Interphotoreceptor coupling: an evolutionary perspective

Abstract

In the vertebrate retina, signals generated by cones of different spectral preference and by highly sensitive rod photoreceptors interact at various levels to extract salient visual information. The first opportunity for such interaction is offered by electrical coupling of the photoreceptors themselves, which is mediated by gap junctions located at the contact points of specialised cellular processes: synaptic terminals, telodendria and radial fins. Here, we examine the evolutionary pressures for and against interphotoreceptor coupling, which are likely to have shaped how coupling is deployed in different species. The impact of coupling on signal to noise ratio, spatial acuity, contrast sensitivity, absolute and increment threshold, retinal signal flow and colour discrimination is discussed while emphasising available data from a variety of vertebrate models spanning from lampreys to primates. We highlight the many gaps in our knowledge, persisting discrepancies in the literature, as well as some major unanswered questions on the actual extent and physiological role of cone-cone, rod-cone and rod-rod communication. Lastly, we point toward limited but intriguing evidence suggestive of the ancestral form of coupling among ciliary photoreceptors.

Electrical synapses for a pooling layer of the convolutional neural network in retinas

“…Low spatial frequencies produce gradually changing voltage differences whereas high frequencies produce sharply changing voltage differences. Both conditions make the current flow slow and fast, respectively, through their membrane capacity (Cangiano and Asteriti, 2021).…”

Where vision begins

“…Cone photoreceptors provide the foundation of most of the photopic-based human visual experience, although the differences between rod and cones across the species and throughout the evolution do not appear as strong as in mammalian retina. The existence and the physiological role of cone–cone, rod–cone, and rod–rod communication is presented in the review by Cangiano and Asteriti [ 3 ] together with a possibly ancestral form of coupling among ciliary photoreceptors. The fact that lamprey rods and cones share the same morphology but their photoresponse is as diverse as in the other vertebrates demonstrates that this diversity does not originate from the different surface/volume ratio and/or from the close proximity of phototransduction enzymes to the CNGC and the exchanger.…”