For citation:
Stasenko S. V. Burst dynamics of a spiking neural network caused by the activity of the extracellular matrix of the brain. Izvestiya of Saratov University. Physics , 2024, vol. 24, iss. 2, pp. 138-149. DOI: 10.18500/1817-3020-2024-24-2-138-149, EDN: EOSDSZ
Burst dynamics of a spiking neural network caused by the activity of the extracellular matrix of the brain
Background and Objectives: The purpose of this work is to study the influence of the extracellular matrix of the brain on the formation of burst dynamics of a spiking neural network. Materials and Methods: The Izhikevich neuron model was used as a neuron model. To describe the dynamics of the extracellular matrix of the brain, the phenomenological model of Kazantsev, constructed using the formalism of the Hodgkin – Huxley model, was used. A model of the formation of burst dynamics of a spiking neural network under the influence of the extracellular matrix of the brain was developed and studied. Results: The main dynamic modes of neural activity have been obtained in the absence of regulation and in the presence of the extracellular matrix of the brain. Conclusion: It has been explored how the modulation by the extracellular matrix of the brain can influence the frequency of burst activity of the neural network. It has been found that the regulation of neural activity, mediated by the extracellular matrix of the brain, promotes the grouping of spikes into quasi-synchronous population discharges, called population bursts. In this case, an increase in the strength of the influence of the extracellular matrix of the brain on postsynaptic currents through synaptic scaling leads to an increase in the degree of synchrony of neuron populations.
- Fell J., Axmacher N. The role of phase synchronization in memory processes. Nature Reviews Neuroscience, 2011, vol. 12, iss. 2, pp. 105–118. https://doi.org/10.1038/nrn2979
- Baldauf D., Desimone R. Neural mechanisms of object-based attention. Science, 2014, vol. 344, iss. 6182, pp. 424–427. https://doi.org/10.1126/science.1247003
- Timofeev I., Bazhenov M., Seigneur J., Sejnowski T. Neuronal synchronization and thalamocortical rhythms in sleep, wake and epilepsy. In: Jasper’s basic mechanisms of the epilepsies [Internet]. 4th ed. Bethesda (MD), National Center for Biotechnology Information (US), 2012. https://doi.org/10.1093/med/9780199746545.001.0001
- Fries P., Reynolds J., Rorie A., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science, 2001, vol. 291, iss. 5508, pp. 1560–1563. https://doi.org/10.1126/science.1055465
- Wagenaar D., Pine J., Potter S. An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neuroscience, 2006, vol. 7, article no. 11. https://doi.org/10.1186/1471-2202-7-11
- Wagenaar D., Nadasdy Z., Potter S. Persistent dynamic attractors in activity patterns of cultured neuronal networks. Physical Review E, 2006, vol. 73, iss. 5, pt. 1, article no. 051907. https://doi.org/10.1103/physreve.73.051907
- Zeldenrust F., Wadman W., Englitz B. Neural coding with bursts-current state and future perspectives. Frontiers in Computational Neuroscience, 2018, vol. 12, article no. 48. https://doi.org/10.3389/fncom.2018.00048
