Abstract
We have analysed the synchronisation scenario and the rich spatiotemporal patterns in the network of Hindmarsh-Rose neurons under the influence of self, mixed and cross coupling of state variables which are realised by varying coupling phase. We have introduced a coupling matrix in the model to vary coupling phase. The excitatory and inhibitory couplings in the membrane potential induce in-phase and anti-phase bursting dynamics, respectively, in the two coupled system. When the off-diagonal elements of the matrix are zero, the system shows self coupling of the three variables, which helps to attain synchrony. The off-diagonal elements give cross interactions between the variables, which reduces synchrony. The stability of the synchrony attained is analysed using Lyapunov function approach. In our study, we found that self coupling in three variables is sufficient to induce chimera states in non-local coupling. The strength of incoherence and discontinuity measure validates the existence of chimera and multichimera states. The inhibitor self coupling in local interaction induces interesting patterns like Mixed Oscillatory State and clusters. The results may help in understanding the spatiotemporal communications of the brain, within the limitations of the size of the network analysed in this study.
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The data that support the findings were generated from numerical simulations by the software MATLAB.
Code availability
Code for data simulation was developed by ourselves in MATLAB and will be made available on request.
Change history
14 June 2023
A Correction to this paper has been published: https://doi.org/10.1007/s10867-023-09637-z
References
Swanson, L.W.: Brain Architecture: Understanding the Basic Plan. Oxford University Press (2012)
Bem, T., Le Feuvre, Y., Rinzel, J., Meyrand, P.: Electrical coupling induces bistability of rhythms in networks of inhibitory spiking neurons. Eur. J. Neurosci. 22(10), 2661–2668 (2005)
Bem, T., Rinzel, J.: Short duty cycle destabilizes a half-center oscillator, but gap junctions can restabilize the anti-phase pattern. J. Neurophysiol. 91(2), 693–703 (2004)
Njitacke, Z.T., Doubla, I.S., Kengne, J., Cheukem, A.: Coexistence of firing patterns and its control in two neurons coupled through an asymmetric electrical synapse. Chaos (Woodbury, NY) 30(2), 023101 (2020)
Martin, E.A., Lasseigne, A.M., Miller, A.C.: Understanding the molecular and cell biological mechanisms of electrical synapse formation. Front. Neuroanat. 14, 12 (2020)
Lee, E., Terman, D.: Stable antiphase oscillations in a network of electrically coupled model neurons. SIAM J. Appl. Dyn. Syst. 12(1), 1–27 (2013)
Bashkirtseva, I., Ryashko, L., Pisarchik, A.N.: Stochastic transitions between in-phase and anti-phase synchronization in coupled map-based neural oscillators. Commun. Nonlinear Sci. Numer. Simul. 95, 105611 (2021)
Protachevicz, P.R., Hansen, M., Iarosz, K.C., Caldas, I.L., Batista, A.M., Kurths, J.: Emergence of neuronal synchronisation in coupled brain areas. Front. Comput. Neurosci. 15, 35 (2021)
Jia, B., Wu, Y., He, D., Guo, B., Xue, L.: Dynamics of transitions from anti-phase to multiple in-phase synchronizations in inhibitory coupled bursting neurons. Nonlinear Dyn. 93(3), 1599–1618 (2018)
