Rapid acquisition of internal models of timing by Purkinje cells enables faster behavioral responses

Abstract

SummaryNeural mechanisms that allow animals to keep track of multi-second time intervals are not clearly understood. Further, the role of the cerebellum in this process is under debate. We show that when periodic optic flow is presented, cerebellar Purkinje cells in larval zebrafish show simple spike and climbing fiber activity that ramps up in anticipation of flow onset. A distinct subset of Purkinje cells reports prediction error signals mediated solely by climbing fiber inputs when the stimulus interval is altered. These signals develop in 2 trials and can quickly adapt to new intervals if stimulus timing is altered. Robust predictive and prediction error signals are associated with faster behavioral responses and the modulation of behavioral latency is dependent on the cerebellum. Based on our results, we built an algorithmic model that explains how Purkinje cells mediate acquisition and updating of an internal model of stimulus time intervals.HighlightsLarval zebrafish learn the timing of optic flow stimuli with minimal sensory evidence.The cerebellum performs an innate, hitherto unknown, supra-second timing function.Purkinje cells use prediction errors to acquire an internal model of stimulus timing.Robust predictions lead to faster reaction times when stimulus arrives as expected.