Nogo Receptor 1 Confines a Disinhibitory Microcircuit to the Critical Period in Visual Cortex

Stephany, Céleste-Élise; Ikrar, Taruna; Nguyen, Collins; Xu, Xiangmin; McGee, Aaron W.

doi:10.1523/jneurosci.0935-16.2016

Cited by 31 publications

(38 citation statements)

References 44 publications

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“…Thalamic axons themselves display plasticity after monocular deprivation, raising the question of specific contributions of cortical PV + interneurons to critical period plasticity (Jaepel et al, 2017;Sommeijer et al, 2017). Our study demonstrates that excitatory, thalamocortical (TC) inputs to PV + interneurons in V1 are essential for critical period closure, in agreement with a central role of cortical inhibition in critical period regulation (Gu et al, 2013;Kuhlman et al, 2013;Stephany et al, 2016;Sun et al, 2016). The identification of SynCAM 1 as a novel, PV + -autonomous molecular brake on plasticity highlights that distinct mechanisms control critical period opening vs critical period closure, and sheds light on the profound impacts of excitatory/inhibitor y imbalance and regulatory feedback loops that are frequently implicated in neurodevelopme nta l disorders (Ebert and Greenberg, 2013;Mullins et al, 2016;Nelson and Valakh, 2015;Zoghbi and Bear, 2012).…”

Section: Discussionsupporting

confidence: 71%

“…Other mechanisms that control excitatory drive onto PV + interneurons include Neuregulin-1/ErbB4 signaling (Fazzari et al, 2010;Sun et al, 2016), pentraxins (Chang et al, 2010;Gu et al, 2013;Pelkey et al, 2016) and the NogoR receptor (Stephany et al, 2016). Interestingly, all three are critical for ocular dominance plasticity (ODP), suggesting a pivotal role of excitatory drive onto PV + interneurons in the initiation of ODP (Gu et al, 2013;Kuhlman et al, 2013;McGee et al, 2005;Sun et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Cell-autonomous synaptic factors that control excitatory inputs on cortical PV + interneurons and thereby the onset and duration of ODP remain uncharacterized. Recent studies have highlighted roles of the ECM protein Narp, as well as PV + -expressed NogoR and Neuregulin 1/ErbB4 signaling in the control of local, intracortical excitatory inputs onto PV + interneurons during ODP (Gu et al, 2013;Stephany et al, 2016;Sun et al, 2016). However, the mechanisms that organize feed-forward thalamic inputs onto PV + interneurons and their role in ODP are unknown.…”

Section: Introductionmentioning

confidence: 99%

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Synapse-selective control of cortical maturation and plasticity engages an interneuron-autonomous synaptic switch

Ribic

Biederer

2018

Preprint

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Highlights• The synaptogenic molecule SynCAM 1 is selectively regulated by visual experience • SynCAM 1 controls thalamic input onto cortical Parvalbumin (PV + ) interneurons • PV + -specific knockdown of SynCAM 1 arrests maturation of cortical inhibition • Thalamic excitation onto PV + interneurons is essential for critical period closure eTOC Blurb Ribic et al. show that network plasticity in both young and adult cortex is restricted by the synapseorganizing molecule SynCAM 1. On a cellular level, it functions in Parvalbumin-positive interneurons to recruit thalamocortical terminals. This controls the maturation of inhibitory drive and restricts plasticity in the cortex. These results reveal the synaptic locus of cortical plasticity and identify the first cell-autonomous synaptic factor for closure of cortical critical periods. SummaryBrain plasticity peaks early in life and tapers in adulthood. This is exemplified in the primary visual cortex, where brief loss of vision to one eye abrogates cortical responses to inputs from that eye during the critical period, but not in adulthood. The synaptic locus of critical period plasticity and the cell-autonomous synaptic factors timing these periods remain unclear. We here demonstrate that the immunoglobulin protein Synaptic Cell Adhesion Molecule 1 (SynCAM 1/Cadm1) is regulated by visual experience and limits visual cortex plasticity. SynCAM 1 selectively controls the number of excitatory thalamocortical (TC) inputs onto Parvalbumin (PV + ) interneurons and loss of SynCAM 1 in turn impairs the maturation of TC-driven feed-forward inhibitio n.SynCAM 1 acts in cortical PV + interneurons to perform these functions and its PV + -specific knockdown prevents the age-related plasticity decline. These results identify a synapse typespecific, cell-autonomous mechanism that governs circuit maturation and closes the visual critical period.

