Experience-Dependent Transfer of Otx2 Homeoprotein into the Visual Cortex Activates Postnatal Plasticity
Open accessAbstract
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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Experience-dependent accumulation of exogenous OTX2 is necessary for the formation of PNNs and critical period closure in the visual cortex.
“On the other hand, an experience-dependent accumulation of exogenous OTX2, a homeoprotein commonly bound to PNNs and PV1 cells in the mPFC (Lee et al., 2017), is necessary for the formation of PNNs and critical period closure in the visual cortex (Sugiyama et al., 2008).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Sugiyama et al., 2008
Reductions of inhibitory neural activity in adulthood have increased visual plasticity in rodents and even restored visual function in amblyopic adult rats.
“For example, reductions of inhibitory neural activity in adulthood have increased visual plasticity in rodents (He et al., 2007, Sugiyama et al., 2008, Harauzov et al., 2010) and even restored visual function in amblyopic adult rats (Vetencourt et al., 2008).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Sugiyama et al., 2008
Disruption of excitatory-inhibitory balance shifts the timing and quality of critical period development in primary visual cortex.
“Accordingly, disruption of E-I balance powerfully shifts the timing and quality of critical period development, as seen in the primary visual cortex (V1) (27–29).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [27]
PNN disruption prevents persistent uptake of Otx2 homeoprotein into enwrapped PV cells required for their maintenance.
“Second, PNN disruption prevents the persistent uptake of Otx2 homeoprotein into the enwrapped PV-cells required for their maintenance (27, 40, 41) (Fig. S3).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [27]
Compromised PNNs prevent persistent uptake of Otx2 homeoprotein into enwrapped PV cells needed for their maturation, including PNN maintenance.
“Compromised PNNs prevent the persistent uptake of Otx2 homeoprotein into the enwrapped PV-cells needed for their maturation (including PNN maintenance itself) (27, 40, 41).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [27]
Blocking Otx2 transport in retina or cortex retards activity-dependent opening of the critical period in visual cortex.
“Blocking Otx2 transport in the retina (between bipolar cells and retinal ganglion cells) or in the cortex (by directly infusing anti-Otx2 antibodies) retards the activity-dependent opening of CP in the visual cortex (Sugiyama et al., 2008).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
Direct infusion of Otx2 before critical period opening opens the critical period ahead of time and also closes it ahead of time.
“In support of the hypothesis is that direct infusion of Otx2 before CP opening opens CP ahead of time and also closes it ahead of time (Sugiyama et al., 2008).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
In dark-reared animals, the opening of plasticity does not take place, and Otx2 and parvalbumin levels remain low in parvalbumin cells.
“Moreover, the opening of plasticity (first threshold) does not take place in dark-reared animals, where the Otx2 and PV levels remain low in PV-cells.”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
Otx2 injected in the eye can travel along the visual pathway and terminate in parvalbumin cells.
“Accordingly, we showed that Otx2 injected in the eye can travel along this pathway and terminates in PV-cells (Sugiyama et al., 2008; Sugiyama et al., 2009).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
Subsequent Otx2 internalization increases intracellular Otx2 and parvalbumin-cell maturation, reflected by further parvalbumin expression and perineuronal net assembly, until a second threshold closes plasticity.
“Subsequent Otx2 internalization increases intracellular Otx2 and PV-cell maturation reflected by further PV expression and PNN assembly (Sugiyama et al., 2008) until a second threshold is reached that closes plasticity.”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
Parvalbumin-cell maturation in dark-reared animals is rescued by direct Otx2 infusion, leading to specific accumulation in parvalbumin cells and critical period opening.
“Instead, PV-cell maturation in dark-reared animals is rescued by direct Otx2 infusion leading to its specific accumulation in PV-cells and CP opening (Sugiyama et al., 2008).”
From Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity (2013) · cites this paper as Sugiyama et al., 2008
Otx2 expression coincides with both PV and PNN expression in the cortex during critical period plasticity.
“Otx2 expression coincides with both PV and PNN expression in the cortex during critical period plasticity (Sugiyama et al., 2008).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Sugiyama et al., 2008
Perineuronal nets regulate parvalbumin cell maturation through internalization of the homeoprotein Otx2, which is required for transcription, normal parvalbumin development, and critical period plasticity in the developing visual cortex.
“PNNs also regulate PV cell maturation via internalization of homeoprotein Otx2, which is needed for transcription, normal PV development and critical period plasticity in developing visual cortex (Sugiyama et al. 2008).”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Sugiyama et al. 2008
Otx2 signals maturation of parvalbumin-containing GABAergic interneurons, contributing to opening and possibly closure of the critical period.
