Vascular and Avascular Retinae in Mammals

Abstract

Intraretinal blood vessels are present in some and absent in other vertebrate species, including the mammals. Among the marsupials, both vascular and avascular retinae are seen. We determined the funduscopic appearance of the eye, investigated the functional aspects of ocular blood flow in both types of retina in marsupials and compared our results with known patterns in placental mammals. The Australian polyprotodont marsupials, the Tasmanian devil, Sarcophilus harrisii, and the quoll, Dasyurus viverrinus, together with an American polyprotodont, the Virginia opossum, Didelphis virginiana, demonstrate variable degrees of tapetal differentiation, pigmentation and a very close parallel course of their intraretinal arteries and veins over considerable distances. Using the technique of fluorescein angiography, we found that retinal blood flow in the 3 vascular Australian species commenced with arterial filling. Early venous was seen next, followed by the capillary blush. This unusual sequence of vascular flow differs from that of the arterial-capillary-venous filling seen in placental mammals. This difference is most likely a consequence of the known looped, end artery organisation found within marsupial nervous systems, of which the retinae are a part. The 2 diprotodont marsupials examined, the brushtail possum, Trichosurus vulpecula, and the sugar glider, Petaurus breviceps, possess avascular retinae. Only a small residual tuft of fluorescein-impermeable vessels projects from the optic disc into the vitreous. Interestingly, the structural complexity of the central visual system in diprotodonts all of whom possess avascular retinae) is commonly accepted as being greater than that of the stem polyprotodont line (which possess vascular retinae). If retinal function matches this internal complexity, then retinal avascularity may, as in birds, be associated with superior vision. However, as the retinae of these mammals clearly lack any nutritive mechanisms directly analogous to those in the retinae of, say, birds or the megachiropteran bats, their retinal nutritive pathways remain enigmatic.