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It is well known that the relative percentage of inhibitory neurons is much smaller than excitatory neurons in the cortex. So, in general, how inhibitory neurons can keep the balance with the surrounding excitatory neurons is an important question. There is much accumulated knowledge about this fundamental question. This study quantitatively evaluated the relatively higher functional contribution of inhibitory neurons in terms of not only properties of individual neurons, such as firing rate, but also in terms of topological mechanisms and controlling ability on other excitatory neurons. We combined simultaneous electrical recording (~2.5 hours) of ~1000 neurons in vitro, and quantitative evaluation of neuronal interactions including excitatory-inhibitory categorization. This study accurately defined recording brain anatomical targets, such as brain regions and cortical layers, by inter-referring MRI and immunostaining recordings. The interaction networks enabled us to quantify topological influence of individual neurons, in terms of controlling ability to other neurons. Especially, the result indicated that highly influential inhibitory neurons show higher controlling ability of other neurons than excitatory neurons, and are relatively often distributed in deeper layers of the cortex. Furthermore, the neurons having high controlling ability are more effectively limited in number than central nodes of k-cores, and these neurons also participate in more clustered motifs. In summary, this study suggested that the high controlling ability of inhibitory neurons is a key mechanism to keep balance with a large number of other excitatory neurons beyond simple higher firing rate. Application of the selection method of limited important neurons would be also applicable for the ability to effectively and selectively stimulate E\/I imbalanced disease states.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1008846","type":"journal-article","created":{"date-parts":[[2021,4,8]],"date-time":"2021-04-08T13:29:40Z","timestamp":1617888580000},"page":"e1008846","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":32,"title":["Inhibitory neurons exhibit high controlling ability in the cortical 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hippocampal inhibition and a selective loss of interneurons in experimental epilepsy","volume":"235","author":"RS Sloviter","year":"1987","journal-title":"Science"},{"issue":"4","key":"pcbi.1008846.ref002","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1038\/nrn1648","article-title":"Cortical inhibitory neurons and schizophrenia","volume":"6","author":"DA Lewis","year":"2005","journal-title":"Nature Reviews Neuroscience"},{"issue":"5","key":"pcbi.1008846.ref003","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1034\/j.1601-183X.2003.00037.x","article-title":"Model of autism: increased ratio of excitation\/inhibition in key neural systems","volume":"2","author":"JLR Rubenstein","year":"2003","journal-title":"Genes, Brain and Behavior"},{"issue":"4","key":"pcbi.1008846.ref004","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1016\/j.neuron.2015.07.033","article-title":"Excitatory\/inhibitory balance and circuit homeostasis in autism spectrum 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Sillito","year":"1975","journal-title":"The Journal of physiology"},{"key":"pcbi.1008846.ref008","doi-asserted-by":"crossref","first-page":"e26724","DOI":"10.7554\/eLife.26724","article-title":"Beyond excitation\/inhibition imbalance in multidimensional models of neural circuit changes in brain disorders","volume":"6","author":"C O\u2019Donnell","year":"2017","journal-title":"Elife"},{"issue":"2","key":"pcbi.1008846.ref009","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1016\/j.neuroimage.2012.01.032","article-title":"The future of the human connectome","volume":"62","author":"DC Van Essen","year":"2012","journal-title":"Neuroimage"},{"issue":"3","key":"pcbi.1008846.ref010","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/nrn2575","article-title":"Complex brain networks: graph theoretical analysis of structural and functional systems","volume":"10","author":"E Bullmore","year":"2009","journal-title":"Nature reviews 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Proceedings of the 21st Annual Conference of the Japanese Neural Network Society, 2011."