Journal of Neuroscience, Vol 15, 7168-7180, Copyright © 1995 by Society for Neuroscience
Presynaptic glutamate levels in tonic and phasic motor axons correlate with properties of synaptic release
O Shupliakov, HL Atwood, OP Ottersen, J Storm-Mathisen and L Brodin
Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Synaptic glutamate release involves the accumulation of cytoplasmic
glutamate in synaptic vesicles, whereafter it is released by triggered
exocytosis. As glutamatergic terminals are known to be functionally diverse
it was of interest to examine whether the presynaptic glutamate supply
differs between individual axon terminals with distinct release properties.
The glutamatergic terminals in the crustacean neuromuscular system system
comprise a "phasic" type which shows fatigue of release during repetitive
stimulation, and a "tonic" type which can maintain transmission for long
periods. Quantitative immunogold analysis showed that the axons in a tonic
nerve innervating slow muscles in the abdomen contained two times higher
levels of glutamate labeling over axoplasmic matrix and over mitochondria,
as compared to the corresponding elements in a phasic nerve. Similar
results were obtained when adjacent phasic and tonic axons in a mixed nerve
innervating leg muscles were compared. In the terminal regions of tonic and
phasic axons the glutamate labeling differed correspondingly over
axoplasmic matrix and mitochondria, while the synaptic vesicles showed a
similar strong accumulation of labeling in both types of terminal. The
level of labeling for 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 conjugates with known glutamate concentration. These results
show that fatigue-resistant tonic axons and terminals contain higher levels
of glutamate than fatiguable phasic axons, presumably representing an
adaptation to the markedly different impulse activities in the two types of
neuron. The axonal glutamate concentrations are in the range of the Km
value for vesicular glutamate transport. Thus in tonic axons the high
glutamate level appears to promote an efficient refilling of synaptic
vesicles during sustained release, while in phasic axons the refilling
should be slower which is compatible with an infrequent release.
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