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Section: Discussionsupporting

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Synapse-selective control of cortical maturation and plasticity engages an interneuron-autonomous synaptic switch

Ribic

Biederer

2018

Preprint

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“…3h-j ). Among the up-regulated genes, Rtn4r was reported to mediate intralaminar synaptic connectivity of visual cortical interneurons or a subclass of PV + interneurons 18,19 , which markedly sharpened grating orientation tuning and enhanced direction selectivity of nearby neurons 5 . Additionally, Nptxr has been hypothesized to be involved in activity-dependent synaptic plasticity 20,21 , as well as synaptic maturation through PV + interneurons in V1 22 .…”

Section: Singe-cell Rna Sequencing Of Somatic Aspiratesmentioning

confidence: 99%

Functional In vivo Single-cell Transcriptome (FIST) Analysis Reveals Molecular Properties of Light-Sensitive Neurons in Mouse V1

Liu

Pan

Sun

et al. 2018

Preprint

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Vision formation is classically based on projections from the retinal ganglion cells (RGC) to the lateral geniculate nucleus (LGN) and the primary visual cortex (V1). Although the cellular information of the retina and the LGN has been widely studied, the transcriptome profiles of single neurons with specific functions in V1 still remain unknown. Some neurons in mouse V1 are tuned to light stimulus. To determine the molecular properties of lightstimulated neurons in layer 2/3 of V1, we developed a method of functional in vivo singlecell transcriptome (FIST) analysis that integrates sensory evoked calcium imaging, wholecell electrophysiological patch-clamp recordings, single-cell mRNA sequencing and threedimensional morphological characterization in a live mouse, based on a two-photon microscope system. In our study, 58 individual cells from layer 2/3 of V1 were identified as either light-sensitive (LS) or non-light-sensitive (NS) by single-cell light-evoked calcium evaluation and action potential spiking. The contents of every single cell after individual functional tests were aspirated through the patch-clamp pipette for mRNA sequencing.Furthermore, the three-dimensional (3-D) morphological characterizations of the neurons were reconstructed in the live mouse after the whole-cell recordings. Our sequencing results indicated that V1 neurons with high expression of genes related to transmission regulation, such as Rtn4r, Nr4a1, and genes involved in membrane transport, such as Na + /K + ATPase, NMDA-type glutamatergic receptor, preferentially respond to light stimulation. Our findings demonstrate the ability of FIST analysis to characterize the functional, morphological and transcriptomic properties of a single cell in alive animal, thereby providing precise neuronal information and predicting its network contribution in the brain.

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“…This initial and transient reduction of PV cell activity establishes the conditions necessary for the experience‐dependent excitatory cortical plasticity for ocular dominance. Previous studies identified neurotrophins, extracellular matrix components, and synapse formation molecules as modulators of visual cortical plasticity (Berardi, Pizzorusso, Ratto, & Maffei, ; Gu et al, ; Huang et al, ; Murase, Lantz, & Quinlan, ; Pizzorusso et al, ; Stephany, Ikrar, Nguyen, Xu, & McGee, ; Sugiyama et al, ; Tropea et al, ). However, they do not account for the translation of brief sensory deprivation into functional changes in circuit connections.…”

Section: Introductionmentioning

confidence: 98%

Neuregulin directed molecular mechanisms of visual cortical plasticity

Grieco

Holmes

2018

J of Comparative Neurology

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Experience-dependent critical period (CP) plasticity has been extensively studied in the visual cortex. Monocular deprivation during the CP affects ocular dominance, limits visual performance, and contributes to the pathological etiology of amblyopia. Neuregulin-1 (NRG1) signaling through its tyrosine kinase receptor ErbB4 is essential for the normal development of the nervous system and has been linked to neuropsychiatric disorders such as schizophrenia. We discovered recently that NRG1/ErbB4 signaling in PV neurons is critical for the initiation of CP visual cortical plasticity by controlling excitatory synaptic inputs onto PV neurons and thus PV-cell mediated cortical inhibition that occurs following visual deprivation. Building on this discovery, we review the existing literature of neuregulin signaling in developing and adult cortex and address the implication of NRG/ErbB4 signaling in visual cortical plasticity at the cellular and circuit levels. NRG-directed research may lead to therapeutic approaches to reactivate plasticity in the adult cortex.

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Nogo Receptor 1 Confines a Disinhibitory Microcircuit to the Critical Period in Visual Cortex

Cited by 31 publications

References 44 publications

Synapse-selective control of cortical maturation and plasticity engages an interneuron-autonomous synaptic switch

Synapse-selective control of cortical maturation and plasticity engages an interneuron-autonomous synaptic switch

Functional In vivo Single-cell Transcriptome (FIST) Analysis Reveals Molecular Properties of Light-Sensitive Neurons in Mouse V1

Neuregulin directed molecular mechanisms of visual cortical plasticity

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