},{"key":"pcbi.1008846.ref015","article-title":"Mesoscopic neuronal activity and neuronal network architecture. Proceedings of the 34th annual meeting of the","author":"M Shimono","year":"2011","journal-title":"Japan Neuroscience Society"},{"key":"pcbi.1008846.ref016","article-title":"Functional clusters, hubs and communities in the cortical microconnectome","author":"M Shimono","year":"2014","journal-title":"Cerebral Cortex"},{"key":"pcbi.1008846.ref017","doi-asserted-by":"crossref","first-page":"290","DOI":"10.5486\/PMD.1959.6.3-4.12","article-title":"On Random Graphs. I","volume":"6","author":"P Erd\u0151s","year":"1959","journal-title":"Publicationes Mathematicae"},{"issue":"12","key":"pcbi.1008846.ref018","doi-asserted-by":"crossref","first-page":"2891","DOI":"10.1093\/cercor\/bhn047","article-title":"A small world of neuronal synchrony","volume":"18","author":"S Yu","year":"2008","journal-title":"Cerebral cortex"},{"issue":"6684","key":"pcbi.1008846.ref019","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1038\/30918","article-title":"Collective dynamics of \u2019small-world\u2019 networks","volume":"393","author":"DJ Watts","year":"1998","journal-title":"Nature"},{"issue":"5958","key":"pcbi.1008846.ref020","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1126\/science.1175509","article-title":"GABAergic hub neurons orchestrate synchrony in developing hippocampal networks","volume":"326","author":"P Bonifazi","year":"2009","journal-title":"Science"},{"issue":"5439","key":"pcbi.1008846.ref021","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1126\/science.286.5439.509","article-title":"Emergence of scaling in random networks","volume":"286","author":"AL Barab\u00e1si","year":"1999","journal-title":"Science"},{"issue":"4","key":"pcbi.1008846.ref022","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/nrn3687","article-title":"The log-dynamic brain: how skewed distributions affect network operations","volume":"15","author":"G Buzs\u00e1ki","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"issue":"7337","key":"pcbi.1008846.ref023","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1038\/nature09802","article-title":"Network anatomy and in vivo physiology of visual cortical neurons","volume":"471","author":"DD Bock","year":"2011","journal-title":"Nature"},{"issue":"4","key":"pcbi.1008846.ref024","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1016\/j.neuron.2013.12.029","article-title":"Structured connectivity in cerebellar inhibitory networks","volume":"81","author":"S Rieubland","year":"2014","journal-title":"Neuron"},{"key":"pcbi.1008846.ref025","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.jtbi.2013.06.009","article-title":"Dynamics and control at feedback vertex sets. II: A faithful monitor to determine the diversity of molecular activities in regulatory networks","volume":"335","author":"A Mochizuki","year":"2013","journal-title":"Journal of theoretical biology"},{"issue":"10","key":"pcbi.1008846.ref026","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1089\/cmb.2018.0019","article-title":"Analysis of critical and redundant vertices in controlling directed complex networks using feedback vertex sets","volume":"25","author":"Y Bao","year":"2018","journal-title":"Journal of Computational Biology"},{"issue":"28","key":"pcbi.1008846.ref027","doi-asserted-by":"crossref","first-page":"7234","DOI":"10.1073\/pnas.1617387114","article-title":"Structure-based control of complex networks with nonlinear dynamics","volume":"114","author":"JGT Zanudo","year":"2017","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1008846.ref028","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1162\/netn_a_00115","article-title":"Synthetic ablations in the C. elegans nervous system","volume":"4","author":"EK Towlson","year":"2020","journal-title":"Network Neuroscience"},{"issue":"1","key":"pcbi.1008846.ref029","first-page":"1","article-title":"Controllability of structural brain networks","volume":"6","author":"S Gu","year":"2015","journal-title":"Nature communications"},{"issue":"1\u20132","key":"pcbi.1008846.ref030","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1002\/hbm.460020107","article-title":"Functional and effective connectivity in neuroimaging: a synthesis","volume":"2","author":"KJ Friston","year":"1994","journal-title":"Human brain mapping"},{"key":"pcbi.1008846.ref031","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/0006-8993(91)90974-Z","article-title":"Structural modeling of functional neural pathways mapped with 2-deoxyglucose: effects of acoustic startle habituation on the auditory system","volume":"547","author":"AR McIntosh","year":"1991","journal-title":"Brain Res."