The Control of Rate and Timing of Spikes in the Deep Cerebellar Nuclei by Inhibition

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Cerebellar nucleus neurons were recorded in vitro, and dynamic clamping was used to simulate inhibitory synaptic input from Purkinje cells likely to occur in vivo. Inhibitory input patterns with varying synaptic amplitudes and synchronicity were applied to determine how spike rate and spike timing can be controlled by inhibition. The excitatory input conductance was held constant to isolate the effect of dynamic inhibitory inputs on spiking. We found that the timing of individual spikes was controlled precisely by short decreases in the inhibitory conductance that were the consequence of synchronization between many inputs. The spike rate of nucleus neurons was controlled in a linear way by the rate of inhibitory inputs. The spike rate, however, also depended strongly on the amount of synchronicity present in the inhibitory inputs. An irregular spike train similar to in vivo data resulted from applied synaptic conductances when the conductance was large enough to overcome intrinsic pacemaker currents. In this situation subthreshold fluctuations in membrane potential closely followed the time course of the combined reversal potential of excitation and inhibition. This indicates that the net synaptic driving force for realistic input levels in vivo may be small and that synaptic input may operate primarily by shunting. The accurate temporal control of output spiking by inhibitory input that can be achieved in this way in the deep cerebellar nuclei may be particularly important to allow fine temporal control of movement via inhibitory output from cerebellar cortex.