The Journal of Neurophysiology Vol. 79 No. 2 February 1998, pp. 727-742
Copyright ©1998 The American Physiological Society

Synaptic Current at the Rat Ganglionic Synapse and Its Interactions With the Neuronal Voltage-Dependent Currents

Oscar Sacchi¹, Maria Lisa Rossi¹, Rita Canella¹, and Riccardo Fesce²

¹ Department of Biology, Section of General Physiology, University of Ferrara, 44100 Ferrara; and ² "Bruno Ceccarelli" Center, Consiglio Nazionale delle Ricerche Center of Cytopharmacology and DIBIT Hospital San Raffaele, 20132 Milan, Italy

Sacchi, Oscar, Maria Lisa Rossi, Rita Canella, and Riccardo Fesce. Synaptic current at the rat ganglionic synapse and its interactions with the neuronal voltage-dependent currents. J. Neurophysiol. 79: 727-742, 1998. The membrane current activated by fast nicotinic excitation of intact and mature rat sympathetic neurons was studied at 37°C, by using the two-microelectrode voltage-clamp technique. The excitatory postsynaptic current (EPSC) was modeled as the difference between two exponentials. A fast time constant (₂; mean value 0.57 ms), which proves to be virtually voltage-independent, governs the current rise phase and a longer time constant (₁; range 5.2-6.8 ms in 2 mM Ca²⁺) describes the current decay and shows a small negative voltage dependence. A mean peak synaptic conductance of 0.58 µS per neuron is measured after activation of the whole presynaptic input in 5 mM Ca²⁺ external solution (0.40 µS in 2 mM Ca²⁺). The miniature EPSCs also rise and decay with exponential time constants very similar to those of the compound EPSC recorded at the same voltage. A mean peak conductance of 4.04 nS is estimated for the unitary event. Deconvolution procedures were employed to decompose evoked macrocurrents. It is shown that under appropriate conditions the duration of the driving function describing quantal secretion can be reduced to <1 ms. The shape of the EPSC is accurately mimicked by a complete mathematical model of the sympathetic neuron incorporating the kinetic properties of five different voltage-dependent current types, which were characterized in a previous work. We show that I_A channels are opened by depolarizing voltage steps or by synaptic potentials in the subthreshold voltage range, provided that the starting holding voltage is sufficiently negative to remove I_A steady-state inactivation (less than 50 mV) and the voltage trajectories are sufficiently large to enter the I_A activation range (greater than 65 mV). Under current-clamp conditions, this gives rise to an additional fast component in the early phase of membrane repolarizationin response to voltage pulsesand to a consistent distortion of the excitatory postsynaptic potential (EPSP) time course around its peakin response to the synaptic signal. When the stimulation initiates an action potential, I_A is shown to significantly increase the synaptic threshold conductance (up to a factor of 2 when I_A is fully deinactivated), compared with that required when I_A is omitted. The voltage dependence of this effect is consistent with the I_A steady-state inactivation curve. It is concluded that I_A, in addition to speeding up the spike repolarization process, also shunts the excitatory drive and delays or prevents the firing of the neuron action potential.

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