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2. Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity.

Author

De Pittà, Maurizio, Volman, Vladislav, Berry, Hugues, Parpura, Vladimir, Volterra, Andrea, and Ben-Jacob, Eshel

Subjects
ASTROCYTES, COMPLEXITY (Philosophy), CALCIUM metabolism, NEUROPLASTICITY, EXPERIMENTAL design, TRIM proteins
Abstract

The complexity of the signaling network that underlies astrocyte-synapse interactions may seem discouraging when tackled from a theoretical perspective. Computational modeling is challenged by the fact that many details remain hitherto unknown and conventional approaches to describe synaptic function are unsuitable to explain experimental observations when astrocytic signaling is taken into account. Supported by experimental evidence is the possibility that astrocytes perform genuine information processing by means of their calcium signaling and are players in the physiological setting of the basal tone of synaptic transmission. Here we consider the plausibility of this scenario from a theoretical perspective, focusing on the modulation of synaptic release probability by the astrocyte and its implications on synaptic plasticity. The analysis of the signaling pathways underlying such modulation refines our notion of tripartite synapse and has profound implications on our understanding of brain function. [ABSTRACT FROM AUTHOR]

Published
2012
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3. G Protein-Coupled Receptor-Mediated Calcium Signaling in Astrocytes

Author

Maurizio De Pittà, Eshel Ben-Jacob, Hugues Berry, Basque Center for Applied Mathematics (BCAM), Basque Center for Applied Mathematics, School of Physics and Astronomy [Tel Aviv] (TAU), Raymond and Beverly Sackler Faculty of Exact Sciences [Tel Aviv] (TAU), Tel Aviv University (TAU)-Tel Aviv University (TAU), Artificial Evolution and Computational Biology (BEAGLE), Laboratoire d'InfoRmatique en Image et Systèmes d'information (LIRIS), Université Lumière - Lyon 2 (UL2)-École Centrale de Lyon (ECL), Université de Lyon-Université de Lyon-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Université Lumière - Lyon 2 (UL2)-École Centrale de Lyon (ECL), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS), Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria), Maurizio De Pittà, Hugues Berry, School of Physics and Astronomy [Tel Aviv], Tel Aviv University [Tel Aviv], Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire d'InfoRmatique en Image et Systèmes d'information (LIRIS), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-École Centrale de Lyon (ECL), Université de Lyon-Université Lumière - Lyon 2 (UL2)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-École Centrale de Lyon (ECL), and Université de Lyon-Université Lumière - Lyon 2 (UL2)

Subjects
5-trisphospate metabolism, 0303 health sciences, Calcium encoding, chemistry.chemical_element, Calcium-induced calcium release threshold, Calcium, Inositol 1, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Calcium in biology, Cell biology, 03 medical and health sciences, 0302 clinical medicine, chemistry, Protein kinase C, Second messenger system, Extracellular, Signal integration, [SDV.NEU]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC], Diacylglycerol, 030217 neurology & neurosurgery, 030304 developmental biology, G protein-coupled receptor, Calcium signaling
Abstract

International audience; Astrocytes express a large variety of G protein-coupled receptors (GPCRs) which mediate the transduction of extracellular signals into intracellular calcium responses. This transduc-tion is provided by a complex network of biochemical reactions which mobilizes a wealth of possible calcium-mobilizing second messenger molecules. Inositol 1,4,5-trisphosphate is probably the best known of these molecules whose enzymes for its production and degradation are nonetheless calcium-dependent. We present a biophysical modeling approach based on the assumption of Michaelis-Menten enzyme kinetics, to effectively describe GPCR-mediated astrocytic calcium signals. Our model is then used to study different mechanisms at play in stimulus encoding by shape and frequency of calcium oscillations in astrocytes.

Published
2019

5. Inhibition enhances spatially-specific calcium encoding of synaptic input patterns in a biologically constrained model

Author

Joanna Jędrzejewska-Szmek, Kim T. Blackwell, and Daniel B. Dorman

Subjects
0301 basic medicine, Dendritic spine, Mouse, Computer science, QH301-705.5, Dendritic Spines, striatum, Science, Models, Neurological, Action Potentials, Dendrite, Dendritic branch, Inhibitory postsynaptic potential, Ion Channels, General Biochemistry, Genetics and Molecular Biology, Synapse, 03 medical and health sciences, 0302 clinical medicine, Calcium encoding, Excitatory synapse, medicine, Computer Simulation, Biology (General), Neurons, General Immunology and Microbiology, General Neuroscience, spine calcium, Excitatory Postsynaptic Potentials, Neural Inhibition, General Medicine, dendritic integration, computational model, 030104 developmental biology, medicine.anatomical_structure, plasticity, Synapses, Rat, Medicine, Calcium, Other, Neuron, Neuroscience, 030217 neurology & neurosurgery, Research Article, Computational and Systems Biology
Abstract

