Astrocytes close the mouse critical period for visual plasticity

Science ◽  
2021 ◽  
Vol 373 (6550) ◽  
pp. 77-81 ◽  
Author(s):  
Jérôme Ribot ◽  
Rachel Breton ◽  
Charles-Félix Calvo ◽  
Julien Moulard ◽  
Pascal Ezan ◽  
...  
Keyword(s):  
Extracellular Matrix ◽  
Visual Cortex ◽  
Neurodevelopmental Disorders ◽  
Critical Period ◽  
Critical Periods ◽  
Cellular Processes ◽  
Brain Circuits ◽  
Guanosine Triphosphatase ◽  
Mouse Visual Cortex ◽  
Metalloproteinase 9

Brain postnatal development is characterized by critical periods of experience-dependent remodeling of neuronal circuits. Failure to end these periods results in neurodevelopmental disorders. The cellular processes defining critical-period timing remain unclear. Here, we show that in the mouse visual cortex, astrocytes control critical-period closure. We uncover the underlying pathway, which involves astrocytic regulation of the extracellular matrix, allowing interneuron maturation. Unconventional astrocyte connexin signaling hinders expression of extracellular matrix–degrading enzyme matrix metalloproteinase 9 (MMP9) through RhoA–guanosine triphosphatase activation. Thus, astrocytes not only influence the activity of single synapses but also are key elements in the experience-dependent wiring of brain circuits.

scholarly journals Astrocytes close the critical period for visual plasticity

2020 ◽  
Author(s):  
Jérôme Ribot ◽  
Rachel Breton ◽  
Charles-Félix Calvo ◽  
Julien Moulard ◽  
Pascal Ezan ◽  
...  
Keyword(s):  
Critical Period ◽  
Critical Periods ◽  
Inhibitory Circuits ◽  
Cellular Processes ◽  
Rhoa Gtpase ◽  
Cellular Target ◽  
The Matrix ◽  
Efficient Information ◽  
Connexin 30 ◽  
Mouse Visual Cortex

Summary paragraphBrain postnatal development is characterized by critical periods of experience-dependent remodeling1,2. Termination of these periods of intense plasticity is associated with settling of neuronal circuits, allowing for efficient information processing3. Failure to end critical periods thus results in neurodevelopmental disorders4,5. Yet, the cellular processes defining the timing of these developmental periods remain unclear. Here we show in the mouse visual cortex that astrocytes control the closure of the critical period. We uncover a novel underlying pathway involving regulation of the extracellular matrix that allows interneurons maturation via an unconventional astroglial connexin signaling. We find that timing of the critical period closure is controlled by a marked developmental upregulation of the astroglial protein connexin 30 that inhibits expression of the matrix degrading enzyme MMP9 through the RhoA-GTPase signaling pathway. Our results thus demonstrate that astrocytes not only influence activity and plasticity of single synapses, but are also key elements in the experience-dependent wiring of brain developing circuits. This work, by revealing that astrocytes promote the maturation of inhibitory circuits, hence provide a new cellular target to alleviate malfunctions associated to impaired closure of critical periods.

scholarly journals Temporal patterns of fluoxetine-induced plasticity in the mouse visual cortex

2018 ◽  
Author(s):  
Anna Steinzeig ◽  
Cecilia Cannarozzo ◽  
Eero Castren
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Ocular Dominance ◽  
Temporal Patterns ◽  
Monocular Deprivation ◽  
Adult Brain ◽  
Postnatal Life ◽  
Critical Periods ◽  
Mouse Visual Cortex

Heightened neuronal plasticity expressed during early postnatal life has been thought to permanently decline once critical periods have ended. For example, monocular deprivation is able to shift ocular dominance in the mouse visual cortex during the first months of life, but this effect is lost later in life. However, various treatments such as the antidepressant fluoxetine can reactivate a critical period-like plasticity in the adult brain. When monocular deprivation is supplemented with chronic fluoxetine administration, a major shift in ocular dominance is produced after the critical period has ended. In the current study, we characterized the temporal patterns of fluoxetine-induced plasticity in the adult mouse visual cortex, using in vivo optical imaging. We found that artificially-induced plasticity in ocular dominance extended beyond the duration of the naturally occurring critical period, and continued as long as fluoxetine was administered. However, this fluoxetine-induced plasticity period ended as soon as the drug was not given. Taken together, our data highlights how a combination of pharmacological treatment and environmental change could be used to improve strategies in antidepressant therapy in humans.

