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Astrocyte calcium wave induces seizure-like behavior in neuron network

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Abstract

It has been revealed experimentally that astrocytes can participate in synaptic transmission by modulating and responding to the release of neurotransmitters with calcium elevations. Researches suggest that seizure-like discharges (SDs) or seizure-like firings (SFs) in neurons, characterizing neurological disorder, may arise locally in restricted areas (focal area) and then propagate throughout the brain. But the underlying mechanism remains unclear. To study the possible role astrocytes playing in the SDs propagation, we construct a minimal neuron-astrocyte network model by connecting a neurons chain and an astrocytes chain. The focal area is modelled by an IP3 reservoir which provides persistent IP3 out-flux. The study suggests that calcium wave propagation in astrocytes determines the propagation of SDs in the connected neurons. On the other hand, SDs in neurons allows the calcium wave propagates longer distance in the astrocytes, which suggests the mutually cooperating of astrocytes and neurons in accomplishing SD propagation. Furthermore, once SDs propagate and occupy the neuron network, it could not be terminated by recovery of the focal area. The results may imply that treatment of brain disorders should not only focus on local area but the whole neuron network.

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References

  1. Deitmer J W, Rose C R, Munch T, et al. Leech glial cell: Functional role in a simple nervous system. Glia, 1999, 28: 175–182

    Article  Google Scholar 

  2. Fan D, Wang Q, Perc M. Disinhibition-induced transitions between absence and tonic-clonic epileptic seizures. Sci Rep, 2015, 5: 12618

    Article  Google Scholar 

  3. Hu B, Wang Q Y. The conditions for onset of beta oscillations in an extended subthalamic nucleus-globus pallidus network. Sci China Tech Sci, 2014, 57: 2020–2027

    Article  Google Scholar 

  4. Wang Q, Perc M, Duan Z, et al. Synchronization transitions on scalefree neuronal networks due to finite information transmission delays. Phys Rev E, 2009, 80: 026206

    Article  Google Scholar 

  5. Tang J, Ma J, Yi M, et al. Delay and diversity-induced synchronization transitions in a small-world neuronal network. Phys Rev E, 2011, 83: 046207

    Article  Google Scholar 

  6. Wang Q Y, Duan Z S, Huang L, et al. Pattern formation and firing synchronization in networks of map neurons. New J Phys, 2007, 9: 383–383

    Article  Google Scholar 

  7. Zhang H, Wang Q, He X, et al. Synchronization stability and firing transitions in two types of class I neuronal networks with short-term plasticity. Neural Netw, 2014, 49: 107–117

    Article  MATH  Google Scholar 

  8. Auld D S, Robitaille R. Glial cells and neurotransmission. Neuron, 2003, 40: 389–400

    Article  Google Scholar 

  9. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci, 2005, 6: 626–640

    Article  Google Scholar 

  10. Giaume C, Koulakoff A, Roux L, et al. Astroglial networks: A step further in neuroglial and gliovascular interactions. Nat Rev Neurosci, 2010, 11: 87–99

    Article  Google Scholar 

  11. Perea G, Navarrete M, Araque A. Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci, 2009, 32: 421–431

    Article  Google Scholar 

  12. Postnov D E, Ryazanova L S, Brazhe N A, et al. Giant glial cell: New insight through mechanism-based modeling. J Biol Phys, 2008, 34: 441–457

    Article  Google Scholar 

  13. De Pittà M, Volman V, Berry H, et al. Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front Comput Neurosci, 2012, 6: 98

    Article  Google Scholar 

  14. Tang J, Luo J M, Ma J. Information transmission in a neuron-astrocyte coupled model. PLoS ONE, 2013, 8: e80324

    Article  Google Scholar 

  15. Tang J, Liu T B, Ma J, et al. Effect of calcium channel noise in astrocytes on neuronal transmission. Commun Nonlinear Sci Numer Simul, 2016, 32: 262–272

    Article  MathSciNet  Google Scholar 

  16. Nadkarni S, Jung P. Spontaneous oscillations of dressed neurons: A new mechanism for epilepsy? Phys Rev Lett, 2003, 91: 268101

    Article  Google Scholar 

  17. Hodgkin A L, Huxley A F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol, 1952, 117: 500–544

    Article  Google Scholar 

  18. Li Y X, Rinzel J. Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: A Hodgkin-Huxley like formalism. J Theor Biol, 1994, 166: 461–473

    Article  Google Scholar 

  19. Parpura V, Haydon P G. Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA, 2000, 97: 8629–8634

    Article  Google Scholar 

  20. Amiri M, Bahrami F, Janahmadi M. Functional modeling of astrocytes in epilepsy: A feedback system perspective. Neural Comput Applic, 2011, 20: 1131–1139

