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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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In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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 the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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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Metadata
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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