Effect of calcium channel noise in astrocytes on neuronal transmission

Abstract In this study, a Langevin model is constructed by modifying a neuron–astrocyte coupled model that comprises a pyramidal neuron, an interneuron, and an astrocyte. This Langevin model considers random open-close transitions of calcium ion channels in the endoplasmic reticulum membrane of astrocytes. The effect of noise in the astrocytes on neuronal transmission is investigated numerically based on a random model under both normal and overexpression conditions of metabotropic glutamate receptors on astrocyte membranes. This study suggests that noise could change the firing patterns of two neurons during neuronal information transmission. Noise facilitates the occurrence of episodic spikes (ESs) in both neurons. However, the noise-induced ESs occur irregularly, compared with ESs in a deterministic model, and the change in regularity with noise exhibits the coherence- resonance phenomenon. Furthermore, synchronicity between noisy ESs in two neurons depends significantly on various parameters. ESs completely occur synchronously but irregularly in certain parameter regions, whereas ESs in other parameter values are antiphase synchronous. This study implies not only that the calcium dynamics in astrocytes could participate in neuronal transmission, but also that noise in astrocytes may be transferred to neurons and may affect synaptic transmission significantly.

[1]  Yang Gao,et al.  Doubly stochastic coherence in complex neuronal networks. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[2]  S. Koizumi,et al.  Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Falcke.  Reading the patterns in living cells —the physics of ca2+ signaling , 2004 .

[4]  Khaleel Bhaukaurally,et al.  Glutamate exocytosis from astrocytes controls synaptic strength , 2007, Nature Neuroscience.

[5]  F. Delcomyn,et al.  Identification of bursts in spike trains , 1992, Journal of Neuroscience Methods.

[6]  P. Swain,et al.  Intrinsic and extrinsic contributions to stochasticity in gene expression , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Jun Ma,et al.  Noise effect on persistence of memory in a positive-feedback gene regulatory circuit. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  A. Oudenaarden,et al.  Enhancement of cellular memory by reducing stochastic transitions , 2005, Nature.

[9]  E Mosekilde,et al.  Giant Glial Cell: New Insight Through Mechanism-Based Modeling , 2008, Journal of biological physics.

[10]  P. Swain,et al.  Stochastic Gene Expression in a Single Cell , 2002, Science.

[11]  Dmitry E. Postnov,et al.  Functional modeling of neural-glial interaction , 2007, Biosyst..

[12]  S. Gobbo,et al.  Neuronal Synchrony Mediated by Astrocytic Glutamate through Activation of Extrasynaptic NMDA Receptors , 2004, Neuron.

[13]  J. Raser,et al.  Noise in Gene Expression: Origins, Consequences, and Control , 2005, Science.

[14]  M. Stamatakis,et al.  Modeling of ATP-mediated signal transduction and wave propagation in astrocytic cellular networks. , 2006, Journal of theoretical biology.

[15]  S. Nadkarni,et al.  Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? , 2003, Physical review letters.

[16]  Z. Hou,et al.  Noise-enhanced energy transduction of molecular machinery , 2002 .

[17]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[18]  Alfredo Pereira,et al.  On the role of synchrony for neuron–astrocyte interactions and perceptual conscious processing , 2009, Journal of biological physics.

[19]  Jun Ma,et al.  Information Transmission in a Neuron-Astrocyte Coupled Model , 2013, PloS one.

[20]  M. Thattai,et al.  Intrinsic noise in gene regulatory networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Rinzel,et al.  Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. , 1994, Journal of theoretical biology.

[22]  T. Fellin,et al.  Astrocytes coordinate synaptic networks: balanced excitation and inhibition. , 2006, Physiology.

[23]  Jun Ma,et al.  Multiplicative-noise-induced coherence resonance via two different mechanisms in bistable neural models. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  P. Jung,et al.  Optimal intracellular calcium signaling. , 2002, Physical review letters.

[25]  B. Khakh,et al.  ATP Excites Interneurons and Astrocytes to Increase Synaptic Inhibition in Neuronal Networks , 2004, The Journal of Neuroscience.

[26]  Peter Jung,et al.  Termination of Ca2+ Release for Clustered IP3R Channels , 2012, PLoS Comput. Biol..

[27]  P. Jung,et al.  Optimal ion channel clustering for intracellular calcium signaling , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Schiff,et al.  The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: II. Network and glial dynamics , 2008, Journal of Computational Neuroscience.

[29]  P. Haydon,et al.  Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Michael M. Halassa,et al.  Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. , 2010, Annual review of physiology.

[31]  Mahmood Amiri,et al.  On the role of astrocytes in synchronization of two coupled neurons: a mathematical perspective , 2011, Biological Cybernetics.

[32]  Mahmood Amiri,et al.  Astrocyte- neuron interaction as a mechanism responsible for generation of neural synchrony: a study based on modeling and experiments , 2012, Journal of Computational Neuroscience.

[33]  Kazuyuki Aihara,et al.  An optimal number of molecules for signal amplification and discrimination in a chemical cascade. , 2006, Biophysical journal.

[34]  Steve M. Potter,et al.  An extremely rich repertoire of bursting patterns during the development of cortical cultures , 2006, BMC Neuroscience.

[35]  S. Boccaletti,et al.  Synchronization of chaotic systems , 2001 .

[36]  Z Wang,et al.  Direct observation of calcium-independent intercellular ATP signaling in astrocytes. , 2000, Analytical chemistry.

[37]  G. Perea,et al.  Tripartite synapses: astrocytes process and control synaptic information , 2009, Trends in Neurosciences.

[38]  L. Roux,et al.  Over Astroglial Networks: a Step Further in Neuroglial and Gliovascular Interactions , 2022 .

[39]  Mahmood Amiri,et al.  Functional modeling of astrocytes in epilepsy: a feedback system perspective , 2011, Neural Computing and Applications.

[40]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[41]  D. Dubnau,et al.  Noise in Gene Expression Determines Cell Fate in Bacillus subtilis , 2007, Science.

[42]  Richard Robitaille,et al.  Glial Cells and Neurotransmission An Inclusive View of Synaptic Function , 2003, Neuron.

[43]  Leone Fronzoni,et al.  The influence of the astrocyte field on neuronal dynamics and synchronization , 2009, Journal of biological physics.

[44]  J. Meldolesi,et al.  Astrocytes, from brain glue to communication elements: the revolution continues , 2005, Nature Reviews Neuroscience.

[45]  Mu-ming Poo,et al.  ATP Released by Astrocytes Mediates Glutamatergic Activity-Dependent Heterosynaptic Suppression , 2003, Neuron.