Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model

Synaptic plasticity, which underlies learning and memory, depends on calcium elevation in neurons, but the precise relationship between calcium and spatiotemporal patterns of synaptic inputs is unclear. Here, we develop a biologically realistic computational model of striatal spiny projection neuron...

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Main Authors: Daniel B Dorman, Joanna Jędrzejewska-Szmek, Kim T Blackwell
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/38588
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author Daniel B Dorman
Joanna Jędrzejewska-Szmek
Kim T Blackwell
author_facet Daniel B Dorman
Joanna Jędrzejewska-Szmek
Kim T Blackwell
author_sort Daniel B Dorman
collection DOAJ
description Synaptic plasticity, which underlies learning and memory, depends on calcium elevation in neurons, but the precise relationship between calcium and spatiotemporal patterns of synaptic inputs is unclear. Here, we develop a biologically realistic computational model of striatal spiny projection neurons with sophisticated calcium dynamics, based on data from rodents of both sexes, to investigate how spatiotemporally clustered and distributed excitatory and inhibitory inputs affect spine calcium. We demonstrate that coordinated excitatory synaptic inputs evoke enhanced calcium elevation specific to stimulated spines, with lower but physiologically relevant calcium elevation in nearby non-stimulated spines. Results further show a novel and important function of inhibition—to enhance the difference in calcium between stimulated and non-stimulated spines. These findings suggest that spine calcium dynamics encode synaptic input patterns and may serve as a signal for both stimulus-specific potentiation and heterosynaptic depression, maintaining balanced activity in a dendritic branch while inducing pattern-specific plasticity.
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spelling doaj.art-5ec4f40676164a79909872871e9b18442022-12-22T04:32:40ZengeLife Sciences Publications LtdeLife2050-084X2018-10-01710.7554/eLife.38588Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained modelDaniel B Dorman0https://orcid.org/0000-0001-7006-4593Joanna Jędrzejewska-Szmek1https://orcid.org/0000-0002-2336-0848Kim T Blackwell2https://orcid.org/0000-0003-4711-2344Interdisciplinary Program in Neuroscience, George Mason University, Fairfax, United StatesKrasnow Institute for Advanced Study, George Mason University, Fairfax, United StatesInterdisciplinary Program in Neuroscience, Bioengineering Department, Krasnow Institute for Advanced Study, George Mason University, Fairfax, United StatesSynaptic plasticity, which underlies learning and memory, depends on calcium elevation in neurons, but the precise relationship between calcium and spatiotemporal patterns of synaptic inputs is unclear. Here, we develop a biologically realistic computational model of striatal spiny projection neurons with sophisticated calcium dynamics, based on data from rodents of both sexes, to investigate how spatiotemporally clustered and distributed excitatory and inhibitory inputs affect spine calcium. We demonstrate that coordinated excitatory synaptic inputs evoke enhanced calcium elevation specific to stimulated spines, with lower but physiologically relevant calcium elevation in nearby non-stimulated spines. Results further show a novel and important function of inhibition—to enhance the difference in calcium between stimulated and non-stimulated spines. These findings suggest that spine calcium dynamics encode synaptic input patterns and may serve as a signal for both stimulus-specific potentiation and heterosynaptic depression, maintaining balanced activity in a dendritic branch while inducing pattern-specific plasticity.https://elifesciences.org/articles/38588striatumdendritic integrationspine calciumplasticitycomputational model
spellingShingle Daniel B Dorman
Joanna Jędrzejewska-Szmek
Kim T Blackwell
Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
eLife
striatum
dendritic integration
spine calcium
plasticity
computational model
title Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
title_full Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
title_fullStr Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
title_full_unstemmed Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
title_short Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model
title_sort inhibition enhances spatially specific calcium encoding of synaptic input patterns in a biologically constrained model
topic striatum
dendritic integration
spine calcium
plasticity
computational model
url https://elifesciences.org/articles/38588
work_keys_str_mv AT danielbdorman inhibitionenhancesspatiallyspecificcalciumencodingofsynapticinputpatternsinabiologicallyconstrainedmodel
AT joannajedrzejewskaszmek inhibitionenhancesspatiallyspecificcalciumencodingofsynapticinputpatternsinabiologicallyconstrainedmodel
AT kimtblackwell inhibitionenhancesspatiallyspecificcalciumencodingofsynapticinputpatternsinabiologicallyconstrainedmodel