},{"issue":"5","key":"pcbi.1008846.ref032","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1152\/jn.1989.61.5.900","article-title":"Dynamics of neuronal firing correlation: modulation of effective connectivity","volume":"61","author":"AM Aertsen","year":"1989","journal-title":"Journal of neurophysiology"},{"key":"pcbi.1008846.ref033","doi-asserted-by":"crossref","first-page":"056117","DOI":"10.1103\/PhysRevE.76.056117","article-title":"Information transfer at multiple scales","volume":"76","author":"M Lungarella","year":"2007","journal-title":"Phys. Rev. E Stat. Nonlin. Soft Matter Phys."},{"issue":"2","key":"pcbi.1008846.ref034","doi-asserted-by":"crossref","first-page":"026222","DOI":"10.1103\/PhysRevE.72.026222","article-title":"Assessing causality from multivariate time series","volume":"72","author":"PF Verdes","year":"2005","journal-title":"Physical Review E"},{"issue":"1","key":"pcbi.1008846.ref035","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/s10827-010-0262-3","article-title":"Transfer entropy\u2014a model-free measure of effective connectivity for the neurosciences","volume":"30","author":"R Vicente","year":"2011","journal-title":"Journal of computational neuroscience"},{"issue":"2","key":"pcbi.1008846.ref036","doi-asserted-by":"crossref","first-page":"026110","DOI":"10.1103\/PhysRevE.77.026110","article-title":"Local information transfer as a spatiotemporal filter for complex systems","volume":"77","author":"JT Lizier","year":"2008","journal-title":"Physical Review E"},{"issue":"1","key":"pcbi.1008846.ref037","doi-asserted-by":"crossref","first-page":"012121","DOI":"10.1103\/PhysRevE.100.012121","article-title":"Reconstructing positive and negative couplings in Ising spin networks by sorted local transfer entropy","volume":"100","author":"F Goetze","year":"2019","journal-title":"Physical Review E"},{"key":"pcbi.1008846.ref038","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1523\/JNEUROSCI.2177-15.2016","article-title":"Rich-club organization in effective connectivity among cortical neurons","volume":"36","author":"S Nigam","year":"2016","journal-title":"Journal of Neuroscience"},{"issue":"147","key":"pcbi.1008846.ref039","article-title":", 3D Scanning Technology Bridging Microcircuits and Macroscale Brain Images in 3D Novel Embedding Overlapping Protocol","author":"S Ide","year":"2019","journal-title":"Journal of visualized experiments: JoVE"},{"key":"pcbi.1008846.ref040","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1093\/biomet\/48.3-4.303","article-title":"Inconsistencies in a schedule of paired comparisons","volume":"48","author":"P Slater","year":"1961","journal-title":"Biometrika"},{"key":"pcbi.1008846.ref041","doi-asserted-by":"crossref","unstructured":"Karp RM, Reducibility Among Combinatorial Problems. Proc. Symposium on Complexity of Computer Computations, 1972;85\u2013103.","DOI":"10.1007\/978-1-4684-2001-2_9"},{"key":"pcbi.1008846.ref042","first-page":"151","article-title":"A system for identifying genetic networks from gene expression patterns produced by gene disruptions and overexpressions","volume":"9","author":"T Akutsu","year":"1998","journal-title":"Genome Informatics"},{"key":"pcbi.1008846.ref043","article-title":"Kaji_EICont","volume":"V1","author":"M Kajiwara","year":"2021","journal-title":"Mendeley Data"},{"key":"pcbi.1008846.ref044","first-page":"423","article-title":"Revealing neuronal function through microelectrode array recordings","volume":"8","author":"MEJ Obien","year":"2015","journal-title":"Frontiers in neuroscience"},{"key":"pcbi.1008846.ref045","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1117\/12.57955","volume-title":"Method for registration of 3-D shapes. Sensor fusion IV: control paradigms and data structures","author":"P Besl","year":"1992"},{"key":"pcbi.1008846.ref046","doi-asserted-by":"crossref","first-page":"e34518","DOI":"10.7554\/eLife.34518","article-title":"A spike sorting toolbox for up to thousands of electrodes validated with ground truth recordings in vitro and in vivo","volume":"7","author":"P Yger","year":"2018","journal-title":"Elife"},{"issue":"6191","key":"pcbi.1008846.ref047","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1126\/science.1242072","article-title":"Clustering by fast search and find of density peaks","volume":"344","author":"A Rodriguez","year":"2014","journal-title":"Science"},{"key":"pcbi.1008846.ref048","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1109\/IM.2001.924423","volume-title":"Efficient variants of