JC, Van, Buskirk EM. Ciliary process microvasculature of the primate eye. Am J Ophthalmol. 1984;97:372–83.

    Article  CAS  PubMed  Google Scholar 

  99. Morrison JC, Van Buskirk EM. Microanatomy and modulation of the ciliary vasculature. Trans Ophthalmol Soc U K. 1986;105:131–9.

    PubMed  Google Scholar 

  100. Rohen JW, Funk RHW. Vasculature of the anterior eye segment. Prog Retin Eye Res. 1994;13:653–85.

    Article  Google Scholar 

  101. Kiel JW, Hollingsworth M, Rao R, Chen M, Reitsamer HA. Ciliary blood flow and aqueous humor production. Prog Retin Eye Res. 2011;30:1–17.

    Article  CAS  PubMed  Google Scholar 

  102. Müller H. Anatomisch-physiologishe Untersuchungen über die Retina des Menschen und der Wirbelthiere. Z für wissenschaftliche Zoologie. 1856;8:1–122.

    Google Scholar 

  103. Nettleship E. Unusual distribution of retinal blood-vessels: three cases. Br Med J. 1876;1:161–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Nettleship E. Cilio-retinal blood vessels (Additional cases and remarks). R Lond Ophthalmic Hosp Rep. 1879;9:161–7.

    Google Scholar 

  105. Lang W, Barrett JW. On the frequency of ciliary-retinal vessels and of pulsating veins. R Lond Ophthalmic Hosp Rep. 1888;12:59–60.

    Google Scholar 

  106. Jackson E. Cilio-retinal and other anomalous retinal vessels. Ophthalmic Rev. 1911;30:264–9.

    Google Scholar 

  107. Salzmann M. The anatomy and histology of the human eyeball in the normal state; its development and senescence. 183. Chicago: University of Chicago Press; 1912. p. 184.

    Google Scholar 

  108. Duke-Elder S. Textbook of ophthalmology. 2. St. Louis: C.V. Mosby; 1932. p. 1389.

    Google Scholar 

  109. Collier M. Frequence des vaisseaux cilioretiniens, leur rapport avec les ametropies, leur association avec d’autres anomalies du fond de l’oeil. Bull Soc Ophtalmol Fr. 1957;64:598–601.

    Google Scholar 

  110. Glees M. Über zilioretinale und optikoziliare Gefässe als allegemein diagnostischer Hinweis [Cilio-retinal and optico-retinal vessels as diagnostic pointers]. Klin Monatsbl Augenheilkd. 1956;128:580–92.

    CAS  Google Scholar 

  111. Loring EG. Anomalous circulation in the eye. Arch Ophthalmol Otolaryngol. 1872;2:1–10. plate B.

    Google Scholar 

  112. Birnbacher A. The cilio-retinal blood-vessels. Arch Ophthalmol. 1887;16:32–4.

    Google Scholar 

  113. Blunt MJ. Implications of the vascular anatomy of the optic nerve and chiasma. Proc R Soc Med. 1956;49:433–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Hayreh SS. The Cilio-Retinal Arteries. Br J Ophthalmol. 1963;47:71–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Bloch H. Ueber abnormen Verlauf der Papillengefässe. Klin Monatsbl Augenheilkd. 1906;44:413–8.

    Google Scholar 

  116. Parsons JH The ocular circulation (Arris and Gale Lecture Series). 903; p. 31 London: John Bale, Sons & Danielsson, Ltd.

  117. Wybar KC. Anastomoses between the retinal and ciliary arterial circulations. Br J Ophthalmol. 1956;40:65–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Steele EJ, Blunt MJ. The blood supply of the optic nerve and chiasma in man. J Anat. 1956;90:486–3.

    PubMed  PubMed Central  Google Scholar 

  119. Randall BA. Cilio-retinal or aberrant vessels. Trans Am Ophthalmol Soc. 1887;4:511–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Elschnig A. Cilioretinale Gefässe. Albrecht von Graefes Arch Ophthalmol. 1897;44:144–71.

    Article  Google Scholar 

  121. Fuchs E. Ueber Anomalien der Blutfässe im Sehnerveneintritt. Klin Monbl Augenheilkd. 1923;71:583–9.

    Google Scholar 

  122. Czermak W. Aus der Augenklinik des Prof. Fuchs. Beitrag zur Kenntniss der sog. Cilioretinalen Gefässe. Wien Klin Wochenschr. 1888;1:251–4.

