Retinal crosstalk in the mammalian visual system

The existence and functional relevance of efferent optic nerve fibers in mammals has long been debated. While anatomical evidence for cortico-retinal and retino-retinal projections is substantial, physiological evidence is lacking as efferent fibers are few in number and severed in studies of excised retinal tissue. Here we show that interocular connections contribute to retinal bioelectrical activity in adult mammals. Full-field flash electroretinograms (ERGs) were recorded from one or both eyes of Brown-Norway rats under dark-adapted (n=16) and light-adapted (n=11) conditions. Flashes were confined to each eye by an opaque tube that blocked stray light. Monocular flashes evoked a small (5-15μV) signal in the non-illuminated eye, which was named "crossed ERG" (xERG). The xERG began under dark-adapted conditions with a positive (xP1) wave that peaked at 70-90ms and ended with slower negative (xN1) and positive (xP2) waves from 200-400ms. xN1 was absent under light-adapted conditions. Injection of tetrodotoxin in either eye (n=15) eliminated the xERG. Intraocular pressure elevation of the illuminated eye (n=6) had the same effect. The treatments also altered the ERG b-wave in both eyes, and the alterations correlated with xERG disappearance. Optic nerve stimulation (n=3) elicited a biphasic compound action potential in the non-stimulated nerve with 10-13ms latency, implying the xERG comes from slow-conducting (W-type) fibers. Monocular dye application (n=7) confirmed the presence of retino-retinal ganglion cells in adult rats. We conclude that mammalian eyes communicate directly with each other via a handful of optic nerve fibers. The crosstalk alters retinal activity in rats, and perhaps other animals.

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