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      A Sweet Talk: The Molecular Systems of Perineuronal Nets in Controlling Neuronal Communication

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          Abstract

          Perineuronal nets (PNNs) are mesh-like structures, composed of a hierarchical assembly of extracellular matrix molecules in the central nervous system (CNS), ensheathing neurons and regulating plasticity. The mechanism of interactions between PNNs and neurons remain uncharacterized. In this review, we pose the question: how do PNNs regulate communication to and from neurons? We provide an overview of the current knowledge on PNNs with a focus on the cellular interactions. PNNs ensheath a subset of the neuronal population with distinct molecular aspects in different areas of the CNS. PNNs control neuronal communication through molecular interactions involving specific components of the PNNs. This review proposes that the PNNs are an integral part of neurons, crucial for the regulation of plasticity in the CNS.

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          Most cited references 68

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          Critical period regulation.

           Takao Hensch (2003)
          Neuronal circuits are shaped by experience during critical periods of early postnatal life. The ability to control the timing, duration, and closure of these heightened levels of brain plasticity has recently become experimentally accessible, especially in the developing visual system. This review summarizes our current understanding of known critical periods across several systems and species. It delineates a number of emerging principles: functional competition between inputs, role for electrical activity, structural consolidation, regulation by experience (not simply age), special role for inhibition in the CNS, potent influence of attention and motivation, unique timing and duration, as well as use of distinct molecular mechanisms across brain regions and the potential for reactivation in adulthood. A deeper understanding of critical periods will open new avenues to "nurture the brain"-from international efforts to link brain science and education to improving recovery from injury and devising new strategies for therapy and lifelong learning.
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            Perineuronal nets protect fear memories from erasure.

            In adult animals, fear conditioning induces a permanent memory that is resilient to erasure by extinction. In contrast, during early postnatal development, extinction of conditioned fear leads to memory erasure, suggesting that fear memories are actively protected in adults. We show here that this protection is conferred by extracellular matrix chondroitin sulfate proteoglycans (CSPGs) in the amygdala. The organization of CSPGs into perineuronal nets (PNNs) coincided with the developmental switch in fear memory resilience. In adults, degradation of PNNs by chondroitinase ABC specifically rendered subsequently acquired fear memories susceptible to erasure. This result indicates that intact PNNs mediate the formation of erasure-resistant fear memories and identifies a molecular mechanism closing a postnatal critical period during which traumatic memories can be erased by extinction.
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              Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity.

              Neural circuits are shaped by experience in early postnatal life. Distinct GABAergic connections within visual cortex determine the timing of the critical period for rewiring ocular dominance to establish visual acuity. We find that maturation of the parvalbumin (PV)-cell network that controls plasticity onset is regulated by a selective re-expression of the embryonic Otx2 homeoprotein. Visual experience promoted the accumulation of non-cell-autonomous Otx2 in PV-cells, and cortical infusion of exogenous Otx2 accelerated both PV-cell development and critical period timing. Conversely, conditional removal of Otx2 from non-PV cells or from the visual pathway abolished plasticity. Thus, the experience-dependent transfer of a homeoprotein may establish the physiological milieu for postnatal plasticity of a neural circuit.
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                Author and article information

                Contributors
                Journal
                Front Integr Neurosci
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Media S.A.
                1662-5145
                01 December 2017
                2017
                : 11
                Affiliations
                1Department of Clinical Neurosciences, John van Geest Centre for Brain Repair, University of Cambridge , Cambridge, United Kingdom
                2Faculty of Biological Sciences, School of Biomedical Sciences, University of Leeds , Leeds, United Kingdom
                3Czech Academy of Sciences, Institute of Experimental Medicine, Centre of Reconstructive Neurosciences , Prague, Czechia
                Author notes

                Edited by: Harry Pantazopoulos, McLean Hospital, United States

                Reviewed by: Pascal Steullet, Centre Hospitalier Universitaire Vaudois (CHUV), Switzerland; Barbara A. Sorg, Washington State University, United States; Amy Lasek, University of Illinois at Chicago, United States

                *Correspondence: Jessica C. F. Kwok j.kwok@ 123456leeds.ac.uk
                Article
                10.3389/fnint.2017.00033
                5717013
                Copyright © 2017 van 't Spijker and Kwok.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 87, Pages: 10, Words: 9351
                Funding
                Funded by: Wings for Life 10.13039/100008191
                Award ID: WFL-UK-008/15
                Funded by: Royal Society 10.13039/501100000288
                Award ID: RG160410
                Funded by: Horizon 2020 10.13039/501100007601
                Award ID: CZ.02.1.01/0.0./0.0/15_003/0000419
                Categories
                Neuroscience
                Review

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