scholarly journals Otx2-PNN Interaction to Regulate Cortical Plasticity

2016 ◽  
Vol 2016 ◽  
pp. 1-7 ◽  
Author(s):  
Clémence Bernard ◽  
Alain Prochiantz
Keyword(s):  
Extracellular Matrix ◽  
Visual Cortex ◽  
Binocular Vision ◽  
Critical Period ◽  
Cortical Plasticity ◽  
Inhibitory Interneurons ◽  
Perineuronal Nets ◽  
Critical Periods ◽  
Cortical Function ◽  
Parvalbumin Interneurons

The ability of the environment to shape cortical function is at its highest during critical periods of postnatal development. In the visual cortex, critical period onset is triggered by the maturation of parvalbumin inhibitory interneurons, which gradually become surrounded by a specialized glycosaminoglycan-rich extracellular matrix: the perineuronal nets. Among the identified factors regulating cortical plasticity in the visual cortex, extracortical homeoprotein Otx2 is transferred specifically into parvalbumin interneurons and this transfer regulates both the onset and the closure of the critical period of plasticity for binocular vision. Here, we review the interaction between the complex sugars of the perineuronal nets and homeoprotein Otx2 and how this interaction regulates cortical plasticity during critical period and in adulthood.

scholarly journals Emerging Roles of Synapse Organizers in the Regulation of Critical Periods

2019 ◽  
Vol 2019 ◽  
pp. 1-9 ◽  
Author(s):  
Adema Ribic ◽  
Thomas Biederer
Keyword(s):  
Visual Cortex ◽  
Neurodevelopmental Disorders ◽  
Critical Period ◽  
Transmembrane Proteins ◽  
Synaptic Cleft ◽  
Molecular Pathways ◽  
Critical Periods ◽  
Synaptic Specificity ◽  
Structural And Functional Properties ◽  
Developmental Windows

Experience remodels cortical connectivity during developmental windows called critical periods. Experience-dependent regulation of synaptic strength during these periods establishes circuit functions that are stabilized as critical period plasticity wanes. These processes have been extensively studied in the developing visual cortex, where critical period opening and closure are orchestrated by the assembly, maturation, and strengthening of distinct synapse types. The synaptic specificity of these processes points towards the involvement of distinct molecular pathways. Attractive candidates are pre- and postsynaptic transmembrane proteins that form adhesive complexes across the synaptic cleft. These synapse-organizing proteins control synapse development and maintenance and modulate structural and functional properties of synapses. Recent evidence suggests that they have pivotal roles in the onset and closure of the critical period for vision. In this review, we describe roles of synapse-organizing adhesion molecules in the regulation of visual critical period plasticity and we discuss the potential they offer to restore circuit functions in amblyopia and other neurodevelopmental disorders.

Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats

1984 ◽  
Vol 52 (5) ◽  
pp. 941-960 ◽  
Author(s):  
L. Tong ◽  
R. E. Kalil ◽  
P. D. Spear
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Ocular Dominance ◽  
Direction Selectivity ◽  
Visual Area ◽  
Critical Periods ◽  
Cortex Lesion ◽  
Thalamic Projections ◽  
Adult Cats ◽  
Visual Cortical

Previous experiments have found that neurons in the cat's lateral suprasylvian (LS) visual area of cortex show functional compensation following removal of visual cortical areas 17, 18, and 19 on the day of birth. Correspondingly, an enhanced retino-thalamic pathway to LS cortex develops in these cats. The present experiments investigated the critical periods for these changes. Unilateral lesions of areas 17, 18, and 19 were made in cats ranging in age from 1 day postnatal to 26 wk. When the cats were adult, single-cell recordings were made from LS cortex ipsilateral to the lesion. In addition, transneuronal autoradiographic methods were used to trace the retino-thalamic projections to LS cortex in many of the same animals. Following lesions in 18- and 26-wk-old cats, there is a marked reduction in direction-selective LS cortex cells and an increase in cells that respond best to stationary flashing stimuli. These results are similar to those following visual cortex lesions in adult cats. In contrast, the percentages of cells with these properties are normal following lesions made from 1 day to 12 wk of age. Thus the critical period for development of direction selectivity and greater responses to moving than to stationary flashing stimuli in LS cortex following a visual cortex lesion ends between 12 and 18 wk of age. Following lesions in 26-wk-old cats, there is a decrease in the percentage of cells that respond to the ipsilateral eye, which is similar to results following visual cortex lesions in adult cats. However, ocular dominance is normal following lesions made from 1 day to 18 wk of age. Thus the critical period for development of responses to the ipsilateral eye following a lesion ends between 18 and 26 wk of age. Following visual cortex lesions in 2-, 4-, or 8-wk-old cats, about 30% of the LS cortex cells display orientation selectivity to elongated slits of light. In contrast, few or no cells display this property in normal adult cats, cats with lesions made on the day of birth, or cats with lesions made at 12 wk of age or later. Thus an anomalous property develops for many LS cells, and the critical period for this property begins later (between 1 day and 2 wk) and ends earlier (between 8 and 12 wk) than those for other properties.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals BDNF Regulates the Maturation of Inhibition and the Critical Period of Plasticity in Mouse Visual Cortex

