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Cited by 118Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMemory Processes and Influences

Removal of perineuronal nets disrupts recall of a remote fear memory

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Thompson, Elise Holter, Lensjø, Kristian Kinden, Wigestrand, Mattis Brænne, Malthe-Sørenssen, Anders, Hafting, Torkel, Fyhn, Marianne·2018·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1713530115PMC PMC5776974
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Abstract

Significance: Perineuronal nets (PNNs), a type of extracellular matrix only found in the central nervous system, wraps tightly around the cell soma and proximal dendrites of a subset of neurons. The PNNs are long-lasting structures that restrict plasticity, making them eligible candidates for memory processing. This work demonstrates that PNNs in the lateral secondary visual cortex (V2L) are essential for the recall of a remote visual fear memory. The results suggest a role of extracellular molecules in storage and retrieval of memories.

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Crossref · 10.1073/pnas.1713530115

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  • Coherence (phase alignment) between theta oscillations in the secondary visual cortex (V2) and the BLA is necessary for successful recall of remote fear memories.

    “For instance, coherence (phase alignment) between theta oscillations in the secondary visual cortex (V2) and the BLA is necessary for successful recall of remote fear memories [93, 94].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [94]

    The Results (Fig. 2C) report increased V2L–BLA theta coherence during successful remote fear-memory recall in controls, but not in chABC-treated animals whose recall was disrupted. The Discussion says PNN degradation may impair memory reactivation, long-range synchronization, or both. These findings link coherence with successful recall but do not establish that coherence itself is necessary. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Attenuation of PNNs in V2 weeks after training reduces theta coherency between BLA and V2 and prevents recall of a remote fear memory.

    “Attenuation of PNNs in V2 weeks after training reduces theta coherency between BLA and V2 and prevents recall of a remote fear memory [94].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [94]

  • Newly formed memory traces can interfere with the fidelity and recall of previously learned information, as evident by impaired reconsolidation and recall of remote memories following perineuronal net ablation.

    “newly formed memory traces can interfere with the fidelity and recall of previously learned information [20], as evident by impaired reconsolidation and recall of remote memories following PNN ablation [25, 26].”

    From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [26]

  • Enzymatic degradation of auditory cortex PNNs with chondroitinase ABC disrupts consolidation of auditory fear learning, which is restored upon PNN recovery, whereas PNN digestion in the amygdala or visual cortex disrupts recall of contextual fear memories and remote visual fear memories, respectively.

    “Of further relevance to AD, the enzymatic degradation of auditory cortex PNNs with chondroitinase ABC (chABC) disrupts consolidation of auditory fear learning [84], which is restored upon PNN recovery, whereas PNN digestion in the amygdala or visual cortex disrupts the recall of contextual fear memories [85] and remote visual fear memories [26], respectively.”

    From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [26]

  • Enhanced plasticity and learning can impair storage and recall of remote memories due to interference from new memory traces, and so enhancement of these factors following PNN loss would still be consistent with impaired reconsolidation and recall of remote, long-term memories.

    “On the other hand, enhanced plasticity and learning can impair the storage and recall of remote memories due to interference from new memory traces [20], and so the enhancement of these factors following PNN loss would still be consistent with the consequently impaired reconsolidation and recall of remote, long-term memories reported by others [25, 26].”

    From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [26]

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Authors
Thompson, E. H., Lensjø, K. K., Wigestrand, M. B., Malthe-Sørenssen, A., Hafting, T., & Fyhn, M.
Affiliations
  • University of Oslo (NO)
  • Center for Integrative Neuroplasticity, University of Oslo, 0316 Oslo, Norway;
Corresponding author
Fyhn, Marianne
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2017-12-26
Volume
115
Issue
3
Pages
607-612
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1713530115
PMC
PMC5776974
OpenAlex
W2777153816
Cited by
118
References
40
Citations by year
2026: 8 · 2025: 17 · 2024: 17 · 2023: 11 · 2022: 14 · 2021: 16 · 2020: 17 · 2019: 16 · 2018: 2
FWCI
5.49
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc-nd)
Funders
Research council of Norway (143730, 549217, 231248)
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
perineuronal nets, fear memory, memory engrams, extracellular matrix, secondary visual cortex, basolateral amygdala, theta oscillations, memory stabilization
MeSH terms
Animals, Behavior, Animal, Fear, Male, Memory, Neuronal Plasticity, Mental Recall, Visual Cortex, Rats, Sprague-Dawley, Rats

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