Synaptic vesicle activity in stimulated and unstimulated photoreceptor axons in the housefly. A freeze-fracture study.

Abstract

Light-stimulated and unstimulated photoreceptor (retinular) axon terminals in the lamina ganglionaris (first optic neuropil) of the housefly are examined using freeze-fracture replication. The presence of numerous, cross-fractured capitate projections permits unmistakable identification of the retinular axon terminal membrane. Regardless of the conditions of illumination, the protoplasmic face (P-face) of the terminal membrane contains numerous bowtie-shaped particle clusters (active zones) which resemble the en face form and disposition of the presynaptic ribbon found in thin sections. Estimates from freeze-fractured material indicate that each retinular axon possesses at least 175 such active zones. In eyes fixed during illumination, active zones are surrounded by many membrane dimples indicative of vesicle fusion sites. Such synaptic vesicle sites are seldom encountered in terminals which are dark-adapted and fixed in the dark. Results from light-adapted eyes placed in the dark following the onset of fixation suggest that endocytosis may occur in the extrasynaptic regions of this inhibitory synapse. P-face particles are uniformly distributed throughout the extrasynaptic regions of unstimulated terminals. Particle density increases in areas peripheral to the active zones in stimulated eyes, particularly within the regions presumed to be undergoing active endocytosis. These structural findings are discussed in the context of the Heuser-Reese model of vesicle exocytosis and recycling.