Korotkov, A.G., Kazakov, A.O., Levanova, T.A., Osipov, G.V.: The dynamics of ensemble of neuron-like elements with excitatory couplings. Commun. Nonlinear Sci. Numer. Simul. 71, 38–49 (2019)
Usha, K., Subha, P.: Hindmarsh-Rose neuron model with memristors. Biosystems 178, 1–9 (2019)
Masoliver, M., Malik, N., Scholl, E., Zakharova, A.: Coherence resonance in a network of FitzHugh-Nagumo systems: interplay of noise, time-delay, and topology. Chaos: An Interdisciplinary Journal of Nonlinear Science 27(10), 101102 (2017)
Boaretto, B., Budzinski, R., Prado, T., Kurths, J., Lopes, S.: Neuron dynamics variability and anomalous phase synchronization of neural networks. Chaos: An Interdisciplinary Journal of Nonlinear Science 28(10), 106304 (2018)
Tang, J., Ma, J., Yi, M., **a, H., Yang, X.: Delay and diversity-induced synchronization transitions in a small-world neuronal network. Phys. Rev. E 83(4), 046207 (2011)
Pakdaman, K., Mestivier, D.: Noise induced synchronization in a neuronal oscillator. Physica D 192(1–2), 123–137 (2004)
Colgin, L.L.: Rhythms of the hippocampal network. Nat. Rev. Neurosci. 17(4), 239–249 (2016)
Lee, E., Terman, D.: Stability of antiphase oscillations in a network of inhibitory neurons. SIAM J. Appl. Dyn. Syst. 14(1), 448–480 (2015)
Vicente, R., Gollo, L.L., Mirasso, C.R., Fischer, I., Pipa, G.: Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays. Proc. Natl. Acad. Sci. U.S.A. 105(44), 17157–17162 (2008)
Lewis, C.M., Baldassarre, A., Committeri, G., Romani, G.L., Corbetta, M.: Learning sculpts the spontaneous activity of the resting human brain. Proc. Natl. Acad. Sci. U.S.A. 106(41), 17558–17563 (2009)
Shmueli, K., van Gelderen, P., de Zwart, J.A., Horovitz, S.G., Fukunaga, M., Jansma, J.M., Duyn, J.H.: Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage 38(2), 306–320 (2007)
Corbetta, M., Shulman, G.L.: Control of goal-directed and stimulus driven attention in the brain. Nat. Rev. Neurosci. 3(3), 201–215 (2002)
Simpson, J.R., Snyder, A.Z., Gusnard, D.A., Raichle, M.E.: Emotion induced changes in human medial prefrontal cortex: I. during cognitive task performance. Proc. Natl. Acad. Sci. U.S.A. 98(2), 683–687 (2001)
Mantini, D., Perrucci, M.G., Del Gratta, C., Romani, G.L., Corbetta, M.: Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U.S.A. 104(32), 13170–13175 (2007)
Horovitz, S.G., Braun, A.R., Carr, W.S., Picchioni, D., Balkin, T.J., Fukunaga, M., Duyn, J.H.: Decoupling of the brain’s default mode network during deep sleep. Proc. Natl. Acad. Sci. U.S.A. 106(27), 11376–11381 (2009)
Cymbalyuk, G.S., Nikolaev, E., Borisyuk, R.: In-phase and antiphase self-oscillations in a model of two electrically coupled pacemakers. Biol. Cybern. 71, 153–160 (1994)
Merrison-Hort, R., Borisyuk, R.: The emergence of two anti-phase oscillatory neural populations in a computational model of the parkinsonian globus pallidus. Front. Comput. Neurosci. 7, 173 (2013)
Li, D., Zhou, C.: Organization of anti-phase synchronization pattern in neural networks: what are the key factors? Front. Syst. Neurosci. 5, 100 (2011)
Koulierakis, I., Verganelakis, D.A., Omelchenko, I., Zakharova, A., Scholl, E., Provata, A.: Structural anomalies in brain networks induce dynamical pacemaker effects. Chaos: An Interdisciplinary Journal of Nonlinear Science 30(11), 113137 (2020)
Wolfrum, M., Omel’chenko, E.: Chimera states are chaotic transients. Phys. Rev. E 84(1), 015204 (2011)
