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Calcium dependence of depolarization-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons

R. A. Lenz *¹ and B. E. Alger ¹

We made whole-cell recordings from CA1 pyramidal cells in the rat hippocampal slice preparation to study the calcium (Ca²⁺) dependence of depolarization-induced suppression of inhibition (DSI). DSI is a retrograde signalling process in which voltage-dependent Ca²⁺ influx into a pyramidal cell leads to a transient decrease in the release of GABA from interneurons.

To investigate the Ca²⁺ dependence of DSI without altering extracellular divalent cations, we varied the type and amount of Ca²⁺ chelator (EGTA or BAPTA) in the recording pipette (keeping the chelator : Ca²⁺ ratio constant). Evoked inhibitory postsynaptic currents (IPSCs) were induced in the presence of antagonists of ionotropic glutamate receptors. DSI was induced by depolarizing voltage steps, lasting from 0·025 to 5 s, to 0 mV.

DSI was directly dependent on the duration of the voltage step used to induce it, from threshold up to a maximal value of IPSC suppression, whether EGTA or BAPTA was used, and whether their concentrations were 0·1, 0·5 or 2 mM. For instance, a voltage step lasting 1·37 s produced half-maximal DSI with 2 mM BAPTA, but with 0·1 mM BAPTA, half-maximal DSI was achieved with a step lasting 0·186 s. Peak DSI was the same in all cases, and DSI was blocked with either 10 mM EGTA or BAPTA in the pipette. Bath application of carbachol could overcome the block of DSI by 10 mM EGTA but not by 10 mM BAPTA.

We calculated that a voltage step lasting ~100 ms would be necessary to activate half-maximal DSI in the absence of exogenous Ca²⁺ buffers.

Log-log plots of calculated total Ca²⁺ influx, estimated from time integrals of Ca²⁺ currents, versus DSI yielded a straight line with a slope of ~1, and increasing extracellular [Ca²⁺] from 2·5 to 5 mM did not change the slope.

The time course of decay of DSI was well described by an exponential function with a time constant of ~20 s and was not affected by changes in either concentration or type of Ca²⁺ buffer.

The data suggest that, in its Ca²⁺ dependence, DSI more closely resembles the slow release of neuropeptides and hormones than it does the process of fast release of many neurotransmitters.

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