    Article  Google Scholar 

  21. Amiri M, Montaseri G, Bahrami F. On the role of astrocytes in synchronization of two coupled neurons: A mathematical perspective. Biol Cybern, 2011, 105: 153–166

    Article  MathSciNet  MATH  Google Scholar 

  22. Amiri M, Hosseinmardi N, Bahrami F, et al. Astrocyte-neuron interaction as a mechanism responsible for generation of neural synchrony: A study based on modeling and experiments. J Comput Neurosci, 2013, 34: 489–504

    Article  MathSciNet  Google Scholar 

  23. Reato D, Cammarota M, Parra L C, et al. Computational model of neuron-astrocyte interactions during focal seizure generation. Front Comput Neurosci, 2012, 6: 81

    Article  Google Scholar 

  24. Izhikevich E M. Simple model of spiking neurons. IEEE Trans Neural Netw, 2003, 14: 1569–1572

    Article  Google Scholar 

  25. Allegrini P, Fronzoni L, Pirino D. The influence of the astrocyte field on neuronal dynamics and synchronization. J Biol Phys, 2009, 35: 413–423

    Article  Google Scholar 

  26. Liu Y, Li C G. Firing rate propagation through neuronal-astrocytic network. IEEE Trans Neural Netw Learn Syst, 2013, 24: 789–799

    Article  Google Scholar 

  27. Fellin T, Pascual O, Gobbo S, et al. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron, 2004, 43: 729–743

    Article  Google Scholar 

  28. Fellin T. Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci, 2006, 26: 9312–9322

    Article  Google Scholar 

  29. Goldberg M, De Pittà M, Volman V, et al. Nonlinear gap junctions enable long-distance propagation of pulsating calcium waves in astrocyte networks. PLoS Comput Biol, 2010, 6: e1000909

    Google Scholar 

  30. De Pittà M, Volman V, Levine H, et al. Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. Phys Rev E, 2008, 77: 030903

    Article  Google Scholar 

  31. Kazantsev V B. Spontaneous calcium signals induced by gap junctions in a network model of astrocytes. Phys Rev E, 2009, 79: 010901

    Article  Google Scholar 

  32. Finkbeiner S M. Glial calcium. Glia, 1993, 9: 83–104

    Article  Google Scholar 

  33. Charles A C, Merrill J E, Dirksen E R, et al. Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron, 1991, 6: 983–992

    Article  Google Scholar 

  34. Carmignoto G. Reciprocal communication systems between astrocytes and neurones. Prog Neurobiol, 2000, 62: 561–581

    Article  Google Scholar 

  35. Oberheim N A, Wang X, Goldman S, et al. Astrocytic complexity distinguishes the human brain. Trends Neurosci, 2006, 29: 547–553

    Article  Google Scholar 

  36. Sherwood C C, Stimpson C D, Raghanti M A, et al. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA, 2006, 103: 13606–13611

    Article  Google Scholar 

  37. Di Garbo A, Barbi M, Chillemi S, et al. Calcium signalling in astrocytes and modulation of neural activity. Biosystems, 2007, 89: 74–83

    Article  Google Scholar 

  38. Losi G, Cammarota M, Chiavegato A, et al. A new experimental model of focal seizures in the entorhinal cortex. Epilepsia, 2010, 51: 1493–1502

    Article  Google Scholar 

  39. Postnov D E, Ryazanova L S, Sosnovtseva O V. Functional modeling of neural-glial interaction. Biosystems, 2007, 89: 84–91

    Article  Google Scholar 

  40. Cressman Jr. J R, Ullah G, Ziburkus J, et al. The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: I. Single neuron dynamics. J Comput Neurosci, 2009, 26: 159–170

    Article  MathSciNet  Google Scholar 

  41. Postnov D E, Koreshkov R N, Brazhe N A, et al. Dynamical patterns of calcium signaling in a functional model of neuron-astrocyte networks. J Biol Phys, 2009, 35: 425–445

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Physics, China University of Mining and Technology, Xuzhou, 221116, China

    Jun Tang, Juan Zhang, GuoYing Zhang & XianQing Yang

  2. Department of Physics, Lanzhou University of Technology, Lanzhou, 730050, China

    Jun Ma

  3. NAAM-Research Group, Department of Mathematics, Faculty of Science, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Jun Ma

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  1. Jun Tang
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  2. Juan Zhang
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  3. Jun Ma
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Correspondence to Jun Tang.

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Tang, J., Zhang, J., Ma, J. et al. Astrocyte calcium wave induces seizure-like behavior in neuron network. Sci. China Technol. Sci. 60, 1011–1018 (2017). https://doi.org/10.1007/s11431-016-0293-9

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  • DOI: https://doi.org/10.1007/s11431-016-0293-9

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