Patterns of Cortical Visual Field Defects From Embolic Stroke Explained by the Anastomotic Organization of Vascular Microlobules

Abstract

The cerebral cortex is supplied by vascular microlobules, each comprised of a half dozen penetrating arterioles that surround a central draining venule. The surface arterioles that feed the penetrating arterioles are interconnected via an extensively anastomotic plexus. Embolic occlusion of a small surface arteriole rarely produces a local infarct, because collateral blood flow is available through the vascular reticulum. Collateral flow also protects against infarct after occlusion of a single penetrating arteriole. Cortical infarction requires blockage of a major arterial trunk, with arrest of blood flow to a relatively large vascular territory. For striate cortex, the major vessels compromised by emboli are the inferior calcarine and superior calcarine arteries, as well as the distal branches of the middle cerebral artery. Their vascular territories have a fairly consistent relationship with the retinotopic map. Consequently, occlusion by emboli results in stereotypical visual field defects. The organization of the arterial supply to the occipital lobe provides an anatomical explanation for a phenomenon that has long puzzled neuro-ophthalmologists, namely, that of the myriad potential patterns of cortical visual field loss, only a few are encountered commonly from embolic cortical stroke.

FIG. 1.

Distribution of arterioles and venules in macaque striate cortex. A. A 150-μm tangential section in layer 3 shows profiles of arterioles and venules in cross-section. They are labeled by diaminobenzidine, reflecting the distribution of red blood cells in the unperfused tissue. Arterioles are small and surrounded by pale, capillary-free zones. The venules are larger, with radiating branches that drain the surrounding capillary bed. B. Same image, identifying arterioles (red dots, n = 101) and venules (blue dots, n = 34). Each microvascular lobule comprises an irregular array of arterioles surrounding a single venule or, occasionally, pair of venules.

FIG. 2.

Surface arterioles are organized into a dense reticulum. A. A 150-μm section through the surface arteriolar circulation of striate cortex prepared from a different macaque after removal of surface venules. Clotted red cells are labeled by diaminobenzidine. Although many vessels are filled incompletely, the anastomotic arrangement of the surface arterioles is evident. B. Drawing of the arteriolar reticulum, prepared by using a microscope with a camera lucida attachment. Dots mark the origin of arterioles that penetrate the cortex, located either on the reticulum or its fine terminal branches.

FIG. 3.

Cutaway diagram reveals vascular microlobules of the cerebral cortex, each comprised of an approximately hexagonal array of penetrating arterioles that supply the capillary bed, which drains into a central venule. A cylindrical capillary-free zone surrounds each penetrating arteriole. The surface arterioles form a reticulum to allow efficient delivery of blood to satisfy local fluctuations in metabolic demand. Flow is controlled by a system of sphincters located at both arteriolar junctions and penetration sites of descending arterioles. The anastomotic organization of the surface arterioles renders the cortex resistant to microinfarction by emboli because after occlusion of a vessel, any given location can still be perfused by blood flowing from another direction. Even occlusion of a penetrating arteriole may be tolerated by collateral flow through the capillary bed.

FIG. 4.

Arterial circulation of the primary visual cortex. A. Medial view of the right occipital lobe with the inferior lip of the calcarine sulcus deflected downward by a muscle hook to show the bifurcation of the calcarine artery. The superior calcarine artery(red arrow) crosses the calcarine sulcus to feed the upper calcarine bank and a portion of the cuneus. The inferior calcarine artery (blue arrow) supplies the lower calcarine bank and some of lingual gyrus. B. Drawing of the occipital circulation, after Polyak (40), demonstrates territories supplied by the superior (red) and inferior (blue) calcarine arteries. He incorrectly shows the arteries bifurcating serially until they end in terminal branches. Dotted line corresponds to perimeter of primary visual cortex. *Foveal representation.

FIG. 5.

Embolic cortical visual field defects. A. Complete homonymous hemianopia from an embolus (arrow) proximal to the bifurcation of the superior (red) and inferior (blue) calcarine arteries. B. Homonymous hemianopia with macular sparing, owing to collateral flow from the distal middle cerebral artery (green). C. Hemimacular scotoma from an embolus occluding distal branches from the middle cerebral artery. D. Quadrantanopia from an embolus distal to the bifurcation of the calcarine artery. The border between the vascular territories of the superior and inferior calcarine arteries is placed arbitrarily along the horizontal meridian. E. Quadrantanopia with macular sparing. F. Quadrantanopia with both macular and peripheral sparing, from an embolus lodged distally in a calcarine artery branch.

FIG. 5.

Embolic cortical visual field defects. A. Complete homonymous hemianopia from an embolus (arrow) proximal to the bifurcation of the superior (red) and inferior (blue) calcarine arteries. B. Homonymous hemianopia with macular sparing, owing to collateral flow from the distal middle cerebral artery (green). C. Hemimacular scotoma from an embolus occluding distal branches from the middle cerebral artery. D. Quadrantanopia from an embolus distal to the bifurcation of the calcarine artery. The border between the vascular territories of the superior and inferior calcarine arteries is placed arbitrarily along the horizontal meridian. E. Quadrantanopia with macular sparing. F. Quadrantanopia with both macular and peripheral sparing, from an embolus lodged distally in a calcarine artery branch.

FIG. 6.

Disallowed embolic cortical visual field defects. A. Hemiannular scotoma, from an infarct that crosses vascular territories. B. Sectoranopia from a long, thin infarct running roughly parallel to an isopolar ray in the visual field map. C. Missing temporal monocular crescent, from infarct confined to its representation (dotted region). D. Peripheral scotoma, sparing the central 24°.E. Homonymous hemianopia, sparing a vertical strip of uniform azimuth along the vertical meridian. F. Isolated homonymous scotomata, from focal cortical infarcts. In these schematic examples, two ~5-mm infarcts are shown from an embolus imagined to arrest surface arteriolar flow despite availability of collaterals. They would produce scotomas in the inferior visual field of vastly different size. A microinfarct from occlusion of a penetrating vessel is also shown, with a corresponding microscotoma in the peripheral upper field. Visual fields riddled with homonymous microscotomata from emboli are not encountered in clinical practice.

FIG. 6.

Disallowed embolic cortical visual field defects. A. Hemiannular scotoma, from an infarct that crosses vascular territories. B. Sectoranopia from a long, thin infarct running roughly parallel to an isopolar ray in the visual field map. C. Missing temporal monocular crescent, from infarct confined to its representation (dotted region). D. Peripheral scotoma, sparing the central 24°.E. Homonymous hemianopia, sparing a vertical strip of uniform azimuth along the vertical meridian. F. Isolated homonymous scotomata, from focal cortical infarcts. In these schematic examples, two ~5-mm infarcts are shown from an embolus imagined to arrest surface arteriolar flow despite availability of collaterals. They would produce scotomas in the inferior visual field of vastly different size. A microinfarct from occlusion of a penetrating vessel is also shown, with a corresponding microscotoma in the peripheral upper field. Visual fields riddled with homonymous microscotomata from emboli are not encountered in clinical practice.