The Journal of Neuroscience, March 1, 2000, 20(5):1754-1766
Activity and Calcium-Dependent Mechanisms Maintain Reliable
Interneuron Synaptic Transmission in a Rhythmic Neural Network
David
Parker
Nobel Institute for Neurophysiology, Department of Neuroscience,
Karolinska Institute, S-17177, Stockholm, Sweden
Inputs from glutamatergic excitatory interneurons (EIN) to motor
neurons in the lamprey spinal cord locomotor network exhibit activity-dependent depression during spike trains. The mechanism underlying this depression has been examined here, and its relevance to
transmitter release during rhythmic activity has been investigated.
The depression of EIN inputs was greater after larger initial EPSPs and
reduced in low-calcium Ringer's solution, effects that are consistent
with depression caused by depletion of releasable transmitter stores.
However, the depression was greater at lower stimulation frequencies
and could be reversed by increasing the stimulation frequency. In
addition, high-calcium Ringer's solution and the slow intracellular
calcium chelator EGTA-AM, which both failed to affect the amplitude of
low frequency-evoked EPSPs, reduced and increased the depression,
respectively. These results are inconsistent with a simple depletion
mechanism but suggest that ongoing activity and calcium-dependent
mechanisms oppose depletion.
The network relevance of this mechanism was examined using
physiologically relevant bursts to simulate EIN spiking during rhythmic
activity. Although considerably more EPSPs were evoked than during
spike trains, burst-evoked EPSPs did not depress. However, single EPSPs
evoked at the interburst interval depressed, and burst transmission was
disrupted by EGTA-AM, again suggesting the involvement of activity and
calcium-dependent mechanisms. By responding to the calcium changes
evoked by increased interneuron activity, this mechanism can monitor
transmitter requirements caused by EIN spiking, allowing reliable
transmission across different patterns of network activity. However,
not all types of spinal interneurons exhibit reliable burst
transmission, suggesting specificity of this mechanism to a subset of neurons.
Key words:
synaptic plasticity; depression; lamprey; spinal cord; neural network; transmitter release
Copyright © 2000 Society for Neuroscience 0270-6474/00/2051754-13$05.00/0