Physiology

Blood Flow

Eighty-five percent of the total blood supply to the eye is distributed to the choroid and only 4 percent to the retina. The remaining is distributed to the ciliary body and the iris. The human retinal blood flow has been calculated to be between 35 and 80 |mL/min. The oxygen extraction for the retinal blood is about 38 percent. In contrast, the oxygen extraction from the uveal blood is very low, with the arteriovenous difference for the choroidal blood about 3 percent. Choroidal blood flow is extremely high, probably because of the large caliber of the vascular lumen. The choroidal blood flow near the fovea and around the optic nerve head is much higher than the blood flow in the periphery of the eye. Despite the low oxygen extraction rate, about 60 percent of oxygen and 75 percent of glucose are delivered by the choroidal circulation. The high volume of choroidal blood flow may contribute to the removal of heat generated during visual transduction, to the removal of fluid from the outer retina, and to meeting the metabolic needs of the retina. Proteins and other substances of high molecular weight can enter the interstitial space through the fenestration of the choroidal capillaries. Retinal binding protein, vitamin A, and many other micronutrients and ions become available to the RPE for transport to the outer layers of the retina. Both active and passive transport mechanisms facilitate the movement of selected nutrients and waste products across the outer blood-retinal barrier. During aging, lipoprotein accumulates in Bruch's membrane from rod outer segment degradation, which may obstruct the movement of water and waste products across the RPE.

Regulation of Blood Flow

The retinal blood flow is determined by the perfusion pressure and the diameter of the retinal capillaries. Local myogenic responses, metabolic factors, and endothelium-derived substances influence the vascular resistance. The retinal blood flow is autoregulated through modifications of the vascular resistance, that is, changes of the contractile state of the retinal arterioles. Because of the lack of precapillary sphincter in retinal arterioles, metabolic and myogenic stimuli are the major modifiers of the retinal arteriolar diameter. The retinal blood flow is maintained relatively constant despite moderate variations in perfusion pressure, up to 41 percent of baseline values of systemic blood pressure or during an increase of intraocular pressure up to 30mmHg. As a result, the inner retina tissue partial pressure of O2 (Po2) is maintained at constant values during moderate reductions of the perfusion pressure. In contrast, there is no autoregulation in the choroidal vasculature. Choroidal blood flow changes little during sudden increments in blood pressure, as an increased sympathetic activity and consequent vasoconstriction of the choroidal vessels maintain a constant choroidal blood flow. The parasympathetic system seems to play little role in the regulation of the choroidal blood flow. Loss of sympathetic innervation may cause accumulation of fluid in the retina and retinal edema. This is important in diseases such as diabetes and hypertension, in which autonomic control is altered. The choroidal vessels contain a-adrenergic vasoconstrictor receptors but no b-adrenergic vasodilator receptors.

Mechanical stretch and increases in the transmural pressure stimulate the endothelial cells to release contracting factors. The factors released by the retinal metabolism also optimize retinal blood flow according to metabolic needs. These factors include Po2, the tissue partial pressure of CO2 (Pco2), nitric oxide (NO), prostaglandins (PGs, including PGE2, PGF2, PGH2, and fo forth), and lactate, released either in the blood or in the surrounding retinal arteriole glial or neuronal tissue. Hyperoxia induces vasoconstriction, whereas hypoxia induces vasodilatation of retinal arterioles. The Po2 values measured in the inner retina up to half of its thickness remained stable during hypoxia. In contrast, the Po2 measured near the choroid and in the outer retina decreased in a linear manner according to the variations of systemic Po2. High oxygen delivery by the choroidal circulation is thus necessary for photoreceptors to function properly. Systemic hypoxia induces an increase in the retinal lactate release, which dilates the arteriolar wall. A rise in Pco2 induces an increase in blood flow.

The endothelium influences the vascular tone by releasing either endothelium-derived relaxing factors, such as NO and PGE2 and PGF2, or contracting factors, such as endothelin-1, thromboxane A2, and PGH2. These molecules induce relaxation or contraction of vascular smooth muscle cells and capillary pericytes, thus affecting the diameters of arterioles and capillaries. NO released by endothelial cells acts on the vascular smooth muscle cells and accounts for the biologic properties of the endothelium-derived relaxing factor. There is a gradient and a continuous production of NO by the retinal tissue. The effect of endothelin on a vascular bed is difficult to predict, because apart from causing vasoconstriction, it can also release the vasodilators prostacyclin and NO. PGE2 and PGF2 are the predominant PGs produced by the retina and choroid, and they induces vasodilatation of the retinal arterioles.

Retinal Oxygen Distribution

The retina has a high rate of oxygen consumption and metabolism for visual transduction. The PO2 is heteroge-neously distributed close to the vitreoretinal interface. O2 diffusion from the retinal arterioles affects the juxta-arteriolar preretinal and inner retinal layer's Po2, which is higher than that of the intervascular areas due to oxygen consumption by retinal cells. In contrast, the preretinal and inner retinal (30% depth) Po2 far beyond the retinal vessels remains constant in all retinal areas. The intraretinal PO2 gradually decreases from both the retinal surface and the choroid toward the midretina, with the minimal value at 50 percent of retinal depth. The Po2 near RPE is significantly higher than it is at the inner limiting membrane level, due to much higher O2 delivery by the choroidal circulation than by the retinal circulation.

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