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Dynamical transitions of the coupled Class I (II) neurons regulated by an astrocyte

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Abstract

Based on the minimal neural network models consisting of a pyramidal (PY) neuron, an interneuron (IN), and an astrocyte (AS), we investigate the regulating effects of astrocyte on dynamical transitions in two coupled neurons of the same type of excitability, either Class I or Class II, which is characterized by saddle-node on invariant circle (SNIC) and Hopf (HB) bifurcation, respectively. It is found that without the regulation of AS, the coupled Class I PY and IN neurons show the regular \(L^s\) mixed-mode oscillations (MMOs) composed of L large amplitude oscillations (LAOs) and s small amplitude oscillations (SAOs) in one period. Under the AS action, the calcium signals in AS can induce and regulate the mixed-mode low-frequency bursting firings. By contrast, for the coupled Class II PY and IN neurons, when AS is ignored, as the coupling strength increases, the system shows the periodic LAO oscillations, \(L^s\) mode of oscillations, and the chaotic behaviors. Furthermore, the period-doubling bifurcation is clearly captured. However, the presence of AS makes the PY neuron exhibit the mixed-mode low-frequency chaotic bursting activities. Interestingly, we also discover a new transition route (\(1^0\rightarrow 1^1\rightarrow 1^2\rightarrow \ldots \)) of calcium signals due to the period adding bifurcation of the system, which can shape the firing patterns of the PY neuron. Our results suggest that calcium signals in AS indeed involve in and even shape the coupling dynamics of PY and IN neurons. In particular, AS may exert differential roles in modulating the dynamical properties of Class I and Class II neurons.

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References

  1. Orkand, R.K., Nicholls, J.G., Kuffler, S.W.: Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29(4), 788–806 (1966)

    Article  Google Scholar 

  2. Vernadakis, A.: Glia-neuron intercommunications and synaptic plasicity. Prog. Neurobiol. 49(3), 185–214 (1996)

    Article  Google Scholar 

  3. Kang, J., Jiang, L., Goldman, S.A., Nedergaard, M.: Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1(8), 683–692 (1998)

    Article  Google Scholar 

  4. Piet, R., Poulain, D.A., Oliet, S.H.: Modulation of synaptic transmission by astrocytes in the rat supraoptic nucleus. J. Physiol. Paris 96(3–4), 231–236 (2002)

    Article  Google Scholar 

  5. Parri, H.R., Gould, T.M., Crunelli, V.: Spontaneous astrocytic \({Ca}^{2+}\) oscillations in situ drive NMDAR-mediated neuronal excitation. Nat. Neurosci. 4(8), 803–812 (2001)

    Article  Google Scholar 

  6. Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G., Carmignoto, G.: Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43(5), 729–743 (2004)

    Article  Google Scholar 

  7. Koizumi, S., Fujishita, K., Tsuda, M., Shigemoto-Mogami, Y., Inoue, K.: Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc. Nat. Acad. Sci. 100(19), 11023–11028 (2003)

    Article  Google Scholar 

  8. Zhang, Jm., Wang, Hk., Ye, Cq., Ge, W., Chen, Y., Jiang, Zl., Wu, Cp., Poo, Mm., Duan, S.: ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40(5), 971–982 (2003)

  9. Lee, S., Yoon, B.E., Berglund, K., Oh, S.J., Park, H., Shin, H.S., Augustine, G.J., Lee, C.J.: Channel-mediated tonic GABA release from glia. Science 330(6005), 790–796 (2010)

    Article  Google Scholar 

  10. Henneberger, C., Papouin, T., Oliet, S.H.R., Rusakov, D.A.: Long-term potentiation depends on release of D-serine from astrocytes. Nature 463(7278), 232–236 (2010)

    Article  Google Scholar 

  11. Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A., Oliet, S.H.: Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125(4), 775–784 (2006)

    Article  Google Scholar 

  12. Takata, N., Mishima, T., Hisatsune, C., Nagai, T., Ebisui, E., Mikoshiba, K., Hirase, H.: Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J. Neurosci. 31(49), 18155–18165 (2011)

    Article  Google Scholar 

  13. Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C., Poo, M., Duan, S.: Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc. Nat. Acad. Sci. 100(25), 15194–15199 (2003)

    Article  Google Scholar 

  14. Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S., Smith, S.J.: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941), 470–473 (1990)

    Article  Google Scholar 

  15. Charles, A.C., Merrill, J.E., Dirksen, E.R., Sandersont, M.J.: Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6(6), 983–992 (1991)

    Article  Google Scholar 

  16. Dani, J.W., Chernjavsky, A., Smith, J.: Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8(3), 429–440 (1992)

    Article  Google Scholar 

  17. Pasti, L., Volterra, A., Pozzan, T., Carmignoto, G.: Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17(20), 7817–7830 (1997)

