PirB Restricts Ocular-Dominance Plasticity in Visual Cortex

Syken, Josh; GrandPré, Tadzia; Kanold, Patrick O.; Shatz, Carla J.

doi:10.1126/science.1128232

Cited by 315 publications

(407 citation statements)

References 39 publications

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“…Previous studies have shown that absence of the Nogo-66 receptor or PirB extends ODP into adulthood (20)(21)(22). However, for Nogo-66, it needs to be tested whether it is the juvenile form and whether PirB plays a role in the adult form of ODP (22).…”

Section: Discussionmentioning

confidence: 99%

“…Among these, the developmental increase of local inhibition appears to be the dominating mechanism to regulate cortical plasticity and CPs (15)(16)(17). Additionally, extracellular matrix remodeling is involved, as well as receptors of immune signaling, such as paired Ig-like receptor B (PirB), or axon pathfinding, such as Nogo (18)(19)(20)(21). However, a specific function to directly regulate synapse remodeling during initial neural network optimization is not known and a potential instructive function of PirB was described for adult cortical plasticity but not plasticity of the initial synapse remodeling during CPs (22).…”

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confidence: 99%

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Progressive maturation of silent synapses governs the duration of a critical period

Huang

Stodieck

Goetze

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

172

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During critical periods, all cortical neural circuits are refined to optimize their functional properties. The prevailing notion is that the balance between excitation and inhibition determines the onset and closure of critical periods. In contrast, we show that maturation of silent glutamatergic synapses onto principal neurons was sufficient to govern the duration of the critical period for ocular dominance plasticity in the visual cortex of mice. Specifically, postsynaptic density protein-95 (PSD-95) was absolutely required for experience-dependent maturation of silent synapses, and its absence before the onset of critical periods resulted in lifelong juvenile ocular dominance plasticity. Loss of PSD-95 in the visual cortex after the closure of the critical period reinstated silent synapses, resulting in reopening of juvenile-like ocular dominance plasticity. Additionally, silent synapse-based ocular dominance plasticity was largely independent of the inhibitory tone, whose developmental maturation was independent of PSD-95. Moreover, glutamatergic synaptic transmission onto parvalbumin-positive interneurons was unaltered in PSD-95 KO mice. These findings reveal not only that PSD-95-dependent silent synapse maturation in visual cortical principal neurons terminates the critical period for ocular dominance plasticity but also indicate that, in general, once silent synapses are consolidated in any neural circuit, initial experience-dependent functional optimization and critical periods end.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Progressive maturation of silent synapses governs the duration of a critical period

Huang

Stodieck

Goetze

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

172

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“…Diffuse synapse loss with altered cortical connectivity, as well as diffuse neuron and axon loss, are all commonly found in MS tissue 28, 29, 30, 31, 32, 33, 34, 60, 61, 62, 63 and could be driven by somatic or axonal MHC I expression. For example, neuronal MHC I has an established role in neuronal plasticity16 via mechanisms involving postsynaptic interactions with glutamate receptors and presynaptic interactions with the immunoreceptor tyrosine‐based inhibitory motif‐containing leukocyte immunoglobulin‐like receptor PirB 64. Neuronal MHC I has also been shown to inhibit glutamatergic receptor function in hippocampal circuits65 and studies in the retinogeniculate system indicate a role for somatic MHC class I in synapse elimination 66, 67.…”

Section: Discussionmentioning

confidence: 99%

Retrograde interferon‐gamma signaling induces major histocompatibility class I expression in human‐induced pluripotent stem cell‐derived neurons

Clarkson

Patel

LaFrance‐Corey

et al. 2017

Ann Clin Transl Neurol

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ObjectiveInjury‐associated axon‐intrinsic signals are thought to underlie pathogenesis and progression in many neuroinflammatory and neurodegenerative diseases, including multiple sclerosis (MS). Retrograde interferon gamma (IFN γ) signals are known to induce expression of major histocompatibility class I (MHC I) genes in murine axons, thereby increasing the susceptibility of these axons to attack by antigen‐specific CD8+ T cells. We sought to determine whether the same is true in human neurons.MethodsA novel microisolation chamber design was used to physically isolate and manipulate axons from human skin fibroblast‐derived induced pluripotent stem cell (iPSC)‐derived neuron‐enriched neural aggregates. Fluorescent retrobeads were used to assess the fraction of neurons with projections to the distal chamber. Axons were treated with IFN γ for 72 h and expression of MHC class I and antigen presentation genes were evaluated by RT‐PCR and immunofluorescence.ResultsHuman iPSC‐derived neural stem cells maintained as 3D aggregate cultures in the cell body chamber of polymer microisolation chambers extended dense axonal projections into the fluidically isolated distal chamber. Treatment of these axons with IFN γ resulted in upregulation of MHC class I and antigen processing genes in the neuron cell bodies. IFN γ‐induced MHC class I molecules were also anterogradely transported into the distal axon.InterpretationThese results provide conclusive evidence that human axons are competent to express MHC class I molecules, suggesting that inflammatory factors enriched in demyelinated lesions may render axons vulnerable to attack by autoreactive CD8+ T cells in patients with MS. Future work will be aimed at identifying pathogenic anti‐axonal T cells in these patients.

