Activity-dependent modulation of synapse-regulating genes in astrocytes

Astrocytes regulate the formation and function of neuronal synapses via multiple signals, however, what controls regional and temporal expression of these signals during development is unknown. We determined the expression profile of astrocyte synapse-regulating genes in the developing mouse visual cortex, identifying astrocyte signals that show differential temporal and layer-enriched expression. These patterns are not intrinsic to astrocytes, but regulated by visually-evoked neuronal activity, as they are absent in mice lacking glutamate release from thalamocortical terminals. Consequently, synapses remain immature. Expression of synapse-regulating genes and synaptic development are also altered when astrocyte signaling is blunted by diminishing calcium release from astrocyte stores. Single nucleus RNA sequencing identified groups of astrocytic genes regulated by neuronal and astrocyte activity, and a cassette of genes that show layer-specific enrichment. Thus, the development of cortical circuits requires coordinated signaling between astrocytes and neurons, highlighting astrocytes as a target to manipulate in neurodevelopmental disorders.

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Activity-Dependent Modulation of Synapse-Regulating Genes in Astrocytes

10.1101/2020.12.30.424365 ◽

2020 ◽

Author(s):

I Farhy-Tselnicker ◽

MM Boisvert ◽

H Liu ◽

C Dowling ◽

GA Erikson ◽

...

Keyword(s):

Calcium Release ◽

Glutamate Release ◽

Cortical Circuits ◽

Temporal Expression ◽

Synaptic Development ◽

Neuronal Synapses ◽

Single Nucleus ◽

And Function ◽

Mouse Visual Cortex ◽

Activity Dependent

SummaryAstrocytes regulate the formation and function of neuronal synapses via multiple signals, however, what controls regional and temporal expression of these signals during development is unknown. We determined the expression profile of astrocyte synapse-regulating genes in the developing mouse visual cortex, identifying astrocyte signals that show differential temporal and layer-enriched expression. These patterns are not intrinsic to astrocytes, but regulated by visually-evoked neuronal activity, as they are absent in mice lacking glutamate release from thalamocortical terminals. Consequently, synapses remain immature. Expression of synapse-regulating genes and synaptic development are also altered when astrocyte signaling is blunted by diminishing calcium release from astrocyte stores. Single nucleus RNA sequencing identified groups of astrocytic genes regulated by neuronal and astrocyte activity, and a cassette of genes that show layer-specific enrichment. Thus, the development of cortical circuits requires coordinated signaling between astrocytes and neurons, identifying astrocytes as a target to manipulate in neurodevelopmental disorders.

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Modulation of Synaptic Plasticity by Glutamatergic Gliotransmission: A Modeling Study

Neural Plasticity ◽

10.1155/2016/7607924 ◽

2016 ◽

Vol 2016 ◽

pp. 1-30 ◽

Cited By ~ 32

Author(s):

Maurizio De Pittà ◽

Nicolas Brunel

Keyword(s):

Synaptic Plasticity ◽

Glutamate Release ◽

Spike Timing ◽

Biophysical Model ◽

Dependent Manner ◽

Inward Currents ◽

Functional Relevance ◽

And Function ◽

Activity Dependent

Glutamatergic gliotransmission, that is, the release of glutamate from perisynaptic astrocyte processes in an activity-dependent manner, has emerged as a potentially crucial signaling pathway for regulation of synaptic plasticity, yet its modes of expression and function in vivo remain unclear. Here, we focus on two experimentally well-identified gliotransmitter pathways, (i) modulations of synaptic release and (ii) postsynaptic slow inward currents mediated by glutamate released from astrocytes, and investigate their possible functional relevance on synaptic plasticity in a biophysical model of an astrocyte-regulated synapse. Our model predicts that both pathways could profoundly affect both short- and long-term plasticity. In particular, activity-dependent glutamate release from astrocytes could dramatically change spike-timing-dependent plasticity, turning potentiation into depression (and vice versa) for the same induction protocol.

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Activity-dependent proteolytic cleavage of cell adhesion molecules regulates excitatory synaptic development and function

Neuroscience Research ◽

10.1016/j.neures.2016.12.003 ◽

2017 ◽

Vol 116 ◽

pp. 60-69 ◽

Cited By ~ 14

Author(s):

Sivapratha Nagappan-Chettiar ◽

Erin M. Johnson-Venkatesh ◽

Hisashi Umemori

Keyword(s):

Cell Adhesion ◽

Adhesion Molecules ◽

Cell Adhesion Molecules ◽

Proteolytic Cleavage ◽

Synaptic Development ◽

And Function ◽

Activity Dependent

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Regulation of perineuronal nets in the adult cortex by the electrical activity of parvalbumin interneurons

10.1101/671719 ◽

2019 ◽

Cited By ~ 2

Author(s):

Gabrielle Devienne ◽

Sandrine Picaud ◽

Ivan Cohen ◽

Juliette Piquet ◽

Ludovic Tricoire ◽

...