Synaptic plasticity, which underlies learning and memory, depends on calcium elevation in neurons, but the precise relationship between calcium and spatiotemporal patterns of synaptic inputs is unclear. Here, we develop a biologically realistic computational model of striatal spiny projection neurons with sophisticated calcium dynamics, based on data from rodents of both sexes, to investigate how spatiotemporally clustered and distributed excitatory and inhibitory inputs affect spine calcium. We demonstrate that coordinated excitatory synaptic inputs evoke enhanced calcium elevation specific to stimulated spines, with lower but physiologically relevant calcium elevation in nearby non-stimulated spines. Results further show a novel and important function of inhibition—to enhance the difference in calcium between stimulated and non-stimulated spines. These findings suggest that spine calcium dynamics encode synaptic input patterns and may serve as a signal for both stimulus-specific potentiation and heterosynaptic depression, maintaining balanced activity in a dendritic branch while inducing pattern-specific plasticity., eLife digest How do we form new memories? The human brain contains almost 90 billion neurons, which communicate with one another at junctions called synapses. Each neuron has a shape a little like that of a tree, and is covered in branches called dendrites. Synapses typically form between the end of one neuron and a dendrite on another. Most scientists believe that the brain forms new memories by changing the strength of these synapses. But a number of questions remain about how this process works. There are two types of synapses: excitatory and inhibitory. When an excitatory synapse becomes active, calcium ions flow into the dendrite of the receiving neuron. The calcium ions then trigger processes inside the cell that are essential for changing the strength of the synapse, and thus forming a memory. But what happens when an inhibitory synapse becomes active? How does this affect memory? Additionally, each neuron forms synapses with thousands of others, with several synapses on a single dendrite. To form a memory about a specific experience, the brain must strengthen only the synapses that relate to that experience. How does the brain manage to target these synapses specifically? Do the synapses need to be clustered on the same dendritic branch, or can they be spread apart? And do all the synapses need to be active at exactly the same time? Dorman et al. investigated these questions by developing a computer model of a neuron. Testing the model revealed that the synapses related to an experience do not all need to be active at exactly the same time to form a memory. Moreover, the synapses can be spread across multiple dendrites. Finally, the model showed that inhibitory synapses are critical for preventing calcium ions from spreading within dendritic branches and entering inactive synapses. This ensures that only the synapses active during a specific experience become stronger. Many brain disorders, including substance abuse and addiction, involve errors in the processes that underlie learning and memory. By increasing our understanding of how the structure of brain cells supports these processes, the current findings could one day lead to better treatments for these and other disorders.

Published
2018

6. Optogenetic Control of Calcium Oscillation Waveform Defines NFAT as an Integrator of Calcium Load

Author

Brian Y. Chow and Pimkhuan Hannanta-anan

Subjects
0301 basic medicine, Histology, chemistry.chemical_element, Optogenetics, Calcium, Calcium in biology, Pathology and Forensic Medicine, 03 medical and health sciences, Calcium encoding, Humans, Calcium Signaling, Calcium signaling, Physics, NFATC Transcription Factors, Calcineurin, NFAT, Cell Biology, Calcium, Dietary, 030104 developmental biology, chemistry, Duty cycle, Biophysics, HeLa Cells
Abstract

It is known that the calcium-dependent transcription factor NFAT initiates transcription in response to pulsatile loads of calcium signal. However, the relative contributions of calcium oscillation frequency, amplitude, and duty cycle to transcriptional activity remain unclear. Here, we engineer HeLa cells to permit optogenetic control of intracellular calcium concentration using programmable LED arrays. This approach allows us to generate calcium oscillations of constant peak amplitude, in which frequency is varied while holding duty cycle constant, or vice versa. Using this setup and mathematical modeling, we show that NFAT transcriptional activity depends more on duty cycle, defined as the proportion of the integrated calcium concentration over the oscillation period, than on frequency alone. This demonstrates that NFAT acts primarily as a signal integrator of cumulative load rather than a frequency-selective decoder. This approach resolves a fundamental question in calcium encoding and demonstrates the value of optogenetics for isolating individual dynamical components of larger signaling behaviors.

