{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T17:48:48Z","timestamp":1783964928939,"version":"3.55.0"},"reference-count":101,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,5,1]],"date-time":"2023-05-01T00:00:00Z","timestamp":1682899200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100001317","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["22-71-00074"],"award-info":[{"award-number":["22-71-00074"]}],"id":[{"id":"10.13039\/100001317","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Entropy"],"abstract":"<jats:p>We investigated a mathematical model composed of a spiking neural network (SNN) interacting with astrocytes. We analysed how information content in the form of two-dimensional images can be represented by an SNN in the form of a spatiotemporal spiking pattern. The SNN includes excitatory and inhibitory neurons in some proportion, sustaining the excitation\u2013inhibition balance of autonomous firing. The astrocytes accompanying each excitatory synapse provide a slow modulation of synaptic transmission strength. An information image was uploaded to the network in the form of excitatory stimulation pulses distributed in time reproducing the shape of the image. We found that astrocytic modulation prevented stimulation-induced SNN hyperexcitation and non-periodic bursting activity. Such homeostatic astrocytic regulation of neuronal activity makes it possible to restore the image supplied during stimulation and lost in the raster diagram of neuronal activity due to non-periodic neuronal firing. At a biological point, our model shows that astrocytes can act as an additional adaptive mechanism for regulating neural activity, which is crucial for sensory cortical representations.<\/jats:p>","DOI":"10.3390\/e25050745","type":"journal-article","created":{"date-parts":[[2023,5,1]],"date-time":"2023-05-01T12:14:08Z","timestamp":1682943248000},"page":"745","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Information Encoding in Bursting Spiking Neural Network Modulated by Astrocytes"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3032-5469","authenticated-orcid":false,"given":"Sergey V.","family":"Stasenko","sequence":"first","affiliation":[{"name":"Laboratory of Advanced Methods for High-Dimensional Data Analysis, Lobachevsky State University of Nizhny Novgorod, 603022 Nizhny Novgorod, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victor B.","family":"Kazantsev","sequence":"additional","affiliation":[{"name":"Laboratory of Advanced Methods for High-Dimensional Data Analysis, Lobachevsky State University of Nizhny Novgorod, 603022 Nizhny Novgorod, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"187","DOI":"10.3233\/ICA-2007-14301","article-title":"Improved spiking neural networks for EEG classification and epilepsy and seizure detection","volume":"14","author":"Adeli","year":"2007","journal-title":"Integr. Comput.-Aided Eng."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Dora, S., and Kasabov, N. (2021). Spiking Neural Networks for Computational Intelligence: An Overview. Big Data Cogn. Comput., 5.","DOI":"10.3390\/bdcc5040067"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Lobov, S., Chernyshov, A., Krilova, N., Shamshin, M., and Kazantsev, V. (2020). Competitive learning in a spiking neural network: Towards an intelligent pattern classifier. Sensors, 20.","DOI":"10.3390\/s20020500"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2202-7-11","article-title":"An extremely rich repertoire of bursting patterns during the development of cortical cultures","volume":"7","author":"Wagenaar","year":"2006","journal-title":"BMC Neurosci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1080\/net.14.1.103.118","article-title":"Information encoding and computation with spikes and bursts","volume":"14","author":"Kepecs","year":"2003","journal-title":"Netw. Comput. Neural Syst."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"9053","DOI":"10.1523\/JNEUROSCI.22-20-09053.2002","article-title":"Bursting neurons signal input slope","volume":"22","author":"Kepecs","year":"2002","journal-title":"J. Neurosci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1146\/annurev.ne.01.030178.002143","article-title":"Neurophysiology of epilepsy","volume":"1","author":"Prince","year":"1978","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"46","DOI":"10.3389\/fncom.2011.00046","article-title":"Spiking signatures of spontaneous activity bursts in hippocampal cultures","volume":"5","author":"Pimashkin","year":"2011","journal-title":"Front. Comput. Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2937","DOI":"10.1152\/jn.00958.2006","article-title":"Identification and dynamics of spontaneous burst initiation zones in unidimensional neuronal cultures","volume":"97","author":"Feinerman","year":"2007","journal-title":"J. Neurophysiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/nrn1296","article-title":"Burst firing in sensory systems","volume":"5","author":"Krahe","year":"2004","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/j.celrep.2015.12.068","article-title":"Information coding through adaptive gating of synchronized thalamic bursting","volume":"14","author":"Whitmire","year":"2016","journal-title":"Cell Rep."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1016\/j.neuron.2022.06.008","article-title":"Thalamic bursting and the role of timing and synchrony in thalamocortical signaling in the awake mouse","volume":"110","author":"Borden","year":"2022","journal-title":"Neuron"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"7228","DOI":"10.1073\/pnas.86.18.7228","article-title":"T-type calcium channels mediate the transition between tonic and phasic firing in thalamic neurons","volume":"86","author":"Suzuki","year":"1989","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4586","DOI":"10.1073\/pnas.81.14.4586","article-title":"Function of the thalamic reticular complex: The searchlight hypothesis","volume":"81","author":"Crick","year":"1984","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"10731","DOI":"10.1523\/JNEUROSCI.3059-04.2004","article-title":"Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus","volume":"24","author":"Lesica","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1017\/S0952523800007446","article-title":"Dual response modes in lateral geniculate neurons: Mechanisms and functions","volume":"13","author":"Sherman","year":"1996","journal-title":"Vis. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1016\/j.neuron.2007.06.039","article-title":"Feedforward excitation and inhibition evoke dual modes of firing in the cat\u2019s visual thalamus during naturalistic viewing","volume":"55","author":"Wang","year":"2007","journal-title":"Neuron"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1152\/jn.1995.74.3.1222","article-title":"Dynamics of neurons in the cat lateral geniculate nucleus: In vivo electrophysiology and computational modeling","volume":"74","author":"Mukherjee","year":"1995","journal-title":"J. Neurophysiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1038\/nn1591","article-title":"Synaptic background activity controls spike transfer from thalamus to cortex","volume":"8","author":"Wolfart","year":"2005","journal-title":"Nat. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1038\/nature04519","article-title":"Adaptive filtering enhances information transmission in visual cortex","volume":"439","author":"Sharpee","year":"2006","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1523\/JNEUROSCI.4209-04.2005","article-title":"Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation","volume":"25","author":"Wagenaar","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"9","DOI":"10.3389\/fncir.2023.1020487","article-title":"Selective inhibition of excitatory synaptic transmission alters the Emergent Bursting Dyn. Vitr. Neural Networks","volume":"17","author":"Weir","year":"2023","journal-title":"Front. Neural Circuits"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"16610","DOI":"10.1073\/pnas.1316071110","article-title":"Short-term synaptic plasticity in the deterministic Tsodyks\u2013Markram model leads to unpredictable network dynamics","volume":"110","author":"Cortes","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/S0166-2236(00)01835-X","article-title":"Short-term synaptic plasticity as a temporal filter","volume":"24","author":"Fortune","year":"2001","journal-title":"Trends Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3153","DOI":"10.4249\/scholarpedia.3153","article-title":"Short-term synaptic plasticity","volume":"8","author":"Tsodyks","year":"2013","journal-title":"Scholarpedia"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.cell.2015.09.029","article-title":"Others Reconstruction and simulation of neocortical microcircuitry","volume":"163","author":"Markram","year":"2015","journal-title":"Cell"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.neuron.2020.01.040","article-title":"Others Systematic integration of structural and functional data into multi-scale models of mouse primary visual cortex","volume":"106","author":"Billeh","year":"2020","journal-title":"Neuron"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Antolik, J., Hofer, S., Bednar, J., and Mrsic-Flogel, T. (2016). Model constrained by visual hierarchy improves prediction of neural responses to natural scenes. PLoS Comput. Biol., 