Electrical coupling controls dimensionality and chaotic firing of inferior olive neurons.

Huu Hoang,Isao T Tokuda,Keisuke Toyama,Mitsuo Kawato,Nicolas Schweighofer,Kazuyuki Aihara,Yoshito Hirata,Eric J Lang,Chris De Zeeuw

doi:10.1371/journal.pcbi.1008075

Abstract

We previously proposed, on theoretical grounds, that the cerebellum must regulate the dimensionality of its neuronal activity during motor learning and control to cope with the low firing frequency of inferior olive neurons, which form one of two major inputs to the cerebellar cortex. Such dimensionality regulation is possible via modulation of electrical coupling through the gap junctions between inferior olive neurons by inhibitory GABAergic synapses. In addition, we previously showed in simulations that intermediate coupling strengths induce chaotic firing of inferior olive neurons and increase their information carrying capacity. However, there is no in vivo experimental data supporting these two theoretical predictions. Here, we computed the levels of synchrony, dimensionality, and chaos of the inferior olive code by analyzing in vivo recordings of Purkinje cell complex spike activity in three different coupling conditions: carbenoxolone (gap junctions blocker), control, and picrotoxin (GABA-A receptor antagonist). To examine the effect of electrical coupling on dimensionality and chaotic dynamics, we first determined the physiological range of effective coupling strengths between inferior olive neurons in the three conditions using a combination of a biophysical network model of the inferior olive and a novel Bayesian model averaging approach. We found that effective coupling co-varied with synchrony and was inversely related to the dimensionality of inferior olive firing dynamics, as measured via a principal component analysis of the spike trains in each condition. Furthermore, for both the model and the data, we found an inverted U-shaped relationship between coupling strengths and complexity entropy, a measure of chaos for spiking neural data. These results are consistent with our hypothesis according to which electrical coupling regulates the dimensionality and the complexity in the inferior olive neurons in order to optimize both motor learning and control of high dimensional motor systems by the cerebellum.

Highlights

The cerebellum plays important roles in motor learning and motor control, how it performs these roles is still unclear
Computational theory suggests that the cerebellum must decrease the dimensionality of its neuronal activity to learn and control high dimensional motor systems effectively, while being constrained by the low firing frequency of inferior olive neurons, one of the two major source of input signals to the cerebellum
We previously proposed that the cerebellum adaptively controls the dimensionality of inferior olive firing by adjusting the level of synchrony and that such control is made possible by modulating the electrical coupling strength between inferior olive neurons

Summary

Introduction

The cerebellum plays important roles in motor learning and motor control, how it performs these roles is still unclear. There is evidence that the olivo-cerebellar system conveys error signals into the cerebellum [1,2,3,4] and induces plasticity in parallel fiber-Purkinje cell synapses (e.g., [5,6,7,8]). Such error-driven plasticity is a central tenet of the original motor learning theory of the cerebellum [8,9,10], as it can allow learning of internal models for motor control [11,12,13,14,15,16]. It has been shown that spontaneous olivo-cerebellar activity can directly influence ongoing spiking in cerebellar nuclear cells, which relay motor commands produced by the cerebellar cortex [21,22]

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Conclusion