Abstract

The climbing fiber input to Purkinje cells acts as a teaching signal by triggering a massive influx of dendritic calcium that marks the occurrence of instructive stimuli during cerebellar learning. Here, we challenge the view that these calcium spikes are all-or-none and only signal whether the instructive stimulus has occurred, without providing parametric information about its features. We imaged ensembles of Purkinje cell dendrites in awake mice and measured their calcium responses to periocular airpuffs that serve as instructive stimuli during cerebellar-dependent eyeblink conditioning. Information about airpuff duration and pressure was encoded probabilistically across repeated trials, and in two additional signals in single trials: the synchrony of calcium spikes in the Purkinje cell population, and the amplitude of the calcium spikes, which was modulated by a non-climbing fiber pathway. These results indicate that calcium-based teaching signals in Purkinje cells contain analog information that encodes the strength of instructive stimuli trial-by-trial.

Highlights

  • The climbing fiber (CF) input to Purkinje cells (PCs) plays a key role in theories of cerebellar learning (Houk et al, 1996; Ito, 2000) by providing a teaching signal that sounds the alarm when an unexpected sensory event is encountered (Simpson et al, 1996; De Zeeuw et al, 1998; Ito, 2013)

  • We used a two-photon microscope to image calcium signals triggered by sensory-driven activation of climbing fiber (CF) inputs to Purkinje cell (PC) dendrites of awake mice

  • We have previously shown that these calcium transients are triggered in each individual PC dendrite by activation of its one-and-only climbing fiber (CF) input, which evokes a complex spike in the PC somata (Ozden et al, 2008)

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Summary

Introduction

The climbing fiber (CF) input to Purkinje cells (PCs) plays a key role in theories of cerebellar learning (Houk et al, 1996; Ito, 2000) by providing a teaching signal that sounds the alarm when an unexpected sensory event is encountered (Simpson et al, 1996; De Zeeuw et al, 1998; Ito, 2013) Support for this hypothesis comes from studies of Pavlovian eyeblink conditioning (Medina et al, 2000), a simple associative task in which subjects learn to blink to an initially neutral cue if it is repeatedly paired with a blink-eliciting instructive stimulus, such as a periocular airpuff. The CF-PC synapse is one of the most powerful and reliable in the brain (Schmolesky et al, 2002; Ohtsuki et al, 2009): each time the CF fires a burst, it evokes in PCs both

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