Rate versus synchrony codes for cerebellar control of motor behavior

Information transmission between neural populations could occur through either coordinated changes in firing rates or the precise transmission of spike timing. We investigate the code for information transmission from a part of the cerebellar cortex that is crucial for the accurate execution of a quantifiable motor behavior. Simultaneous recordings from Purkinje cell pairs in the cerebellum of rhesus macaques reveal how these cells coordinate their activity to drive smooth pursuit eye movements. Purkinje cells show millisecond-scale coordination of spikes (synchrony), but the level of synchrony is small and insufficient to impact the firing of downstream vestibular nucleus neurons. Analysis of previous metrics that purported to reveal Purkinje cell synchrony demonstrates that these metrics conflate changes in firing rate and neuron-neuron covariance. We conclude that the output of the cerebellar cortex uses primarily a rate rather than a synchrony code to drive the activity of downstream neurons and thus control motor behavior.