Cell ◽  
1999 ◽  
Vol 98 (6) ◽  
pp. 739-755 ◽  
Author(s):  
Z.Josh Huang ◽  
Alfredo Kirkwood ◽  
Tommaso Pizzorusso ◽  
Vittorio Porciatti ◽  
Bernardo Morales ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Mouse Visual Cortex

scholarly journals Critical periods in amblyopia

2018 ◽  
Vol 35 ◽  
Author(s):  
TAKAO K. HENSCH ◽  
ELIZABETH M. QUINLAN
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Molecular Mechanisms ◽  
Ocular Dominance ◽  
Molecular Genetic ◽  
Monocular Deprivation ◽  
Critical Periods ◽  
Developmental Constraints ◽  
Early Postnatal Development ◽  
Visual Cortical

AbstractThe shift in ocular dominance (OD) of binocular neurons induced by monocular deprivation is the canonical model of synaptic plasticity confined to a postnatal critical period. Developmental constraints on this plasticity not only lend stability to the mature visual cortical circuitry but also impede the ability to recover from amblyopia beyond an early window. Advances with mouse models utilizing the power of molecular, genetic, and imaging tools are beginning to unravel the circuit, cellular, and molecular mechanisms controlling the onset and closure of the critical periods of plasticity in the primary visual cortex (V1). Emerging evidence suggests that mechanisms enabling plasticity in juveniles are not simply lost with age but rather that plasticity is actively constrained by the developmental up-regulation of molecular ‘brakes’. Lifting these brakes enhances plasticity in the adult visual cortex, and can be harnessed to promote recovery from amblyopia. The reactivation of plasticity by experimental manipulations has revised the idea that robust OD plasticity is limited to early postnatal development. Here, we discuss recent insights into the neurobiology of the initiation and termination of critical periods and how our increasingly mechanistic understanding of these processes can be leveraged toward improved clinical treatment of adult amblyopia.

scholarly journals Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse

2005 ◽  
Vol 22 (5) ◽  
pp. 685-691 ◽  
Author(s):  
JIANHUA CANG ◽  
VALERY A. KALATSKY ◽  
SIEGRID LÖWEL ◽  
MICHAEL P. STRYKER
Keyword(s):  
Visual Cortex ◽  
Optical Imaging ◽  
Critical Period ◽  
Cortical Plasticity ◽  
Ocular Dominance ◽  
Screening Method ◽  
Intrinsic Signals ◽  
Intrinsic Signal ◽  
The Mean ◽  
Mouse Visual Cortex

The responses of cells in the visual cortex to stimulation of the two eyes changes dramatically following a period of monocular visual deprivation (MD) during a critical period in early life. This phenomenon, referred to as ocular dominance (OD) plasticity, is a widespread model for understanding cortical plasticity. In this study, we designed stimulus patterns and quantification methods to analyze OD in the mouse visual cortex using optical imaging of intrinsic signals. Using periodically drifting bars restricted to the binocular portion of the visual field, we obtained cortical maps for both contralateral (C) and ipsilateral (I) eyes and computed OD maps as (C − I)/(C + I). We defined the OD index (ODI) for individual animals as the mean of the OD map. The ODI obtained from an imaging session of less than 30 min gives reliable measures of OD for both normal and monocularly deprived mice under Nembutal anesthesia. Surprisingly, urethane anesthesia, which yields excellent topographic maps, did not produce consistent OD findings. Normal Nembutal-anesthetized mice have positive ODI (0.22 ± 0.01), confirming a contralateral bias in the binocular zone. For mice monocularly deprived during the critical period, the ODI of the cortex contralateral to the deprived eye shifted negatively towards the nondeprived, ipsilateral eye (ODI after 2-day MD: 0.12 ± 0.02, 4-day: 0.03 ± 0.03, and 6- to 7-day MD: −0.01 ± 0.04). The ODI shift induced by 4-day MD appeared to be near maximal, consistent with previous findings using single-unit recordings. We have thus established optical imaging of intrinsic signals as a fast and reliable screening method to study OD plasticity in the mouse.

scholarly journals Optimization of Somatic Inhibition at Critical Period Onset in Mouse Visual Cortex

Neuron ◽  
2007 ◽  
Vol 53 (6) ◽  
pp. 805-812 ◽  
Author(s):  
Hiroyuki Katagiri ◽  
Michela Fagiolini ◽  
Takao K. Hensch
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Mouse Visual Cortex ◽  
Somatic Inhibition
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