Abstract
In this study, we consider the problem of signal processing in neuron–astrocyte networks where the intercellular communication is described on the basis of a tripartite synapse concept. This type of communication involves combined contributions of pre- and postsynaptic neuronal compartments and components of the surrounding astrocyte to the processes of information transmission. Astrocyte-mediated regulation of neuronal activity is considered through the analysis of the response changes in the classical Hodgkin–Huxley model driven by excitatory synaptic current. It is shown that the complicated astrocyte-dependent dynamics of this current can lead to non-trivial changes in individual postsynaptic neuronal activity and, hence, in the cooperative activation of neuronal groups linked by the “astrocyte-mediated bridge”.
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Llinas, R., Sugimori, M.: Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. 305, 197–213 (1980)
Agmon-Snir, H., Carr, C.E., Rinzel, J.: The role of dendrites in auditory coincidence detection. Nature 393, 268–272 (1998)
Hille, B.: Ion Channels of Excitable Membranes. Sinauer Associates, Sunderland (2001)
Matsumoto, G., Aihara, K., Hanyu, Y., Takahashi, N., Yoshizawa, S., Nagumo, J.: Chaos and phase locking in normal squid axons. Phys. Lett. A 123, 162–166 (1987)
Parmananda, P., Mena, C.H., Baier, G.: Resonant forcing of a silent Hodgkin–Huxley neuron. Phys. Rev. E 66, 047202 (2002)
Lee, S.-G., Neiman, A., Kim, S.: Coherence resonance in a Hodgkin–Huxley neuron. Phys. Rev. E 57(3), 3292–3297 (1998)
Pankratova, E.V., Polovinkin, A.V., Mosekilde, E.: Resonant activation in a stochastic Hodgkin–Huxley model: interplay between noise and suprathreshold driving effects. Eur. Phys. J. B 45(3), 391–397 (2005)
Pankratova, E.V., Belykh, V.N., Mosekilde, E.: Role of the driving frequency in a randomly perturbed Hodgkin–Huxley neuron with suprathreshold forcing. Eur. Phys. J. B 53(4), 529–536 (2006)
Tsodyks, M.V., Markram, H.: The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. PNAS 94(2), 719–723 (1997)
Uzuntarla, M.: Inverse stochastic resonance induced by synaptic background activity with unreliable synapses. Phys. Lett. A 377(38), 2585–2589 (2013)
Uzuntarla, M., Ozer, M., Ileri, U., Calim, A., Torres, J.J.: Effects of dynamic synapses on noise-delayed response latency of a single neuron. Phys. Rev. E 92(6), 062710 (2015)
Uzuntarla, M., Torres, J.J., So, P., Ozer, M., Barreto, E.: Double inverse stochastic resonance with dynamic synapses. Phys. Rev. E 95, 012404 (2017)
Verkhratsky, A., Butt, A.: Glial Neurobiology. A Textbook, 1st edn, p. 224. Wiley, Hoboken (2007)
Li, J., Tang, J., Ma, J., Du, M., Wang, R., Wu, Y.: Dynamic transition of neuronal firing induced by abnormal astrocytic glutamate oscillation. Sci. Rep. 6, 32343 (2016)
Guo, S., Tang, J., Ma, J., Wang, C.: Autaptic modulation of electrical activity in a network of neuron-coupled astrocyte. Complexity 2017, 4631602 (2017)
Araque, A.: Astrocytes process synaptic information. Neuron Glia Biol. 4, 3–10 (2008)
Hülsmann, S., Oku, Y., Zhang, W., Richter, D.W.: Metabolic coupling between glia and neurons is necessary for maintaining respiratory activity in transverse medullary slices of neonatal mouse. Eur. J. Neurosci. 12, 856–862 (2000)
Baudoux, S., Parker, D.: Glial-toxin-mediated disruption of spinal cord locomotor network function and its modulation by 5-HT. Neuroscience 153, 1332–1343 (2008)
Angulo, M.C., Kozlov, A.S., Charpak, S., Audina, E.: Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J. Neurosci. 24, 6920–6927 (2004)
Fellin, T., Halassa, M.M., Terunuma, M., Succol, F., Takano, H., Frank, M., Moss, S.J., Haydon, P.G.: Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc. Natl. Acad. Sci. USA 106, 15037–15042 (2009)
