Quantitative light and electron microscopy was used to monitor the extent of retinal degeneration as a function of age and temperature in the white-eyed rdgBKS222 mutant of Drosophila melanogaster. Parallel measurements of the electroretinogram (ERG) of the degenerating retina reveal a new phenomenon--the appearance of spike potentials following illumination with bright light. These spikes, which do not appear in the normal fly retina, have a relatively long duration (20-50 ms), regenerative properties, and a rate of occurrence which increases with increasing light intensity. The spikes differed from the light response in being more susceptible to CO2 and to cuts in the eye. The spikes completely disappeared at low extracellular Ca2+ levels which did not reduce the amplitude of the light response. The spike potentials become triphasic when the recording electrode is advanced to the level of the basement membrane. This suggests that the spike potentials originate from the photoreceptor axons as a result of synchronous opening of voltage-dependent channels in a large number of photoreceptor cells. The occurrence of spike potentials during the process of degeneration was studied. Two pahses can be distinguished: (1) Spike potentials appear in retinae of 2-3-day-old flies which display few morphological signs of degeneration. The frequency of appearance of spike potentials decreases in retinae of 14-16-day-old flies which show extensive degeneration of the R1-6 photoreceptor cells but no degeneration of the central R7,8 cells. (2) Spike potentials appear more frequently again in flies of 22-24 d of age. This is probably a consequence of degeneration of the remaining R7,8 photoreceptor cells. Temperature and the light-dark cycle had a critical effect on degeneration. Eight-day-old mutants raised at 19 degrees C in a normal light-dark cycle showed only little degeneration. Eight-day-old mutants raised at 24 degrees C showed only a slight degeneration when raised in the dark. However, the degree of degeneration was greatly enhanced in the mutants raised at 24 degrees C under a light-dark cycle regime. The combined electrophysiological and morphological study of the degeneration, as a function of age and temperature, revealed that (1) the degeneration process takes place even in darkness, but at a slow rate, while light greatly accelerates the degeneration. (2) The degeneration is negligible at 19 degrees C, even during light, in the first week after eclosion.(ABSTRACT TRUNCATED AT 400 WORDS)