Fast and slow photoreceptors - a comparative study of the functional diversity of coding and conductances in the Diptera

Abstract

1. From a comparison of the photoresponses and membrane properties of photoreceptors from 20 species of Diptera, we conclude that coding in the time domain is matched to the dictates of visual ecology. This matching involves the dynamics of phototransduction and the use of an appropriate mix of potassium conductances to tune the photoreceptor membrane. 2. Rapidly flying, manoeuvrable diurnal Diptera from several families have fast photoreceptors, with corner frequencies (the frequency at which signal power falls by a half) of between 50 and 107 Hz. The ponderous and predominantly nocturnal tipulids have slow photoreceptors with fully light adapted corner frequencies of 16 to 19 Hz. 3. Dark adapted fast photoreceptors have a lower gain (as indicated by lower noise levels), a lower sensitivity, and light adapt more rapidly than dark adapted slow photoreceptors. Fast cells also have much lower input resistances and shorter time constants. 4. Fast photoreceptors rectify more strongly in the steady state because of a weakly inactivating delayed rectifier potassium conductance with fast and slow components of activation. Slow photoreceptors rectify less strongly in the steady state because their membrane properties are dominated by strongly inactivating outward currents with reversal potentials in the range - 80 to -90 mV. 5. The differences between potassium conductances match the differing functional requirements of fast and slow photoreceptors. The non-inactivating delayed rectifier promotes the rapid response of fast cells by reducing the membrane time constant. This is an expensive strategy, involving large conductances and currents. Slowly flying nocturnal insects do not require a high speed of response. The potassium conductances in their slow photoreceptors inactivate to avoid costly and unnecessary ion fluxes. 8. Both the dynamics of the photoresponse and photoreceptor membrane properties exhibit sexual dimorphism. Light adapted photoreceptors in the enlarged male dorsal eye of Bibio markii have a corner frequency of 42 Hz, compared with 27 Hz for cells in the smaller female eye. This difference in frequency response correlates with the male's higher spatial acuity and is accompanied by consistent differences in potassium conductance activation rate. We conclude that the divison between fast and slow cells is the product of cellular constraints, metabolic costs and the requirements of coding efficiency at different light levels and retinal image velocities. © 1993 Springer-Verlag.