12.","DOI":"10.1371\/journal.pcbi.1004927"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1007\/s10827-013-0473-5","article-title":"Conductance-based refractory density model of primary visual cortex","volume":"36","author":"Chizhov","year":"2014","journal-title":"J. Comput. Neurosci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1093\/cercor\/bhs358","article-title":"The cell-type specific cortical microcircuit: Relating structure and activity in a full-scale spiking network model","volume":"24","author":"Potjans","year":"2014","journal-title":"Cereb. Cortex"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Kazantsev, V., Gordleeva, S., Stasenko, S., and Dityatev, A. (2012). A Homeostatic Model of Neuronal Firing Governed by Feedback Signals from the Extracellular Matrix, Public Library of Science.","DOI":"10.1371\/journal.pone.0041646"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Lazarevich, I., Stasenko, S., Rozhnova, M., Pankratova, E., Dityatev, A., and Kazantsev, V. (2020). Activity-dependent switches between dynamic regimes of extracellular matrix expression. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0227917"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"111253","DOI":"10.1016\/j.chaos.2021.111253","article-title":"Bifurcation analysis of multistability and oscillation emergence in a model of brain extracellular matrix","volume":"151","author":"Rozhnova","year":"2021","journal-title":"Chaos Solitons Fractals"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Stasenko, S., and Kazantsev, V. (2023). Bursting Dynamics of Spiking Neural Network Induced by Active Extracellular Medium. Mathematics, 11.","DOI":"10.3390\/math11092109"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.brainresbull.2017.01.027","article-title":"From in silico astrocyte cell models to neuron-astrocyte network models: A review","volume":"136","author":"Oschmann","year":"2018","journal-title":"Brain Res. Bull."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1146\/annurev-physiol-021909-135843","article-title":"Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior","volume":"72","author":"Halassa","year":"2010","journal-title":"Annu. Rev. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1002\/glia.24178","article-title":"Astrocyte regulation of neural circuit activity and network states","volume":"70","author":"Oliveira","year":"2022","journal-title":"Glia"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"631485","DOI":"10.3389\/fncel.2021.631485","article-title":"Modeling working memory in a spiking neuron network accompanied by astrocytes","volume":"15","author":"Gordleeva","year":"2021","journal-title":"Front. Cell. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"022410","DOI":"10.1103\/PhysRevE.103.022410","article-title":"Estimating integrated information in bidirectional neuron-astrocyte communication","volume":"103","author":"Abrego","year":"2021","journal-title":"Phys. Rev. E"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"9147","DOI":"10.1007\/s00521-022-06936-9","article-title":"Astrocytes mediate analogous memory in a multi-layer neuron\u2013astrocyte network","volume":"34","author":"Tsybina","year":"2022","journal-title":"Neural Comput. Appl."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1046\/j.1460-9568.1998.00221.x","article-title":"Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons","volume":"10","author":"Araque","year":"1998","journal-title":"Eur. J. Neurosci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/S0166-2236(98)01349-6","article-title":"Tripartite synapses: Glia, the unacknowledged partner","volume":"22","author":"Araque","year":"1999","journal-title":"Trends Neurosci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1002\/hipo.10102","article-title":"Synaptic reentry reinforcement based network model for long-term memory consolidation","volume":"12","author":"Wittenberg","year":"2002","journal-title":"Hippocampus"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"9587","DOI":"10.1523\/JNEUROSCI.19-21-09587.1999","article-title":"Synaptic basis of cortical persistent activity: The importance of NMDA receptors to working memory","volume":"19","author":"Wang","year":"1999","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1038\/35058528","article-title":"GLIA: Listening and talking to the synapse","volume":"2","author":"Haydon","year":"2001","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.tins.2009.05.001","article-title":"Tripartite synapses: Astrocytes process and control synaptic information","volume":"32","author":"Perea","year":"2009","journal-title":"Trends