Regulation of Perineuronal Nets in the Adult Cortex by the Activity of the Cortical Network

Devienne, Gabrielle; Picaud, Sandrine; Cohen, Ivan; Piquet, Juliette; Tricoire, Ludovic; Testa, D.; Nardo, Ariel A. Di; Rossier, Jean; Cauli, Bruno; Lambolez, Bertrand

doi:10.1523/jneurosci.0434-21.2021

Cited by 47 publications

(40 citation statements)

References 56 publications

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“…It should be recognized that outside of critical periods, PNNs are capable of rapid remodeling, as has been recently demonstrated in several studies (Marchand and Schwartz, 2020;Pantazopoulos et al, 2020;Uriarte et al, 2020). Evidence suggests that changes in PNNs can occur through alterations in neuronal activity both during development and in adulthood (Dityatev et al, 2007;Carstens et al, 2021;Devienne et al, 2021). Thus, stress-induced changes in neuronal activity (Della Valle et al, 2019;Murthy et al, 2019;Del Arco et al, 2020;Fee et al, 2020) could be a mechanism by which alterations in PNNs occur.…”

Section: Stress Effects On Perineuronal Netsmentioning

confidence: 89%

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

Laham

Gould

2022

Front. Cell. Neurosci.

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Diffuse and structured extracellular matrix (ECM) comprise ∼20% of the brain’s volume and play important roles in development and adult plasticity. Perineuronal nets (PNNs), specialized ECM structures that surround certain types of neurons in the brain, emerge during the postnatal period, making their development and maintenance potentially sensitive to experience. Recent studies have shown that stress affects diffuse ECM as well as PNNs, and that such effects are dependent on life stage and brain region. Given that the ECM participates in synaptic plasticity, the generation of neuronal oscillations, and synchronous firing across brain regions, all of which have been linked to cognition and emotional regulation, ECM components may be candidate therapeutic targets for stress-induced neuropsychiatric disease. This review considers the influence of stress over diffuse and structured ECM during postnatal life with a focus on functional outcomes and the potential for translational relevance.

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Section: Stress Effects On Perineuronal Netsmentioning

confidence: 89%

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

Laham

Gould

2022

Front. Cell. Neurosci.

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“…Built with diverse components originating from neurons, astrocytes, and oligodendrocytes, PNNs are lattice-like structures primarily composed of hyaluronan (HA), CSPGs, and cross-linking proteins from the link protein family (HAPLNs) and tenascin-R (TNR; for reviews, see Fawcett et al, 2019 ; Testa et al, 2019 ). PNN assembly is activity-dependent (Dityatev et al, 2007 ), requiring sensory input during postnatal development in order to form (Pizzorusso et al, 2002 ; McRae et al, 2007 ; Kind et al, 2013 ), and their maintenance in adulthood can be regulated by local network activity (Devienne et al, 2021 ). Physiologically, PNNs act as molecular brakes that progressively decrease plasticity as they condense around FS-PV cell soma and proximal dendrites during the CP, and eventually restrict plasticity in adulthood (Pizzorusso et al, 2002 ).…”

Section: Non-cell-autonomous Factors From Local Cells For Short-range...mentioning

confidence: 99%

“…The picture is further complicated by the regulation of PNN structure by multiple metalloproteases (described below) that again come from multiple sources. In fact, although PNNs are often thought of as fixed structures, they remain dynamic in adulthood in response to changes in FS-PV activity and diurnal fluctuations (Pantazopoulos et al, 2020 ; Devienne et al, 2021 ; Harkness et al, 2021 ).…”

Section: Non-cell-autonomous Factors From Local Cells For Short-range...mentioning

confidence: 99%

Non-Cell-Autonomous Factors Implicated in Parvalbumin Interneuron Maturation and Critical Periods