- Pimashkin A., Kastalskiy I., Simonov A., Koryagina E., Mukhina I., Kazantsev V. Spiking signatures of spontaneous activity bursts in hippocampal cultures. Frontiers in Computational Neuroscience, 2011, vol. 5, article no. 46. https://doi.org/10.3389/fncom.2011.00046
- Wang X. Neurophysiological and computational principles of cortical rhythms in cognition. Physiological Reviews, 2010, vol. 90, iss. 3, pp. 1195–1268. https://doi.org/10.1152/physrev.00035.2008
- Zeitler M., Daffertshofer A., Gielen C. Asymmetry in pulse-coupled oscillators with delay. Physical Review E, 2009, vol. 79, article no. 065203. https://doi.org/10.1103/PhysRevE.79.065203
- Pikovsky A., Rosenblum M., Kurths J. Synchronization: A universal concept in nonlinear science. Cambridge University Press, 2001. 432 p. https://doi.org/10.1017/CBO9780511755743
- Tsybina Y., Kastalskiy I., Kazantsev V., Gordleeva S. Synchronization events in a spiking neural network. 2022 Fourth International Conference Neurotechnologies And Neurointerfaces (CNN), 2022, pp. 206–208. https://doi.org/10.1109/CNN56452.2022.9912521
- Simonov A., Gordleeva S. Synchronization with an arbitrary phase shift in a pair of synaptically coupled neural oscillators. JETP Letters, 2014, vol. 98, iss. 10, pp. 632–637. https://doi.org/10.1134/S0021364013230136
- Barabash N., Levanova T., Stasenko S. Rhythmogenesis in the mean field model of the neuron-glial network. The European Physical Journal Special Topics, 2023, pp. 1–6. https://doi.org/10.1140/epjs/s11734-023-00778-9
- Stasenko S., Kazantsev V. 3D model of bursting activity generation. 2022 Fourth International Conference Neurotechnologies And Neurointerfaces (CNN), 2022, pp. 176–179. https://doi.org/10.1109/CNN56452.2022.9912507
- Olenin S., Levanova T., Stasenko S. Dynamics in the Reduced Mean-Field Model of Neuron-Glial Interaction. Mathematics, 2023, vol. 11, iss. 9, pp. 2143. https://doi.org/10.3390/math11092143
- Makovkin S., Kozinov E., Ivanchenko M., Gordleeva S. Controlling synchronization of gamma oscillations by astrocytic modulation in a model hippocampal neural network. Scientific Reports, 2022, vol. 12, article no. 6970. https://doi.org/10.1038/s41598-022-10649-3
- Stasenko S., Hramov A., Kazantsev V. Loss of neuron network coherence induced by virus-infected astrocytes: A model study. Scientific Reports, 2023, vol. 13, article no. 6401. https://doi.org/10.1038/s41598-023-33622-0
- Stasenko S., Kazantsev V. Dynamic Image Representation in a Spiking Neural Network Supplied by Astrocytes. Mathematics, 2023, vol. 11, iss. 3, article no. 561. https://doi.org/10.3390/math11030561
- Dityatev A., Rusakov D. Molecular signals of plasticity at the tetrapartite synapse. Current Opinion in Neurobiology, 2011, vol. 21, iss. 2, pp. 353–359. https://doi.org/10.1016/j.conb.2010.12.006
- Kazantsev V., Gordleeva S., Stasenko S., Dityatev A. A homeostatic model of neuronal firing governed by feedback signals from the extracellular matrix. PloS ONE, 2012, vol. 7, iss. 7, article no. e41646.
