Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons

Competition between synapses contributes to activity-dependent refinement of the nervous system during development. Does local competition between neighboring synapses drive circuit remodeling during experience-dependent plasticity in the cerebral cortex? Here, we examined the role of activity-media...

Full description

Bibliographic Details
Main Authors: Won Chan Oh, Laxmi Kumar Parajuli, Karen Zito
Format: Article
Language:English
Published: Elsevier 2015-01-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124714010456
_version_ 1818204093946003456
author Won Chan Oh
Laxmi Kumar Parajuli
Karen Zito
author_facet Won Chan Oh
Laxmi Kumar Parajuli
Karen Zito
author_sort Won Chan Oh
collection DOAJ
description Competition between synapses contributes to activity-dependent refinement of the nervous system during development. Does local competition between neighboring synapses drive circuit remodeling during experience-dependent plasticity in the cerebral cortex? Here, we examined the role of activity-mediated competitive interactions in regulating dendritic spine structure and function on hippocampal CA1 neurons. We found that high-frequency glutamatergic stimulation at individual spines, which leads to input-specific synaptic potentiation, induces shrinkage and weakening of nearby unstimulated synapses. This heterosynaptic plasticity requires potentiation of multiple neighboring spines, suggesting that a local threshold of neural activity exists beyond which inactive synapses are punished. Notably, inhibition of calcineurin, IP3Rs, or group I metabotropic glutamate receptors (mGluRs) blocked heterosynaptic shrinkage without blocking structural potentiation, and inhibition of Ca2+/calmodulin-dependent protein kinase II (CaMKII) blocked structural potentiation without blocking heterosynaptic shrinkage. Our results support a model in which activity-induced shrinkage signal, and not competition for limited structural resources, drives heterosynaptic structural and functional depression during neural circuit refinement.
first_indexed 2024-12-12T03:35:46Z
format Article
id doaj.art-6cca7c3ab7134e7187adc9759d59c518
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-12-12T03:35:46Z
publishDate 2015-01-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-6cca7c3ab7134e7187adc9759d59c5182022-12-22T00:39:49ZengElsevierCell Reports2211-12472015-01-0110216216910.1016/j.celrep.2014.12.016Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 NeuronsWon Chan Oh0Laxmi Kumar Parajuli1Karen Zito2Center for Neuroscience, University of California Davis, Davis, CA 95616, USACenter for Neuroscience, University of California Davis, Davis, CA 95616, USACenter for Neuroscience, University of California Davis, Davis, CA 95616, USACompetition between synapses contributes to activity-dependent refinement of the nervous system during development. Does local competition between neighboring synapses drive circuit remodeling during experience-dependent plasticity in the cerebral cortex? Here, we examined the role of activity-mediated competitive interactions in regulating dendritic spine structure and function on hippocampal CA1 neurons. We found that high-frequency glutamatergic stimulation at individual spines, which leads to input-specific synaptic potentiation, induces shrinkage and weakening of nearby unstimulated synapses. This heterosynaptic plasticity requires potentiation of multiple neighboring spines, suggesting that a local threshold of neural activity exists beyond which inactive synapses are punished. Notably, inhibition of calcineurin, IP3Rs, or group I metabotropic glutamate receptors (mGluRs) blocked heterosynaptic shrinkage without blocking structural potentiation, and inhibition of Ca2+/calmodulin-dependent protein kinase II (CaMKII) blocked structural potentiation without blocking heterosynaptic shrinkage. Our results support a model in which activity-induced shrinkage signal, and not competition for limited structural resources, drives heterosynaptic structural and functional depression during neural circuit refinement.http://www.sciencedirect.com/science/article/pii/S2211124714010456
spellingShingle Won Chan Oh
Laxmi Kumar Parajuli
Karen Zito
Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
Cell Reports
title Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
title_full Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
title_fullStr Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
title_full_unstemmed Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
title_short Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
title_sort heterosynaptic structural plasticity on local dendritic segments of hippocampal ca1 neurons
url http://www.sciencedirect.com/science/article/pii/S2211124714010456
work_keys_str_mv AT wonchanoh heterosynapticstructuralplasticityonlocaldendriticsegmentsofhippocampalca1neurons
AT laxmikumarparajuli heterosynapticstructuralplasticityonlocaldendriticsegmentsofhippocampalca1neurons
AT karenzito heterosynapticstructuralplasticityonlocaldendriticsegmentsofhippocampalca1neurons