“this homeoprotein signals the maturation of the parvalbumin-containing GABAergic interneurons, which contributes to the opening and possibly also the closure of the critical period”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Sugiyama et al., 2008
PNNs facilitate the capture and uptake of the transcription factor Otx2.
“PNNs also facilitate the capture and uptake of the transcription factor Otx2, which in turn promotes PVBC maturation as well as further PNN development (100, 173, 912, 1063).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1063]
Otx2 promotes PVBC maturation as well as further PNN development.
“PNNs also facilitate the capture and uptake of the transcription factor Otx2, which in turn promotes PVBC maturation as well as further PNN development (100, 173, 912, 1063).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1063]
Postnatal maturation of cortical inhibitory networks is needed to start the critical period.
“The maturation of cortical inhibitory networks in the postnatal brain is important for initiating this critical period (Fagiolini and Hensch, 2000; Sugiyama et al., 2008).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Sugiyama et al., 2008
Increasing BDNF or Otx2 to accelerate PV-cell maturation produces precocious plasticity.
“Acceleration of PV-cell maturation by over-expressing non-cell-autonomous factors, such as brain-derived neurotrophic factor (BDNF) or orthodenticle homeobox 2 (Otx2), induces precocious plasticity (Huang et al., 1999; Sugiyama et al., 2008).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Sugiyama et al., 2008
PNNs are linked to OTX2.
“PNNs have been linked to the transcription factor orthodenticle homeobox protein 2 (OTX2) (35)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [35]
OTX2 specifically accumulates in PV+ cells through exogenous transfer from the choroid plexus, the region where it is produced.
“Additionally, OTX2 has been shown to specifically accumulate in PV+ cells through exogenous transfer from the choroid plexus, the region where it is produced (35; 46).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [35]
OTX2 expression coincides with the maturation of PV+ cells and the closure of the critical period.
“Orthodenticle homeobox protein 2 (OTX2) is a transcription factor known to be important in the regulation of the critical period of plasticity in the visual cortex of developing mice (46) and its expression coincides with the maturation of PV+ cells and the closure of the critical period (35).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [35]
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InfluentialSelf-citationRemoving brakes on adult brain plasticity: From molecular to behavioral interventions
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Self-citationThe roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
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Animals lacking link protein have attenuated perineuronal nets and persistent plasticity
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“PNNs also attract the homeobox protein Otx2 to parvalbumin positive interneurons affecting their maturation and physiological properties (Sugiyama et al., 2008).”
BackgroundCritical period regulation across multiple timescales
Reh, R. K., Dias, B. G., Nelson, C. A., Kaufer, D., Werker, J. F., Kolb, B., Levine, J. D., & Hensch, T. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820836117 · Cited by 492 · see citing works
Self-citationBiosynthesis and function of chondroitin sulfate
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GABAergic Interneurons Shape the Functional Maturation of the Cortex
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Critical-Period Plasticity in the Visual Cortex
Levelt, C. N., & Hübener, M. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113813 · Cited by 402 · see citing works
Otx2 Binding to Perineuronal Nets Persistently Regulates Plasticity in the Mature Visual Cortex
Beurdeley, M., Spatazza, J., Lee, H. H. C., Sugiyama, S., Bernard, C., Di Nardo, A. A., Hensch, T. K., & Prochiantz, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0394-12.2012 · Cited by 398 · see citing works
“Otx2 persists throughout life in PV cells, and its capture is dependent on visual input (Sugiyama et al., 2008).”
BackgroundMethodInfluentialSelf-citationEarly life stress confers lifelong stress susceptibility in mice via ventral tegmental area OTX2
Peña, C. J., Kronman, H. G., Walker, D. M., Cates, H. M., Bagot, R. C., Purushothaman, I., Issler, O., Loh, Y.-H. E., Leong, T., Kiraly, D. D., et al. (2017) · Science · doi:10.1126/science.aan4491 · Cited by 394 · see citing works
Persistent cortical plasticity by upregulation of chondroitin 6-sulfation
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“In particular, maturation of a subset of inhibitory interneurons expressing the calcium-binding protein parvalbumin has been proposed to be crucial for defining the timing of the critical perio”
BackgroundDevelopment and critical period plasticity of the barrel cortex
Erzurumlu, R. S., & Gaspar, P. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08075.x · Cited by 344 · see citing works
“aggregates, parvalbumin-positive GABAergic neurons and embryonic homeoprotein, Otx2, reportedly regulate the timing of the critical period for ocular dominance plasticity in the visual cortex (Pizzorusso et al., 2002; Sugiyama et al., 2008).”
BackgroundReducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity
Harauzov, A., Spolidoro, M., DiCristo, G., De Pasquale, R., Cancedda, L., Pizzorusso, T., Viegi, A., Berardi, N., & Maffei, L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2233-09.2010 · Cited by 319 · see citing works
“…of cortical parvalbumin-positive GABAergic interneurons and promotes perineuronal net (PNN) formation; Otx2 is transported from the retina to the visual cortex in an activitydependent way, and it contributes to the regulation of visual cortex critical period plasticity (Sugiyama et al., 2008).”
BackgroundAutism: A “Critical Period” Disorder?
LeBlanc, J. J., & Fagiolini, M. (2011) · Neural Plasticity · doi:10.1155/2011/921680 · Cited by 301 · see citing works
“In the visual cortex, PV-cells mature in an experience-dependent manner, and dark-rearing delays their maturation as well as critical period expression [77, 78].”
InfluentialCortical Plasticity Induced by Inhibitory Neuron Transplantation
Southwell, D. G., Froemke, R. C., Alvarez-Buylla, A., Stryker, M. P., & Gandhi, S. P. (2010) · Science · doi:10.1126/science.1183962 · Cited by 271 · see citing works
Crosstalk between glia, extracellular matrix and neurons
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“…express the calcium binding protein parvalbumin (PV) by increasing the levels of growth factors (Huang et al., 1999; Hanover et al., 1999; Otx2: Sugiyama et al., 2008; Spatazza et al., 2013) or by removing cell adhesion (PSA: Di Cristo et al., 2007) or DNA binding proteins (MeCP2: Durand et…”
BackgroundSelf-citationNeuronal Plasticity: Beyond the Critical Period
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The impact of developmental timing for stress and recovery
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“For example, reductions of inhibitory neural activity in adulthood have increased visual plasticity in rodents (He et al., 2007; Sugiyama et al., 2008; Harauzov et al., 2010) and even restored visual function in ambly-”
BackgroundTargeting the neural extracellular matrix in neurological disorders
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The Cell-Intrinsic Requirement of Sox6 for Cortical Interneuron Development
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“These two latter properties of FS cells are crucial in regulating plasticity within the cortex (Pizzorusso et al., 2002; Sugiyama et al., 2008).”
Bidirectional plasticity in fast-spiking GABA circuits by visual experience
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Self-citationMechanisms of specificity in neuronal activity-regulated gene transcription
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BackgroundNMDA Receptor Regulation Prevents Regression of Visual Cortical Function in the Absence of Mecp2
Durand, S., Patrizi, A., Quast, K. B., Hachigian, L., Pavlyuk, R., Saxena, A., Carninci, P., Hensch, T. K., & Fagiolini, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.12.004 · Cited by 172 · see citing works
“Notably, sensory experience regulates the postnatal maturation of these PV circuits in visual cortex: dark-rearing from birth (DR) specifically reduces perisomatic inhibition (Katagiri et al., 2007; Sugiyama et al., 2008).”
Self-citationMarques-Smith, A., Lyngholm, D., Kaufmann, A.-K., Stacey, J. A., Hoerder-Suabedissen, A., Becker, E. B. E., Wilson, M. C., Molnár, Z., & Butt, S. J. B. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.015 · Cited by 173 · see citing works
Interneurons from Embryonic Development to Cell-Based Therapy
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Extracellular matrix abnormalities in schizophrenia
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The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders
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Early life nutrition and neural plasticity
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“Eventually, closure of the critical period is accompanied by the appearance of consolidating perineuronal nets, an extracellular matrix that wraps around parvalbuminsecreting basket cells (Celio, Spreafico, De Biasi, & Vitellaro-Zuccarello, 1998; Markram et al., 2004; Morishita & Hensch, 2008; Sugiyama et al., 2008).”
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Choroid-Plexus-Derived Otx2 Homeoprotein Constrains Adult Cortical Plasticity
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“Consistent with our previous work indicating an Otx2 requirement for PV expression and PNN assembly early in life (Sugiyama et al., 2008), a parallel decrease of PV (Figures 3B, 3G, 3K, and 3L; cell number: 74.”
InfluentialSelf-citationMiyata, S., & Kitagawa, H. (2017) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2017.06.010 · Cited by 171 · see citing works
“Conversely, blocking Otx2 function by either knocking down its expression or using specific antibodies reduces the formation of PNNs [140].”
