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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eLife Sciences Publications Ltd
2021
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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) |
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interneuron dendritic integration synaptic transmission development cerebellum neuronal computation Medicine R Science Q Biology (General) QH301-705.5 |
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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 |
work_keys_str_mv |
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1718430406545506304 |