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“…To explore this issue, we measured the expression of Arc, an immediate early gene that is rapidly expressed in visual cortical neurons after brief visual stimulation (11,(29)(30)(31) with in situ hybridization. The visually induced expression pattern of Arc is a sensitive indicator of OD plasticity in both mice and cats (11,(29)(30)(31). As expected, after monocular enucleation (ME) in control, the functional representation of the NDE increased in control (Fig.…”

Section: Resultsmentioning

confidence: 99%

Electrical synapses formed by connexin36 regulate inhibition- and experience-dependent plasticity

Postma

Liu²,

Dietsche³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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The mammalian brain constantly adapts to new experiences of the environment, and inhibitory circuits play a crucial role in this experience-dependent plasticity. A characteristic feature of inhibitory neurons is the establishment of electrical synapses, but the function of electrical coupling in plasticity is unclear. Here we show that elimination of electrical synapses formed by connexin36 altered inhibitory efficacy and caused frequency facilitation of inhibition consistent with a decreased GABA release in the inhibitory network. The altered inhibitory efficacy was paralleled by a failure of theta-burst long-term potentiation induction and by impaired ocular dominance plasticity in the visual cortex. Together, these data suggest a unique mechanism for regulating plasticity in the visual cortex involving synchronization of inhibitory networks via electrical synapses.gap junctions | development | cannabinoid receptor 1 | synchrony S ynaptic interactions in the mammalian brain are sculpted by experience, particularly during "critical periods" in development. Accumulating evidence suggests that inhibitory neurons play a crucial role in reshaping neural networks in response to sensory perturbations (1). Inhibitory neurons in many areas of the brain, including the cerebral cortex, are coupled via gap junctions containing connexin36 (Cx36), which allow subthreshold fluctuations in membrane potential to spread between cells and promote synchrony of firing (2-5). Cx36-null mice (Cx36KO) display decreased coherence of rhythmic activity in populations of cortical interneurons in brain slices and decreased strength of evoked cortical inhibition in vivo (6-8). Similar effects of Cx36 signaling might underlie the behavioral deficits in cerebellar learning tasks in Cx36KO (7). However, the possible functions of Cx36 in sensory cortical development and plasticity are unknown.A common model for experience-dependent synaptic modification is ocular dominance (OD) plasticity of visual cortex. In the visual cortex, decreasing neural activity in one eye (monocular deprivation; MD) leads to weakening and removal of connections representing the deprived eye (DE) and strengthening and expansion of connections representing the nondeprived eye (NDE; refs. 9-13). These manipulations are particularly effective during the critical period, which extends from postnatal day (P) 19 to ∼P55 and peaks at ∼P25-28 in mice (11,14,15). Both inhibition and synaptic plasticity mechanisms, such as long-term potentiation (LTP) and long-term depression (LTD), play a key role in OD plasticity, and inhibition can alter synaptic plasticity (1,16,17). Cx36 is present in most cortical layers during the critical period for OD plasticity (6). We therefore investigated to what degree Cx36 controls inhibitory function and, consequently, synaptic and OD plasticity.Here we report altered dynamics of the evoked inhibitory synaptic currents in mice lacking Cx36, such that there is a reduction when probed at low-frequency stimulation but a facilitation at higher frequ...

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PirB Restricts Ocular-Dominance Plasticity in Visual Cortex

Cited by 315 publications

References 39 publications

Progressive maturation of silent synapses governs the duration of a critical period

Progressive maturation of silent synapses governs the duration of a critical period

Retrograde interferon‐gamma signaling induces major histocompatibility class I expression in human‐induced pluripotent stem cell‐derived neurons

Electrical synapses formed by connexin36 regulate inhibition- and experience-dependent plasticity

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