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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Main Authors: Andreas Hoehne, Maureen H McFadden, David A DiGregorio
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/57344
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spelling 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
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AT davidadigregorio feedforwardrecruitmentofelectricalsynapsesenhancessynchronousspikinginthemousecerebellarcortex
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