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Cited by 143Neuroscience and Neuropharmacology ResearchEpilepsy research and treatmentNeurogenesis and neuroplasticity mechanisms

The perineuronal net component of the extracellular matrix in plasticity and epilepsy

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McRae, Paulette A., Porter, Brenda E.·2012·Neurochemistry International
DOI 10.1016/j.neuint.2012.08.007PMC PMC3930202
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Abstract

During development the extracellular matrix (ECM) of the central nervous system (CNS) facilitates proliferation, migration, and synaptogenesis. In the mature nervous system due to changes in the ECM it provides structural stability and impedes proliferation, migration, and synaptogensis. The perineuronal net (PN) is a specialized ECM structure found primarily surrounding inhibitory interneurons where it forms a mesh-like structure around points of synaptic contact. The PN organizes the extracellular space by binding multiple components of the ECM and bringing them into close proximity to the cell membrane, forming dense aggregates surrounding synapses. The PN is expressed late in postnatal development when the nervous system is in the final stages of maturation and the critical periods are closing. Once fully expressed the PN envelopes synapses and leads to decreased plasticity and increases synaptic stability in the CNS. Disruptions in the PN have been studied in a number of disease states including epilepsy. Epilepsy is one of the most common neurologic disorders characterized by excessive neuronal activity which results in recurrent spontaneous seizures. A shift in the delicate balance between excitation and inhibition is believed to be one of the underlying mechanisms in the development of epilepsy. During epileptogenesis, the brain undergoes numerous changes including synaptic rearrangement and axonal sprouting, which require structural plasticity. Because of the PNs location around inhibitory cells and its role in limiting plasticity, the PN is an important candidate for altering the progression of epilepsy. In this review, an overview of the ECM and PN in the CNS will be presented with special emphasis on potential roles in epileptogenesis.

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Crossref · 10.1016/j.neuint.2012.08.007

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  • PNNs play key roles in neural development, synaptogenesis, neuroprotection, and experience-dependent synaptic plasticity.

    “As such, PNNs play key roles in neural development, synaptogenesis, neuroprotection, and experience-dependent synaptic plasticity (Celio et al., 1998;Dityatev and Schachner, 2003;McRae and Porter, 2012;Soleman et al., 2013;Suttkus et al., 2016).”

    From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as McRae and Porter, 2012

    The Introduction and §3 describe PNN formation during development and activity-dependent expression, while §4 links PNNs to synapse stabilization and reduced plasticity. But §4.1 says PNNs are unlikely to participate in early synaptogenesis, and the passages found do not establish a neuroprotective role. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • PNN degradation may also alter synaptic activity and hence network excitability.

    “However, it is important to recognize that in addition to changes in the excitability of inhibitory neurons as suggested here and by others55, PNN degradation may also alter synaptic activity56 and hence network excitability.”

    From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [56]

  • Perineuronal nets help close critical periods, modulate synaptic plasticity, and respond to oxidative stress.

    “involved in the closure of developmental critical periods, regulation of synaptic plasticity, and are altered by oxidative stress (Cabungcal et al, 2013b;McRae and Porter, 2012)”

    From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as McRae and Porter, 2012

  • Increased parvalbumin and Wisteria floribunda agglutinin labeling during closure of critical periods in sensory cortices is likely driven by increased excitatory input.

    “For example, increased PV and WFA labeling during the closure of critical periods in sensory cortices is likely driven by increased excitatory input (McRae and Porter, 2012).”

    From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as McRae and Porter, 2012

  • PNN and PNN-component changes have been tied to several brain disorders, including stroke, epilepsy, multiple sclerosis, prion disease, and Alzheimer's disease.

    “a number of studies have shown alterations in PNNs and their constituents to be linked to various brain diseases, such as Alzheimer’s disease (Morawski et al., 2010, 2012; Kobayashi et al., 1989; Baig et al., 2005), epilepsy (McRae and Porter, 2012), multiple sclerosis (Gray et al., 2008), prion disease (Guentchev et al., 1999, Franklin et al., 2008) and stroke”

    From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as McRae and Porter, 2012

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2 of the 148 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Meyer-Puttlitz B Junker E Margolis RU Margolis RK Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan J Comp Neurol 1996 366 1 44 54 8866845

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Authors
McRae, P. A., & Porter, B. E.
Affiliations
Children's Hospital of Philadelphia (US)
Corresponding author
McRae, Paulette A.
ORCID
Porter, Brenda E.
Venue
Neurochemistry International
Publisher
Elsevier BV
Published
2012-12
Volume
61
Issue
7
Pages
963-972
ISSN
0197-0186 (ISSN-L)
DOI
10.1016/j.neuint.2012.08.007
PMC
PMC3930202
OpenAlex
W2004229492
Cited by
143
References
148
Citations by year
2026: 7 · 2025: 7 · 2024: 11 · 2023: 15 · 2022: 9 · 2021: 15 · 2020: 12 · 2019: 7 · 2018: 16 · 2017: 12 · 2016: 13 · 2015: 6 · 2014: 11 · 2013: 2
FWCI
0.64
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neurochemistry International (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Neurological Disorders and Stroke (R01NS056222)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
perineuronal nets, extracellular matrix, synaptic plasticity, epilepsy, epileptogenesis, inhibitory interneurons, synaptic stability, excitation-inhibition balance, axonal sprouting, synaptogenesis, central nervous system development
MeSH terms
Epilepsy, Extracellular Matrix, Humans, Nerve Net, Neuronal Plasticity

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