Published
2016

7. Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity

Author

Maurizio eDe Pitta', Vladislav eVolman, Hugues eBerry, Vladimir eParpura, Andrea eVolterra, Eshel eBen-Jacob, De Pittà, Maurizio, Ben-Jacob, Eshel, School of Physics and Astronomy [Tel Aviv], Tel Aviv University [Tel Aviv], Center for Theoretical Biological Physics (CTBP), University of San Diego, Computational Neurobiology Laboratory (CNL), The Salk Institute for Biological Studies, Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria), Laboratoire d'InfoRmatique en Image et Systèmes d'information (LIRIS), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-École Centrale de Lyon (ECL), Université de Lyon-Université Lumière - Lyon 2 (UL2), Artificial Evolution and Computational Biology (BEAGLE), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire d'InfoRmatique en Image et Systèmes d'information (LIRIS), Université de Lyon-Université Lumière - Lyon 2 (UL2)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-École Centrale de Lyon (ECL), Department of Biotechnology [Rijeka], University of Rijeka, Department of Neurobiology [Birmingham] (UAB), University of Alabama [Tuscaloosa] (UA), Department of Basic Neurosciences, Université de Lausanne (UNIL), The authors' research was supported by the Tauber Family Foundation (MDP and EBJ), the Italy-Israel Joint Neuroscience Lab(MDP), the Maguy-Glass Chair in Physics of Complex Systems at Tel Aviv University (EBJ), the Center for Theoretical Biological Physics at Rice University sponsored by the National Science Fundation (NSF) (grant PHY-0822283) (EBJ), the NSF program in Physics of Living Systems (PoLS) at the University of Michigan (grant PHY-1058034) (EBJ), the National Institute of Health (grants R01 NS059740 and R01 NS060870 to T. Sejnowski and M. Bazhenov) (VV), the High Council for Scientific and Technological Cooperation between France-Israel (HB), the National Science Foundation (grant CBET 0943343) (VP), and the Swiss National Science Foundation (grant 31003A-140999 and NCCRs 'Synapsy' and 'Transcure') (AV)., School of Physics and Astronomy [Tel Aviv] (TAU), Raymond and Beverly Sackler Faculty of Exact Sciences [Tel Aviv] (TAU), Tel Aviv University (TAU)-Tel Aviv University (TAU), Université Lumière - Lyon 2 (UL2)-École Centrale de Lyon (ECL), Université de Lyon-Université de Lyon-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Université Lumière - Lyon 2 (UL2)-École Centrale de Lyon (ECL), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), and Université de Lausanne = University of Lausanne (UNIL)

Subjects
Bioinformatics, [SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology, Neuroscience (miscellaneous), cortical maps, calcium encoding, calcium signaling, astrocyte modeling, gliotransmission, astrocyte-synapse interactions, synaptic plasticity, metaplasticity, Review Article, Neurotransmission, Biology, Synaptic Transmission, lcsh:RC321-571, modelling, 03 medical and health sciences, Cellular and Molecular Neuroscience, 0302 clinical medicine, Calcium encoding, astrocyte, Neurobiology, signalisation, Tripartite synapse, Metaplasticity, lcsh:Neurosciences. Biological psychiatry. Neuropsychiatry, 030304 developmental biology, Calcium signaling, 0303 health sciences, calcium, [SCCO.NEUR]Cognitive science/Neuroscience, Information processing, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Neurobiologie, Astrocytes, Synaptic plasticity, plasticité synaptique, Bio-informatique, Neurosciences (Sciences cognitives), Signal transduction, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], Neuroscience, 030217 neurology & neurosurgery
Abstract

International audience; The complexity of the signaling network that underlies astrocyte-synapse interactions may seem discouraging when tackled from a theoretical perspective. Computational modeling is challenged by the fact that many details remain hitherto unknown and conventional approaches to describe synaptic function are unsuitable to explain experimental observations when astrocytic signaling is taken into account. Supported by experimental evidence is the possibility that astrocytes perform genuine information processing by means of their calcium signaling and are players in the physiological setting of the basal tone of synaptic transmission. Here we consider the plausibility of this scenario from a theoretical perspective, focusing on the modulation of synaptic release probability by the astrocyte and its implications on synaptic plasticity. The analysis of the signaling pathways underlying such modulation refines our notion of the tripartite synapse and has profound implications on our understanding of brain function.

Published
2012
Full Text
View/download PDF

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