Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. I. Characteristics of electrotonic and chemical postsynaptic potentials

Abstract

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.