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Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA.

ABSTRACT: Inhibitory projection neurons in the deep cerebellar nuclei (DCN) provide GABAergic input to neurons of the inferior olive (IO) that in turn produce climbing fiber synapses onto Purkinje cells. Anatomical evidence suggests that DCN to IO synapses control electrical coupling between IO neurons. In vivo studies suggest that they also control the synchrony of IO neurons and play an important role in cerebellar learning. Here we describe the DCN to IO synapse. Remarkably, GABA release was almost exclusively asynchronous, with little conventional synchronous release. Synaptic transmission was extremely frequency dependent, with low-frequency stimulation being largely ineffective. However, due to the prominence of asynchronous release, stimulation at frequencies above 10 Hz evoked steady-state inhibitory currents. These properties seem ideally suited to transform the firing rate of DCN neurons into sustained inhibition that both suppresses the firing of IO cells and regulates the effective coupling between IO neurons.

SUBMITTER: Best AR

PROVIDER: S-EPMC3261724 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA.

Best Aaron R AR Regehr Wade G WG

Neuron 20090501 4

Inhibitory projection neurons in the deep cerebellar nuclei (DCN) provide GABAergic input to neurons of the inferior olive (IO) that in turn produce climbing fiber synapses onto Purkinje cells. Anatomical evidence suggests that DCN to IO synapses control electrical coupling between IO neurons. In vivo studies suggest that they also control the synchrony of IO neurons and play an important role in cerebellar learning. Here we describe the DCN to IO synapse. Remarkably, GABA release was almost exc ...[more]

PMID: 19477156

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Project description: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.

Dataset Information

Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA.

Publications

Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA.

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