Choroidal vascular permeability in visually regulated eye growth.

Abstract

The choroidal thickness fluctuates both diurnally and in response to changes in visual input. The fluctuations may represent a physiologic means of aligning the retinal photoreceptors with the focal position of distant images during the emmetropization process. To evaluate the basis for choroidal thickness changes, we studied the sources of the extravascular fluid in the chick choroid in two visually-regulated ocular growth conditions: accelerated ocular growth in goggle-induced form-deprivation myopia and ocular growth retardation in the recovery from myopia after goggle removal. Two week old chicks, controls, myopic and those recovering from myopia, received fluorescein dextran (MW = 140,000) as a tracer. It was given by intravenous injection to identify a potential vascular pathway and by intracameral injection to identify a potential pathway from the anterior chamber to the suprachoroidal space. Using a microscopically positioned needle, clear fluid was aspirated from the suprachoroidal space of the enucleated chick eye; this fluid presumably corresponds to the contents of the lacunae, prominent lymphatic-like structures of the chick choroid. Plasma, aqueous humor and suprachoroidal fluid were sampled 1 hr after injection and assayed for both protein content and the tracer dye. Sulfated glycosaminoglycans were assayed in the suprachoroidal fluid, choroid and sclera under each experimental condition. In control chicks, aqueous humor and suprachoroidal fluid protein concentrations were about 0.8 and 9% of plasma levels respectively. Aqueous humor protein concentration was unaltered in myopic or recovering eyes. Suprachoroidal fluid protein concentration in myopic eyes fell dramatically to 1.5% of plasma levels (P < 0.001). In contrast, recovery from myopia led to a marked increase in suprachoroidal fluid protein level to 30% of that in plasma (P < 0.001). None of the procedures affected suprachoroidal fluid protein in the contralateral control eyes. In all three groups of chicks, fluorescein dextran distribution in the suprachoroidal fluid at 1 hr after intravenous injection tracked protein levels, with reduced levels in myopic eyes and elevated levels in recovering eyes. After intracameral injection, suprachoroidal fluid dextran levels were higher in injected eyes of control chicks (P < 0.01) and in recovering eyes (P < 0.001) but lower in myopic eyes (P < 0.01), compared to the levels in the respective contralateral non-injected eyes in each group. Sulfated glycosaminoglycan levels were at the limits of detection in the suprachoroidal fluid under all conditions and, on a whole choroid basis, were unaltered in the choroid in either myopia or recovery. Suprachoroidal fluid is lymph-like in nature and largely derives from plasma. Sulfated glycosaminoglycan levels do not seem to regulate the fluid content of the choroid in either myopia or recovery. Instead, the changes in protein and marker dye levels in myopic and recovering eyes suggest markedly altered choroidal circulatory dynamics and capillary permeability in both conditions.