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 i n temporal properties, especially at the level of the photoreceptor for whi ch no account exists. Using light flashes and white-noise- modulated light and current stimuli, we examined the spatial and temporal properties of a s ingle class of photoreceptor (R1-6) within the compound eyes of male blowfl y, Calliphora vicina. We find that there is a trend toward higher performan ce at the front of the eye, both in terms of spatiotemporal resolution and signal-to-noise ratio. The receptive fields of frontal photoreceptors are n arrower than those of photoreceptors at the side and back of the eye and re sponse 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 informa tion rate. The power spectra of signals and noise indicate that this elevat ion of performance results both from shorter responses to individual photon s and from a more reliable registration of photon arrival times. These dist inctions are characteristic of adaptational changes that normally occur on increasing illumination. However, all photoreceptors were absorbing light a t approximately the same mean photon rate during our recordings. We therefo re suggest that frontal photoreceptors attain a higher state of light adapt ation for a given photon rate. This difference may be achieved by a higher density of (Ca2+ permeable) light-gated channels. Consistent with this hypo thesis, membrane-impedance measurements show that frontal photoreceptors ha ve a higher specific conductance than other photoreceptors. This higher con ductance provides a better temporal performance but is metabolically expens ive. Across the eye, temporal resolution is not proportional to spatial (op tical) resolution. Neither is it matched obviously to optic flow. Instead w e examine the consequences of an improved temporal resolution in the fronta l 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 re tinal neuron can vary within a single retina and that this variation may be functionally related to the behavioral requirements of the animal.