Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex
In the cerebellar cortex, molecular layer interneurons use chemical and electrical synapses to form subnetworks that fine-tune the spiking output of the cerebellum. Although electrical synapses can entrain activity within neuronal assemblies, their role in feed-forward circuits is less well explored...
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2020-09-01
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doaj-b529dee35ece4f67b1ae5332b69f65562021-05-05T21:33:37ZengeLife Sciences Publications LtdeLife2050-084X2020-09-01910.7554/eLife.57344Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortexAndreas Hoehne0Maureen H McFadden1https://orcid.org/0000-0001-9770-7069David A DiGregorio2https://orcid.org/0000-0002-6417-4566Laboratory of Synapse and Circuit Dynamics, Institut Pasteur, Paris Cedex, France; Sorbonne University, ED3C, Paris, FranceLaboratory of Synapse and Circuit Dynamics, Institut Pasteur, Paris Cedex, FranceLaboratory of Synapse and Circuit Dynamics, Institut Pasteur, Paris Cedex, FranceIn the cerebellar cortex, molecular layer interneurons use chemical and electrical synapses to form subnetworks that fine-tune the spiking output of the cerebellum. Although electrical synapses can entrain activity within neuronal assemblies, their role in feed-forward circuits is less well explored. By combining whole-cell patch-clamp and 2-photon laser scanning microscopy of basket cells (BCs), we found that classical excitatory postsynaptic currents (EPSCs) are followed by GABAA receptor-independent outward currents, reflecting the hyperpolarization component of spikelets (a synapse-evoked action potential passively propagating from electrically coupled neighbors). FF recruitment of the spikelet-mediated inhibition curtails the integration time window of concomitant excitatory postsynaptic potentials (EPSPs) and dampens their temporal integration. In contrast with GABAergic-mediated feed-forward inhibition, the depolarizing component of spikelets transiently increases the peak amplitude of EPSPs, and thus postsynaptic spiking probability. Therefore, spikelet transmission can propagate within the BC network to generate synchronous inhibition of Purkinje cells, which can entrain cerebellar output for driving temporally precise behaviors.https://elifesciences.org/articles/57344electrical synapsesinterneuronsfeed-forward circuitsynchronycerebellum |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Andreas Hoehne Maureen H McFadden David A DiGregorio |
spellingShingle |
Andreas Hoehne Maureen H McFadden David A DiGregorio Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex eLife electrical synapses interneurons feed-forward circuit synchrony cerebellum |
author_facet |
Andreas Hoehne Maureen H McFadden David A DiGregorio |
author_sort |
Andreas Hoehne |
title |
Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
title_short |
Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
title_full |
Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
title_fullStr |
Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
title_full_unstemmed |
Feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
title_sort |
feed-forward recruitment of electrical synapses enhances synchronous spiking in the mouse cerebellar cortex |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2020-09-01 |
description |
In the cerebellar cortex, molecular layer interneurons use chemical and electrical synapses to form subnetworks that fine-tune the spiking output of the cerebellum. Although electrical synapses can entrain activity within neuronal assemblies, their role in feed-forward circuits is less well explored. By combining whole-cell patch-clamp and 2-photon laser scanning microscopy of basket cells (BCs), we found that classical excitatory postsynaptic currents (EPSCs) are followed by GABAA receptor-independent outward currents, reflecting the hyperpolarization component of spikelets (a synapse-evoked action potential passively propagating from electrically coupled neighbors). FF recruitment of the spikelet-mediated inhibition curtails the integration time window of concomitant excitatory postsynaptic potentials (EPSPs) and dampens their temporal integration. In contrast with GABAergic-mediated feed-forward inhibition, the depolarizing component of spikelets transiently increases the peak amplitude of EPSPs, and thus postsynaptic spiking probability. Therefore, spikelet transmission can propagate within the BC network to generate synchronous inhibition of Purkinje cells, which can entrain cerebellar output for driving temporally precise behaviors. |
topic |
electrical synapses interneurons feed-forward circuit synchrony cerebellum |
url |
https://elifesciences.org/articles/57344 |
work_keys_str_mv |
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