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Journal of Neuroscience, Vol 8, 1302-1312, Copyright © 1988 by Society for Neuroscience
Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. I. Characteristics of electrotonic and chemical postsynaptic potentials
JW Lin and DS Faber
Department of Physiology, State University of New York, Buffalo 14214.
Simultaneous pre- and postsynaptic intracellular recordings, combined with
HRP injections, were used to study the properties of junctional
transmission between club endings of saccular nerve afferents and the
Mauthner (M-) cell in goldfish. All endings were electrotonically coupled
to the M-cell, but impulses in less than 20% of the afferents produced
chemically mediated excitatory postsynaptic potentials as well. There were
no differences between the coupling potentials of those endings that
mediated chemical transmission and those that did not, and presynaptic
injections of HRP confirmed that in both cases the studied fibers
terminated on the M-cell as single club endings. Since electron microscopic
studies (Nakajima, 1974; Kohno and Noguchi, 1986; Tuttle et al., 1986) have
consistently revealed structural correlates of chemical synapses in all the
endings, we propose that the chemical synapses in the majority of the club
endings are functionally silent. The electrotonic coupling at these
junctions was characterized on the basis of coupling coefficients and DC
transfer resistances. Coupling coefficients for anti- and orthodromic
action potentials averaged 0.076 and 0.011, respectively. The transfer
resistances measured with injections of constant-current pulses were the
same in both directions (approximately 18.6 k omega), indicating the
junctions do not rectify. Two separate calculations of the gap junctional
resistance indicated that it is in the range of 6.7-35.8 M omega, with a
mean value of 15.5 M omega. This calculated junctional resistance
corresponds to 670 open gap junction channels, assuming a single-channel
conductance of 100 pS. As that estimate is about 2 orders of magnitude
smaller than the number of the presumed morphological correlates of the
channels, i.e., intramembranous particles observed with the technique of
freeze- fracture (Kohno and Noguchi, 1986; Tuttle et al., 1986), we
conclude that only a small fraction of the morphologically observed
channels are open at any time. The characteristics of the chemically
mediated EPSPs were as follows: amplitude, 0.139 +/- 0.075 mV (mean +/- SD;
n = 16); latency from onset of the coupling potential, 636 +/- 26 mu sec (n
= 24); 10-90% rise time, 244 +/- 33 mu sec (n = 14); and decay time
constant, 1.32 +/- 0.51 msec (n = 6). The decay phase was fit by a single
exponential, and its time constant presumably is the same as that of the
underlying conductance change since the M-cell's membrane time constant is
significantly faster, 0.3-0.4 msec.
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