Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons

Synaptic transmission, connectivity, and dendritic morphology mature in parallel during brain development and are often disrupted in neurodevelopmental disorders. Yet how these changes influence the neuronal computations necessary for normal brain function are not well understood. To identify cellul...

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Autores principales: Celia Biane, Florian Rückerl, Therese Abrahamsson, Cécile Saint-Cloment, Jean Mariani, Ryuichi Shigemoto, David A DiGregorio, Rachel M Sherrard, Laurence Cathala
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Publicado: eLife Sciences Publications Ltd 2021
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Acceso en línea:https://doaj.org/article/e901c6bb1a0b4100a07a29c39d4e8419
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spelling oai:doaj.org-article:e901c6bb1a0b4100a07a29c39d4e84192021-11-12T14:40:10ZDevelopmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons10.7554/eLife.659542050-084Xe65954https://doaj.org/article/e901c6bb1a0b4100a07a29c39d4e84192021-11-01T00:00:00Zhttps://elifesciences.org/articles/65954https://doaj.org/toc/2050-084XSynaptic transmission, connectivity, and dendritic morphology mature in parallel during brain development and are often disrupted in neurodevelopmental disorders. Yet how these changes influence the neuronal computations necessary for normal brain function are not well understood. To identify cellular mechanisms underlying the maturation of synaptic integration in interneurons, we combined patch-clamp recordings of excitatory inputs in mouse cerebellar stellate cells (SCs), three-dimensional reconstruction of SC morphology with excitatory synapse location, and biophysical modeling. We found that postnatal maturation of postsynaptic strength was homogeneously reduced along the somatodendritic axis, but dendritic integration was always sublinear. However, dendritic branching increased without changes in synapse density, leading to a substantial gain in distal inputs. Thus, changes in synapse distribution, rather than dendrite cable properties, are the dominant mechanism underlying the maturation of neuronal computation. These mechanisms favor the emergence of a spatially compartmentalized two-stage integration model promoting location-dependent integration within dendritic subunits.Celia BianeFlorian RückerlTherese AbrahamssonCécile Saint-ClomentJean MarianiRyuichi ShigemotoDavid A DiGregorioRachel M SherrardLaurence CathalaeLife Sciences Publications Ltdarticleinterneurondendritic integrationsynaptic transmissiondevelopmentcerebellumneuronal computationMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic interneuron
dendritic integration
synaptic transmission
development
cerebellum
neuronal computation
Medicine
R
Science
Q
Biology (General)
QH301-705.5
spellingShingle interneuron
dendritic integration
synaptic transmission
development
cerebellum
neuronal computation
Medicine
R
Science
Q
Biology (General)
QH301-705.5
Celia Biane
Florian Rückerl
Therese Abrahamsson
Cécile Saint-Cloment
Jean Mariani
Ryuichi Shigemoto
David A DiGregorio
Rachel M Sherrard
Laurence Cathala
Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
description Synaptic transmission, connectivity, and dendritic morphology mature in parallel during brain development and are often disrupted in neurodevelopmental disorders. Yet how these changes influence the neuronal computations necessary for normal brain function are not well understood. To identify cellular mechanisms underlying the maturation of synaptic integration in interneurons, we combined patch-clamp recordings of excitatory inputs in mouse cerebellar stellate cells (SCs), three-dimensional reconstruction of SC morphology with excitatory synapse location, and biophysical modeling. We found that postnatal maturation of postsynaptic strength was homogeneously reduced along the somatodendritic axis, but dendritic integration was always sublinear. However, dendritic branching increased without changes in synapse density, leading to a substantial gain in distal inputs. Thus, changes in synapse distribution, rather than dendrite cable properties, are the dominant mechanism underlying the maturation of neuronal computation. These mechanisms favor the emergence of a spatially compartmentalized two-stage integration model promoting location-dependent integration within dendritic subunits.
format article
author Celia Biane
Florian Rückerl
Therese Abrahamsson
Cécile Saint-Cloment
Jean Mariani
Ryuichi Shigemoto
David A DiGregorio
Rachel M Sherrard
Laurence Cathala
author_facet Celia Biane
Florian Rückerl
Therese Abrahamsson
Cécile Saint-Cloment
Jean Mariani
Ryuichi Shigemoto
David A DiGregorio
Rachel M Sherrard
Laurence Cathala
author_sort Celia Biane
title Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
title_short Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
title_full Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
title_fullStr Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
title_full_unstemmed Developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
title_sort developmental emergence of two-stage nonlinear synaptic integration in cerebellar interneurons
publisher eLife Sciences Publications Ltd
publishDate 2021
url https://doaj.org/article/e901c6bb1a0b4100a07a29c39d4e8419
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