Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes

Most vertebrates have one layer of the dim-light active rod
photoreceptors. However, multiple rod layers, known as a multibank retina,
can be found in over 100 species of fish, including several deep-sea
species and one family of nocturnally active reef fish, the Holocentridae.
Although seemingly associated with increased photon catch, the function of
multibank retinas remained unknown. We used an integrative approach,
combining histology, electrophysiology, and amino acid sequence analysis,
applied to three species of nocturnal reef fishes, two holocentrids with a
multibank retina (Neoniphon sammara and Myripristis violacea) and an
apogonid with a single rod bank (Ostorhinchus compressus), to determine
the sensory advantage of multiple rod layers. Our results showed that fish
with multibank retinas have both faster vision and enhanced sensitivity to
bright and dim light intensities. Faster vision was indicated by higher
flicker fusion frequencies during temporal resolution electroretinography
as well as faster retinal release kinetics estimated from their rhodopsin
proteins. Enhanced sensitivity was demonstrated by broadened
intensity-response curves derived from luminous sensitivity
electroretinography. Overall, our findings provide the first functional
evidence for enhanced dim-light sensitivity using a multibank retina while
also suggesting novel roles for the adaptation in enhancing bright-light
sensitivity and the speed of vision.