Journal of Neuroscience, Vol 3, 2336-2349, Copyright © 1983 by Society for Neuroscience
Quantitative features of synapse formation in the fly's visual system. I. The presynaptic photoreceptor terminal
A Frohlich and IA Meinertzhagen
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.