Perineuronal nets affect memory and learning after synapse withdrawal

Abstract Perineuronal nets (PNNs) enwrap mature neurons, playing a role in the control of plasticity and synapse dynamics. PNNs have been shown to have effects on memory formation, retention and extinction in a variety of animal models. It has been proposed that the cavities in PNNs, which contain s...

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Main Authors: Jiri Ruzicka, Marketa Dalecka, Kristyna Safrankova, Diego Peretti, Pavla Jendelova, Jessica C. F. Kwok, James W. Fawcett
Format: Article
Language:English
Published: Nature Publishing Group 2022-11-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-022-02226-z
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author Jiri Ruzicka
Marketa Dalecka
Kristyna Safrankova
Diego Peretti
Pavla Jendelova
Jessica C. F. Kwok
James W. Fawcett
author_facet Jiri Ruzicka
Marketa Dalecka
Kristyna Safrankova
Diego Peretti
Pavla Jendelova
Jessica C. F. Kwok
James W. Fawcett
author_sort Jiri Ruzicka
collection DOAJ
description Abstract Perineuronal nets (PNNs) enwrap mature neurons, playing a role in the control of plasticity and synapse dynamics. PNNs have been shown to have effects on memory formation, retention and extinction in a variety of animal models. It has been proposed that the cavities in PNNs, which contain synapses, can act as a memory store and that they remain stable after events that cause synaptic withdrawal such as anoxia or hibernation. We examine this idea by monitoring place memory before and after synaptic withdrawal caused by acute hibernation-like state (HLS). Animals lacking hippocampal PNNs due to enzymatic digestion by chondroitinase ABC or knockout of the PNN component aggrecan were compared with wild type controls. HLS-induced synapse withdrawal caused a memory deficit, but not to the level of untreated naïve animals and not worsened by PNN attenuation. After HLS, only animals lacking PNNs showed memory restoration or relearning. Absence of PNNs affected the restoration of excitatory synapses on PNN-bearing neurons. The results support a role for hippocampal PNNs in learning, but not in long-term memory storage for correction of deficits.
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spelling doaj.art-50eda852b9e34524b993f97aead303462022-12-22T03:42:12ZengNature Publishing GroupTranslational Psychiatry2158-31882022-11-0112111310.1038/s41398-022-02226-zPerineuronal nets affect memory and learning after synapse withdrawalJiri Ruzicka0Marketa Dalecka1Kristyna Safrankova2Diego Peretti3Pavla Jendelova4Jessica C. F. Kwok5James W. Fawcett6Institute of Experimental Medicine, CASImaging Methods Core Facility, BIOCEV, CASInstitute of Experimental Medicine, CASUK Dementia Research Institute and Department of Clinical Neurosciences, University of CambridgeInstitute of Experimental Medicine, CASInstitute of Experimental Medicine, CASInstitute of Experimental Medicine, CASAbstract Perineuronal nets (PNNs) enwrap mature neurons, playing a role in the control of plasticity and synapse dynamics. PNNs have been shown to have effects on memory formation, retention and extinction in a variety of animal models. It has been proposed that the cavities in PNNs, which contain synapses, can act as a memory store and that they remain stable after events that cause synaptic withdrawal such as anoxia or hibernation. We examine this idea by monitoring place memory before and after synaptic withdrawal caused by acute hibernation-like state (HLS). Animals lacking hippocampal PNNs due to enzymatic digestion by chondroitinase ABC or knockout of the PNN component aggrecan were compared with wild type controls. HLS-induced synapse withdrawal caused a memory deficit, but not to the level of untreated naïve animals and not worsened by PNN attenuation. After HLS, only animals lacking PNNs showed memory restoration or relearning. Absence of PNNs affected the restoration of excitatory synapses on PNN-bearing neurons. The results support a role for hippocampal PNNs in learning, but not in long-term memory storage for correction of deficits.https://doi.org/10.1038/s41398-022-02226-z
spellingShingle Jiri Ruzicka
Marketa Dalecka
Kristyna Safrankova
Diego Peretti
Pavla Jendelova
Jessica C. F. Kwok
James W. Fawcett
Perineuronal nets affect memory and learning after synapse withdrawal
Translational Psychiatry
title Perineuronal nets affect memory and learning after synapse withdrawal
title_full Perineuronal nets affect memory and learning after synapse withdrawal
title_fullStr Perineuronal nets affect memory and learning after synapse withdrawal
title_full_unstemmed Perineuronal nets affect memory and learning after synapse withdrawal
title_short Perineuronal nets affect memory and learning after synapse withdrawal
title_sort perineuronal nets affect memory and learning after synapse withdrawal
url https://doi.org/10.1038/s41398-022-02226-z
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