Regulation in the number of fly photoreceptor synapses: the effects of alterations in the number of presynaptic cells.

At the equator of the fly's eye, between dorsal and ventral eye halves, a systematic, natural addition of photoreceptor terminal input occurs at each of the fixed populations of uniquely identifiable postsynaptic interneurons in each cartridge of the first optic neuropile, or lamina. The equatorial cartridges are identical in composition except in having seven and eight receptor terminals (7R and 8R, respectively), compared with six elsewhere (6R cartridges). The effects of this augmented presynaptic input upon the frequency of the chief afferent class of photoreceptor tetrad synapse were studied compared with control data for 6R cartridges (Nicol and Meinertzhagen, '82). The synapse population size and distribution within five depth levels of the lamina is, on average, approximately constant for all receptor terminals whether from 6R, 7R, or 8R cartridges. The overall determinant of synapse frequency is therefore presynaptic. Small (5-6%) average decreases in synapse frequency per receptor in 7R and 8R cartridges compared with 6R co-vary with similar decreases in membrane area, each synapse occupying a patch of membrane of similar area in all cases. The tetradic postsynaptic composition of synapses was also similar in all cases. Because of the augmented synaptic input to the postsynaptic neurons, a morphometric analysis was undertaken of two (L1 and L2), which receive input as a pair from every synapse. There is the same dendrite number (about 180) in 8R L1/L2 as in 6R L1/L2 but they have different branching patterns, conforming to the different number and configuration of receptor terminals. Thus in an 8R cartridge each terminal is serviced by a comb of fewer dendrites, but each dendrite is longer, fatter, and services more synapses. The area of L1/L2 dendritic membrane exposed is increased, compared with 6R cartridges, in proportion with the number of synapses it participates at postsynaptically, so that all dendrites (6R and 8R) allocate the same mean area (about 0.55 micrometer2) of postsynaptic membrane per synapse.