Abstract
Light-microscopic and ultrastructural analysis of the ocular tissues of the North American opossum (Didelphis virginiana) revealed that the arterial and venous segments of retinal vessels, including capillaries of the smallest calibre, occur in pairs. They do not form anastomotic networks, the common pattern in mammals with vascularised retinae, but instead the two segments of the pair join to form hairpin end loops. The pairedd vessels, with the arteriolar limb usually on the vitread aspect, penetrate the retina and branch to form three distinct layers of capillaries. The most superficial lies in the nerve fiber layer, the middle is situated in the inner nuclear layer and the deepest extends to the external limiting membrane, which is considerably deeper than in normal mammalian holangiotic retinae. The paired capillaries display classical morphological features of central nervous system capillaries, i.e., they are lined by continuous endothelial cells united by tight junctions. The lining endothelium is supported by a distinct basal lamina that splits to envelop pericytes. The latter, although abundant, are invariably interposed between the two vessels that form each vascular unit. Phylogenetic and functional aspects of this unique form of retinal vascularisation are discussed.
Similar content being viewed by others
References
Bloodworth JMB, Gutgesell HP (1965) Retinal vasculature of the pig. Light and electron microscope studies. Exp Eye Res:174–178
Braekevelt CR (1976) Fine structure of the retinal pigment epithelium and tapetum lucidum of the opossum (Didelphis virginiana). J Morphol 150:213–226
Bubis JJ (1962) The blood vessels in the central nervous system of the opossum. In: SS Breese (ed) Electron Microscopy, vol 2. Fifth International Congress For Electron Microscopy—Philadelphia. Academic Press, New York, N-12
Buttery RG, Haight JR, Bell K (1990) Vascular and avascular retinae in mammals. A funduscopic and fluorescein angiographic study. Brain Behav Evol 35:156–175
Chase J (1982) The evolution of retinal vascularization in mammals: a comparison of vascular and avascular retinae. Ophthalmology 89:1518–1525
Chase J, Graydon ML (1990) The eye of the northern brown bandicoot,Isoodon macrourus. In: Seebeck JH, Brown PR, Wallis RL, Kemper CM (eds) Bandicoots and Bilbies. Surrey Beatty and Sons, Sydney, pp 117–122
Craigie EH (1938) The blood vessels in the central nervous system of the kangaroo. Science 88:359–360
Duke-Elder S (1958) The eye of evolution. In: System of Ophthalmology, Henry Kimpton, London, pp 438–441
Freeman B, Tancred E (1978) The number and distribution of ganglion cells in the retina of the brush-tailed possum,Trichosurus vulpecula. J Comp Neurol 177:557–568
Johnson GL (1901) Contributions to the comparative anatomy of the mammalian eye, chiefly based on ophthalmoscopic examination. Phil Trans R Soc Lond [Biol] 197:1–82
Johnson GL (1968) Ophthalmoscopic studies on the eyes of mammals. Phil Trans R Soc Lond [Biol] 254:207–220
Kirsch JAW (1977) The classification of marsupials, with specia reference to karyotypes and serum proteins. In: Hunsker D (ed) The Biology of Marsupials. Academic Press, New York, pp 1–50
Kissen AT, Bloodworth JMB (1961) Ultrastructure of retinal capillaries of the rat. Exp Eye Res 1:1–4
Kolb H, Wang HH (1985) The distribution of photoreceptors, dopaminergic amacrine cells and ganglion cells in the retina of the North American opossum (Didelphis virginiana). Vision Res 25:1207–1221
Leeson TS (1979) Rat retinal blood vessels. Canad J Ophthal 17:21–28
Mark RF, Marotte LR (1992) Australian marsupials as models for the developing mammalian visual system. Trends Neurosci 15:51–57
O'Day KC (1936) A preliminary note on the presence of double cones and oil droplets in the retina of marsupials. J Anat 70:465–467
O'Day KC (1938) The retina of the Australian mammal. Med J Aust 1:326–328
Rapaport DH, Wilson PD, Rowe MH (1981) The distribution of ganglion cells in the retina, of the North American opossum (Didelphis virginiana). J Comp Neurol 199:465–480
Scharrer E (1939a) The functional significance of the capillary bed in the brain of the opossum. Anat Rec 75:319–340
Scharrer E (1939b) The regeneration of end-arteries in the opossum brain. J Comp Neurol 70:69–76
Sunderland S (1941) The vascular pattern in the central nervous system of the monotromes and Australian marsupials. J Comp Neurol 75:123–129
Tancred E (1981) The distribution and sizes of ganglion cells in the retinas of five Australian marsupials. J Comp Neurol 196:585–603
Tilton RG, Miller EJ, Kilo C, Williamson JR (1985) Pericyte form and distribution in rat retinal and uveal capillaries. Invest Ophthal Vis Sci 26:68–73
Walls GL (1939) Notes on the retinae of two opossum genera. J Morphol 64:67–87
Wislocki GB (1939) The unusual mode of development of the blood vessels of the opossum's brain. Anat Rec 74:409–427
Wislocki GB (1940) Peculiarities of the cerebral blood vessels of the opossum: diencephalon, area postrema and retina. Anat Rec 78:119–131
Wislocki GB, Campbell ACP (1937) The unusual manner of vascularization of the brain of the opossum (Didelphis virginiana). Anat Rec 67:177–191
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
McMenamin, P.G., Krause, W.J. Morphological observations on the unique paired capillaries of the opossum retina. Cell Tissue Res 271, 461–468 (1993). https://doi.org/10.1007/BF02913728
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02913728