Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.

Pyramidal neurons (PNs) are covered by thousands of dendritic spines receiving excitatory synaptic inputs. The ultrastructure of dendritic spines shapes signal compartmentalization, but ultrastructural diversity is rarely taken into account in computational models of synaptic integration. Here, we d...

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Autores principales: Olivier Gemin, Pablo Serna, Joseph Zamith, Nora Assendorp, Matteo Fossati, Philippe Rostaing, Antoine Triller, Cécile Charrier
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:cad009f0e7c0472b9ccbd417f984f4fb2021-12-02T19:54:38ZUnique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.1544-91731545-788510.1371/journal.pbio.3001375https://doaj.org/article/cad009f0e7c0472b9ccbd417f984f4fb2021-08-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001375https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Pyramidal neurons (PNs) are covered by thousands of dendritic spines receiving excitatory synaptic inputs. The ultrastructure of dendritic spines shapes signal compartmentalization, but ultrastructural diversity is rarely taken into account in computational models of synaptic integration. Here, we developed a 3D correlative light-electron microscopy (3D-CLEM) approach allowing the analysis of specific populations of synapses in genetically defined neuronal types in intact brain circuits. We used it to reconstruct segments of basal dendrites of layer 2/3 PNs of adult mouse somatosensory cortex and quantify spine ultrastructural diversity. We found that 10% of spines were dually innervated and 38% of inhibitory synapses localized to spines. Using our morphometric data to constrain a model of synaptic signal compartmentalization, we assessed the impact of spinous versus dendritic shaft inhibition. Our results indicate that spinous inhibition is locally more efficient than shaft inhibition and that it can decouple voltage and calcium signaling, potentially impacting synaptic plasticity.Olivier GeminPablo SernaJoseph ZamithNora AssendorpMatteo FossatiPhilippe RostaingAntoine TrillerCécile CharrierPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 8, p e3001375 (2021)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Olivier Gemin
Pablo Serna
Joseph Zamith
Nora Assendorp
Matteo Fossati
Philippe Rostaing
Antoine Triller
Cécile Charrier
Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
description Pyramidal neurons (PNs) are covered by thousands of dendritic spines receiving excitatory synaptic inputs. The ultrastructure of dendritic spines shapes signal compartmentalization, but ultrastructural diversity is rarely taken into account in computational models of synaptic integration. Here, we developed a 3D correlative light-electron microscopy (3D-CLEM) approach allowing the analysis of specific populations of synapses in genetically defined neuronal types in intact brain circuits. We used it to reconstruct segments of basal dendrites of layer 2/3 PNs of adult mouse somatosensory cortex and quantify spine ultrastructural diversity. We found that 10% of spines were dually innervated and 38% of inhibitory synapses localized to spines. Using our morphometric data to constrain a model of synaptic signal compartmentalization, we assessed the impact of spinous versus dendritic shaft inhibition. Our results indicate that spinous inhibition is locally more efficient than shaft inhibition and that it can decouple voltage and calcium signaling, potentially impacting synaptic plasticity.
format article
author Olivier Gemin
Pablo Serna
Joseph Zamith
Nora Assendorp
Matteo Fossati
Philippe Rostaing
Antoine Triller
Cécile Charrier
author_facet Olivier Gemin
Pablo Serna
Joseph Zamith
Nora Assendorp
Matteo Fossati
Philippe Rostaing
Antoine Triller
Cécile Charrier
author_sort Olivier Gemin
title Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
title_short Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
title_full Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
title_fullStr Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
title_full_unstemmed Unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3D correlative light and electron microscopy.
title_sort unique properties of dually innervated dendritic spines in pyramidal neurons of the somatosensory cortex uncovered by 3d correlative light and electron microscopy.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/cad009f0e7c0472b9ccbd417f984f4fb
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