Neurosci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1002\/glia.20431","article-title":"Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission","volume":"55","author":"Perea","year":"2007","journal-title":"Glia"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"tgaa053","DOI":"10.1093\/texcom\/tgaa053","article-title":"Astrocytic regulation of synchronous bursting in cortical cultures: From local to global","volume":"1","author":"Kumar","year":"2020","journal-title":"Cereb. Cortex Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.neuropharm.2017.04.019","article-title":"Astrocytes modulate thalamic sensory processing via mGlu2 receptor activation","volume":"121","author":"Copeland","year":"2017","journal-title":"Neuropharmacology"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1016\/j.neuron.2020.08.013","article-title":"Others Astrocytes control sensory acuity via tonic inhibition in the thalamus","volume":"108","author":"Kwak","year":"2020","journal-title":"Neuron"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1088\/1478-3967\/1\/1\/004","article-title":"Dressed neurons: Modeling neural-glial interactions","volume":"1","author":"Nadkarni","year":"2004","journal-title":"Phys. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1088\/1478-3975\/4\/1\/001","article-title":"Modeling synaptic transmission of the tripartite synapse","volume":"4","author":"Nadkarni","year":"2007","journal-title":"Phys. Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1162\/neco.2007.19.2.303","article-title":"The astrocyte as a gatekeeper of synaptic information transfer","volume":"326","author":"Volman","year":"2007","journal-title":"Neural Comput."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"De Pitta, M., Volman, V., Berry, H., and Ben-Jacob, E. (2011). A tale of two stories: Astrocyte regulation of synaptic depression and facilitation. PloS Comput. Biol., 7, Available online: http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1002293.","DOI":"10.1371\/journal.pcbi.1002293"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.biosystems.2006.04.012","article-title":"Functional modeling of neural-glial interaction","volume":"89","author":"Postnov","year":"2007","journal-title":"Bio-System"},{"key":"ref_56","first-page":"60","article-title":"Functional contributions of astrocytes in synchronization of a neuronal network model","volume":"292C","author":"Amiri","year":"2009","journal-title":"J. Theor. Biol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Wade, J., McDaid, L., Harkin, J., Crunelli, V., and Kelso, J. (2011). Bidirectional Coupling between Astrocytes and Neurons Mediates Learning and Dynamic Coordination in the Brain: A Multiple Modeling Approach. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0029445"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s10827-012-0432-6","article-title":"Astrocyte-neuron interaction as a mechanism responsible for generation of neural synchrony: A study based on modeling and experiments","volume":"34","author":"Amiri","year":"2013","journal-title":"J. Comput. Neurosci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1007\/s11071-019-05004-7","article-title":"Neuronal synchronization enhanced by neuron\u2013astrocyte interaction","volume":"97","author":"Pankratova","year":"2019","journal-title":"Nonlinear Dyn."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"6401","DOI":"10.1038\/s41598-023-33622-0","article-title":"Loss of neuron network coherence induced by virus-infected astrocytes: A model study","volume":"13","author":"Stasenko","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Stasenko, S., and Kazantsev, V. (2023). Dynamic Image Representation in a Spiking Neural Network Supplied by Astrocytes. Mathematics, 11.","DOI":"10.3390\/math11030561"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Stasenko, S., and Kazantsev, V. (2022, January 17\u201321). Astrocytes Enhance Image Representation Encoded in Spiking Neural Network. Proceedings of the Advances In Neural Computation, Machine Learning, And Cognitive Research VI: Selected Papers From The XXIV International Conference On Neuroinformatics, Moscow, Russia.","DOI":"10.1007\/978-3-031-19032-2_20"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"92","DOI":"10.3389\/fncom.2012.00092","article-title":"Bi-directional astrocytic regulation of neuronal activity within a network","volume":"6","author":"Gordleeva","year":"2012","journal-title":"Front. Comput. Neurosci."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"De Pitt\u00e0, M. (2019). Gliotransmitter exocytosis and its consequences on synaptic transmission. Comput. Gliosci., 245\u2013287.","DOI":"10.1007\/978-3-030-00817-8_10"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"92","DOI":"10.3389\/fncom.2019.00092","article-title":"A computational model of interactions between neuronal and astrocytic networks: The role of astrocytes in the stability of the neuronal firing rate","volume":"13","author":"Lenk","year":"2020","journal-title":"Front. Comput. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1134\/S0021364017030092","article-title":"Synaptic multistability and network synchronization induced by the neuron\u2013glial interaction in the brain","volume":"105","author":"Lazarevich","year":"2017","journal-title":"JETP Lett."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/j.procs.2020.02.175","article-title":"Quasi-synchronous neuronal activity of the network induced by astrocytes","volume":"169","author":"Stasenko","year":"2020","journal-title":"Procedia Comput. Sci."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Barabash, N., Levanova, T., and Stasenko, S. (2021, January 13\u201315). STSP model with neuron-glial interaction produced bursting activity. Proceedings of the 2021 Third International Conference Neurotechnologies And Neurointerfaces (CNN), Kaliningrad, Russia.","DOI":"10.1109\/CNN53494.2021.9580314"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Stasenko, S., and Kazantsev, V. (2022, January 14\u201316). 3D model of bursting activity generation. Proceedings of the 2022 Fourth International Conference Neurotechnologies and Neurointerfaces (CNN), Kaliningrad, Russia.","DOI":"10.1109\/CNN56452.2022.9912507"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Barabash, N., Levanova, T., and Stasenko, S. (2023). Rhythmogenesis in the mean field model of the neuron\u2013glial network. Eur. Phys. J. Spec. Top., 1\u20136.","DOI":"10.1140\/epjs\/s11734-023-00778-9"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s10867-009-9156-x","article-title":"Dynamical patterns of calcium signaling in a functional model of neuron\u2013astrocyte networks","volume":"35","author":"Postnov","year":"2009","journal-title":"J. Biol. Phys."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e2207912119","DOI":"10.1073\/pnas.2207912119","article-title":"Multiple forms of working memory emerge from synapse\u2013astrocyte interactions in a neuron\u2013glia network model","volume":"119","author":"Brunel","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Blum Moyse, L., and Berry, H. (2022). Modelling the modulation of cortical Up-Down state switching by astrocytes. PLoS Comput. Biol., 18.","DOI":"10.1101\/2022.03.10.483735"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Izhikevich, E. (2007). Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting, The MIT Press.","DOI":"10.7551\/mitpress\/2526.001.0001"},{"key":"ref_75","first-page":"83","article-title":"Noise-induced coherent firing patterns in small neural ensembles with ionic coupling","volume":"16","author":"Postnov","year":"2008","journal-title":"Izv. VUZ. Appl. Nonlinear Dyn."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1109\/TNN.2004.832719","article-title":"Which model to use for cortical spiking neurons?","volume":"15","author":"Izhikevich","year":"2004","journal-title":"IEEE Trans. Neural Netw."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"6920","DOI":"10.1523\/JNEUROSCI.0473-04.2004","article-title":"Glutamate released from glial cells synchronizes neuronal activity in the hippocampus","volume":"24","author":"Angulo","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/j.neuropharm.2009.06.031","article-title":"Tripartite synapses: Roles for astrocytic purines in the control of synaptic physiology and behavior","volume":"57","author":"Halassa","year":"2009","journal-title":"Neuropharmacology"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1126\/science.1144640","article-title":"Astrocytes potentiate transmitter release at single hippocampal synapses","volume":"317","author":"Perea","year":"2007","journal-title":"Science"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/nn1849","article-title":"Glutamate exocytosis from astrocytes controls synaptic strength","volume":"10","author":"Jourdain","year":"2007","journal-title":"Nat. Neurosci."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1523\/JNEUROSCI.2859-03.2004","article-title":"Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons","volume":"24","author":"Fiacco","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_82","unstructured":"Lecarme, O., and Delvare, K. (2013). The Book of GIMP: A Complete Guide to Nearly Everything, No Starch Press."