Keyword(s):

Adult Mouse ◽

High Plasticity ◽

Critical Periods ◽

Cortical Circuits ◽

Perineuronal Net ◽

Parvalbumin Interneurons ◽

Mouse Visual Cortex ◽

Activity Dependent ◽

Dependent Mechanism

ABSTRACTPerineuronal net (PNN) accumulation around parvalbumin-expressing (PV) inhibitory interneurons marks the closure of critical periods of high plasticity, whereas PNN removal reinstates juvenile plasticity in the adult cortex. Using targeted chemogenetic in vivo approaches in the adult mouse visual cortex, we found that transient electrical silencing of PV interneurons, directly or through inhibition of local excitatory neurons, induced PNN regression. Conversely, excitation of either neuron types did not reduce the PNN. We also observed that chemogenetically inhibited PV interneurons exhibited reduced PNN compared to their untransduced neighbors, and confirmed that single PV interneurons express multiple genes enabling cell-autonomous control of their own PNN density. Our results indicate that PNNs are dynamically regulated in the adult by PV neurons acting as sensors of their local microcircuit activities. PNN regulation provides individual PV neurons with an activity-dependent mechanism to control the local remodeling of adult cortical circuits.

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Faculty Opinions recommendation of Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.13371088.14741249 ◽

2011 ◽

Author(s):

David Sweatt ◽

Faraz Sultan

Keyword(s):

Nervous System ◽

System Development ◽

Nervous System Development ◽

Genome Wide ◽

And Function ◽

Activity Dependent

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Spatio-temporal expression of Prospero is finely tuned to allow the correct development and function of the nervous system in Drosophila melanogaster

Developmental Biology ◽

10.1016/j.ydbio.2006.12.016 ◽

2007 ◽

Vol 304 (1) ◽

pp. 62-74 ◽

Cited By ~ 3

Author(s):

Laure Guenin ◽

Yaël Grosjean ◽

Stéphane Fraichard ◽

Angel Acebes ◽

Fawzia Baba-Aissa ◽

...

Keyword(s):

Nervous System ◽

Drosophila Melanogaster ◽

Temporal Expression ◽

Spatio Temporal ◽

And Function

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Evidence for Activity-Dependent Modulation of Sensory-Terminal Excitability in Spindles by Glutamate Release From Synaptic-Like Vesicles

Advances in Experimental Medicine and Biology - Sensorimotor Control of Movement and Posture ◽

10.1007/978-1-4615-0713-0_2 ◽

2002 ◽

pp. 13-18 ◽

Cited By ~ 16

Author(s):

Robert W. Banks ◽

Guy S. Bewick ◽

Brian Reid ◽

Christine Richardson

Keyword(s):

Glutamate Release ◽

Activity Dependent ◽

Terminal Excitability

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Variations in photoreceptor throughput to mouse visual cortex and the unique effects on tuning

10.1101/2020.11.03.366682 ◽

2020 ◽

Cited By ~ 1

Author(s):

I. Rhim ◽

G. Coello-Reyes ◽

I. Nauhaus

Keyword(s):

Visual Cortex ◽

Visual Field ◽

Adaptive Filtering ◽

Frequency Tuning ◽

Cortical Circuits ◽

Spatial Frequency Tuning ◽

Upper Visual Field ◽

Spatio Temporal ◽

Mouse Visual Cortex ◽

Common Laboratory

ABSTRACTVisual input to primary visual cortex (V1) depends on highly adaptive filtering in the retina. In turn, isolation of V1 computations to study cortical circuits requires control over retinal adaption and its corresponding spatio-temporal-chromatic output. Here, we first measure the balance of input to V1 from the three main photoreceptor opsins – M-opsin, S-opsin, and rhodopsin – as a function of light adaption and retinotopy. Results show that V1 is rod-mediated in common laboratory settings, yet cone-mediated in natural daylight, as evidenced by exclusive sensitivity to UV wavelengths via cone S-opsin in the upper visual field. Next, we show that cone-mediated V1 responds to 2.5-fold higher temporal frequencies than rod-mediated V1. Furthermore, cone-mediated V1 has smaller RFs, yet similar spatial frequency tuning. V1 responses in rod-deficient (Gnat1−/−) mice confirm that the effects are due to differences in photoreceptor contribution. This study provides foundation for using mouse V1 to study cortical circuits.

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