Frequency-dependent recruitment of inhibition mediated by stellate cells in the rat cerebellar cortex

In the cerebellum, dendritic inhibition of Purkinje cells (PCs) is mediated by stellate cells (SCs). These inhibitory interneurons are critically involved in the cerebellar network; they control the timing and firing frequency of PCs, the only output cells of the cerebellar cortex. However, the underlying properties of parallel fiber (PF) to SC excitatory synapses have not been fully determined. To characterize the conditions favoring the recruitment of SCs in the cerebellum, we analyzed evoked and spontaneous excitatory postsynaptic currents (EPSCs) recorded from SCs of rat cerebellar slices. We found that SC EPSCs evoked with single suprathreshold-intensity stimulations were mostly unitary, with a large amplitude and variable latencies, and failed with a high rate. Increasing the frequency of stimulation above 60 Hz significantly reduced failures, whereas mean SC EPSC amplitude was increased by less than 20%. Decreasing failures at PF-SC synapses experimentally enhanced the number of asynchronous SC EPSCs per stimulation but, again, moderately increased the mean SC EPSC amplitude. Finally, brief presynaptic bursts transiently depressed synaptic transmission. This depression resulted from the release of endocannabinoids and might act as a negative-feedback mechanism. Thus, we conclude that SC EPSCs evoked with single suprathreshold-intensity stimulations are mostly unitary and that PF-SC synapse efficacy is highly regulated by the presynaptic temporal pattern of activity and the frequency of afferent inputs. Such synaptic properties may control the responsiveness of SC synapses to the frequency of PF stimulations, which may control the spatial extent and duration of the recruitment of inhibition in the cerebellar cortex.