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/0306-4522(89)90402-8","article-title":"Populations of GABAergic neurons and axons in layer I of rat auditory cortex","volume":"33","author":"Winer","year":"1989","journal-title":"Neuroscience"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"40","DOI":"10.3389\/fnana.2014.00040","article-title":"Trajectory of the main GABAergic interneuron populations from early development to old age in the rat primary auditory cortex","volume":"8","author":"Ouellet","year":"2014","journal-title":"Front. Neuroanat."},{"key":"ref_85","unstructured":"Braitenberg, V., and Sch\u00fcz, A. (2013). Cortex: Statistics and Geometry of Neuronal Connectivity, Springer."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"8441","DOI":"10.1523\/JNEUROSCI.1400-04.2004","article-title":"A quantitative map of the circuit of cat primary visual cortex","volume":"24","author":"Binzegger","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"15927","DOI":"10.1073\/pnas.1010356107","article-title":"Neuron densities vary across and within cortical areas in primates","volume":"107","author":"Collins","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Alreja, A., Nemenman, I., and Rozell, C. (2022). Constrained brain volume in an efficient coding model explains the fraction of excitatory and inhibitory neurons in sensory cortices. PLoS Comput. Biol., 18.","DOI":"10.1371\/journal.pcbi.1009642"},{"key":"ref_89","unstructured":"Stimberg, M., Goodman, D., Brette, R., and Pitt\u00e0, M. (2019). Computational Glioscience, Springer."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3158","DOI":"10.1523\/JNEUROSCI.18-09-03158.1998","article-title":"Extrasynaptic glutamate diffusion in the hippocampus: Ultrastructural constraints, uptake, and receptor activation","volume":"18","author":"Rusakov","year":"1998","journal-title":"J. Neurosci."},{"key":"ref_91","unstructured":"Van Rossum, G., and Drake, F. (1995). Python Tutorial, Centrum voor Wiskunde en Informatica."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"e47314","DOI":"10.7554\/eLife.47314","article-title":"Brian 2, an intuitive and efficient neural simulator","volume":"8","author":"Stimberg","year":"2019","journal-title":"eLife"},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Bisong, E. (2019). Building Machine Learning and Deep Learning Models on Google Cloud Platform: A Comprehensive Guide for Beginners, Apress.","DOI":"10.1007\/978-1-4842-4470-8"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"8","DOI":"10.4236\/jcc.2019.73002","article-title":"Image quality assessment through FSIM, SSIM, MSE and PSNR\u2014A comparative study","volume":"7","author":"Sara","year":"2019","journal-title":"J. Comput. Commun."},{"key":"ref_95","first-page":"9989","article-title":"The level weighted structural similarity loss: A step away from MSE","volume":"33","author":"Lu","year":"2019","journal-title":"Proc. AAAI Conf. Artif. Intell."},{"key":"ref_96","unstructured":"S\u00f8gaard, J., Krasula, L., Shahid, M., Temel, D., Brunnstr\u00f6m, K., and Razaak, M. (2016). Electronic Imaging, Image Quality And System Performance XIII, Society for Imaging Science and Technology."},{"key":"ref_97","first-page":"918","article-title":"Video quality assessment through PSNR estimation for different compression standards","volume":"11","author":"Deshpande","year":"2018","journal-title":"Indones. J. Electr. Eng. Comput. Sci."},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Hore, A., and Ziou, D. (2010, January 23\u201326). Image quality metrics: PSNR vs. SSIM. Proceedings of the 2010 20th International Conference On Pattern Recognition, Istanbul, Turkey.","DOI":"10.1109\/ICPR.2010.579"},{"key":"ref_99","unstructured":"Khalel, A. (2023, February 20). Sewar: A Python Package for Image Quality Assessment Using Different Metrics. GitHub Repository. Available online: https:\/\/github.com\/andrewekhalel\/sewar."},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"De Pitt\u00e0, M., and Berry, H. (2019). Computational Glioscience, Springer.","DOI":"10.1007\/978-3-030-00817-8"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"2100669","DOI":"10.1002\/aelm.202100669","article-title":"Artificial astrocyte memristor with recoverable linearity for neuromorphic computing","volume":"8","author":"Cheng","year":"2022","journal-title":"Adv. Electron. Mater."}],"container-title":["Entropy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1099-4300\/25\/5\/745\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:27:56Z","timestamp":1760124476000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1099-4300\/25\/5\/745"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,1]]},"references-count":101,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["e25050745"],"URL":"https:\/\/doi.org\/10.3390\/e25050745","relation":{},"ISSN":["1099-4300"],"issn-type":[{"value":"1099-4300","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,1]]}}}