Quantitative features of synapse formation in the fly's visual system. I. The presynaptic photoreceptor terminal

Abstract

Photoreceptors of the adult fly's compound eye each form a population of stereotyped output synapses distributed over the surface of their terminal. The formation of this class of afferent synapses during development has been followed from serial electron microscopy of the same eye region in four pupal and several adult stages, all of female Musca domestica. These synapses, or tetrads, have an invariant postsynaptic composition of four members and so may provide a model for multiple-contact synapses in general. In the adult fly the four postsynaptic elements of each synapse are contributed by two interneurons, L1 and L2, and, usually, two alpha processes of an amacrine cell. These postsynaptic elements assemble at individual developing synapses by selective sequential addition. Assembly starts with L1 or L2, subsequent elements of the final tetrad adding in all conceivable permutations, at least as fast as one per 7 hr. They rarely (only once) incorporate incorrect or supernumerary elements, however. The synaptic population as a whole was also sampled during development to analyze the possible factors determining the normal precision of the size of the adult population. The number of synapses per terminal increases gradually until 74% pupal development. Thereafter it decreases so that the final number of synapses in each receptor's population is the consequence of a net loss. Synapses enlarge with age, chiefly by incorporating new elements, but the loss of synaptic sites is only partially offset by the increase in size of those that remain. Throughout all stages examined in pupal and adult life, total synaptic area is linearly proportional to the surface area of the axon terminal. Thus, from the 74% pupal development stage onward, a population of many small synapses closely spaced, on average, over the terminal's surface transforms into one characteristic of the adult with progressively fewer, larger, more widely spaced synapses.