Very long-term memories may be stored in the pattern of holes in the perineuronal net
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A hypothesis and the experiments to test it propose that very long-term memories, such as fear conditioning, are stored as the pattern of holes in the perineuronal net (PNN), a specialized ECM that envelops mature neurons and restricts synapse formation. The 3D intertwining of PNN and synapses would be imaged by serial-section EM. Lifetimes of PNN vs. intrasynaptic components would be compared with pulse-chase 15 N labeling in mice and 14 C content in human cadaver brains. Genetically encoded indicators and antineoepitope antibodies should improve spatial and temporal resolution of the in vivo activity of proteases that locally erode PNN. Further techniques suggested include genetic KOs, better pharmacological inhibitors, and a genetically encoded snapshot reporter, which will capture the pattern of activity throughout a large ensemble of neurons at a time precisely defined by the triggering illumination, drive expression of effector genes to mark those cells, and allow selective excitation, inhibition, or ablation to test their functional importance. The snapshot reporter should enable more precise inhibition or potentiation of PNN erosion to compare with behavioral consequences. Finally, biosynthesis of PNN components and proteases would be imaged.
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PNNs have been proposed as the molecular substrate underpinning long-term memory storage, by serving as a scaffold that retains synapse position and strength.
“In light of such data, PNNs have been proposed as the molecular substrate underpinning long-term memory storage, by serving as a scaffold that retains synapse position and strength [86].”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [86]
PNNs are stable structures known to lock synapses in place upon closure of the developmental window of plasticity, and several CNS pathologies present with upregulated ECM and PNN remodeling enzymes including MMPs.
“Although PNNs are stable structures and known to lock synapses in place upon closure of the developmental window of plasticity17,38,39, several CNS pathologies40, including glioma and epilepsy, present with upregulated ECM and PNN remodeling enzymes including MMPs.”
From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [17]
Recent reports have demonstrated the importance of proteases in neuronal plasticity by reshaping the PNN.
“Recent reports have demonstrated the importance of proteases in neuronal plasticity by reshaping the PNN.3, 4, 5, 6”
From Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin (2015) · cites this paper as [6]
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- Authors
- Tsien, R. Y.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Tsien, Roger Y.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-07-05
- Volume
- 110
- Issue
- 30
- Pages
- 12456-12461
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3725115
- OpenAlex
- W2164667485
- Cited by
- 244
- References
- 80
- Citations by year
- 2026: 12 · 2025: 15 · 2024: 20 · 2023: 21 · 2022: 16 · 2021: 20 · 2020: 20 · 2019: 22 · 2018: 21 · 2017: 26 · 2016: 21 · 2015: 16 · 2014: 9 · 2013: 5
- FWCI
- 9.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (NS27177)
- National Institute of Neurological Disorders and Stroke (NS27177, R37NS027177, R01NS027177)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- perineuronal nets, long-term memory storage, fear conditioning, extracellular matrix, synaptogenesis, genetically encoded indicators, pulse-chase labeling, 15N labeling, carbon-14 labeling, memory reconsolidation
- MeSH terms
- Animals, Behavior, Animal, Humans, Memory, Nerve Net, Neurons, Synapses, Mice, Knockout, Matrix Metalloproteinase 2, Matrix Metalloproteinase 9, Mice
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