Perineuronal Nets and Their Role in Synaptic Homeostasis

Bosiacki, Mateusz; Gąssowska-Dobrowolska, Magdalena; Kojder, Klaudyna; Fabiańska, Marta; Jeżewski, Dariusz; Gutowska, Izabela; Lubkowska, Anna

doi:10.3390/ijms20174108

Cited by 72 publications

(60 citation statements)

References 125 publications

(173 reference statements)

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“…PNs can regulate and promote functional synaptic plasticity (Bukalo et al, 2001;Balmer et al, 2009;de Vivo et al, 2013;Blosa et al, 2015;Bosiacki et al, 2019). Interestingly, a recent study has shown that PN expression in the medial subdivisions of the auditory thalamus may be responsible for precise neural firing in the aging brain (Quraishe et al, 2019).…”

Section: Potential Functional Roles Of Pns In Age-related Hearing Lossmentioning

confidence: 99%

“…PNs can surround a variety of types of neurons throughout the brain although most reports focus on their relationship to GABAergic cells (Kosaka and Heizmann, 1989;Härtig et al, 1992;Sonntag et al, 2015). PNs and their primary molecular component, chondroitin sulfate proteoglycans (CSPGs), are critical for numerous functions including ion buffering, stabilizing high-rate synaptic transmission, modulating cellular integrity, neuroprotection, mechanical stabilization of synaptic contacts, and inhibition of structural plasticity (see reviews Sonntag et al, 2015;Bosiacki et al, 2019;Testa et al, 2019). Of these functions the inhibition of plasticity has garnered the most attention as the enzymatic disruption of PNs can restore juvenile-like plasticity in the adult cortex (Pizzorusso et al, 2002(Pizzorusso et al, , 2006Gogolla et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…Of these functions the inhibition of plasticity has garnered the most attention as the enzymatic disruption of PNs can restore juvenile-like plasticity in the adult cortex (Pizzorusso et al, 2002(Pizzorusso et al, , 2006Gogolla et al, 2009). This apparent role for PNs in the diminished neural plasticity that characterizes the aging brain, along with an increasing aging population, has generated strong interest in the role of PNs in the cortex during neurodegenerative diseases and aging (see reviews Burke and Barnes, 2006;Karetko and Skangiel-Kramska, 2009;Bosiacki et al, 2019;Duncan et al, 2019;Testa et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

Mafi

Hofer

Russ

et al. 2020

Front. Aging Neurosci.

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Age-related hearing loss, one of the most frequently diagnosed disabilities in industrialized countries, may result from declining levels of GABA in the aging inferior colliculus (IC). However, the mechanisms of aging and subsequent disruptions of temporal processing in elderly hearing abilities are still being investigated. Perineuronal nets (PNs) are a specialized form of the extracellular matrix and have been linked to GABAergic neurotransmission and to the regulation of structural and synaptic plasticity. We sought to determine whether the density of PNs in the IC changes with age. We combined Wisteria floribunda agglutinin (WFA) staining with immunohistochemistry to glutamic acid decarboxylase in three age groups of Fischer Brown Norway (FBN) rats. The density of PNs on GABAergic and non-GABAergic cells in the three major subdivisions of the IC was quantified. Results first demonstrate that the density of PNs in the FBN IC increase with age. The greatest increases of PN density from young to old age occurred in the central IC (67% increase) and dorsal IC (117% increase). Second, in the young IC, PNs surround non-GABAergic and GABAergic cells with the majority of PNs surrounding the former. The increase of PNs with age in the IC occurred on both non-GABAergic and GABAergic populations. The average density of PN-surrounded non-GABAergic cells increased from 84.9 PNs/mm 2 in the young to 134.2 PNs/mm 2 in the old. While the density of PN-surrounded GABAergic cells increased from 26 PNs/mm 2 in the young to 40.6 PNs/mm 2 in the old. The causality is unclear, but increases in PN density in old age may play a role in altered auditory processing in the elderly, or may lead to further changes in IC plasticity.

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Section: Potential Functional Roles Of Pns In Age-related Hearing Lossmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

Mafi

Hofer

Russ

et al. 2020

Front. Aging Neurosci.

