Chondroitin Sulfate Is Required for Onset and Offset of Critical Period Plasticity in Visual Cortex

Hou, Xubin; Yoshioka, Nozomu; Tsukano, Hiroaki; Sakai, Akiko; Miyata, Shinji; Watanabe, Yumi; Yanagawa, Yuchio; Sakimura, Kenji; Takeuchi, Kosei; Kitagawa, Hiroshi; Hensch, Takao K.; Shibuki, Katsuei; Igarashi, Michihiro; Sugiyama, Sayaka

doi:10.1038/s41598-017-04007-x

Cited by 69 publications

(72 citation statements)

References 74 publications

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“…In early postnatal cortical development, expression of PNNs increases progressively with the maturation of that network. An excellent example is the primary visual cortex where the developmental increase of PNNs is regulated by visual experience (Beurdeley et al, 2012;Hou et al, 2017). PNNs in mature primary visual cortex mainly surround the soma and proximal dendrites of PV+ interneurons (Celio, 1993;Hartig et al, 1992;Ueno et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Perineuronal nets (PNNs) are specialized extracellular matrix structures that can act as physical barriers or modulators of plasticity, restrict axon regeneration, and form molecular brakes that actively control synaptic maturation and the function of cortical parvalbumin+ (PV+) GABAergic interneurons that drive gamma oscillations (Bartos et al, 2002;Begum and Sng, 2017;Bernard and Prochiantz, 2016;Carstens et al, 2016;Deepa et al, 2002;Dityatev et al, 2007;Donato et al, 2013;Durand et al, 2012;Frischknecht et al, 2009;Gundelfinger et al, 2010;Hartig et al, 1992;Hou et al, 2017;Kalemaki et al, 2018;Kosaka and Heizmann, 1989;Krishnan et al, 2015Krishnan et al, , 2017Nakagawa et al, 1986;Orlando et al, 2012;Pizzorusso et al, 2002Pizzorusso et al, , 2006Sigal et al, 2019;Sugiyama et al, 2009;Suttkus et al, 2012;Ueno et al, 2018;Vo et al, 2013;de Winter et al, 2016;Ye and Miao, 2013). Mature PNNs in the adult cortices are thought to be stable structures, inhibitory to plasticity, and perhaps play roles in long term memory such as "engrams" (Carstens et al, 2016;Gogolla et al, 2009;Thompson et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

Lau

Layo

Emery

et al. 2019

Preprint

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Cortical neuronal circuits along the sensorimotor pathways are shaped by experience during critical periods of heightened plasticity in early postnatal development. After closure of critical periods, measured histologically by the formation and maintenance of extracellular matrix structures called perineuronal nets (PNNs), the adult mouse brain exhibits restricted plasticity and maturity. Mature PNNs are typically considered to be stable structures that restrict synaptic plasticity on cortical parvalbumin+ GABAergic neurons. Changes in environment (i.e. novel behavioral training) or social contexts (i.e. motherhood) are known to elicit synaptic plasticity in relevant neural circuitry. However, little is known about concomitant changes in the PNNs surrounding the cortical parvalbumin+ GABAergic neurons. Here, we show novel changes in PNN density in the primary somatosensory cortex (SS1) of adult female mice after maternal experience, using systematic microscopy analysis of a whole brain region. On average, PNNs were increased in the right barrel field and decreased in the left forelimb regions. Individual mice had left hemisphere dominance in PNN density. Using adult female mice deficient in methyl-CpG-binding protein 2 (MECP2), an epigenetic regulator involved in regulating experience-dependent plasticity, we found that MECP2 is critical for this precise and dynamic expression of PNN. Adult naïve Mecp2-heterozygous females (Het) had increased PNN density in specific subregions in both hemispheres before maternal experience. The laterality in PNN expression seen in naïve Het was lost after maternal experience, suggesting possible intact mechanisms for plasticity. Together, our results identify subregion and hemisphere-specific alterations in PNN expression in adult females, suggesting extracellular matrix plasticity as a possible neurobiological mechanism for adult behaviors in rodents.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

Lau

Layo

Emery

et al. 2019

Preprint

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“…Once Otx2 is enriched around PV cells via the interaction with PNN, it seems to penetrate the cells through a positively charged internalization sequence (Prochiantz & Joliot, ; Sugiyama et al., ). In contrast to the prevailing notion that PNN inhibits the plasticity as a physical barrier, a new study using mice lacking a key CS‐synthesizing enzyme, chondroitin sulfate N ‐acetylgalactosaminyltransferase 1 (CSGalNAcT1), showed that a small amount of PNN is essential to open the critical period by promoting accumulation of Otx2 in PV cells (Hou et al., ; Igarashi, Takeuchi, & Sugiyama, ). As CSGalNAcT1 is a target gene of Otx2 (Sakai et al., ), continuous internalization of Otx2 then accelerates further PNN formation, which in turn consolidates PV cell function and closes the critical period.…”

