FAST AND SLOW PHOTORECEPTORS - A COMPARATIVE-STUDY OF THE FUNCTIONAL DIVERSITY OF CODING AND CONDUCTANCES IN THE DIPTERA

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 mat ching involves the dynamics of phototransduction and the use of an app ropriate mix of potassium conductances to tune the photoreceptor membr ane. 2. Rapidly flying, manoeuvrable diurnal Diptera from several fami lies have fast photoreceptors, with comer frequencies (the frequency a t which signal power falls by a half) of between 50 and 107 Hz. The po nderous and predominantly nocturnal tipulids have slow photoreceptors with fully light adapted corner frequencies of 16 to 19 Hz. 3. Dark ad apted fast photoreceptors, have a lower gain (as indicated by lower no ise levels), a lower sensitivity, and light adapt more rapidly than da rk 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 de layed rectifier potassium conductance with fast and slow components of activation. Slow photoreceptors rectify less strongly in the steady s tate because their membrane properties are dominated by strongly inact ivating 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 fas t cells by reducing the membrane time constant. This is an expensive s trategy, involving large conductances and currents. Slowly flying noct urnal insects do not require a high speed of response. The potassium c onductances in their slow photoreceptors inactivate to avoid costly an d unnecessary ion fluxes. 8. Both the dynamics of the photoresponse an d photoreceptor membrane properties exhibit sexual dimorphism. Light a dapted 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 tha t the divison between fast and slow cells is the product of cellular c onstraints, metabolic costs and the requirements of coding efficiency at different light levels and retinal image velocities.