    Article  Google Scholar 

  18. Porter, J.T., McCarthy, K.D.: Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16(16), 5073–5081 (1996)

    Article  Google Scholar 

  19. Erkan, Y., Saraç, Z., Y\(_l{lmaz}\) E.: Effects of astrocyte onweak signal detection performance of Hodgkin–Huxley neuron. Nonlinear Dyn. 95(4), 3411–3421 (2019)

  20. Araque, A., Parpura, V., Sanzgiri, R.P., Haydon, P.G.: Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22(5), 208–215 (1999)

    Article  Google Scholar 

  21. De Pittà, M., Volman, V., Berry, H., Parpura, V., Volterra, A., Ben-Jacob, E.: Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front. Comput. Neurosci. 6, 98–98 (2012)

    Article  Google Scholar 

  22. Pankratova, E.V., Kalyakulina, A.I., Stasenko, S.V., Gordleeva, S.Y., Lazarevich, I.A., Kazantsev, V.B.: Neuronal synchronization enhanced by neuron-astrocyte interaction. Nonlinear Dyn. 97(1), 647–662 (2019)

    Article  Google Scholar 

  23. Tang, J., Luo, J.M., Ma, J.: Information transmission in a neuron-astrocyte coupled model. PLoS ONE 8(11), e80324 (2013)

    Article  Google Scholar 

  24. Chun, H., Lee, C.J.: Reactive astrocytes in Alzheimer’s disease: a double-edged sword. Neurosci. Res. 126, 44–52 (2018)

    Article  Google Scholar 

  25. Booth, H.D., Hirst, W.D., Wade-Martins, R.: The role of astrocyte dysfunction in Parkinson’s disease pathogenesis. Trends Neurosci. 40(6), 358–370 (2017)

    Article  Google Scholar 

  26. Steinhäuser, C., Grunnet, M., Carmignoto, G.: Crucial role of astrocytes in temporal lobe epilepsy. Neuroscience 323, 157–169 (2016)

    Article  Google Scholar 

  27. Fan, D., Zheng, Y., Yang, Z., Wang, Q.: Improving control effects of absence seizures using single-pulse alternately resetting stimulation (SARS) of corticothalamic circuit. Appl. Math. Mech. 41(9), 1287–1302 (2020)

    Article  Google Scholar 

  28. Valori, C.F., Guidotti, G., Brambilla, L., Rossi, D.: Astrocytes: emerging therapeutic targets in neurological disorders. Trends Mol. Med. 25(9), 750–759 (2019)

    Article  Google Scholar 

  29. Fan, D., Wang, Q.: Synchronization and bursting transition of the coupled Hindmarsh-Rose systems with asymmetrical time-delays. Sci. China Technol. Sci. 60(7), 1019–1031 (2017)

    Article  Google Scholar 

  30. Rakshit, S., Bera, B.K., Ghosh, D.: Synchronization in a temporal multiplex neuronal hypernetwork. Phys. Rev. E 98(3), 032305 (2018)

    Article  MathSciNet  Google Scholar 

  31. Amiri, M., Hosseinmardi, N., Bahrami, F., Janahmadi, M.: Astrocyte- neuron interaction as a mechanism responsible for generation of neural synchrony: a study based on modeling and experiments. J. Comput. Neurosci. 34(3), 489–504 (2013)

    Article  MathSciNet  Google Scholar 

  32. Makovkin, S.Y., Shkerin, I.V., Gordleeva, S.Y., Ivanchenko, M.V.: Astrocyte-induced intermittent synchronization of neurons in a minimal network. Chaos Solitons Fractals 138, 109951 (2020)

    Article  MathSciNet  Google Scholar 

  33. Motter, A.E.: Spontaneous synchrony breaking. Nat. Phys. 6(3), 164–165 (2010)

    Article  Google Scholar 

  34. Bera, B.K., Rakshit, S., Ghosh, D., Kurths, J.: Spike chimera states and firing regularities in neuronal hypernetworks. Chaos 29(5), 053115 (2019)

    Article  MathSciNet  Google Scholar 

  35. Bera, B.K., Ghosh, D., Lakshmanan, M.: Chimera states in bursting neurons. Phys. Rev. E 93(1), 012205 (2016)

    Article  MathSciNet  Google Scholar 

  36. Majhi, S., Bera, B.K., Ghosh, D., Perc, M.: Chimera states in neuronal networks: a review. Phys. Life Rev. 28, 100–121 (2019)

