Reliable control of spike rate and spike timing by rapid input transients in cerebellar stellate cells

Granule cell activity in cerebellar cortex directly excites Purkinje cells via parallel fibers, but it also inhibits Purkinje cells via cerebellar cortical interneurons. This contribution of inhibitory interneurons to cerebellar cortical processing remains poorly understood. In the present study we examined the response properties of stellate cells in vitro to input patterns that may result from granule cell activity in vivo. We constructed input waveforms that represented the sum of inputs from all individual synapses and applied these waveforms to the soma of stellate cells during whole cell recordings in acute brain slices. The stimulus waveforms contained fluctuations in a broad range of frequencies and were applied at different amplitudes. To determine the contribution of synaptic shunting to stellate cell spike responses we applied the same input waveforms either as a simulated synaptic conductance using dynamic clamping or as a direct current injection stimulus. Only the dynamic clamp stimulus has the shunting properties of real synapses, i.e. leads to different-sized synaptic current as a function of membrane potential. We found that stellate cells spike with millisecond precision in response to fast temporal fluctuations in the total synaptic input. Transient increases in excitatory input frequency led to pronounced stellate cell spike responses, indicating that this pathway may be very responsive to even small assemblies of co-activated granule cells. This was observed regardless of whether the input waveform was applied as a conductance with dynamic clamping, or as a direct current injection. Thus the shunting properties of a conductance input did not play a major role in determining the control of precisely timed spiking. In contrast, a more tonic increase in excitatory conductance did not lead to a sustained spike response as obtained with prolonged positive current injection. However, even with tonic current injection the precision of spiking was lost, as previously observed. Overall, the synaptic response function of stellate cells suggests that this cell type may pick out transients in granule cell activity, and may generate precisely timed inhibition of Purkinje cells during behavior.