Voltage-dependent nonlinearities in the membrane of locust nonspiking local interneurons, and their significance for synaptic integration.

Some aspects of the electronic and active membrane properties of nonspiking local interneurons were studied in isolated locust thoracic ganglia, using the switched current- and voltage-clamp techniques in neuropilar recordings. The average transmembrane potential (Vr) of the interneurons was -58 +/- 6mV (n = 85), and the input resistance (in the linear region of the current-voltage curve) was 16.5 +/- 8 M omega (n = 19, range 8 to 32 M omega). The membrane and equalizing time constants were estimated from charging curves evoked by the injection of low density hyperpolarizing current pulses from about -80 mV, i.e., from voltages in the linear region of the I-V curve. The curves yielded 2 time constants (tau m and tau l) whose average values were 33.2 +/- 9 msec and 3.3 +/- 1 msec (n = 18), respectively. The mean specific membrane resistance is therefore about 33 k omega.cm2, assuming that the membrane capacitance is ca. 1 microF.cm-2. An outward rectification was always observed upon depolarization from potentials more negative than Vr and was accompanied by a decrease in input resistance and membrane time constant. The "resting" membrane, for example, had a time constant of 26.4 +/- 8 msec (n = 31). This outward rectification was due to at least 2 conductances with different inactivation kinetics, similar to the transient "A" and "delayed-rectifier" potassium conductances. No inward rectification was ever observed upon injection of hyperpolarizing current. In about 60% of the recordings, an active and TTX-resistant depolarizing process could be evoked by rapid depolarization around Vr. The voltage-dependent properties of the membrane of the nonspiking local interneurons had dramatic effects on the shape and time course of natural or evoked unitary PSPs. The half-width of EPSPs, for example, decreased by a factor of 7.5 if the membrane potential was shifted from -93 to -50 mV. When the membrane potential of an interneuron was altered with a triangular current waveform, the reduction of tonically occurring IPSPs depended more on the sign and rate of the induced voltage change than on the absolute transmembrane potential. For 2 identical instantaneous values of membrane potential, for example, the reduction of the PSPs was greater during the depolarizing phase than during the hyperpolarizing phase of the current waveform. The possible nature of the active membrane conductances underlying the nonlinear electrical behavior of the membrane is discussed, together with their functional significance for local circuit synaptic integration.