The Representation of Retinal Blood Vessels in Primate Striate Cortex

Abstract

The blood vessels that nourish the inner retina cast shadows on photoreceptors, creating "angioscotomas" in the visual field. We have found the representations of angioscotomas in striate cortex of the squirrel monkey. They were detected in 9 of 12 normal adult animals by staining flatmounts for cytochrome oxidase activity after enucleation of one eye. They appeared as thin profiles in layer 4C radiating from the blind spot representation. Angioscotomas can be regarded as a local form of amblyopia. After birth, when light strikes the retina, photoreceptors beneath blood vessels are denied normal visual stimulation. This deprivation induces remodeling of geniculocortical afferents in a distribution that corresponds to the retinal vascular tree. Angioscotoma representations were most obvious in monkeys with fine ocular dominance columns and were invisible in monkeys with large, well segregated columns. In monkeys without columns, their width corresponded faithfully to the inducing retinal shadow, making it possible to calculate the minimum shadow required to produce a cortical representation. The "amblyogenic threshold" was calculated as the fraction of the pupil area eclipsed to trigger remodeling of geniculocortical afferents. It was found to be constant over retinal eccentricity, vessel size, and shadow size. Ambliogenic shadows only three to four cones wide were sufficient to generate a cortical representation, testifying to the remarkable precision of the cortical map. The representations of retinal blood vessels separated by only 0.65 degrees were resolvable in the cortex, yielding an upper limit on cortical resolution of 340 microm in layer 4C.

Human trichromacy revisited

“…Shadow of the retinal blood vessels. The cones in the deep shadow of the blood vessels do not signal to cortex (45,46). The rate of cone photopigment isomerizations in the penumbra of the blood vessels could play a role at the detection threshold; our simulations show that there is enough information in the penumbral isomerization rates to detect the cone-silent signal.…”

The Effect of Angioscotomas on Map Structure in Primary Visual Cortex

“…The discovery of cortical representations of angioscotomas provides additional clear evidence that imbalance of visual activity can influence the structure of the visual cortex. Adams and Horton (2003b) found that the degree of angioscotoma representation varied greatly between individuals and was correlated with OD column periodicity ( Fig. 1C-F ).…”

“…The thin processes extending from the optic disc are the right-eye angioscotoma representations. C-F, Schematic characterization of the relationship between OD column periodicity and angioscotoma visibility in the cortex (pictures are diagrams rather than actual data) (Adams and Horton, 2003b Adams and Horton (2002). C-F, Reprinted with permission from Adams and Horton (2003b).…”

“…1C-F ). In animals with fine columns, the angioscotoma representations were outlined by a strip of opposing contrast, an effect that Adams and Horton (2003b) termed "frosting" (Fig. 1 D).…”

Special features of human retinal angiogenesis

“…Approximately 40% of incident photons encounter intraretinal vessels in the extrafoveal macula, and retinal vessels cast shadows upon underlying photoreceptors that produce 'angioscotomas' in the striate cortex. 20,21 Early investigators thought that the presumptive fovea was initially vascularized, but that vessels then degenerated to leave an avascular zone. Engerman 22 long ago provided contrary evidence, and we and others 2,23 firmly established in monkeys and humans that the presumptive fovea is never vascularized, and that radially growing vessels simply skirt around it.…”