the ICP algorithm. In: Proceedings third international conference on 3-D digital imaging and modeling","author":"S Rusinkiewicz","year":"2001"},{"key":"pcbi.1008846.ref049","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.1162\/0899766054322973","article-title":"Analyzing functional connectiv ity using a network likelihood model of ensemble neural spiking activity","volume":"17","author":"M Okatan","year":"2005","journal-title":"Neural Comput"},{"key":"pcbi.1008846.ref050","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.physrep.2006.12.004","article-title":"Causality detection based on information-theoretic approaches in time series analysis","volume":"441","author":"SK Hlav\u00e1\u010dkov\u00e1","year":"2007","journal-title":"Phys. Rep."},{"key":"pcbi.1008846.ref051","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1038\/nature07140","article-title":"Spatio-temporal correlations and visual signalling in a complete neuronal population","volume":"454","author":"JW Pillow","year":"2008","journal-title":"Nature"},{"key":"pcbi.1008846.ref052","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fncom.2011.00004","article-title":"Extraction of network topology from multi-electrode recordings: is there a small-world effect?","volume":"5","author":"F Gerhard","year":"2011","journal-title":"Frontiers in computational neuroscience"},{"issue":"2","key":"pcbi.1008846.ref053","doi-asserted-by":"crossref","first-page":"e55809","DOI":"10.1371\/journal.pone.0055809","article-title":"Measuring Information-Transfer Delays","volume":"8","author":"M Wibral","year":"2013","journal-title":"PLoS ONE"},{"issue":"8","key":"pcbi.1008846.ref054","doi-asserted-by":"crossref","first-page":"e6482","DOI":"10.1371\/journal.pone.0006482","article-title":"Evaluation of the performance of information theory-based methods and cross-correlation to estimate the functional connectivity in cortical networks","volume":"4","author":"M Garofalo","year":"2009","journal-title":"PloS one"},{"key":"pcbi.1008846.ref055","first-page":"8","article-title":"Model-free reconstruction of excitatory neuronal connectivity from calcium imaging signals","author":"O Stetter","year":"2012","journal-title":"PLOS Computational Biology"},{"key":"pcbi.1008846.ref056","doi-asserted-by":"crossref","first-page":"10240","DOI":"10.1073\/pnas.0701519104","article-title":"Network structure of cerebral cortex shapes functional connectivity on multiple time scales","volume":"104","author":"CJ Honey","year":"2007","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1008846.ref057","doi-asserted-by":"crossref","first-page":"e27431","DOI":"10.1371\/journal.pone.0027431","article-title":"Extending transfer entropy improves identification of effective connectivity in a spiking cortical network model","author":"S Ito","year":"2011","journal-title":"PloS One"},{"issue":"5","key":"pcbi.1008846.ref058","doi-asserted-by":"crossref","first-page":"e1004858","DOI":"10.1371\/journal.pcbi.1004858","article-title":"High-degree neurons feed cortical computations","volume":"12","author":"NM Timme","year":"2016","journal-title":"PLoS computational biology"},{"key":"pcbi.1008846.ref059","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1103\/PhysRevLett.85.461","article-title":"Measuring information transfer","volume":"85","author":"T Schreiber","year":"2000","journal-title":"Physical Review Letters"},{"issue":"16","key":"pcbi.1008846.ref060","doi-asserted-by":"crossref","first-page":"5454","DOI":"10.1523\/JNEUROSCI.4350-13.2014","article-title":"Long-term recordings improve the detection of weak excitatory\u2013excitatory connections in rat prefrontal cortex","volume":"34","author":"CD Schwindel","year":"2014","journal-title":"Journal of Neuroscience"},{"issue":"4","key":"pcbi.1008846.ref061","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/j.neuron.2016.03.036","article-title":"&Buzs\u00e1ki G, Network homeostasis and state dynamics of neocortical sleep","volume":"90","author":"BO Watson","year":"2016","journal-title":"Neuron"},{"issue":"8","key":"pcbi.1008846.ref062","doi-asserted-by":"crossref","first-page":"e1006381","DOI":"10.1371\/journal.pcbi.1006381","article-title":"Identification of excitatory-inhibitory links and network topology in large-scale neuronal assemblies from multi-electrode recordings","volume":"14","author":"VP Pastore","year":"2018","journal-title":"PLoS computational biology"},{"key":"pcbi.1008846.ref063","article-title":"Distinct Structure of Cortical Population Activity on Fast and Infraslow Timescales","author":"M