The effects of light reversals on photoreceptor synaptogenesis in the fly Musca domestica

Abstract

The short-term influence of visual experience was studied in the first-order tetrad synapses of the first optic neuropil, or lamina, underlying the compound eye in the housefly (Musca domestica). We report the effects of single light reversals, in which flies reared in constant darkness were exposed to light or those in constant light were exposed to darkness, on this defined population of synapses. The synaptic population was characterized by quantitative electron microscopic methods using three parameters: (i) the number of synaptic contacts per photoreceptor terminal; (ii) the size of these synapses, given by the mean platform width of their presynaptic ribbons; and (iii) the proportion (up to approximately 20%) of small synapses-those having a ribbon platform less than 0.17 micron wide. The effects of light exposures in flies reared in constant darkness include decreased mean synaptic size and increased numbers of synapses. These effects are seen in flies of all ages (to 10 days). Long light exposures (2-6 h) are much less effective than short exposures (down to 20 s), with maximum effects obtained at 15 min (up to 45% more synapses). Small synapses are reasoned to be new junctions formed only recently; the decreased mean synaptic size and the increased number of synapses seen after short light exposures are both interpreted to result from a recent burst of synaptogenesis in the adult lamina. The effects of dark exposure in flies reared in constant light are the reciprocal of those seen in dark-reared flies exposed to light, but they are less pronounced. Although the function of such changes is not yet known, they may form part of the light adaptation mechanism of the photoreceptor, and occur along with a redistribution of other organelles involving membrane invaginations into its terminal. These changes occur against a background trend for control flies reared under constant conditions to have fewer, larger synapses with increasing age up to 10 days, an effect that is most pronounced in constant darkness, when synaptic number decreases by 21% and size increases by 13%.