BackgroundInfluentialDevelopment and specification of GABAergic cortical interneurons
Kelsom, C., & Lu, W. (2013) · Cell & Bioscience · doi:10.1186/2045-3701-3-19 · Cited by 171 · see citing works
“Orthodenticle homeobox 2 (Otx2) is a homeoprotein whose expression is required to both open and close a critical period of neural plasticity in the visual cortex of PV-expressing interneurons in mice [128,129].”
BackgroundToyoizumi, T., Miyamoto, H., Yazaki-Sugiyama, Y., Atapour, N., Hensch, T. K., & Miller, K. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.022 · Cited by 158 · see citing works
“Similarly, wild-type (WT) mice enter a CP prematurely upon early diazepam treatment (Fagiolini and Hensch, 2000; Fagiolini et al., 2004) or molecular interventions that promote early GABA circuit development (Hanover et al., 1999; Di Cristo et al., 2007; Sugiyama et al., 2008).”
BackgroundMethodInfluentialSelf-citationWorldwide trends in bilateral cochlear implantation
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Brain Plasticity and Disease: A Matter of Inhibition
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“Interestingly, recent studies suggest that PNNs facilitate the transfer of Otx2, accelerating maturation of the PV-positive interneurons that are necessary and sufficient to open, then close, a critical period of plasticity in the developing mouse visual cortex (Sugiyama et al., 2008; Beurdeley et al., 2012).”
BackgroundInfluentialMechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
“1b K + channels specifically in these target neurons (Sugiyama et al., 2008).”
BackgroundWiring the Brain: The Biology of Neuronal GuidancePreprint
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“Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a001917 3 autonomously during brain development (Sugiyama et al. 2008).”
BackgroundInfluentialThe homeobox gene Otx2 in development and disease
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Perineuronal nets in brain physiology and disease
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Self-citationExtracellular Movement of Signaling Molecules
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BackgroundChondroitin sulfates and their binding molecules in the central nervous system
Djerbal, L., Lortat-Jacob, H., & Kwok, J. (2017) · Glycoconjugate Journal · doi:10.1007/s10719-017-9761-z · Cited by 144 · see citing works
“During this period, Otx2 is transferred from choroid plexus into the visual cortex and accumulates on the PNN of PVcells [164].”
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Experience-dependent regulation of NG2 progenitors in the developing barrel cortex
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The transcription factor Otx2 regulates choroid plexus development and function
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“Notably, the Otx2 protein itself is also secreted (Sugiyama et al., 2008) and might hence be present in different amounts in the CSF from Gdf7-Cre/Otx2fl/fl embryos compared with control embryos.”
BackgroundDirect Detection of Biotinylated Proteins by Mass Spectrometry
Schiapparelli, L., McClatchy, D. B., Liu, H.-H., Sharma, P., Yates, J. R., & Cline, H. T. (2014) · Journal of Proteome Research · doi:10.1021/pr5002862 · Cited by 127 · see citing works
Progressive maturation of silent synapses governs the duration of a critical period
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An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity
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“Neural activity drives the release of developmental regulators, which promote PV neuron maturation, including brain-derived neurotrophic factor (BDNF) [14], neuronal pentraxins (NARP) [15], neuregulins [16], and orthodenticle homeobox 2 (Otx2) [17].”
InfluentialImpact of Early Life Stress on Reward Circuit Function and Regulation
Hanson, J. L., Williams, A. V., Bangasser, D. A., & Peña, C. J. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.744690 · Cited by 123 · see citing works
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Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity
Sun, Y., Ikrar, T., Davis, M. F., Gong, N., Zheng, X., Luo, Z. D., Lai, C., Mei, L., Holmes, T. C., Gandhi, S. P., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.033 · Cited by 117 · see citing works
“Previous studies have identified that signaling through neurotrophins (nerve growth factor and brain-derived neurotrophic factor), insulin-like growth factor-1, transcriptional control by OTX2, maturation of the extracellular matrix, and synapse formation molecules contribute to regulation of visual cortical plasticit…”
BackgroundExtracellular Engrailed Participates in the Topographic Guidance of Retinal Axons In Vivo
Wizenmann, A., Brunet, I., Lam, J. S. Y., Sonnier, L., Beurdeley, M., Zarbalis, K. S., Weisenhorn, D. M. V., Weinl, C., Dwivedy, A., Joliot, A., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.018 · Cited by 117 · see citing works
Self-citationGABAergic inhibition in visual cortical plasticity
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“Sugiyama et al. (2008) have demonstrated that another factor might impinge on IGI development to promote CP onset.”
