Abstract

The cerebellar granule cells (GrCs) are classically described as a homogeneous neuronal population discharging regularly without adaptation. We show that GrCs in fact generate diverse response patterns to current injection and synaptic activation, ranging from adaptation to acceleration of firing. Adaptation was predicted by parameter optimization in detailed computational models based on available knowledge on GrC ionic channels. The models also predicted that acceleration required additional mechanisms. We found that yet unrecognized TRPM4 currents specifically accounted for firing acceleration and that adapting GrCs outperformed accelerating GrCs in transmitting high-frequency mossy fiber (MF) bursts over a background discharge. This implied that GrC subtypes identified by their electroresponsiveness corresponded to specific neurotransmitter release probability values. Simulations showed that fine-tuning of pre- and post-synaptic parameters generated effective MF-GrC transmission channels, which could enrich the processing of input spike patterns and enhance spatio-temporal recoding at the cerebellar input stage.

Highlights

  • The cerebellar granule cells (GrCs) are classically described as a homogeneous neuronal population discharging regularly without adaptation

  • GrCs are located at the input stage of cerebellum, where they are thought to perform the fundamental operations of combinatorial expansion and spatio-temporal recoding predicted by the motor learning theory[5,6]

  • This paper shows that cerebellar GrCs, in contrast to the canonical view describing them as a homogeneous population of neurons generating regular firing, show a rich repertoire of firing patterns

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Summary

Introduction

The cerebellar granule cells (GrCs) are classically described as a homogeneous neuronal population discharging regularly without adaptation. We found that yet unrecognized TRPM4 currents accounted for firing acceleration and that adapting GrCs outperformed accelerating GrCs in transmitting high-frequency mossy fiber (MF) bursts over a background discharge This implied that GrC subtypes identified by their electroresponsiveness corresponded to specific neurotransmitter release probability values. GrCs are located at the input stage of cerebellum, where they are thought to perform the fundamental operations of combinatorial expansion and spatio-temporal recoding predicted by the motor learning theory[5,6] While these operations would greatly benefit of a rich repertoire of signal transformation properties, GrCs appeared very homogeneous in size and shape since their original description[7,8]. We observed that adapting GrCs exploit low-p synapses attaining a much higher signal-to-noise ratio (S/N) than accelerating GrCs

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