- Rich M., Wenner P. Sensing and expressing homeostatic synaptic plasticity. Trends in Neurosciences, 2007, vol. 30, iss. 3, pp. 119–125. https://doi.org/10.1371/journal.pone.0041646
- Turrigiano G. Homeostatic signaling: The positive side of negative feedback. Current Opinion in Neurobiology, 2007, vol. 17, iss. 3, pp. 318–324. https://doi.org/10.1016/j.conb.2007.04.004
- Kochlamazashvil G., Henneberger C., Bukalo O., Dvoretskova E., Senkov O., Lievens P., Westenbroek R., Engel A., Catterall W., Rusakov D., Schachner M., Dityatev A. The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-type Ca2+ channels. Neuron, 2010, vol. 67, iss. 1, pp. 116–128. https://doi.org/10.1016/j.neuron.2010.05.030
- Hodgkin A., Huxley A. A quantitative description of membrane current and its application to conduction and excitation in nerve. The Journal of Physiology, 1952, vol. 117, iss. 4, pp. 500–544. https://doi.org/10.1113%2Fjphysiol.1952.sp004764
- Fawcett J., Fyhn M., Jendelova P., Kwok J., Ruzicka J., Sorg B. The extracellular matrix and perineuronal nets in memory. Molecular Psychiatry, 2022, vol. 27, pp. 3192–3203. https://doi.org/10.1038/s41380-022-01634-3
- Dityatev A. Remodeling of extracellular matrix and epileptogenesis. Epilepsia, 2010, vol. 51, iss. 3, pp. 61–65. https://doi.org/10.1111/j.1528-1167.2010.02612.x
- Dityatev A., Fellin T. Extracellular matrix in plasticity and epileptogenesis. Neuron Glia Biology, 2008, vol. 4, iss. 3, pp. 235–247. https://doi.org/10.1017/s1740925x09000118
- Jong J., Broekaart D., Bongaarts A., Mühlebner A., Mills J., Vliet E., Aronica E. Altered Extracellular Matrix as an Alternative Risk Factor for Epileptogenicity in Brain Tumors. Biomedicines, 2022, vol. 10, iss. 10, article no. 2475. https://doi.org/10.3390/biomedicines10102475
- Lobov S., Zharinov A., Makarov V., Kazantsev V. Spatial memory in a spiking neural network with robot embodiment. Sensors, 2021, vol. 21, iss. 8, article no. 2678. https://doi.org/10.3390/s21082678
- Kim J., Lee H., Cho W., Lee K. Encoding information into autonomously bursting neural network with pairs of time-delayed pulses. Scientific Reports, 2019, vol. 9, article no. 1394. https://doi.org/10.1038/s41598-018-37915-7
- Lundqvis M., Rose J., Herman P., Brincat S., Buschman T. Miller E. Gamma and beta bursts underlie working memory. Neuron, 2016, vol. 90, iss. 1, pp. 152–164. https://doi.org/10.1016/j.neuron.2016.02.028
- Sokolov I., Azieva A., Burtsev M. Patterns of spiking activity of neuronal networks in vitro as memory traces. Biologically Inspired Cognitive Architectures (BICA) for Young Scientists: Proceedings of The First International Early Research Career Enhancement School (FIERCES 2016), 2016, pp. 241–247. https://doi.org/10.1007/978-3-319-32554-5_31
- Lam D., Enright H., Cadena J., Peters S., Sales A., Osburn J., Soscia D., Kulp K., Wheeler E., Fischer N. Tissue-specific extracellular matrix accelerates the formation of neural networks and communities in a neuronglia co-culture on a multi-electrode array. Scientific Reports, 2019, vol. 9, article no. 4159. https://doi.org/10.1038/s41598-019-40128-1
- Bikbaev A., Frischknecht R., Heine M. Brain extracellular matrix retains connectivity in neuronal networks. Scientific Reports, 2015, vol. 5, article no. 14527. https://doi.org/10.1038/srep14527
- Izhikevich E. Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting. Dynamical Systems. The MIT Press, 2007, First. 458 p. https://doi.org/10.7551/mitpress/2526.001.0001
- Lazarevich I., Stasenko S., Rozhnova M., Pankratova E., Dityatev A., Kazantsev V. Activity-dependent switches between dynamic regimes of extracellular matrix expression. PLoS ONE, 2020, vol. 15, iss. 1, article no. e0227917. https://doi.org/10.1371/journal.pone.0227917
- Rozhnova M., Pankratova E., Stasenko S., Kazantsev V. Bifurcation analysis of multistability and oscillation emergence in a model of brain extracellular matrix. Chaos, Solitons & Fractals, 2021, vol. 151, article no. 111253. https://doi.org/10.1016/j.chaos.2021.111253
- Sterrat D., Graham B., Gillies A., Willshaw D. Principles of computational modelling in neuroscience. Cambridge University Press, 2011. 404 p. https://doi.org/10.1017/CBO9780511975899
- Frischknecht R., Gundelfinger E. The brain’s extracellular matrix and its role in synaptic plasticity. Synaptic Plasticity, 2012, vol. 970, pp. 153–171. https://doi.org/10.1007/978-3-7091-0932-8_7
- Van Rossum Guido, Drake Fred L. Python 3 Reference Manual. CreateSpace Independent Publishing Platform, 2015. 364 p.
