Evolution of rod bipolar cells and rod vision.

Abstract

Bipolar cells are vertebrate retinal interneurons conveying signals from rod and cone photoreceptors to amacrine and ganglion cells. Bipolar cells are found in all vertebrates and have many structural and molecular affinities with photoreceptors; they probably appeared very early during vertebrate evolution in conjunction with rod and cone progenitors. There are two types of bipolar cells, responding to central illumination with depolarization (ON) or hyperpolarization (OFF). In most vertebrate species, rod signals are conveyed to specialized rod bipolar cells, which sum signals from many rods and facilitate detection at the visual threshold. Lamprey, which diverged from all other vertebrates in the late Cambrian, have both rod ON and rod OFF bipolar cells, but mammals have only rod ON cells. Rod signals in mammals are conveyed to output neurons indirectly via AII (or A2) amacrine cells, which synapse onto cone ON and cone OFF bipolar-cells and then to ganglion cells. These findings raise the question of when during retinal evolution rod OFF bipolar cells were lost. Because physiological recordings have been made from rod OFF bipolar cells in both cartilaginous fishes (dogfish) and urodeles (salamanders), rod OFF bipolar cells and their circuits must have been retained in vertebrate progenitors at least until the Devonian. Recent evidence showing that zebrafish retina processes rod signals similar to those in mammals indicates that rod OFF bipolar cells were lost at least twice. The sole utilization of rod ON bipolar cells may have provided a selective advantage from increased signal-to-noise discrimination near the visual threshold. KEY POINTS: Rods and cones have many structural and molecular similarities to bipolar cells, which are retinal interneurons conveying signals from photoreceptors to the retinal output. Bipolar cells can be either ON (centre depolarizing) or OFF (centre hyperpolarizing) and either rod or cone dominant. Lamprey, which diverged from all other vertebrates 500 million years ago, have both ON and OFF bipolar cells, which can each be either rod or cone dominant. We argue that this configuration of separate rod/cone bipolar-cell pathways is representative of early vertebrates. Rod ON and rod OFF bipolars persisted at least until the progenitors of amphibians in the Devonian, but mammals and teleost fishes have only rod ON bipolar cells and convey rod OFF signals via a specialized amacrine cell. We argue that rod OFF bipolar cells were lost in at least two different lineages during vertebrate evolution, probably to increase the signal-to-noise of rod vision.