PRESYNAPTIC GLUTAMATE LEVELS IN TONIC AND PHASIC MOTOR AXONS CORRELATE WITH PROPERTIES OF SYNAPTIC RELEASE

Synaptic glutamate release involves the accumulation of cytoplasmic gl utamate in synaptic vesicles, whereafter it is released by triggered e xocytosis. As glutamatergic terminals are known to be functionally div erse it was of interest to examine whether the presynaptic glutamate s upply differs between individual axon terminals with distinct release properties. The glutamatergic terminals in the crustacean neuromuscula r system system comprise a ''phasic'' type which shows fatigue of rele ase during repetitive stimulation, and a ''tonic'' type which can main tain transmission for long periods, Quantitative immunogold analysis s howed that the axons in a tonic nerve innervating slow muscles in the abdomen contained two times higher levels of glutamate labeling over a xoplasmic matrix and over mitochondria, as compared to the correspondi ng elements in a phasic nerve. Similar results were obtained when adja cent phasic and tonic axons in a mixed nerve innervating leg muscles w ere compared. In the terminal regions of tonic and phasic axons the gl utamate labeling differed correspondingly over axoplasmic matrix and m itochondria, while the synaptic vesicles showed a similar strong accum ulation of labeling in both types of terminal. The level of labeling f or glutamine, a glutamate precursor, was closely similar in phasic and tonic axons. The axoplasmic glutamate concentration was estimated to be in the low millimolar range, through comparison with coprocessed co njugates with known glutamate concentration. These results show that f atigue-resistant tonic axons and terminals contain higher levels of gl utamate than fatiguable phasic axons, presumably representing an adapt ation to the markedly different impulse activities in the two types of neuron, The axonal glutamate concentrations ale in the range of the K -m value for vesicular glutamate transport. Thus in tonic axons the hi gh glutamate level appears to promote an efficient refilling of synapt ic vesicles during sustained release, while in phasic axons the refill ing should be slower which is compatible with an infrequent release.