- Nelli F. Python data analytics: Data analysis and science using pandas, matplotlib, and the python programming language. Apress, 2015. 364 pp.
- Stimberg M., Brette R., Goodman D. Brian 2, an intuitive and efficient neural simulator. Elife, 2019, vol. 8, article no. e47314. https://doi.org/10.7554/eLife.47314
- Bisong E. Building machine learning and deep learning models on google cloud platform. Apress Berkeley, CA, 2019. 740 p. https://doi.org/10.1007/978-1-4842-4470-8
- Virtanen P., Gommers R., Oliphant T., Haberland M., Reddy T., Cournapeau D., Burovski E., Peterson P., Weckesser W., Bright J. SciPy 1.0: Fundamental algorithms for scientific computing in Python. Nature Methods, 2020, vol. 17, pp. 261–272. https://doi.org/10.1038/s41592-019-0686-2
- Duarte M. detecta: A Python module to detect events in data. GitHub Repository, 2020. Available at: https://github.com/demotu/detecta (accessed March 10, 2024).
- Gerstner W., Kistler W., Naud R., Paninski L. Neuronal dynamics: From single neurons to networks and models of cognition [Internet]. Cambridge University Press, 2014. https://doi.org/10.1017/CBO9781107447615
- Stasenko S., Kazantsev V. Mean-field model of tetrapartite synapse. 2022 Fourth International Conference Neurotechnologies And Neurointerfaces (CNN), 2022, pp. 180–184. https://doi.org/10.1109/CNN56452.2022.9912561
- Dityatev A. Remodeling of extracellular matrix and epileptogenesis. Epilepsia, 2010, vol. 51, iss. 3, pp. 61–65. https://doi.org/10.1111/j.1528-1167.2010.02612.x
- Dityatev A., Fellin T. Extracellular matrix in plasticity and epileptogenesis. Neuron Glia Biology, 2008, vol. 4, iss. 3, pp. 235–247. https://doi.org/10.1017/s1740925x09000118
- Bonneh-Barkay D., Wiley C. Brain extracellular matrix in neurodegeneration. Brain Pathology, 2009, vol. 19, iss. 4, pp. 573–585. https://doi.org/10.1111/j.1750-3639.2008.00195.x
- Khoshneviszadeh M., Jandke S., Kaushik R., Ulbrich P., Norman O., Jukkola J., Heikkinen A., Schreiber S., Dityatev A. Microvascular damage, neuroinflammation and extracellular matrix remodeling in Col18a1 knockout mice as a model for early cerebral small vessel disease. Matrix Biol., 2024, vol. 128, pp. 39–64. https://doi.org/10.1016/j.matbio.2024.02.007
- Ulbrich P., Khoshneviszadeh M., Jandke S., Schreiber S., Dityatev A. Interplay between perivascular and perineuronal extracellular matrix remodelling in neurological and psychiatric diseases. European Journal of Neuroscience, 2021, vol. 53, iss. 12, pp. 3811–3830. https://doi.org/10.1111/ejn.14887
- Broekaart D. W., Bertran A., Jia S., Korotkov A., Senkov O., Bongaarts A., Mills J. D., Anink J. J., Seco J., Baayen J. C., Idema S., Chabrol E., Becker A. J., Wadman W. J., Tarragó T., Gorter J. A., Aronica E., Prades R., Dityatev A., Vliet E. A. van The matrix metalloproteinase inhibitor IPR-179 has antiseizure and antiepileptogenic effects. The Journal of Clinical Investigation, 2021, vol. 131, iss. 1, article no. e138332. https://doi.org/10.1172/jci138332
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