ACTIVITY-INDUCED CHANGES IN SYNAPTIC RELEASE SITES AT THE CRAYFISH NEUROMUSCULAR-JUNCTION

Crustacean motor axons provide a model in which activity-dependent cha nges in synaptic physiology and synaptic structure can be concurrently observed in single identifiable neurons. In response to a train of st imulation, crustacean neuromuscular junctions undergo pronounced facil itation of transmitter release. The effects of maintained high-frequen cy stimulation may persist for at least several hours (''long-term fac ilitation''). Electrophysiological studies suggest that the number of ''active'' synapses contributing transmitter quanta at low frequencies of stimulation increases during and after a train of high-frequency s timulation. However, at different terminal recording sites the effect of stimulation varies, and it was observed that not all released quant a produce a voltage change in the postsynaptic muscle cell. Electron m icroscopic examinations of serial sections from nerve terminals subjec ted to stimulation were made to determine whether changes in synaptic structure could be correlated with activity-induced long-lasting enhan cement of transmission. A procedure was introduced for marking a recor ded terminal with fluorescent polystyrene microspheres, which are visi ble in electron micrographs of the recording site. Crustacean nerve te rminals possess a large number of discrete synapses, a small fraction of which have multiple presynaptic ''active zones'' (dense bodies with clustered synaptic vesicles, thought to represent sites of evoked tra nsmitter release). In terminals previously stimulated, the proportion of synapses with multiple ''active zones'' is greater than in control unstimulated terminals. Total synaptic vesicle counts and readily rele asable vesicles at synapses are not significantly different in previou sly stimulated terminals and controls. In terminals fixed during stimu lation, a few synapses show evidence of division in ''active zones,'' and synaptic vesicle counts are lower than in controls. The observatio ns lead to the hypothesis that activity-dependent enhancement of synap tic transmission in these neurons is associated with an increase in sy napses with multiple ''active zones,'' but not with long-lasting chang es in releasable synaptic vesicles. It is postulated that synapses end owed with multiple ''active zones'' are responsible for most of the tr ansmitter release at low frequencies of stimulation, while synapses wi th fewer ''active zones'' are recruited at higher frequencies of stimu lation. Adaptive transformation of synaptic physiology and structure c an occur in a relatively short time, but involves relatively few of th e synapses available on a nerve terminal.