    Article  Google Scholar 

  37. Wang, Z., Baruni, S., Parastesh, F., Jafari, S., Ghosh, D., Perc, M., Hussain, I.: Chimeras in an adaptive neuronal network with burst-timing-dependent plasticity. Neurocomputing 406, 117–126 (2020)

    Article  Google Scholar 

  38. Liang, S., Wang, Z.: Controlling a neuron by stimulating a coupled neuron. Appl. Math. Mech. 40(1), 13–24 (2019)

    Article  MathSciNet  MATH  Google Scholar 

  39. Mondal, A., Upadhyay, R.K., Ma, J., Yadav, B.K., Sharma, S.K., Mondal, A.: Bifurcation analysis and diverse firing activities of a modified excitable neuron model. Cogn. Neurodyn. 13(4), 393–407 (2019)

    Article  Google Scholar 

  40. Parastesh, F., Rajagopal, K., Karthikeyan, A., Alsaedi, A., Hayat, T., Pham, V.T.: Complex dynamics of a neuron model with discontinuous magnetic induction and exposed to external radiation. Cogn. Neurodyn. 12(6), 607–614 (2018)

    Article  Google Scholar 

  41. Hodgkin, A.L.: The local electric changes associated with repetitive action in a non-medullated axon. J. Physiol. 107(2), 165–181 (1948)

    Article  Google Scholar 

  42. Izhikevich, E.M.: Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting. MIT Press, Cambridge (2006)

    Book  Google Scholar 

  43. Prescott, S.A., De Koninck, Y., Sejnowski, T.J.: Biophysical basis for three distinct dynamical mechanisms of action potential initiation. PLoS Comput. Biol. 4(10), e1000198 (2008)

    Article  MathSciNet  Google Scholar 

  44. Wang, H., Wang, L., Yu, L., Chen, Y.: Response of Morris–Lecar neurons to various stimuli. Phys. Rev. E 83(2), 021915 (2011)

    Article  Google Scholar 

  45. Nguyen, L.H., Hong, K.S., Park, S.: Bifurcation control of the Morris–Lecar neuron model via a dynamic state-feedback control. Biol. Cybern. 106(10), 587–594 (2012)

    Article  MathSciNet  MATH  Google Scholar 

  46. Liu, Y., Li, C.: Stochastic resonance in feedforward-loop neuronal network motifs in astrocyte field. J. Theor. Biol. 335, 265–275 (2013)

    Article  MathSciNet  MATH  Google Scholar 

  47. Li, Y.X., Rinzel, J.: Equations for \(InsP_3\) receptor-mediated \({[Ca^{2+}]}_i\) oscillations derived from a detailed kinetic model: a Hodgkin–Huxley like formalism. J. Theor. Biol. 166(4), 461–473 (1994)

    Article  Google Scholar 

  48. Sneyd, J., Wetton, B.T., Charles, A.C., Sanderson, M.J.: Intercellular calcium waves mediated by diffusion of inositol trisphosphate: a two-dimensional model. Am. J. Physiol. 268(6), C1537–C1545 (1995)

    Article  Google Scholar 

  49. Höfer, T., Venance, L., Giaume, C.: Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J. Neurosci. 22(12), 4850–4859 (2002)

    Article  Google Scholar 

  50. Volman, V., Ben-Jacob, E., Levine, H.: The astrocyte as a gatekeeper of synaptic information transfer. Neural Comput. 19(2), 303–326 (2007)

    Article  MathSciNet  MATH  Google Scholar 

  51. Bowser, D.N., Khakh, B.S.: ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J. Neurosci. 24(39), 8606–8620 (2004)

    Article  Google Scholar 

  52. Koizumi, S., Fujishita, K., Tsuda, M., Shigemoto-Mogami, Y., Inoue, K.: Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc. Nat. Acad. Sci. U.S.A. 100(19), 11023–11028 (2003)

    Article  Google Scholar 

  53. Schell, M., Albahadily, F.N.: Mixed-mode oscillations in an electrochemical system. II. A periodic–chaotic sequence. J. Chem. Phys. 90(2), 822–828 (1989)

    Article  MathSciNet  Google Scholar 

  54. Ray, A., Rakshit, S., Basak, G.K., Dana, S.K., Ghosh, D.: Understanding the origin of extreme events in El-Niño southern oscillation. Phys. Rev. E 101(6), 062210 (2020)

    Article  MathSciNet  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grants No. 11932003).

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Correspondence to Qingyun Wang.

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Zhao, J., Fan, D., Wang, Q. et al. Dynamical transitions of the coupled Class I (II) neurons regulated by an astrocyte. Nonlinear Dyn 103, 913–924 (2021). https://doi.org/10.1007/s11071-020-06122-3

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