Evidence for passive electrotonic interactions in red rods of toad retina

Abstract

SINCE Baylor, Fuortes and O'Bryan¹ first demonstrated interactions between vertebrate photoreceptor cells, many types of inter-receptor influences have been described^2–10. While some of these interactions are mediated by horizontal cells^1,2,6, others apparently result from direct contact between the photorecep-tors themselves^1,3,4,7–10. Fain et al.¹⁰ reported that the red rods of the toad Bufo marinus were coupled by gap (electronic) junctions, and that single rods received detectable signals from other receptors over a retinal area of about 0.5 mm². This receptive field area is 4–100 times larger than those measured for photoreceptors of a variety of species^{1,4,7,9,11,12,15}. Fain et al. found this extensive spread of rod signals to be inconsistent with network models containing only passive elements and this raised the possibility that some active process, perhaps in the rod membrane, contributed to the spread of rod signals. We report here results which indicate that single rods sum signals over only 1/16th the area previously estimated; this smaller receptive field area implies more intrinsic noise, a larger response to single photon absorptions, and a larger signal-to-noise ratio than predicted by the previously reported results¹⁰. Furthermore we find that, as in other species (ref. 13, and Copenhagen and Owen, personal communication),the spread of low-amplitude, light-evoked responses between photoreceptors can be accounted for by purely passive electrical properties.