Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo

Takata, Norio; Mishima, Tatsuya; Hisatsune, Chihiro; Nagai, Torao; Ebisui, Etsuko; Mikoshiba, Katsuhiko; Hirase, Hajime

doi:10.1016/j.neures.2011.07.1142

Cited by 70 publications

(131 citation statements)

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“…7). Astrocyte populations throughout the cortex are known to display widespread, coordinated calcium signaling and synchronicity, particularly within somata, in response to norepinephrine from the locus coeruleus (Ding et al 2013;Paukert et al 2014) and acetylcholine from the nucleus basalis (Takata et al 2011). In the present study, we did not observe sensory-stimulus evoked calcium signals outside the corresponding somatosensory region (Supplementary Fig.…”

Section: Discussioncontrasting

confidence: 45%

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

et al. 2016

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Localized, heterogeneous calcium transients occur throughout astrocytes, but the characteristics and long-term stability of these signals, particularly in response to sensory stimulation, remain unknown. Here, we used a genetically encoded calcium indicator and an activity-based image analysis scheme to monitor astrocyte calcium activity in vivo. We found that different subcellular compartments (processes, somata, and endfeet) displayed distinct signaling characteristics. Closer examination of individual signals showed that sensory stimulation elevated the number of specific types of calcium peaks within astrocyte processes and somata, in a cortical layer-dependent manner, and that the signals became more synchronous upon sensory stimulation. Although mice genetically lacking astrocytic IP3R-dependent calcium signaling (Ip3r2−/−) had fewer signal peaks, the response to sensory stimulation was sustained, suggesting other calcium pathways are also involved. Long-term imaging of astrocyte populations revealed that all compartments reliably responded to stimulation over several months, but that the location of the response within processes may vary. These previously unknown characteristics of subcellular astrocyte calcium signals provide new insights into how astrocytes may encode local neuronal circuit activity. AbstractLocalized, heterogeneous calcium transients occur throughout astrocytes, but the characteristics and

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Section: Discussioncontrasting

confidence: 45%

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

et al. 2016

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“…We generally assume that our mind is dictated solely by the activity of neurons. Contrary to this prevailing notion, recent evidence proposed a potential role of glia in actively participating in the neural information processing (1,(12)(13)(14)(15). In this study, we directly demonstrate that signals initiated from glial cells can drive neuronal activity and animal behavior.…”

Section: Discussionmentioning

confidence: 47%

“…S1). Release of transmitter from glia (gliotransmitter) has been demonstrated in several brain areas (12)(13)(14)(15)(16) and we sought to address whether such gliotransmitter could mediate glia-to-neuron communication in the cerebellum.…”

mentioning

confidence: 99%

Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation

Sasaki

Beppu

Tanaka

et al. 2012

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

143

172

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Dynamic activity of glia has repeatedly been demonstrated, but if such activity is independent from neuronal activity, glia would not have any role in the information processing in the brain or in the generation of animal behavior. Evidence for neurons communicating with glia is solid, but the signaling pathway leading back from glialto-neuronal activity was often difficult to study. Here, we introduced a transgenic mouse line in which channelrhodopsin-2, a light-gated cation channel, was expressed in astrocytes. Selective photostimulation of these astrocytes in vivo triggered neuronal activation. Using slice preparations, we show that glial photostimulation leads to release of glutamate, which was sufficient to activate AMPA receptors on Purkinje cells and to induce long-term depression of parallel fiber-to-Purkinje cell synapses through activation of metabotropic glutamate receptors. In contrast to neuronal synaptic vesicular release, glial activation likely causes preferential activation of extrasynaptic receptors that appose glial membrane. Finally, we show that neuronal activation by glial stimulation can lead to perturbation of cerebellar modulated motor behavior. These findings demonstrate that glia can modulate the tone of neuronal activity and behavior. This animal model is expected to be a potentially powerful approach to study the role of glia in brain function.cerebellum | Bergmann glia | gliotransmitter | plasticity | c-fos

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“…Astrocytic ATP, converted to adenosine and acting on A1Rs, is one candidate as it is implicated in heterosynaptic depression [73][74][75] (but also see [66]). Astrocytic glutamate is another candidate, as cholinergic activation of astrocytes induces mGluR or NMDAR-dependent LTP in neurons in vivo [60,79,80]. Moreover, astrocytic activation of neuronal A1Rs and NMDARs regulates plasticity thresholds [81,82].…”

Section: Intercellular Pathwaysmentioning

confidence: 99%

Mechanisms of heterosynaptic metaplasticity

Hulme

Jones

Raymond³

et al. 2014

Phil. Trans. R. Soc. B

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Synaptic plasticity is fundamental to the neural processes underlying learning and memory. Interestingly, synaptic plasticity itself can be dynamically regulated by prior activity, in a process termed ‘metaplasticity’, which can be expressed both homosynaptically and heterosynaptically. Here, we focus on heterosynaptic metaplasticity, particularly long-range interactions between synapses spread across dendritic compartments, and review evidence for intra cellular versus inter cellular signalling pathways leading to this effect. Of particular interest is our previously reported finding that priming stimulation in stratum oriens of area CA1 in the hippocampal slice heterosynaptically inhibits subsequent long-term potentiation and facilitates long-term depression in stratum radiatum. As we have excluded the most likely intracellular signalling pathways that might mediate this long-range heterosynaptic effect, we consider the hypothesis that intercellular communication may be critically involved. This hypothesis is supported by the finding that extracellular ATP hydrolysis, and activation of adenosine A2 receptors are required to induce the metaplastic state. Moreover, delivery of the priming stimulation in stratum oriens elicited astrocytic calcium responses in stratum radiatum. Both the astrocytic responses and the metaplasticity were blocked by gap junction inhibitors. Taken together, these findings support a novel intercellular communication system, possibly involving astrocytes, being required for this type of heterosynaptic metaplasticity.

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Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo

Cited by 70 publications

References 0 publications

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation

Mechanisms of heterosynaptic metaplasticity

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