Functional end-arterial circulation of the choroid assessed by using fat embolism and electric circuit simulation

Abstract

The discrepancy in the choroidal circulation between anatomy and function has remained unsolved for several decades. Postmortem cast studies revealed extensive anastomotic channels, but angiographic studies indicated end-arterial circulation. We carried out experimental fat embolism in cats and electric circuit simulation. Perfusion defects were observed in two categories. In the scatter perfusion defects suggesting an embolism at the terminal arterioles, fluorescein dye filled the non-perfused lobule slowly from the adjacent perfused lobule. In the segmental perfusion defects suggesting occlusion of the posterior ciliary arteries, the hypofluorescent segment became perfused by spontaneous resolution of the embolism without subsequent smaller infarction. The angiographic findings could be simulated with an electric circuit. Although electric currents flowed to the disconnected lobule, the level was very low compared with that of the connected ones. The choroid appeared to be composed of multiple sectors with no anastomosis to other sectors, but to have its own anastomotic arterioles in each sector. Blood flows through the continuous choriocapillaris bed in an end-arterial nature functionally to follow a pressure gradient due to the drainage through the collector venule.

Figure 1

Two types of perfusion defects in the choroid were observed in the fat embolism model by using triolein emulsion. (a) Multiple patch defects indicate that arterioles feeding the choriocapillary lobule are occluded. (b) Segmental hypofluorescence indicates that the short posterior ciliary artery supplying the segment is embolized.

Figure 2

Fluorescein angiography obtained in cat eyes after triolein fat embolism. (a–d) Multiple hyperfluorescent and hypofluorescent patches are observed, representing perfused and embolized choriocapillaris lobules. Red dots and circles represent the locations of the perfused and embolized terminal arterioles, respectively. The expansion of the hyperfluorescent area clearly demonstrates the blood flow beyond the boundary of each lobule (arrowheads). (e–h) Sectorial hyperfluorescence and hypofluorescence represent the occlusion of the short posterior ciliary arteries. After approximately 10 seconds, perfusion defects were resolved without any subsequent defects.

Figure 3

Electric circuit simulation of the choroid. (a–c) The normal choroid shows that electric currents follow the voltage gradient and do not cross the boundary of the hexagon. As the resistance of the boundary becomes lower, the blood flows become more evenly distributed in the hexagon. (d) When one anode is disconnected from the hexagon, the voltage gradient is reversed. Electric currents flow from the adjacent hexagons and cross the boundary to the disconnected hexagon, but at very low level. (e) Reduction of electric current is more severe in sectorial disconnection. Diameter ratio indicates ratio of the collector venule at the lobular boundary and the choriocapillaris. Electric resistance is inversely proportional to the fourth power of the radius (r⁴) by Poiseuille’s equation.

Figure 4

Changes in electric current influx into a hexagon due to change in boundary resistance. When the resistance of the boundary is lower, more currents flow normally, but to a lesser degree in the disconnected hexagons.

Figure 5

A functional end-arterial model of the choroidal circulation. Red and gray vascular channels represent perfused and non-perfused status, respectively. (a) When a terminal arteriole is obstructed, the choriocapillaris lobule becomes ischemic because the blood is drained through the venous channel in the periphery of the lobule. (b) A sector becomes ischemic when the posterior ciliary artery is occluded, as there is no arteriolar anastomosis among the other sectors. (c) When triolein embolus flows down to a small arteriole, perfusion of the choriocapillaris is restored owing to the extensive arteriolar anastomosis within the sector.

Figure 6

Schematic drawings of the choroidal lobule and its electric circuit model. (a) A simple example to explain Kirchhoff’s law. (b) The choriocapillaris of the posterior pole is arranged in a lobular pattern surrounded by the collector venules (cv). The feeding arteriole (*) joins the choriocapillaris at the center of the lobule. The draining venules (dv) are connected to the periphery of the lobules. (c) The electric circuit model of the choroidal lobule is arranged as a dual-layered hexagon. The boundary represents the collector venules (cv), and its electric resistance was set to 1 to 1/16 of the resisters arranged in the inner circuit representing the choriocapillaris. The voltage of the anode (*) was set at the center of the hexagon as 50 V. The cathode (dv) was arranged at the periphery of the hexagon representing the draining venules, and its voltage was set as 10 V. (d) Hexagons were arrayed as 5 × 5 to represent the choriocapillary bed. (e) Disconnecting an anode from one hexagon represents embolism of a single feeding arteriole. (f) Disconnecting anodes from a sector of hexagons represents embolism of a posterior ciliary artery.