Perea, G., Araque, A.: Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J. Neurosci. 25, 2192–2203 (2005)
Kozlov, A.S., Angulo, M.C., Audinat, E., Charpak, S.: Target cell-specific modulation of neuronal activity by astrocytes. Proc. Natl. Acad. Sci. USA 103, 10058–10063 (2006)
Navarrete, M., Araque, A.: Endocannabinoids mediate neuron-astrocyte communication. Neuron 57, 883–893 (2008)
Nadkarni, S., Jung, P.: Dressed neurons: modeling neural-glial interactions. Phys. Biol. 1, 35–41 (2004)
Nadkarni, S., Jung, P.: Modeling synaptic transmission of the tripartite synapse. Phys. Biol. 4, 1–9 (2007)
Volman, V., Ben-Jacob, E., Levine, H.: The astrocyte as a gate keeper of synaptic information transfer. Neural Comput. 19, 303–326 (2006)
Perea, G., Navarrete, M., Araque, A.: Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421–431 (2009)
De Pittá, M., Volman, V., Berry, H., Ben-Jacob, E.: A tale of two stories: astrocyte regulation of synaptic depression and facilitation. PLoS Comput. Biol. 7, e1002293 (2011). https://doi.org/10.1371/journal.pcbi.1002293
Postnov, D.E., Ryazanova, L.S., Sosnovtseva, O.V.: Functional modeling of neural-glial interaction. Biosystems 89, 84–91 (2007)
Wade, J.J., McDaid, L.J., Harkin, J., Crunelli, V., Kelso, J.A.S.: Bidirectional coupling between astrocytes and neurons mediates learning and dynamic coordination in the brain: a multiple modeling approach. PLoS ONE 6, e29445 (2011). https://doi.org/10.1371/journal.pone.0029445
Amiri, M., Bahrami, F., Janahmadi, M.: Functional contributions of astrocytes in synchronization of a neuronal network model. J. Theor. Biol. 292C, 60–70 (2011)
Sasaki, T., Ishikawa, T., Abe, R., Nakayama, R., Asada, A., Matsuki, N., Ikegaya, Y.: Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices. J. Physiol. 592(13), 2771–2783 (2014)
Pirttimaki, T.M., Sims, R.E., Saunders, G., Antonio, S.A., Codadu, N.K., Parri, H.R.: Astrocyte-mediated neuronal synchronization properties revealed by false gliotransmitter release. J. Neurosci. 37(41), 9859–9870 (2017)
Szabó, Z., Héja, L., Szalay, G., Kékesi, O., Füredi, A., Szebényi, K., Dobolyi, A., Orbán, T.I., Kolacsek, O., Tompa, T., Miskolczy, Z., Biczók, L., Rózsa, B., Sarkadi, B., Kardos, J.: Extensive astrocyte synchronization advances neuronal coupling in slow wave activity in vivo. Sci. Rep. 7(1), 6018 (2017)
Poskanzer, K.E., Yuste, R.: Astrocytes regulate cortical state switching in vivo. Proc. Natl. Acad. Sci. 113(19), E2675–E2684 (2016)
Lazarevich, I.A., Stasenko, S.V., Kazantsev, V.B.: Synaptic multistability and network synchronization induced by the neuron-glial interaction in the brain. JETP Lett. 105(3), 210–213 (2017)
Gordleeva, SYu., Stasenko, S.V., Semyanov, A.V., Dityatev, A.E., Kazantsev, V.B.: Bi-directional astrocytic regulation of neuronal activity within a network. Front. Comput. Neurosci. 6(92), 1–11 (2012)
Parpura, V., Zorec, R.: Gliotransmission: exocytotic release from astrocytes. Brain Res. Rev. 63, 83–92 (2010)
Volterra, A., Meldolesi, J.: Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626–640 (2005)
Perea, G., Araque, A.: Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086 (2007)
McGuinness, L., Taylor, C., Taylor, R.D.T., Yau, C., Langenhan, T., Hart, M.L., Christian, H., Tynan, P.W., Donnelly, P., Emptage, N.J.: Presynaptic NMDARs in the hippocampus facilitate transmitter release at theta frequency. Neuron 68, 1109–1127 (2010)
Semyanov, A., Kullmann, D.M.: Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25, 663–672 (2000)
Henneberger, C., Papouin, T., Oliet, S., Rusakov, D.: Long-term potentiation depends on release of D-serinefromastrocytes. Nature 463, 232–236 (2010)
