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Protein phosphatase 1 is a molecular constraint on learning and memory

Genoux, David, Haditsch, Ursula, Knobloch, Marlen, Michalon, Aubin, Storm, Daniel, Mansuy, Isabelle M.·2002·Nature

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Abstract

Repetition in learning is a prerequisite for the formation of accurate and long-lasting memory. Practice is most effective when widely distributed over time, rather than when closely spaced or massed. But even after efficient learning, most memories dissipate with time unless frequently used. The molecular mechanisms of these time-dependent constraints on learning and memory are unknown. Here we show that protein phosphatase 1 (PP1) determines the efficacy of learning and memory by limiting acquisition and favouring memory decline. When PP1 is genetically inhibited during learning, short intervals between training episodes are sufficient for optimal performance. The enhanced learning correlates with increased phosphorylation of cyclic AMP-dependent response element binding (CREB) protein, of Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) and of the GluR1 subunit of the AMPA receptor; it also correlates with CREB-dependent gene expression that, in control mice, occurs only with widely distributed training. Inhibition of PP1 prolongs memory when induced after learning, suggesting that PP1 also promotes forgetting. This property may account for ageing-related cognitive decay, as old mutant animals had preserved memory. Our findings emphasize the physiological importance of PP1 as a suppressor of learning and memory, and as a potential mediator of cognitive decline during ageing.

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Self-citation

Authors: Genoux, D., Haditsch, U., Knobloch, M., Michalon, A., Storm, D., & Mansuy, I. M.
Affiliations: ETH Zurich (CH)
University of Washington (US)
Corresponding author: Mansuy, Isabelle M.
ORCID: Haditsch, Ursula
Knobloch, Marlen
Michalon, Aubin
Storm, Daniel
Mansuy, Isabelle M.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2002-08
Volume: 418
Issue: 6901
Pages: 970-975
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature00928
OpenAlex: W1992020799
Cited by: 472
References: 30
Citations by year: 2026: 4 · 2025: 9 · 2024: 18 · 2023: 7 · 2022: 16 · 2021: 17 · 2020: 15 · 2019: 16 · 2018: 15 · 2017: 10 · 2016: 22 · 2015: 21 · 2014: 24 · 2013: 26 · 2012: 21
FWCI: 15.36
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: protein phosphatase 1, learning and memory, forgetting, memory consolidation, CREB phosphorylation, CaMKII, GluR1, AMPA receptors, cognitive decline, protein dephosphorylation
MeSH terms: Aging, Animals, Cognition, Discrimination, Psychological, Gene Expression Regulation, Hippocampus, Learning, Memory, Mice, Transgenic, Mutation, Phosphoprotein Phosphatases, Phosphorylation, Space Perception, Time Factors, Cyclic AMP Response Element-Binding Protein, Calcium-Calmodulin-Dependent Protein Kinases, Receptors, AMPA, Protein Subunits, Mice, Protein Phosphatase 1, Calcium-Calmodulin-Dependent Protein Kinase Type 2

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Protein phosphatase 1 is a molecular constraint on learning and memory

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