Large functional variability in cockroach photoreceptors: optimization to low light levels.

The compound eyes of insects contain photoreceptors in small eyelets, ommatidia. The photoreceptors generally vary very little from ommatidium to ommatidium. However, in the large compound eyes of the cockroach (Periplaneta americana), previous studies have shown large differences in the optical structure between the ommatidia. The anatomy suggests pooling of 6-20 photoreceptor signals into one second-order cell in the first synapse. Here, we show and characterize an unexpectedly large and seemingly random functional variability in the cockroach photoreceptors in terms of sensitivity, adaptation speed, angular sensitivity, and signal-to-noise ratio. We also investigate the implications of action potentials, triggered by the light-induced membrane depolarization in the photoreceptor axons. The combination of the functional features reported here is unique among the compound eyes. Recordings from the proximal parts of the thin and long photoreceptor axons or small and distant second-order neurons are not practical with the present methods. To alleviate this lack of data, we used computer simulations mimicking the functional variability, spike coding, and pooling of 12 photoreceptor signals, on the basis of our recordings from the photoreceptor somata and distal axons. The predicted responses of a simulated second-order cell follow surprisingly reliably the simulated light stimuli when compared with a simulation of functionally identical photoreceptors. We hypothesize that cockroach photoreceptors use action potential coding and a kind of population coding scheme for making sense of the inherently unreliable light signals at low luminance and for optimization of vision in its mainly dim living conditions.