Electrical coupling controls dimensionality and chaotic firing of inferior olive neurons

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. 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. Here, we developed a novel method that uses a biophysical model of the inferior olive to accurately estimate the effective coupling strengths between inferior olive neurons from in vivo recordings of spike activity in three different coupling conditions. We found that high coupling strengths induce synchronous firing and decrease the dimensionality of inferior olive firing dynamics. In contrast, intermediate coupling strengths lead to chaotic firing and increase the dimensionality of the firing dynamics. Thus, electrical coupling is a feasible mechanism to control dimensionality and chaotic firing of inferior olive neurons. In sum, our results provide insights into possible mechanisms underlying cerebellar function and, in general, a biologically plausible framework to control the dimensionality of neural coding.