S100β-mediated astroglial control of firing and input processing in layer 5 pyramidal neurons of the mouse visual cortex.


Journal

The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262

Informations de publication

Date de publication:
01 2021
Historique:
received: 10 07 2020
accepted: 23 11 2020
pubmed: 9 12 2020
medline: 13 4 2021
entrez: 8 12 2020
Statut: ppublish

Résumé

Inputs impinging on layer 5 pyramidal neurons perform essential operations as these cells represent one of the most important output carriers of the cerebral cortex. However, the contribution of astrocytes, a type of glial cell, to these operations is poorly documented. Here we found that optogenetic activation of astrocytes in the vicinity of layer 5 in the mouse primary visual cortex induces spiking in local pyramidal neurons through Nav1.6 ion channels and prolongs the responses elicited in these neurons by stimulation of their distal inputs in cortical layer 1. This effect partially involved glutamatergic signalling but relied mostly on the astrocytic calcium-binding protein S100β, which regulates the concentration of calcium in the extracellular space around neurons. These findings show that astrocytes contribute to the fundamental computational operations of the cortex by acting on the ionic environment of neurons. The most complex cerebral functions are performed by the cortex, whose most important output is carried out by its layer 5 pyramidal neurons. Their firing reflects integration of the sensory and contextual information that they receive. There is evidence that astrocytes influence cortical neuron firing through the release of gliotransmitters such as ATP, glutamate or GABA. These effects have been described at the network and at the synaptic levels, but it is still unclear how astrocytes influence neuron input-output transfer function at the cellular level. Here, we used optogenetic tools coupled with electrophysiological, imaging and anatomical approaches to test whether and how astrocytic activation affected processing of distal inputs to layer 5 pyramidal neurons (L5PNs). We show that optogenetic activation of astrocytes near L5PN cell body prolonged firing induced by distal inputs to L5PNs and potentiated their ability to trigger spikes. The observed astrocytic effects on L5PN firing involved glutamatergic transmission to some extent but relied mostly on release of S100β, an astrocytic Ca

Identifiants

pubmed: 33289081
doi: 10.1113/JP280501
doi:

Substances chimiques

S100 Calcium Binding Protein beta Subunit 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

677-707

Subventions

Organisme : CIHR
ID : 14932
Pays : Canada
Organisme : CIHR
ID : 407083
Pays : Canada

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.

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Auteurs

Dimitri Ryczko (D)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.
Département de Pharmacologie-Physiologie, Université de Sherbrooke, Sherbrooke, QC, Canada.
Centre de recherche du CHUS, Sherbrooke, QC, Canada.
Institut de Pharmacologie de Sherbrooke, Sherbrooke, QC, Canada.
Centre d'excellence en neurosciences de l'Université de Sherbrooke, Sherbrooke, QC, Canada.

Maroua Hanini-Daoud (M)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.

Steven Condamine (S)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.

Benjamin J B Bréant (BJB)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.

Maxime Fougère (M)

Département de Pharmacologie-Physiologie, Université de Sherbrooke, Sherbrooke, QC, Canada.

Roberto Araya (R)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.

Arlette Kolta (A)

Département de Neurosciences, Université de Montréal, Montréal, QC, Canada.
Faculté de Médecine Dentaire, Université de Montréal, Montréal, QC, Canada.

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