Identification and characterization of striatal cell subtypes using in vivo intracellular recording in rats: II. Membrane factors underlying paired‐pulse response profiles

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Abstract
Two subtypes of neurons in the striatum have been defined on the basis of their different response patterns to paired‐impulse stimulation of corticostriatal afferents, with type I cells showing a longer spike latency, facilitation at short intervals, and inhibition at long intervals, and type II cells defined by the facilitation occurring at long interstimulus intervals. Nevertheless, the companion report has shown that this distinction of cell types cannot be accounted for by differences in the basic physiological properties of these cells, but instead is likely to be due to differences in their synaptic connectivity. The experiments performed in this study were directed at examining in detail the membrane factors and synaptic responses that may contribute to these distinct response patterns.When pairs of stimuli were delivered to the corticostriatal fibers at 10‐30 ms interstimulus intervals, the EPSPs elicited in type I neurons exhibited a temporal summation, resulting in a facilitation of spike firing to the second stimulus relative to the first. In contrast, type II cells showed decreased EPSP amplitude at short intervals, and in cells showing a short‐interval inhibition, there was a significant increase in spike threshold (+5.3 ± 1.4 mV) during the second response. All type II neurons recorded with KCl‐filled microelectrodes showed short‐interval facilitation with little or no change in spike threshold. Although the use of KCI electrodes did not alter the facilitation at short intervals in type I neurons it did increase the rate of rise of the EPSP, causing spikes to be triggered at a latency similar to that of type II cells.Paired stimuli delivered at 75–150 ms interstimulus intervals showed inverse effects on type I and type II cells with respect to the probability of spike firing. In type I cells, the evoked EPSP was followed by a long‐latency membrane hyperpolarization that prevented the second EPSP from reaching spike threshold. In contrast, the smaller‐amplitude hyperpolarization evoked in type II cells enabled the second stimulus to activate an EPSP at the same membrane potential as the first stimulus, resulting in a facilitation of spiking.Therefore, despite the similarity in the basic physiological properties of type I and type II cells, the differences in their spike latencies and paired impulse response profiles appear to be dependent on the timing of their GABAergic inhibition at short intervals: A GABA‐mediated conductance change occurs simultaneously with the EPSP in type I cells leading to a delay in triggering the evoked spike, whereas a later‐developing GABA conductance change in type II cells results in an inhibition of spiking at short intervals. In contrast, the pronounced long‐duration membrane hyperpolarization of type I cells appears to underlie the inhibition of spiking at long intervals, whereas in the type II cells the GABA‐mediated decrease in cell excitability necessitated the use of larger‐amplitude stimulation pulses to reach threshold with respect to the first stimulus, resulting in a higher probability of spike discharge to the second stimulus at long intervals.

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