Section: Otx2 Homeoprotein Is a Messenger Of Experience To Regulate Tmentioning

confidence: 99%

“…How is Otx2 targeted to PV cells? Recent studies showed that Otx2 binds to chondroitin sulfate proteoglycan (CSPG) in PNN via its glycosaminoglycan‐binding motif (Beurdeley et al., ; Miyata, Komatsu, Yoshimura, Taya, & Kitagawa, ) and also interacts with a major CSPG, aggrecan (Hou et al., ). Once Otx2 is enriched around PV cells via the interaction with PNN, it seems to penetrate the cells through a positively charged internalization sequence (Prochiantz & Joliot, ; Sugiyama et al., ).…”

Section: Otx2 Homeoprotein Is a Messenger Of Experience To Regulate Tmentioning

confidence: 99%

“…As CSGalNAcT1 is a target gene of Otx2 (Sakai et al., ), continuous internalization of Otx2 then accelerates further PNN formation, which in turn consolidates PV cell function and closes the critical period. Inhibition of Otx2 internalization in adults, by infusing a peptide that interferes with PNN interaction or by exogenous antibody to trap Otx2, leads to a decrease of PV circuits and reactivation of the critical period (Bernard et al., ; Beurdeley et al., ; Hou et al., ). Thus, the mutually dependent increase in amount of Otx2‐PNN induces molecular events at two different steps, respectively, determining the onset and offset of the critical period.…”

Section: Otx2 Homeoprotein Is a Messenger Of Experience To Regulate Tmentioning

confidence: 99%

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Experience‐dependent transcriptional regulation in juvenile brain development

Sakai

Sugiyama

2018

Dev Growth Differ

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During brain development, once primary neural networks are formed, they are largely sculpted by environmental stimuli. The juvenile brain has a unique time window termed the critical period, in which neuronal circuits are remodeled by experience. Accumulating evidence indicates that abnormal rewiring of circuits in early life contributes to various neurodevelopmental disorders at later stages of life. Recent studies implicate two important aspects for activation of the critical period, both of which are experience‐dependent: (a) proper excitatory/inhibitory (E/I) balance of neural circuit achieved during developmental trajectory of inhibitory interneurons, and (b) epigenetic regulation allowing flexible gene expression for neuronal plasticity. In this review, we discuss the molecular mechanisms of juvenile brain plasticity from the viewpoints of transcriptional and chromatin regulation, with a focus on Otx2 homeoprotein. Depending on experience, Otx2 is transported into cortical parvalbumin‐positive interneurons (PV cells), where it induces PV cell maturation to activate the critical period. Understanding the unique behavior and function of Otx2 as a “messenger” of experience should therefore provide insights into mechanisms of juvenile brain development. Recently identified downstream targets of Otx2 suggest novel roles of Otx2 in homeostasis of PV cells, and, moreover, in regulation of chromatin state, which is important for neuronal plasticity. We further discuss epigenetic changes during postnatal brain development spanning the critical period. Different aspects of chromatin regulation may underlie experience‐dependent neuronal development and plasticity.

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Ocular dominance plasticity: Molecular mechanisms revisited

Kasamatsu

Imamura

2020

J of Comparative Neurology

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Ocular dominance plasticity (ODP) is a type of cortical plasticity operating in visual cortex of mammals that are endowed with binocular vision based on the competition-driven disparity. Earlier, a molecular mechanism was proposed that catecholamines play an important role in the maintenance of ODP in kittens. Having survived the initial test, the hypothesis was further advanced to identify noradrenaline (NA) as a key factor that regulates ODP in the immature cortex. Later, the ODPpromoting effect of NA is extended to the adult with age-related limitations. Following the enhanced NA availability, the chain events downstream lead to the β-adrenoreceptor-induced cAMP accumulation, which in turn activates the protein kinase A. Eventually, the protein kinase translocates to the cell nucleus to activate cAMP responsive element binding protein (CREB). CREB is a cellular transcription factor that controls the transcription of various genes, underpinning neuronal plasticity and long-term memory. In the advent of molecular genetics in that various types of new tools have become available with relative ease, ODP research has lightly adopted in the rodent model the original concepts and methodologies. Here, after briefly tracing the strategic maturation of our quest, the review moves to the later development of the field, with the emphasis placed around the following issues: (a) Are we testing ODP per se? (b) What does monocular deprivation deprive of the immature cortex? (c) The critical importance of binocular competition, (d) What is the adult plasticity? (e) Excitation-Inhibition balance in local circuits, and (f) Species differences in the animal models.

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Chondroitin Sulfate Is Required for Onset and Offset of Critical Period Plasticity in Visual Cortex

Cited by 69 publications

References 74 publications

Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

Experience‐dependent transcriptional regulation in juvenile brain development

Ocular dominance plasticity: Molecular mechanisms revisited

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