Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations
Abstract
Perineuronal nets (PNs) are known as chondroitin sulphate-rich, lattice-like coatings of the extracellular matrix. In the cortex of mammalian species investigated so far, they were mainly found around GABAergic neurons, but to a lesser degree also around pyramidal cells. Previous investigations in the rat revealed similar distribution patterns of fast-firing neurons expressing both the Kv3.1b subunit of voltage-gated potassium channels and the calcium-binding protein parvalbumin. In the present study, triple fluorescence labelling was applied for the simultaneous demonstration of PNs with the N-acetylgalactosamine-specific Wisteria floribunda agglutinin (WFA), parvalbumin-immunoreactivity (ir) with a monoclonal antibody and of Kv3.1b-ir with several rabbit antibodies. Subsets of non-pyramidal neurons - enwrapped by PNs and expressing parvalbumin and Kv3.1b - were detected in the rat and monkey neocortex and hippocampus. In the rat, faintly stained PNs were additionally found around several layer II/III and V pyramidal cells immunonegative for Kv3.1b, but contacted by Kv3.1b-containing boutons. In the monkey, more intensely labelled PNs frequently occurred around pyramidal cells which themselves appeared to be Kv3. 1b-immunopositive. We also observed minor Kv3.1b-ir and parvalbumin-ir cortical cell populations which were devoid of PNs; occasionally, nets were detected around neurons lacking both immunoreactivities. By confocal laser scanning microscopy, Kv3.1b-ir and WFA-binding sites were found adjoining at the soma and proximal dendritic surface, while lectin-binding sites usually extended on more distal dendritic segments and the axon initial segments which failed to express detectable Kv3.1b-ir. This spatial relationship of both markers was also confirmed by combined WFA-gold labelling and Kv3.1b-immunoperoxidase staining at the electron microscopic level. The data are used for a critical examination of current hypotheses concerning the functional role of PNs. We conclude that PNs may serve as rapid local buffers of excess cation changes in the extracellular space. Somatic membranes of fast-spiking neurons seem to be a main, but not the only source of such changes.
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PNNs may restrict local ionic concentration due to a high density of negatively charged glycosaminoglycans, thereby regulating the microenvironment of FSNs and influencing their intrinsic properties.
“PNNs may also restrict local ionic concentration due to a high density of their negatively charged constituent glycosaminoglycans (GAGs)18, thereby regulating the microenvironment of FSNs and influencing their intrinsic properties19.”
From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [19]
PNs frequently surround neurons containing parvalbumin, which are fast-firing GABAergic neurons co-expressing the voltage-gated potassium channel Kv3.1b.
“PNs frequently surround neurons containing parvalbumin (Kosaka and Heizmann, 1989; Härtig et al., 1992), known as a marker for fast-firing GABAergic neurons co-expressing the voltage-gated potassium channel Kv3.1b (Härtig et al., 1999).”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Härtig et al., 1999
Evidence links PNNs to ion homeostasis near neurons with high activity.
“PNNs have been implicated in ion homeostasis around highly active neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Hartig et al., 1999
PNNs can potentially act as a buffering system for calcium, potassium, and sodium around highly active neurons, although direct evidence is lacking.
“They can thus potentially act as a buffering system for physiologically relevant ions such as calcium, potassium, and sodium around highly active types of neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Hartig et al., 1999
PNNs are most commonly associated with fast-spiking parvalbumin interneurons.
“they are most commonly associated with the highly metabolically active fast-spiking parvalbumin interneurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Hartig et al., 1999
The dense perineuronal net characteristic of PV interneurons is required to stabilise NPTX2 in the synaptic cleft at these synapses.
“The dense perineuronal net (proteoglycan network structure on the cell surface), characteristic of PV interneurons (Carceller et al. 2020; Härtig et al. 1999), is required to stabilise NPTX2 in the synaptic cleft at these synapses (Chang et al. 2010).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Härtig et al. 1999
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- Authors
- Härtig, W., Derouiche, A., Welt, K., Brauer, K., Grosche, J., Mäder, M., Reichenbach, A., & Brückner, G.
- Affiliations
- Leipzig University (DE)
- Max Planck Institute for Brain Research (DE)
- University of Göttingen (DE)
- Corresponding author
- Härtig, Wolfgang
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1999-09
- Volume
- 842
- Issue
- 1
- Pages
- 15-29
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2032124585
- Cited by
- 339
- References
- 10
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 13 · 2023: 15 · 2022: 19 · 2021: 24 · 2020: 19 · 2019: 14 · 2018: 22 · 2017: 15 · 2016: 17 · 2015: 15 · 2014: 15 · 2013: 13 · 2012: 12
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- perineuronal nets, voltage-gated potassium channels, parvalbumin, fast-spiking neurons, extracellular matrix, chondroitin sulfate, pyramidal neurons, non-pyramidal neurons, neocortex, hippocampus, dendritic localization, lectin binding, Wisteria floribunda agglutinin
- MeSH terms
- Animals, Axons, Cations, Cerebral Cortex, Fluorescent Dyes, Immunoenzyme Techniques, Immunohistochemistry, Macaca mulatta, Microscopy, Electron, Nerve Net, Nerve Tissue Proteins, Neurons, Oligodendroglia, Parvalbumins, Potassium Channels, Potassium Channels, Voltage-Gated, Rats, Shaw Potassium Channels
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