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Cited by 29Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurogenesis and neuroplasticity mechanisms

Perineuronal Nets Restrict the Induction of Long-Term Depression in the Mouse Hippocampal CA1 Region

Khoo, Guan Hock, Lin, Yu-Ting, Tsai, Tsung-Chih, Hsu, Kuei-Sen·2019·Molecular Neurobiology
DOI 10.1007/s12035-019-1526-1
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Abstract

Long-term depression (LTD) of synaptic efficacy is widely regarded as a cellular basis of learning and memory. The magnitude of hippocampal CA1 LTD induced by low-frequency stimulation (LFS) declines with age, but the mechanisms involved remain poorly understood. Perineuronal nets (PNNs) are specialized extracellular matrix structures that function in dampening synaptic plasticity during postnatal development, suggesting that PNN formation may restrict LTD induction in the adult hippocampus. Here, we show that PNNs tightly enwrap a subpopulation of parvalbumin (PV) interneurons in the hippocampal CA1 region and enzymatic removal of PNNs with the chondroitinase ABC alters the excitatory/inhibitory synaptic balance toward more excitation and restores the ability of LFS to induce an N-methyl-D-aspartate receptor-dependent LTD at Schaffer collateral-CA1 synapses in slices from male adult mice. Early interference with depolarizing GABA with Na + -K + -2Cl - cotransporter inhibitor bumetanide impairs the maturation of PNNs and enhances LTD induction. These results provide novel insights into a previously unrecognized role for PNNs around PV interneurons in restricting long-term synaptic plasticity at excitatory synapses on hippocampal CA1 neurons in adulthood.

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  • Long-term depression (LTD) is altered after PNN degradation, with both increases and decreases reported.

    “Long-term depression (LTD) is also altered after PNN degradation, with both increases [67] and decreases [53, 60] reported.”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [67]

  • Genetic or enzymatic attenuation of PNNs can increase synaptic transmission and facilitate long-term depression (LTD) in the perirhinal cortex or CA1 region, and this correlates with enhanced recognition memory.

    “Genetic or enzymatic attenuation of PNNs can increase synaptic transmission and facilitate long-term depression (LTD) in the perirhinal cortex [53] or CA1 region [67], and this correlates with enhanced recognition memory.”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [67]

  • Both forms of LTD were hardly induced at adult as reported.

    “Whereas both forms of LTD were hardly induced at adult as reported 40, they are similarly induced in WT and KO hippocampus at young postnatal age, suggesting that LTD is intact in KO mice (Supplementary Figure 9).”

    From Autism-like social deficit generated by Dock4 deficiency is rescued by restoration of Rac1 activity and NMDA receptor function. (2021) · cites this paper as [40]

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Authors
Khoo, G. H., Lin, Y.-T., Tsai, T.-C., & Hsu, K.-S.
Affiliations
National Cheng Kung University (TW)
Corresponding author
Hsu, Kuei-Sen
ORCID
Venue
Molecular Neurobiology
Publisher
Springer Science and Business Media LLC
Published
2019-03-02
Volume
56
Issue
9
Pages
6436-6450
ISSN
  • 0893-7648 (ISSN-L)
  • 1559-1182
DOI
10.1007/s12035-019-1526-1
OpenAlex
W2920793266
Cited by
29
References
11
Citations by year
2026: 2 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 4 · 2019: 2 · 2017: 1
FWCI
1.67
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Molecular Neurobiology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Health Research Institute, Taiwan (NHRI-EX107-10613NI)
  • Ministry of Science and Technology, Taiwan (106-2320-B-006-026-MY3, 107-2320-B-006-037-MY3)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
perineuronal nets, long-term depression, hippocampal CA1, parvalbumin interneurons, chondroitinase ABC, NMDA receptor, Schaffer collateral synapses, excitation-inhibition balance, synaptic plasticity, bumetanide, Na+-K+-2Cl- cotransporter, extracellular matrix, aging, learning and memory
MeSH terms
Animals, Bumetanide, Electric Stimulation, Male, Mice, Inbred C57BL, Neurons, Parvalbumins, Receptors, GABA-A, Synapses, Pyramidal Cells, Long-Term Synaptic Depression, CA1 Region, Hippocampal

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