Two-state membrane potential transitions of striatal spiny neurons as evidenced by numerical simulations and electrophysiological recordings in awake monkeys.

Abstract

Spontaneous membrane potential fluctuations of striatal spiny projection neurons play a crucial role in their spike generation. Previous intracellular recording studies in anesthetized rats have shown that the membrane potential of striatal spiny neurons shifts between the depolarized "up" state and the hyperpolarized "down" state. Here we report evidence for the occurrence of such two-state membrane potential transitions by numerical simulations and electrophysiological recordings in awake monkeys. Data from our simulations of a striatal spiny neuron model demonstrated that spike latency histograms of the model neuron displayed two separate (i.e., early and late) peaks in response to excitatory cortical input, corresponding to neuronal activity in the up or down state, respectively. Then, we addressed experimentally whether the latency distribution of cortically induced spike firing of striatal spiny neurons might show dual peaks. Striatal neuron activity was extracellularly recorded in response to electrical stimulation in the two cortical motor-related areas, the primary motor cortex and the supplementary motor area, of awake monkeys. Analysis of spike latency histograms has defined that striatal spiny neurons typically exhibit two temporally distinct peaks, as obtained by the numerical simulations. Thus, the membrane potential shifts between the up and down states appear to occur in striatal spiny neurons of the behaving animal.