Terminal degeneration and synaptic disassembly following receptor photoablation in the retina of the fly's compound eye

Abstract

A long-term objective of our studies on the first optic neuropil (or lamina) underlying the fly's compound eye is to explore how afferent photoreceptor synapses disappear during normal adult experience. To increase the frequency of this loss and the chances for its detection artificially, we have examined in this study the synapses during the degeneration of their presynaptic elements, the synaptic terminals of the receptor cells. This may be reliably procured by illuminating for 12 min with strong green light eyes that have received an injection of the dye sulforhodamine 101 (Picaud et al., 1988). The lesion is local and develops rapidly. Degeneration among terminals is progressive but asynchronous. There are several different types of degeneration, most interpretable as stages in a temporal progression after illumination-induced injury. Degenerative changes include shrinkage and darkening of terminals and mitochondrial swelling. Synaptic sites are lost in a defined sequence: (1) the T-shaped presynaptic ribbon disappears first; (2) the members of what is normally a tetrad of postsynaptic elements withdraw as an ensemble from the receptor terminal's membrane, and the surrounding epithelial glial cells extend between former pre- and postsynaptic partners; and (3) the postsynaptic elements then separate from each other. In the most rapidly affected terminals, the frequencies for those synaptic sites at which both presynaptic ribbons and postsynaptic elements remain intact decline by 85%, even in the first 8 hr postillumination.