Target-specific control of olfactory bulb periglomerular cells by GABAergic and cholinergic basal forebrain inputs

Abstract
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Abstract

The olfactory bulb (OB), the first relay for odor processing in the brain, receives dense GABAergic and cholinergic long-range projections from basal forebrain (BF) nuclei that provide information about the internal state and behavioral context of the animal. However, the targets, impact and dynamic of these afferents are still unclear. I studied how BF synaptic inputs modulate activity in diverse subtypes of periglomerular (PG) interneurons using optogenetic stimulation and loose cell-attached or whole-cell patch-clamp recording in OB slices from adult mice. GABAergic BF inputs potently blocked PG cells firing except in a minority of calretinin-expressing cells in which GABA release elicited spiking. Parallel cholinergic projections excited a previously overlooked PG cell subtype via synaptic activation of M1 muscarinic receptors. Low frequency stimulation of the cholinergic axons drove persistent firing in these PG cells thereby increasing tonic inhibition in principal neurons. Taken together, these findings suggest that modality-specific BF inputs can orchestrate synaptic inhibition in OB glomeruli using multiple, potentially independent, inhibitory or excitatory target-specific pathways.

Data availability

All numerical data used to construct graphs in each figure are available on ZENODO, https://doi.org/10.5281/zenodo.6259698

The following data sets were generated

1. De Saint Jan Didier
(2022) Target-specific control of olfactory bulb periglomerular cells by GABAergic and cholinergic basal forebrain inputs
Zenodo open data repository. doi:10.5281/zenodo.6259698.

https://doi.org/10.5281/zenodo.6259698

Article and author information

Author details

Didier De Saint Jan

Institut des Neurosciences Cellulaires et Intégratives, Centre National de la Recherche Scientifique, Strasbourg, France

For correspondence
desaintjan@inci-cnrs.unistra.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2459-9703

Funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments procedures were approved by the French Ministry and by the local ethic committee for animal experimentation (CREMEAS)(authorization number APAFIS#5250-2016042115058488v3 and v7) . Mice were housed in the animal facility with ad libidum access to food and water. Animals were sacrificed by cervical dislocation following the methods approved by the directive 2010/63/EU of the European Parliament and Council. Surgeries were performed under anesthesia and every effort was made to minimize suffering.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.