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

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Cite this article as: eLife 2018;7:e38588 doi: 10.7554/eLife.38588

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Abstract

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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All model simulation and analysis code are publicly and freely available on ModelDB (http://senselab.med.yale.edu/ModelDB/showModel.cshtml?model=245411).

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Daniel B Dorman

Interdisciplinary Program in Neuroscience, George Mason University, Fairfax, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7006-4593
Joanna Jędrzejewska-Szmek

Krasnow Institute for Advanced Study, George Mason University, Fairfax, United States

Competing interests
The authors declare that no competing interests exist.
Kim T Blackwell

Bioengineering Department, George Mason University, Fairfax, United States

For correspondence
kblackw1@gmu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4711-2344

Funding

National Institute on Drug Abuse (R01DA033390)

Kim T Blackwell

National Institute on Alcohol Abuse and Alcoholism (R01AA16022)

Kim T Blackwell

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

Reviewing Editor

Mary B Kennedy, California Institute of Technology, United States

Publication history

Received: May 23, 2018
Accepted: October 24, 2018
Accepted Manuscript published: October 25, 2018 (version 1)
Version of Record published: November 14, 2018 (version 2)

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.