Bergersen, L.H., Morland, C., Ormel, L., Rinholm, J.E., Larsson, M., Wold, J.F., Roe, A.T., Stranna, A., Santello, M., Bouvier, D., Ottersen, O.P., Volterra, A., Gundersen, V.: Immunogold detection of L-glutamate and D-serine in small synaptic like microvesicles in adult hippocampal astrocytes. Cereb. Cortex 22, 1690–1697 (2011)
Hodgkin, A.L., Huxley, A.F.: A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544 (1952)
Shih, J.Y., Atencio, C.A., Schreiner, C.E.: Improved stimulus representation by short interspike intervals in primary auditory cortex. J. Neurophysiol. 105(4), 1908–1917 (2011)
Martiniuc, A.V., Knoll, A.: Interspike interval based filtering of directional selective retinal ganglion cells spike trains. Comput. Intell. Neurosci. 2012, 918030 (2012)
Abarbanel, H.D.I., Huerta, R., Rabinovich, M.I., Rulkov, N.F., Rovat, P.F., Selverston, A.I.: Synchronized action of synaptically coupled chaotic model neurons. Neural Comput. 8, 1567–1602 (1996)
Zhou, C., Kurths, J.: Noise-induced synchronization and coherence resonance of a Hodgkin–Huxley model of thermally sensitive neurons. Chaos 13, 401 (2003)
Ivanchenko, M.V., Osipov, G.V., Shalfeev, V.D., Kurths, J.: Phase synchronization in ensembles of bursting oscillators. Phys. Rev. Lett. 93, 134101–4 (2004)
Wang, Q., Lu, Q., Chen, G., Guo, D.: Chaos synchronization of coupled neurons with gap junction. Phys. Lett. A 356, 17 (2006)
Belykh, V.N., Pankratova, E.V.: Synchronization and control in ensembles of periodic and chaotic neuronal elements with time dependent coupling. IFAC Proc. Vol. 40(14), 120–125 (2007)
Komarov, M.A., Osipov, G.V., Suykens, J.A.K.: Variety of synchronous regimes in neuronal ensembles. Chaos 18, 037121 (2008)
Erichsen, R., Brunnet, L.G.: Multistability in networks of Hindmarsh-Rose neurons. Phys. Rev. E 78(6), 061917 (2008)
Pankratova, E.V., Belykh, V.N., Mosekilde, E.: Dynamics and synchronization of noise perturbed ensembles of periodically activated neuron cells. Int. J. Bifurc. Chaos 18(10), 2807–2815 (2008)
Wang, Z., Shi, X.: Lag synchronization of multiple identical Hindmarsh-Rose neuron models coupled in a ring structure. Nonlinear Dyn. 60, 375–383 (2010)
Torres, J.J., Kappen, H.J.: Emerging phenomena in neural networks with dynamic synapses and their computational implications. Front. Comput. Neurosci. 7, 30 (2013)
Ehrich, S., Pikovsky, A., Rosenblum, M.: From complete to modulated synchrony in networks of identical Hindmarsh-Rose neurons. Eur. Phys. J. Spec. Topics 222, 2407–2416 (2013)
Araque, A., Navarrete, M.: Glial cells in neuronal network function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365(1551), 2375–2381 (2010)
Syková, E., Nicholson, C.: Diffusion in brain extracellular space. Physiol. Rev. 88, 1277–1340 (2008)
Theodosis, D.T., Poulain, D.A., Oliet, S.H.: Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol. Rev. 88, 983–1008 (2008)
Seifert, G., Schilling, K., Steinhaüser, C.: Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat. Rev. Neurosci. 7, 194–206 (2006)
Tzingounis, A.V., Wadiche, J.I.: Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 8, 935–947 (2007)
Maragakis, N.J., Rothstein, J.D.: Glutamate transporters: animal models to neurologic disease. Neurobiol. Dis. 15, 461–473 (2004)
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The numerical computations were carried out on high-performance cluster of Lobachevsky State University of Nizhny Novgorod.
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The work was supported by the Ministry of Science and Higher Education of the Russian Federation (Project No. 14.Y26.31.0022).
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Pankratova, E.V., Kalyakulina, A.I., Stasenko, S.V. et al. Neuronal synchronization enhanced by neuron–astrocyte interaction. Nonlinear Dyn 97, 647–662 (2019). https://doi.org/10.1007/s11071-019-05004-7
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DOI: https://doi.org/10.1007/s11071-019-05004-7