Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons
Open accessAbstract
Perineuronal nets (PNNs) are specialized complexes of extracellular matrix molecules that surround the somata of fast-spiking neurons throughout the vertebrate brain. PNNs are particularly prevalent throughout the auditory brainstem, which transmits signals with high speed and precision. It is unknown whether PNNs contribute to the fast-spiking ability of the neurons they surround. Whole-cell recordings were made from medial nucleus of the trapezoid body (MNTB) principal neurons in acute brain slices from postnatal day 21 (P21) to P27 mice. PNNs were degraded by incubating slices in chondroitinase ABC (ChABC) and were compared to slices that were treated with a control enzyme (penicillinase). ChABC treatment did not affect the ability of MNTB neurons to fire at up to 1000 Hz when driven by current pulses. However, f – I (frequency–intensity) curves constructed by injecting Gaussian white noise currents superimposed on DC current steps showed that ChABC treatment reduced the gain of spike output. An increase in spike threshold may have contributed to this effect, which is consistent with the observation that spikes in ChABC-treated cells were delayed relative to control-treated cells. In addition, parvalbumin-expressing fast-spiking cortical neurons in >P70 slices that were treated with ChABC also had reduced excitability and gain. The development of PNNs around somata of fast-spiking neurons may be essential for fast and precise sensory transmission and synaptic inhibition in the brain.
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Microglia-mediated loss of PNNs likely plays an important role in AD pathogenesis.
“As PNNs are implicated in neuronal health and function, protecting cells against neurotoxins such as Aβ1–42 [39] and oxidative stress [65] in addition to modulating neuronal activity [63, 66], the microglia-mediated loss of these structures in disease likely plays an important role in AD pathogenesis.”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [63]
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 [55]
The role of PNNs in neural and network excitability is only beginning to be understood.
“However, the role of PNNs in neural and network excitability is only beginning to be understood (Balmer, 2016; Murase et al., 2017; Wen et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
Perineuronal net dysfunction in schizophrenia may drive changes in GABAergic cell function leading to network dysfunction, as normal PNN expression regulates excitability of PV cells.
“Perineuronal net dysfunction in schizophrenia may also drive changes in GABAergic cell function leading to network dysfunction, as normal PNN expression regulates excitability of PV cells (Liu et al., 2013; Balmer, 2016).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
chABC-mediated removal of chondroitin sulfate side chains from PNNs reduced spiking of PV cells in adult rats and increased spiking variability.
“While this mechanism has not been confirmed, chABC-mediated removal of chondroitin sulfate side chains from PNNs reduced spiking of PV cells in adult rats (Balmer, 2016; Lensjø et al., 2017) and increased spiking variability (Lensjø et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
As PNNs regulate PV cell activity and protect PV cells from oxidative stress, PNNs can be potentially targeted to control seizures.
“As PNNs regulate PV cell activity (Balmer, 2016; Lensjø et al., 2017) and protect PV cells from oxidative stress (Cabungcal et al., 2013), PNNs can be potentially targeted to control seizures.”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
chABC-mediated degradation of PNNs around PV cells in brainstem and central auditory neurons results in reduced PV cell excitability and gain.
“chABC-mediated degradation of PNNs around PV cells in brainstem and central auditory neurons has similar effects, resulting in reduced PV cell excitability and gain (Balmer, 2016).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
Chondroitinase ABC, which cleaves perineuronal net proteoglycans, reduces GABA A inhibitory postsynaptic currents and reduces the excitability of parvalbumin fast-spiking cortical interneurons.
“Chondroitinase ABC, an enzyme that cleaves PNN proteoglycans, reduces GABA A inhibitory postsynaptic currents (Liu et al. 2013) and reduces excitability of PV fast-spiking cortical interneurons (Balmer 2016).”
Digestion of PNNs around PV+ cells reduces the fast spiking properties and excitability of PV+ cells.
“Our findings reporting increased intensities of WFA labelled PNNs around PV+ interneurons suggest altered plasticity of PV+ cells as PNNs have been known to regulate synaptic and cellular plasticity of the cells they encapsulate (45) and digestion of PNNs around PV+ cells has been shown to reduce the fast spiking properties and excitability of PV+ cells (73)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [73]
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- Authors
- Balmer, T. S.
- Affiliations
- Marine Biological Laboratory (US)
- Corresponding author
- Balmer, Timothy S.
- ORCID
- Balmer, Timothy S.
- Venue
- eneuro
- Publisher
- Society for Neuroscience
- Published
- 2016-07
- Volume
- 3
- Issue
- 4
- Pages
- ENEURO.0112-16.2016
- ISSN
- 2373-2822 (ISSN-L)
- PMC
- PMC4987413
- OpenAlex
- W2467652827
- Cited by
- 220
- References
- 63
- Citations by year
- 2026: 13 · 2025: 26 · 2024: 24 · 2023: 18 · 2022: 19 · 2021: 22 · 2020: 28 · 2019: 24 · 2018: 28 · 2017: 18
- FWCI
- 13.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eNeuro (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion, cc-by)
- Funders
- Grass Foundation
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- perineuronal nets, fast-spiking neurons, neuronal excitability, medial nucleus of the trapezoid body, auditory brainstem, chondroitinase ABC, extracellular matrix, parvalbumin interneurons, spike threshold, synaptic inhibition, sensory transmission
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Central Nervous System Agents, Extracellular Matrix, Female, Immunohistochemistry, Male, Mice, Inbred C57BL, Microscopy, Fluorescence, Neurons, Penicillinase, Patch-Clamp Techniques, Chondroitin ABC Lyase, Tissue Culture Techniques, Superior Olivary Complex
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