Variations in photoreceptor response dynamics across the fly retina

Gradients in the spatial properties of retinal cells and their relation to image statistics are well documented. However, less is known of gradients in temporal properties, especially at the level of the photoreceptor for which no account exists. Using light flashes and white-noise- modulated light and current stimuli, we examined the spatial and temporal properties of a single class of photoreceptor (R1-6) within the compound eyes of male blowfly, Calliphora vicina. We find that there is a trend toward higher performance at the front of the eye, both in terms of spatiotemporal resolution and signal-to-noise ratio. The receptive fields of frontal photoreceptors are narrower than those of photoreceptors at the side and back of the eye and response speeds are 20% faster. The signal-to-noise ratio at high frequencies is also greatest at the front of the eye, allowing a 30-40% higher information rate. The power spectra of signals and noise indicate that this elevation of performance results both from shorter responses to individual photons and from a more reliable registration of photon arrival times. These distinctions are characteristic of adaptational changes that normally occur on increasing illumination. However, all photoreceptors were absorbing light at approximately the same mean photon rate during our recordings. We therefore suggest that frontal photoreceptors attain a higher state of light adaptation for a given photon rate. This difference may be achieved by a higher density of (Ca2+ permeable) light-gated channels. Consistent with this hypothesis, membrane-impedance measurements show that frontal photoreceptors have a higher specific conductance than other photoreceptors. This higher conductance provides a better temporal performance but is metabolically expensive. Across the eye, temporal resolution is not proportional to spatial (optical) resolution. Neither is it matched obviously to optic flow. Instead we examine the consequences of an improved temporal resolution in the frontal region for the tracking of small moving targets, a behavior exhibited by male flies. We conclude that the temporal properties of a given class of retinal neuron can vary within a single retina and that this variation may be functionally related to the behavioral requirements of the animal.