Spike burst-pause dynamics of Purkinje cells regulate sensorimotor adaptation

Abstract

Cerebellar Purkinje cells mediate accurate eye movement coordination. However, it remains unclear how oculomotor adaptation depends on the interplay between the characteristic Purkinje cell response patterns, namely tonic, bursting, and spike pauses. Here, a spiking cerebellar model assesses the role of Purkinje cell firing patterns in vestibular ocular reflex (VOR) adaptation. The model captures the cerebellar microcircuit properties and it incorporates spike-based synaptic plasticity at multiple cerebellar sites. A detailed Purkinje cell model reproduces the three spike-firing patterns that are shown to regulate the cerebellar output. Our results suggest that pauses following Purkinje complex spikes (bursts) encode transient disinhibition of targeted medial vestibular nuclei, critically gating the vestibular signals conveyed by mossy fibres. This gating mechanism accounts for early and coarse VOR acquisition, prior to the late reflex consolidation. In addition, properly timed and sized Purkinje cell bursts allow the ratio between long-term depression and potentiation (LTD/LTP) to be finely shaped at mossy fibre-medial vestibular nuclei synapses, which optimises VOR consolidation. Tonic Purkinje cell firing maintains the consolidated VOR through time. Importantly, pauses are crucial to facilitate VOR phase-reversal learning, by reshaping previously learnt synaptic weight distributions. Altogether, these results predict that Purkinje spike burst-pause dynamics are instrumental to VOR learning and reversal adaptation.

Publication
PLoS Computational Biology
Niceto Luque
Niceto Luque
Associate Professor

Associate Professor at the Department of Computer Engineering, Automation and Robotics and Principal Investigator at the Applied Computational Neuroscience Group.

Francisco Naveros
Francisco Naveros
Postdoctoral Researcher

Senior postdoc at the Applied Computational Neuroscience Research Group at the University of Granada.

Ríchard R. Carrillo
Ríchard R. Carrillo
Assistant Professor

Associate Professor at the Department of Computer Engineering, Automation and Robotics and Principal Investigator at the Applied Computational Neuroscience Group.

Eduardo Ros
Eduardo Ros
Full Professor

Full professor in computer architecture, principal investigator at the Computational Neuroscience and Neurorobotics Lab and principal investigator of the VALERIA lab of the University of Granada.