Silent and bursting states of Purkinje cell activity modulate VOR adaptation

Abstract

Within the cerebellar cortex, the inhibitory projections of Purkinje cells to deep cerebellar nuclei mediate fine motor coordination. Understanding the dynamics of Purkinje cell discharges can thus provide insights into sensorimotor adaptation. It is known that Purkinje cells exhibit three firing modes, namely tonic, silent, and bursting. However, the relation between these firing patterns and cerebellar-dependent behavioural adaptation remains poorly understood. Here, we present a spiking cerebellar model that explores the putative role of the multiple Purkinje operating modes in vestibular ocular reflex (VOR) adaptation. VOR stabilizes images on the retina during head ipsilateral rotations using contralateral eye-movement compensations. The model captures the main cerebellar microcircuit properties and incorporates multiple synaptic plasticity mechanisms at different cerebellar sites (parallel fibres - Purkinje cells, mossy fibres - deep cerebellar nuclei, and Purkinje cells - deep cerebellar nuclei). An analytically reduced version of a detailed Purkinje cell model is at the core of the overall cerebellar function. This allows us to examine the impact of different Purkinje firing modes on VOR adaptation performance. We show that the Purkinje silent mode, through transient disinhibition of targeted cells, gates the neural signals conveyed by mossy fibres to deep cerebellar nuclei. This gating mechanism accounts for early and coarse VOR, prior to the late consolidation of the reflex. In turn, properly timed and sized Purkinje bursts can finely shape the balance between long-term depression and potentiation (LTD/LTP) at mossy fibre - deep cerebellar nuclei synapses. This fine tuning of LTD/LTP balance increases the rate of VOR consolidation. Finally, the silent mode can facilitate the VOR reversal phase by reshaping previously learned synaptic weight distributions. Altogether, these results predict that the interburst dynamics of Purkinje cell activity is instrumental to VOR learning and reversal phase adaptation.

Publication
CNS*2017
Date
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