Majhi, S., Bera, B.K., Ghosh, D., Perc, M.: Chimera states in neuronal networks: A review. Phys. Life Rev. 28, 100–121 (2019)
Bera, B.K., Ghosh, D., Lakshmanan, M.: Chimera states in bursting neurons. Phys. Rev. E 93(1), 012205 (2016)
Simo, G.R., Louodop, P., Ghosh, D., Njougouo, T., Tchitnga, R., Cerdeira, H.A.: Traveling chimera patterns in a two-dimensional neuronal network. Phys. Lett. A 127519 (2021)
Dudkowski, D., Czolczynski, K., Kapitaniak, T.: Traveling chimera states for coupled pendula. Nonlinear Dyn. 95(3), 1859–1866 (2019)
Majhi, S., Ghosh, D.: Alternating chimeras in networks of ephaptically coupled bursting neurons. Chaos: An Interdisciplinary Journal of Nonlinear Science 28(8), 083113 (2018)
Zhang, Y., Nicolaou, Z.G., Hart, J.D., Roy, R., Motter, A.E.: Critical switching in globally attractive chimeras. Phys. Rev. X 10(1), 011044 (2020)
Usha, K., Subha, P., Nayak, C.R.: The route to synchrony via drum head mode and mixed oscillatory state in star coupled Hindmarsh-Rose neural network. Chaos, Solitons Fractals 108, 25–31 (2018)
Bandyopadhyay, B., Khatun, T., Dutta, P.S., Banerjee, T.: Symmetry breaking by power-law coupling. Chaos, Solitons Fractals 139, 110289 (2020)
Remi, T., Subha, P., Usha, K.: Collective dynamics of neural network with distance dependent field coupling. Commun. Nonlinear Sci. Numer. Simul. 110, 106390 (2022)
Zakharova, A., Kapeller, M., Scholl, E.: Chimera death: Symmetry breaking in dynamical networks. Phys. Rev. Lett. 112(15), 154101 (2014)
Wang, Z., Xu, Y., Li, Y., Kapitaniak, T., Kurths, J.: Chimera states in coupled Hindmarsh-Rose neurons with \(\alpha\)-stable noise. Chaos Solitons Fractals 148, 110976 (2021)
Kundu, S., Bera, B.K., Ghosh, D., Lakshmanan, M.: Chimera patterns in three-dimensional locally coupled systems. Phys. Rev. E 99(2), 022204 (2019)
Zhang, Y., Motter, A.E.: Mechanism for strong chimeras. Phys. Rev. Lett. 126(9), 094101 (2021)
Asllani, M., Siebert, B.A., Arenas, A., Gleeson, J.P.: Symmetry-breaking mechanism for the formation of cluster chimera patterns. Chaos: An Interdisciplinary Journal of Nonlinear Science 32(1), 013107 (2022)
Shanahan, M.: Metastable chimera states in community-structured oscillator networks. Chaos: An Interdisciplinary Journal of Nonlinear Science 20(1), 013108 (2010)
Budzinski, R.C., Nguyen, T.T., Joan, J., Minac, J., Sejnowski, T.J., Muller, L.E.: Geometry unites synchrony, chimeras, and waves in nonlinear oscillator networks. Chaos: An Interdisciplinary Journal of Nonlinear Science 32(3), 031104 (2022)
Omelchenko, I., Omel’chenko, E., Hovel, P., Scholl, E.: When nonlocal coupling between oscillators becomes stronger: patched synchrony or multichimera states. Phys. Rev. Lett. 110(22), 224101 (2013)
Wang, Z., Liu, Z.: A brief review of chimera state in empirical brain networks. Front. Physiol. 11, 724 (2020)
Pinto, R.D., Varona, P., Volkovskii, A., Szucs, A., Abarbanel, H.D., Rabinovich, M.I.: Synchronous behavior of two coupled electronic neurons. Phys. Rev. E 62(2), 2644 (2000)
Erichsen, R., Jr, Mainieri, M., Brunnet, L.: Periodicity and chaos in electrically coupled Hindmarsh-Rose neurons. Phys. Rev. E 74(6), 061906 (2006)
Pecora, L.M., Carroll, T.L.: Master stability functions for synchronized coupled systems. Phys. Rev. Lett. 80(10), 2109 (1998)
Krasovskii, N.N.: Stability of Motion. Stanford University Press (1963)
