The 3D Retinal Capillary Circulation in Pigs Reveals a Predominant Serial Organization

Abstract

PURPOSE. To establish a model of the retinal capillary circulation in pigs, which in many aspects is close to the human retina.METHODS. Using high density confocal microscopy image stacks of immunolabeled porcine retinal whole mounts, microvessels close to the optic nerve head were traced in three dimensions. The direction of flow of individual capillaries was deduced from their arteriolar and/or venous connections.RESULTS. From major arteries, second-order arteries traversed the nerve fiber layer and resolved exclusively into the superficial vascular plexus (SVP), which dichotomized the blood flow between radial peripapillary capillaries (RPCs) on one side and the intermediate (IVP) and deep vascular plexus (DVP) on the other. Each RPC was supplied by one or several capillaries from the SVP and drained to the IVP or DVP. The DVP was a mosaic of approximately 300 to 600 lm wide anastomotic watersheds, each drained by one or two venules connected to major veins. A presumptive direction of flow could be determined for >90% of capillaries. These results suggest a model of the capillary circulation in which the three microvessel layers are serially organized with RPCs are in parallel between the SVP and IVP or DVP.CONCLUSIONS. In the peripapillary retina of pigs, microvascular layers have a serial arrangement, with RPCs emerging from the SVP and draining to the IVP or DVP; hence, connected in parallel of this scheme. The bulk of flow, therefore, traverses the SVP and DVP successively. This organization contributes to the higher oxygen saturation in the SVP and RPCs than in the DVP. Physiopathologic implications of this model regarding retinal diseases are discussed.

Segmentation of the Four-Layered Retinal Vasculature Using High-Resolution Optical Coherence Tomography Angiography Reveals the Microcirculation Unit

“…Toussaint et al 1 reported that RPCs came from the disc and differed from other retinal capillaries, whereas Henkind et al 2,17 suggested that these capillaries originated from retinal arterioles. Moreover, in a recent study by Fouquet et al, 18 With circumpapillary OCT B-scans, Muraoka et al 19 demonstrated the existence of major retinal vessels in the RNFL. However, HR-OCTA in the present study revealed the presence of major vessels in the central macular area in a slab for the GCL; importantly, this slab showed the capillary-free zone around arteries and arterioles, facilitating differentiation of arterial and venous systems as well as capillary beds and retinal microcirculatory units consisting of arterial and venous channels with intervening capillaries.…”

Human Parafoveal Capillary Vascular Anatomy and Connectivity Revealed by Optical Coherence Tomography Angiography

“… 8 , 16 , 31 , 43 There is excellent evidence for the anatomical arrangement of capillaries in peculiar spider-like “vortices” in the DCP, in the current, as well as other OCTA 14 , 15 and histologic studies. 4 , 5 , 44 However, the presence of the central venular connection of these vortices should not be conflated with a primary venous function of the DCP, given the requirement for high oxygen in the OPL. Physiologically, it seems the high demand and consumption of oxygen in the OPL precludes the possibility that this capillary layer (DCP) would consist exclusively of a venular drainage basin, carrying deoxygenated blood.…”

Three-Dimensional Microscopy Demonstrates Series and Parallel Organization of Human Peripapillary Capillary Plexuses

“…Our results support the seminal work by Paul Henkind 39 in 1967 who found that the RPC are not derived from arterioles within the optic disk but rather from arterioles that supply the peripapillary regions. Toussaint and colleagues 17 speculated that the RPC might be supplied by the SCP, but it was the recent work using pig eyes, by Fouquet et al 40 that showed that the SCP is the exclusive recipient of blood flow from retinal arterioles. Our study was able to confirm similar findings in human eyes.…”