    Google Scholar 

  123. Bailliart P. La circulation retinienne a l'Ètat normal et pathologique. Paris: G. Doin; 1923. p. 10–12.

    Google Scholar 

  124. Elschnig A. Ueber opticociliare Gefässe. Klin Monatsbl Augenheilkd. 1898;36:93–6.

    Google Scholar 

  125. Benson AH. Drawing showing an unusual course taken by a branch of the central artery of the disc. Trans Ophthalmol Soc U K 1883;3:101–2. plate IV, fig 101.

    Google Scholar 

  126. Hayreh SS A study of the central artery of the retina in human beings [Thesis for the Master of Surgery]: Panjab University (India); 1958.

  127. Coats G. Visible anastomoses on the papilla after obstruction of the central artery. R Lond Ophthalmic Hosp Rep. 1913;19:78–81.

    Google Scholar 

  128. Justice J Jr., Lehmann RP. Cilioretinal arteries. A study based on review of stereo fundus photographs and fluorescein angiographic findings. Arch Ophthalmol. 1976;94:1355–58.

    Article  PubMed  Google Scholar 

  129. Wang RS. [Cilioretinal arteries under fundus fluorescein angiography] (in Chinese). Zhonghua Yan Ke Za Zhi. 1991;27:219–20.

    CAS  PubMed  Google Scholar 

  130. Shihab ZM, Beebe WE, Wentlandt T. Possible significance of cilioretinal arteries in open-angle glaucoma. Ophthalmology 1985;92:880–3.

    Article  CAS  PubMed  Google Scholar 

  131. Hayreh SS. Acute retinal arterial occlusive disorders. Prog Retin Eye Res. 2011;30:359–94.

    Article  PubMed  PubMed Central  Google Scholar 

  132. Hegde V, Deokule S, Matthews T. A case of a cilioretinal artery supplying the entire retina. Clin Anat. 2006;19:645–7.

    Article  CAS  PubMed  Google Scholar 

  133. Parsa CF, Cheeseman EW, Maumenee IH. Demonstration of exclusive cilioretinal vascular system supplying the retina in man: vacant discs. Tr Am Ophthalmol Soc 1998;96:95–106.

    CAS  Google Scholar 

  134. Nettleship E. Notes on the blood-vessels of the optic disc in some of the lower animals. Trans Ophthalmol Soc U K 1905;25:338–9.

    Google Scholar 

  135. Singh (Hayreh) S, Dass R. The central artery of the retina. I. Origin and course. Br J Ophthalmol. 1960;44:193–212.

    Article  Google Scholar 

  136. Mann IC. Development of the Human Eye. Cambridge: Cambridge University Press, for the British Journal of Ophthalmology; 1928. p. 230–4.

    Google Scholar 

  137. Johnson GL. Contributions to the comparative anatomy of the mammalian eye, chiefly based on ophthalmoscopic examination. Philos Trans R Soc Lond B. 1901;194:1–82.

    Article  Google Scholar 

  138. Franck JL. Handbuch der Anatomie der Hausthiere, mit besonderer Berücksichtigung der Pferdes. 2 ed. Stuttgart: Schickhardt & Ebner; 1883.

    Google Scholar 

  139. Bach L. Ueber die Gefässe des Pferdeauges mit besonderer Berücksichtigung der Gefässversorgung der Aderhaut. Arch fűr wiss und praktische Tierheilkd. 1894;20:241–56.

    Google Scholar 

  140. Langenbacher L. Vergleichend anatomische Untersuchungen über die Blutfässe in der Netzhaut des Auges. Österreichische Vierteljahresschr für wiss. 1880;53:121–50.

    Google Scholar 

  141. Salzmann M. Über Rückbildung (Schwund) von cilio-retinalen arterien [Atrophy of the cilio-retinal arteries]. Albrecht Von Graefes Arch Ophthalmol. 1953;153:451–8.

    Article  CAS  PubMed  Google Scholar 

  142. Lim MC, Bateman JB, Glasgow BJ. Vortex vein exit sites. Scleral Coord Ophthalmol. 1995;102:942–6.

    CAS  Google Scholar 

  143. Kutoglu T, Yalcin B, Kocabiyik N, Ozan H. Vortex veins: anatomic investigations on human eyes. Clin Anat. 2005;18:269–73.