Parastesh, F., Azarnoush, H., Jafari, S., Hatef, B., Perc, M., Repnik, R.: Synchronizability of two neurons with switching in the coupling. Appl. Math. Comput. 350, 217–223 (2019)
Hussain, I., Jafari, S., Ghosh, D., Perc, M.: Synchronization and chimeras in a network of photosensitive FitzHugh-Nagumo neurons. Nonlinear Dynamics, 1–11 (2021)
Zhou, P., Hu, X., Zhu, Z., Ma, J.: What is the most suitable Lyapunov function? Chaos, Solitons Fractals 150, 111154 (2021)
Joshi, S.K.: Synchronization of coupled Hindmarsh-Rose neuronal dynamics: Analysis and experiments. Express Briefs, IEEE Transactions on Circuits and Systems II (2021)
Hindmarsh, J.L., Rose, R.: A model of neuronal bursting using three coupled first order differential equations. Proceedings of the Royal society of London. Series B. Biological sciences 221(1222), 87-102 (1984)
Usha, K., Subha, P.: Star-coupled Hindmarsh-Rose neural network with chemical synapses. Int. J. Mod. Phys. C 29(03), 1850023 (2018)
Usha, K., Subha, P.: Energy feedback and synchronous dynamics of Hindmarsh-Rose neuron model with memristor. Chin. Phys. B 28(2), 020502 (2019)
Remi, T., Subha, P., Usha, K.: Controlling phase synchrony in the mean field coupled Hindmarsh-Rose neurons. Int. J. Mod. Phys. C 33(05), 2250058 (2022)
Buric, N., Todorovic, K., Vasovic, N.: Synchronization of bursting neurons with delayed chemical synapses. Phys. Rev. E 78(3), 036211 (2008)
Usha, K., Subha, P.: Collective dynamics and energy aspects of star coupled Hindmarsh-Rose neuron model with electrical, chemical and field couplings. Nonlinear Dyn. 96(3), 2115–2124 (2019)
Erichsen, R., Jr, Brunnet, L.: Multistability in networks of Hindmarsh-Rose neurons. Phys. Rev. E 78(6), 061917 (2008)
Shi, X., Wang, Z.: Adaptive synchronization of time delay Hindmarsh-Rose neuron system via self-feedback. Nonlinear Dyn. 69(4), 2147–2153 (2012)
Buscarino, A., Frasca, M., Branciforte, M., Fortuna, L., Sprott, J.C.: Synchronization of two Rossler systems with switching coupling. Nonlinear Dyn. 88(1), 673–683 (2017)
Yamakou, M.E.: Chaotic synchronization of memristive neurons: Lyapunov function versus Hamilton function. Nonlinear Dyn. 101(1), 487–500 (2020)
Xu, Y., Jia, Y., Ma, J., Hayat, T., Alsaedi, A.: Collective responses in electrical activities of neurons under field coupling. Sci. Rep. 8(1), 1–10 (2018)
Gopal, R., Chandrasekar, V., Venkatesan, A., Lakshmanan, M.: Observation and characterization of chimera states in coupled dynamical systems with nonlocal coupling. Phys. Rev. E 89(5), 052914 (2014)
Acknowledgements
TR would like to thank UGC, India, for the research fellowship through MANF and PAS would like to acknowledge DST, India, for the financial assistance through FIST program.
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All authors contributed to the study conception and design. The work, data simulation and analysis were performed by T. Remi. P. A. Subha made substantial contributions to the conception or design of the work. The first draft of the manuscript was written by T. Remi and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Remi, T., Subha, P. In-phase and anti-phase bursting dynamics and synchronisation scenario in neural network by varying coupling phase. J Biol Phys 49, 345–361 (2023). https://doi.org/10.1007/s10867-023-09635-1
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DOI: https://doi.org/10.1007/s10867-023-09635-1