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Journal of Neuroscience, Vol 13, 3075-3089, Copyright © 1993 by Society for Neuroscience
Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release
PS Katz, MD Kirk and CK Govind
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77225.
This study provides evidence that a neuron can exhibit differences in
activity-dependent transmitter release at two synaptic sites due to
variations in the properties of its presynaptic terminals. Two muscles in
the stomatogastric system of the lobster Homarus americanus are innervated
by a single motor neuron but respond differently to that motor neuron's
input, resulting in two different movements evoked by one motor neuron.
During continued motor neuron stimulation, the gm8 muscle contracts slowly
and maintains contraction, while the gm9 muscle contracts rapidly and then
relaxes. These different muscle responses can be accounted for, in large
part, by the properties of the respective neuromuscular synapses: the
excitatory junctional potentials recorded in gm8 are initially small but
summate and facilitate with repeated stimulation, while those in gm9 are
initially large but depress with repeated stimulation. Presynaptic
differences in neurotransmitter release contribute strongly to the
divergent responses; reduction of the excitatory junction potential
amplitude by partial postsynaptic receptor blockade or by desensitization
does not change the amount of depression at gm9. However, reduction of
neurotransmitter release with low-Ca2+, high-Mg2+ saline removes gm9
synaptic depression and reveals that both neuromuscular junctions exhibit
frequency-dependent homosynaptic facilitation. Postsynaptic differences in
muscle input resistance and muscle composition may enhance the effects of
the divergent release properties, but are not responsible for the
activity-dependent changes. Ultrastructural features of the nerve terminals
on the two muscles are consistent with the differential output of the
terminals; the synapses on gm9 are larger and have more presynaptic dense
bars than their counterparts on gm8. These data suggest that the basis for
the differences in transmitter release between the two muscles may be a
higher density of release sites in the gm9 synapses that leads to a higher
output of neurotransmitter, rapid depletion of transmitter stores, and
synaptic depression.
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