Nowicka, D., Soulsby, S., Skangiel‐Kramska, J., & Glazewski, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06996.x · Cited by 110 · see citing works
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BackgroundObligatory Role for the Immediate Early Gene NARP in Critical Period Plasticity
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“For example, promotion of the early maturation of inhibitory synapses onto principle neurons induces a precocious initiation of the critical period (Huang et al., 1999; Di Cristo et al., 2007; Sugiyama et al., 2008).”
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“Especially the maturation of synapses formed by parvalbumin (PV) positive interneurons seems to determine the start of the sensitive period [3].”
BackgroundNatural Restoration of Critical Period Plasticity in the Juvenile and Adult Primary Auditory Cortex
Zhou, X., Panizzutti, R., de Villers‐Sidani, E., Madeira, C., & Merzenich, M. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6470-10.2011 · Cited by 114 · see citing works
“Recent studies also argue that the embryonic Otx2 homeoprotein controls changes in parvalbumin GABAA neurons that may open and close the critical period in the visual cortex (Sugiyama et al., 2008).”
BackgroundNetwork homeostasis: a matter of coordination
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BackgroundClock Genes Control Cortical Critical Period Timing
Kobayashi, Y., Ye, Z., & Hensch, T. K. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.036 · Cited by 99 · see citing works
Self-citationFunctions of Chondroitin Sulfate and Heparan Sulfate in the Developing Brain
Maeda, N., Ishii, M., Nishimura, K., & Kamimura, K. (2010) · Neurochemical Research · doi:10.1007/s11064-010-0324-y · Cited by 105 · see citing works
Age-dependent effect of hearing loss on cortical inhibitory synapse function
Takesian, A. E., Kotak, V. C., & Sanes, D. H. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00515.2011 · Cited by 105 · see citing works
Axon-Seq Decodes the Motor Axon Transcriptome and Its Modulation in Response to ALS
Nijssen, J., Benitez, J. A., Hoogstraaten, R. I., Kee, N., & Hedlund, E. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.11.005 · Cited by 98 · see citing works
“Some TFs were recently shown to function outside the soma and to be important in neuronal circuitry plasticity, axon pathfinding, and neuroprotection (Sugiyama et al., 2008; Torero Ibad et al., 2011; Wizenmann et al., 2009).”
BackgroundYamada, J., Ohgomori, T., & Jinno, S. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12792 · Cited by 99 · see citing works
“Maturation of the PV+ neuron network that controls plasticity onset is regulated by selective re-expression of embryonic orthodenticle homeobox 2 (Otx2) in the visual cortex (Sugiyama et al., 2008).”
BackgroundInfluentialOtx2-PNN interaction to regulate cortical plasticity
Bernard, C., & Prochiantz, A. (2016) · Neural Plasticity · doi:10.1155/2016/7931693 · Cited by 102 · see citing works
“Interestingly, Otx2 conditional knockdown heterozygous mice have a delayed onset of ocular dominance critical period, suggesting that a 50% reduction in Otx2 protein is sufficient to alter PV-cell maturation [32].”
BackgroundInfluentialSelf-citationPatrizi, A., Picard, N., Simon, A. J., Gunner, G., Centofante, E., Andrews, N. A., & Fagiolini, M. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.018 · Cited by 100 · see citing works
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“Several manipulations of inhibition have been shown to stimulate plasticity in mouse visual cortex up to postnatal day 70 (P70) (Beurdeley et al., 2012; Fagiolini and Hensch, 2000; Kuhlman et al., 2013; Southwell et al., 2010; Stephany et al., 2014; Sugiyama et al., 2008).”
Adult cortical plasticity following injury: Recapitulation of critical period mechanisms?
Nahmani, M., & Turrigiano, G. G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.029 · Cited by 95 · see citing works
“…level of GABAergic inhibition (Hensch et al., 1998; Iwai et al., 2003; Fagiolini et al., 2004), likely originating from the maturation of FS interneuron connections (Huang et al., 1999; Pizzorusso et al., 2002; Chattopadhyaya et al., 2004; Maffei et al., 2006, 2010; Sugiyama et al., 2008).”
InfluentialProlonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons
Morishita, H., Cabungcal, J.-H., Chen, Y., Do, K. Q., & Hensch, T. K. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.026 · Cited by 92 · see citing works
Self-citationPerineuronal nets and schizophrenia: The importance of neuronal coatings
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.03.018 · Cited by 95 · see citing works
Origins of strabismus and loss of binocular vision
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Nabel, E. M., & Morishita, H. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00146 · Cited by 85 · see citing works
Baker, K., Gray, A. R., & Richardson, R. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000203 · Cited by 89 · see citing works
Bozzelli, P. L., Alaiyed, S., Kim, E., Villapol, S., & Conant, K. E. (2018) · Neural Plasticity · doi:10.1155/2018/5735789 · Cited by 90 · see citing works
“Expression of PNN components by PV neurons in particular is intriguing in a way that it may be regulated in significant part by the homeobox protein orthodenticle homeobox-2 (Otx2) [32].”
BackgroundGABA through the Ages: Regulation of Cortical Function and Plasticity by Inhibitory Interneurons
Lehmann, K., Steinecke, A., & Bolz, J. (2012) · Neural Plasticity · doi:10.1155/2012/892784 · Cited by 89 · see citing works
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“…barrier to structural plasticity, the regu- lation of neuronal excitability via the accumulation of cations and other effectors (Härtig et al., 1999; Sugiyama et al., 2008), the protection of neurons from oxidative stress (Cabungcal et al., 2013) and the sequestration of molecules that inhibit…”
Larsen, B., Sydnor, V. J., Keller, A. S., Yeo, B. T. T., & Satterthwaite, T. D. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.07.007 · Cited by 90 · see citing works
Cortical plasticity induced by transplantation of embryonic somatostatin or parvalbumin interneurons
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The Chemorepulsive Protein Semaphorin 3A and Perineuronal Net-Mediated Plasticity
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A Sweet Talk: The Molecular Systems of Perineuronal Nets in Controlling Neuronal Communication
Spijker, H. M. V. ‘., & Kwok, J. C. F. (2017) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2017.00033 · Cited by 82 · see citing works
“When Otx2 reaches the visual cortex, it binds the PNNs and enters the neuron to regulate maturation and thus affect plasticity (Sugiyama et al., 2008).”
BackgroundTranscriptome of embryonic and neonatal mouse cortex by high-throughput RNA sequencing
Han, X., Wu, X., Chung, W.-Y., Li, T., Nekrutenko, A., Altman, N. S., Chen, G., & Ma, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902417106 · Cited by 83 · see citing works
Social Origins of Developmental Risk for Mental and Physical Illness
Cameron, J. L., Eagleson, K. L., Fox, N. A., Hensch, T. K., & Levitt, P. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1822-17.2017 · Cited by 81 · see citing works
“Factors that may accelerate or delay GABA circuit maturation, such as BDNF (Huang et al., 1999; Bath et al., 2013), Clock gene expression (Kobayashi et al., 2015; Marco et al., 2016), Otx2 (Sugiyama et al., 2008; Pena et al., 2017), or the GUCY1A3 mentioned above (Sabatini et al., 2007), may be vulnerable to ELS, pred…”
BackgroundSelf-citationGenetic Otx2 mis-localization delays critical period plasticity across brain regions
Lee, H. H. C., Bernard, C., Ye, Z., Acampora, D., Simeone, A., Prochiantz, A., Di Nardo, A. A., & Hensch, T. K. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.1 · Cited by 82 · see citing works
Self-citation
- Authors
- Sugiyama, S., Di Nardo, A. A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A., & Hensch, T. K.
- Affiliations
- Boston Children's Hospital (US)
- RIKEN (JP)
- Osaka Women's and Children's Hospital (JP)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Prochiantz, Alain
- Hensch, Takao K.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2008-08
- Volume
- 134
- Issue
- 3
- Pages
- 508-520
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2150947848
- Cited by
- 491
- References
- 76
- Citations by year
- 2026: 11 · 2025: 23 · 2024: 22 · 2023: 23 · 2022: 16 · 2021: 32 · 2020: 33 · 2019: 25 · 2018: 26 · 2017: 31 · 2016: 20 · 2015: 38 · 2014: 42 · 2013: 41 · 2012: 28
- FWCI
- 8.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1847 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Otx2, homeoproteins, parvalbumin interneurons, visual cortex, critical period, ocular dominance, visual experience, GABAergic circuits, neural circuit development
- MeSH terms
- Animals, Humans, Interneurons, Neuronal Plasticity, Parvalbumins, Recombinant Proteins, Sensory Deprivation, Visual Cortex, Visual Pathways, Mice, Otx Transcription Factors
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