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“…It is worth remembering that the brain cell activity as well as its effects are influenced by the surrounding environment, which includes a variety of cells, but also the molecules of the ECM, produced by the cells themselves. The complex of these components form the perineural net (PNN) [141]. A reduction in the expression of ECM components can affect synaptic plasticity, but an increase in ECM activity (for example, as a result of pathologic astrogliosis) can also be harmful [141].…”

Section: Evs In the Nervous System: General Considerationsmentioning

confidence: 99%

Cell-to-Cell Communication in Learning and Memory: From Neuro- and Glio-Transmission to Information Exchange Mediated by Extracellular Vesicles

Schiera

Liegro

2019

IJMS

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Most aspects of nervous system development and function rely on the continuous crosstalk between neurons and the variegated universe of non-neuronal cells surrounding them. The most extraordinary property of this cellular community is its ability to undergo adaptive modifications in response to environmental cues originating from inside or outside the body. Such ability, known as neuronal plasticity, allows long-lasting modifications of the strength, composition and efficacy of the connections between neurons, which constitutes the biochemical base for learning and memory. Nerve cells communicate with each other through both wiring (synaptic) and volume transmission of signals. It is by now clear that glial cells, and in particular astrocytes, also play critical roles in both modes by releasing different kinds of molecules (e.g., D-serine secreted by astrocytes). On the other hand, neurons produce factors that can regulate the activity of glial cells, including their ability to release regulatory molecules. In the last fifteen years it has been demonstrated that both neurons and glial cells release extracellular vesicles (EVs) of different kinds, both in physiologic and pathological conditions. Here we discuss the possible involvement of EVs in the events underlying learning and memory, in both physiologic and pathological conditions.

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“…The most well-studied type of ECM is Perineuronal Nets (PNN). This lattice-like structure envelop the soma, stabilizing interneuron activity, regulating synaptic homeostasis (Bosiacki et al, 2019) and protecting interneurons from oxidative damage (Morawski et al, 2004). The role of PNN in mouse model of Aβ amyloidosis have been inconsistent and contradictory.…”

Section: Introductionmentioning

confidence: 99%

Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis

Al-Amin

Grandjean

Klohs

et al. 2020

Preprint

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Although amyloid beta (Aβ) deposition is one of the major causes of white matter (WM) alterations in Alzheimer's disease (AD), little is known about the underlying basis of WM damage and its association with global structural connectivity and network topology. We aimed to dissect the contributions of WM microstructure to structural connectivity and network properties in the ArcAβ mice model of Aβ amyloidosis.We acquired diffusion-weighted images (DWI) of wild type (WT) and ArcAβ transgenic (TG) mice using a 9.4 T MRI scanner. Fixel-based analysis (FBA) was performed to measure fiber tract-specific properties. We also performed three complementary experiments; to identify the global differences in structural connectivity, to compute network properties and to measure cellular basis of white matter alterations.Transgenic mice displayed disrupted structural connectivity centered to the entorhinal cortex (EC) and a lower fiber density and fiber bundle cross-section. In addition, there was a reduced network efficiency and degree centrality in weighted structural connectivity in the transgenic mice. To further examine the underlying neuronal basis of connectivity and network deficits, we performed histology experiments. We found no alteration in myelination and an increased level of neurofilament light (NFL) in the brain regions with disrupted connectivity in the TG mice. Furthermore, TG mice had a reduced number of perineuronal nets (PNN) in the EC.The observed FDC reductions may indicate a decrease in axonal diameter or axon count which would explain the basis of connectivity deficits and reduced network efficiency in TG mice. The increase in NFL suggests a breakdown of axonal integrity, which would reduce WM fiber health.Considering the pivotal role of the EC in AD, Aβ deposition may primarily increase NFL release, damaging PNN in the entorhinal pathway, resulting in disrupted structural connectivity.

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Perineuronal Nets and Their Role in Synaptic Homeostasis

Cited by 72 publications

References 125 publications

The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

Cell-to-Cell Communication in Learning and Memory: From Neuro- and Glio-Transmission to Information Exchange Mediated by Extracellular Vesicles

Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis

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