Gibel-Russo

Benacom

Nardo

2022

Front. Neural Circuits

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From birth to adolescence, the brain adapts to its environmental stimuli through structural and functional remodeling of neural circuits during critical periods of heightened plasticity. They occur across modalities for proper sensory, motor, linguistic, and cognitive development. If they are disrupted by early-life adverse experiences or genetic deficiencies, lasting consequences include behavioral changes, physiological and cognitive deficits, or psychiatric illness. Critical period timing is orchestrated not only by appropriate neural activity but also by a multitude of signals that participate in the maturation of fast-spiking parvalbumin interneurons and the consolidation of neural circuits. In this review, we describe the various signaling factors that initiate critical period onset, such as BDNF, SPARCL1, or OTX2, which originate either from local neurons or glial cells or from extracortical sources such as the choroid plexus. Critical period closure is established by signals that modulate extracellular matrix and myelination, while timing and plasticity can also be influenced by circadian rhythms and by hormones and corticosteroids that affect brain oxidative stress levels or immune response. Molecular outcomes include lasting epigenetic changes which themselves can be considered signals that shape downstream cross-modal critical periods. Comprehensive knowledge of how these signals and signaling factors interplay to influence neural mechanisms will help provide an inclusive perspective on the effects of early adversity and developmental defects that permanently change perception and behavior.

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“…In the central nervous system (CNS), a specialized ECM called perineuronal net (PNN) can occur around certain neuron populations. Even though the discovery of PNNs by Camillo Golgi took place at the late 19 th century (Celio et al, 1998), their important roles in cortical plasticity, regulation of neural activity and in association with neurodegenerative diseases began to emerge only recently (Devienne et al, 2021, Wang and Fawcett, 2012, Lemarchant et al, 2016, Dzyubenko et al, 2016). PNNs enwrap primarily inhibitory gamma-aminobutyric acid (GABA)ergic interneurons by forming a net-like structure around the soma and proximal dendrites (Lensjo et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…This arrangement of PNN components around the cell is often described as a honeycomb-shaped ECM structure with holes for synaptic contact. The largest population of neurons enwrapped by PNNs in the brain consists of parvalbumin-expressing neurons (Devienne et al, 2021, Hartig et al, 1992). PNNs show considerable molecular heterogeneity in terms of their composition (Miyata et al, 2018), but the main components of a basic general PNN structure consist of a hyaluronan backbone to attach the ECM to the cell surface (Deepa et al, 2006), the chondroitin sulfate proteoglycans (CSPGs) aggrecan, brevican, neurocan, and versican, which belong to the lectican family (Yamaguchi, 2000), and link proteins.…”

Section: Introductionmentioning

confidence: 99%

Brevican, Neurocan, Tenascin-C and Tenascin-R Act as Important Regulators of the Interplay between Perineuronal Nets, Synaptic Integrity, Inhibitory Interneurons and Otx2

Mueller-Buehl

Reinhard

Roll

et al. 2022

Preprint

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Fast-spiking parvalbumin interneurons are critical for the function of mature cortical inhibitory circuits. Most of these neurons are enwrapped by a specialized extracellular matrix structure (ECM) called perineuronal net (PNN), which can regulate their synaptic input. In this study, we investigated the relationship between PNNs, parvalbumin interneurons and synaptic distribution on these cells in the adult primary visual cortex (V1) of quadruple knockout mice deficient for the ECM molecules brevican, neurocan, tenascin-C and tenascin-R. We used super-resolution structured illumination microscopy (SIM) to analyze PNN structure and associated synapses. Additionally, we examined parvalbumin and calretinin interneuron populations. We observed a reduction in the number of PNN-enwrapped cells and a clear disorganization of the PNN structure in the quadruple knockout V1. This was accompanied by an imbalance of inhibitory and excitatory synapses with a reduction of inhibitory and an increase of excitatory synaptic elements along the PNNs. Also, the number of parvalbumin interneurons was reduced in the quadruple knockout, while calretinin interneurons, which do not wear PNNs did not display differences in number. Interestingly, we found the transcription factor Otx2 homeoprotein positive cell population also reduced. Otx2 is crucial for parvalbumin and PNN maturation and a positive feedback loop between these parameters has been described. Collectively, these data indicate an important role of brevican, neurocan, tenascin-C and tenascin-R in regulating the interplay between PNNs, inhibitory interneurons, synaptic distribution as well as Otx2 in the V1.

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Regulation of Perineuronal Nets in the Adult Cortex by the Activity of the Cortical Network

Cited by 47 publications

References 56 publications

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

Non-Cell-Autonomous Factors Implicated in Parvalbumin Interneuron Maturation and Critical Periods

Brevican, Neurocan, Tenascin-C and Tenascin-R Act as Important Regulators of the Interplay between Perineuronal Nets, Synaptic Integrity, Inhibitory Interneurons and Otx2

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