    Article  PubMed  Google Scholar 

  144. Spaide RF, Ledesma-Gil G, Gemmy Cheung CM. Intervortex venous anastomosis in pachychoroid-related disorders. Retina 2021;41:997–1004.

    Article  CAS  PubMed  Google Scholar 

  145. Hayreh SS, Baines JA. Occlusion of the vortex veins. An experimental study. Br J Ophthalmol. 1973;57:217–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Coats G. On the pathology of chorio-vaginal (posterior vortex) veins. Ophthalmol Rev. 1906;25:99–112.

    Google Scholar 

  147. Ruskell GL. Peripapillary venous drainage from the choroid: a variable feature in human eyes. Br J Ophthalmol. 1997;81:76–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Flugel-Koch C, May CA, Lutjen-Drecoll E. Presence of a contractile cell network in the human choroid. Ophthalmologica 1996;210:296–302.

    Article  CAS  PubMed  Google Scholar 

  149. Hayreh SS. In vivo choroidal circulation and its watershed zones. Eye (Lond). 1990;4:273–89.

    Article  PubMed  Google Scholar 

  150. Hayreh SS. Anterior ischemic optic neuropathy. Arch Neurol. 1981;38:675–8.

    Article  CAS  PubMed  Google Scholar 

  151. Torvik A. The pathogenesis of watershed infarcts in the brain. Stroke 1984;15:221–3.

    Article  CAS  PubMed  Google Scholar 

  152. Bogousslavsky J, Regli F. Unilateral watershed cerebral infarcts. Neurology 1986;36:373–7.

    Article  CAS  PubMed  Google Scholar 

  153. Hayreh SS. Inter-individual variation in blood supply of the optic nerve head. Its importance in various ischemic disorders of the optic nerve head, and glaucoma, low-tension glaucoma and allied disorders. Doc Ophthalmol. 1985;59:217–46.

    Article  CAS  PubMed  Google Scholar 

  154. Hayreh SS. Submacular choroidal vascular bed watershed zones and their clinical importance. Am J Ophthalmol. 2010;150:940–1.

    Article  PubMed  Google Scholar 

  155. Hayreh SS, Baines JA. Occlusion of the posterior ciliary artery. III. Effects on the optic nerve head. Br J Ophthalmol. 1972;56:754–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Hayreh SS. Anterior ischaemic optic neuropathy. I. Terminology and pathogenesis. Br J Ophthalmol. 1974;58:955–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Hayreh SS. Acute ischemic disorders of the optic nerve: pathogenesis, clinical manifestations, and management. Ophthalmol Clin North Am. 1996;9:407–42.

    Google Scholar 

  158. Hayreh SS, Podhajsky PA, Zimmerman B. Ocular manifestations of giant cell arteritis. Am J Ophthalmol. 1998;125:509–20.

    Article  CAS  PubMed  Google Scholar 

  159. Virdi PS, Hayreh SS. Anterior segment ischemia after recession of various recti. An experimental study. Ophthalmology. 1987;94:1258–71.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Supported by research grants from the British Medical Research Council, EY-1151, EY-1576, EY3330, and RR-59 from the U.S. National Institutes of Health, in part by unrestricted grants from Research to prevent Blindness, Inc., New York.

Author information

Authors and Affiliations

  1. Department of Ophthalmology and Visual, College of Medicine, University of Iowa, Iowa City, IA, USA

    Sohan Singh Hayreh

  2. (no affiliation), Iowa City, IA, USA

    Shelagh Bell Hayreh

Authors
  1. Sohan Singh Hayreh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shelagh Bell Hayreh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SSH was responsible for the writing and editing of the final manuscript. SBH provided feedback on the manuscript.

Corresponding author

Correspondence to Shelagh Bell Hayreh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Due to Dr. Hayreh's death, some errors and omissions may exist in the article as published.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hayreh, S.S., Hayreh, S.B. Uveal vascular bed in health and disease: uveal vascular bed anatomy. Paper 1 of 2. Eye 37, 2590–2616 (2023). https://doi.org/10.1038/s41433-023-02416-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41433-023-02416-z

Search

Advanced search

Quick links