Okun","year":"2019","journal-title":"Cerebral Cortex"},{"key":"pcbi.1008846.ref064","first-page":"556795","article-title":"Excitatory and inhibitory intracortical circuits for orientation and direction selectivity","author":"LF Rossi","year":"2019","journal-title":"bioRxiv"},{"issue":"1","key":"pcbi.1008846.ref065","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1152\/jn.01170.2003","article-title":"Characterization of neocortical principal cells and interneurons by network interactions and extracellular features","volume":"92","author":"P Barth\u00f3","year":"2004","journal-title":"Journal of neurophysiology"},{"key":"pcbi.1008846.ref066","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1016\/j.neuron.2006.10.023","article-title":"Integration and segregation 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Neurosci."},{"issue":"2","key":"pcbi.1008846.ref069","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1152\/jn.1994.71.2.437","article-title":"Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs","volume":"71","author":"HA Swadlow","year":"1994","journal-title":"Journal of neurophysiology"},{"key":"pcbi.1008846.ref070","first-page":"319","article-title":"Pharmacology and nerve endings","volume":"28","author":"HH Dale","year":"1934","journal-title":"Proc. R. Soc. Med"},{"key":"pcbi.1008846.ref071","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1162\/089976606775093882","article-title":"Polychronization: computation with spikes","volume":"18","author":"EM Izhikevich","year":"2006","journal-title":"Neural Comput."},{"key":"pcbi.1008846.ref072","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/S0896-6273(03)00507-5","article-title":"Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity","volume":"39","author":"M Woodin","year":"2003","journal-title":"Neuron"},{"key":"pcbi.1008846.ref073","doi-asserted-by":"crossref","first-page":"3305","DOI":"10.1152\/jn.00551.2006","article-title":"Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex","volume":"96","author":"JS Haas","year":"2006","journal-title":"Journal of neurophysiology"},{"issue":"6","key":"pcbi.1008846.ref074","doi-asserted-by":"crossref","first-page":"1923","DOI":"10.1152\/jn.00200.2020","article-title":"A spike analysis method for characterizing neurons based on phase locking and scaling to the interval between two behavioral events","volume":"124","author":"M Kawabata","year":"2020","journal-title":"Journal of Neurophysiology"},{"issue":"2","key":"pcbi.1008846.ref075","doi-asserted-by":"crossref","first-page":"371","DOI":"10.3934\/nhm.2008.3.371","article-title":"K-core decomposition of Internet graphs: hierarchies, self-similarity and measurement biases","volume":"3","author":"JI Alvarez-Hamelin","year":"2008","journal-title":"Networks and heterogeneous media"},{"issue":"3","key":"pcbi.1008846.ref076","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1109\/TAC.1974.1100557","article-title":"Structural controllability","volume":"19","author":"CT Lin","year":"1974","journal-title":"IEEE Transactions on Automatic Control"},{"issue":"7346","key":"pcbi.1008846.ref077","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/nature10011","article-title":"Controllability of complex networks","volume":"473","author":"YY Liu","year":"2011","journal-title":"nature"},{"key":"pcbi.1008846.ref078","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.ymeth.2015.12.017","article-title":"Minimum dominating set-based methods for analyzing biological networks","volume":"102","author":"JC Nacher","year":"2016","journal-title":"Methods"},{"key":"pcbi.1008846.ref079","doi-asserted-by":"crossref","first-page":"2002","DOI":"10.1038\/ncomms3002","article-title":"Emergence of bimodality in controlling complex networks","volume":"4","author":"T Jia","year":"2013","journal-title":"Nature communications"},{"issue":"12","key":"pcbi.1008846.ref080","doi-asserted-by":"crossref","first-page":"3685","DOI":"10.1523\/JNEUROSCI.4500-08.2009","article-title":"Correlated connectivity and the distribution of firing rates in the neocortex","volume":"29","author":"AA Koulakov","year":"2009","journal-title":"Journal of Neuroscience"},{"key":"pcbi.1008846.ref081","doi-asserted-by":"crossref","first-page":"9481","DOI":"10.1523\/JNEUROSCI.6130-10.2011","article-title":"Multiplicative dynamics underlie the emergence of the log-normal distribution of spine sizes in the neocortex in vivo","volume":"31","author":"Y Loewenstein","year":"2011","journal-title":"J. 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