{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T03:33:11Z","timestamp":1775187191908,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1012130","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,23]],"date-time":"2024-05-23T00:00:00Z","timestamp":1716422400000}}],"reference-count":159,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2024,5,13]],"date-time":"2024-05-13T00:00:00Z","timestamp":1715558400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004329","name":"Javna Agencija za Raziskovalno Dejavnost RS","doi-asserted-by":"publisher","award":["P3-0396"],"award-info":[{"award-number":["P3-0396"]}],"id":[{"id":"10.13039\/501100004329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004329","name":"Javna Agencija za Raziskovalno Dejavnost RS","doi-asserted-by":"publisher","award":["J3-3077"],"award-info":[{"award-number":["J3-3077"]}],"id":[{"id":"10.13039\/501100004329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004329","name":"Javna Agencija za Raziskovalno Dejavnost RS","doi-asserted-by":"publisher","award":["N3-0133"],"award-info":[{"award-number":["N3-0133"]}],"id":[{"id":"10.13039\/501100004329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004329","name":"Javna Agencija za Raziskovalno Dejavnost RS","doi-asserted-by":"publisher","award":["I0-0029"],"award-info":[{"award-number":["I0-0029"]}],"id":[{"id":"10.13039\/501100004329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000861","name":"Burroughs Wellcome Fund","doi-asserted-by":"publisher","award":["25B1756"],"award-info":[{"award-number":["25B1756"]}],"id":[{"id":"10.13039\/100000861","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["R01 DK102950"],"award-info":[{"award-number":["R01 DK102950"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"Foundation for the National Institutes of Health","doi-asserted-by":"publisher","award":["R01 DK106412"],"award-info":[{"award-number":["R01 DK106412"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Within the islets of Langerhans, beta cells orchestrate synchronized insulin secretion, a pivotal aspect of metabolic homeostasis. Despite the inherent heterogeneity and multimodal activity of individual cells, intercellular coupling acts as a homogenizing force, enabling coordinated responses through the propagation of intercellular waves. Disruptions in this coordination are implicated in irregular insulin secretion, a hallmark of diabetes. Recently, innovative approaches, such as integrating multicellular calcium imaging with network analysis, have emerged for a quantitative assessment of the cellular activity in islets. However, different groups use distinct experimental preparations, microscopic techniques, apply different methods to process the measured signals and use various methods to derive functional connectivity patterns. This makes comparisons between findings and their integration into a bigger picture difficult and has led to disputes in functional connectivity interpretations. To address these issues, we present here a systematic analysis of how different approaches influence the network representation of islet activity. Our findings show that the choice of methods used to construct networks is not crucial, although care is needed when combining data from different islets. Conversely, the conclusions drawn from network analysis can be heavily affected by the pre-processing of the time series, the type of the oscillatory component in the signals, and by the experimental preparation. Our tutorial-like investigation aims to resolve interpretational issues, reconcile conflicting views, advance functional implications, and encourage researchers to adopt connectivity analysis. As we conclude, we outline challenges for future research, emphasizing the broader applicability of our conclusions to other tissues exhibiting complex multicellular dynamics.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1012130","type":"journal-article","created":{"date-parts":[[2024,5,13]],"date-time":"2024-05-13T17:42:53Z","timestamp":1715622173000},"page":"e1012130","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["Network representation of multicellular activity in pancreatic islets: Technical considerations for functional connectivity analysis"],"prefix":"10.1371","volume":"20","author":[{"given":"Marko","family":"\u0160terk","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yaowen","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Viljem","family":"Pohorec","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eva Paradi\u017e","family":"Leitgeb","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jurij","family":"Dolen\u0161ek","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Richard K. P.","family":"Benninger","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andra\u017e","family":"Sto\u017eer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vira","family":"Kravets","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9735-0485","authenticated-orcid":true,"given":"Marko","family":"Gosak","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,5,13]]},"reference":[{"key":"pcbi.1012130.ref001","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1042\/bio_2021_116","article-title":"Metabolic regulation of insulin secretion in health and disease.","volume":"43","author":"E Haythorne","year":"2021","journal-title":"The Biochemist"},{"key":"pcbi.1012130.ref002","doi-asserted-by":"crossref","first-page":"2211","DOI":"10.1098\/rstb.2005.1762","article-title":"Glucose-sensing mechanisms in pancreatic beta-cells","volume":"360","author":"PE MacDonald","year":"2005","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pcbi.1012130.ref003","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1111\/dom.12995","article-title":"\u03b2-Cell signalling and insulin secretagogues: A path for improved diabetes therapy.","volume":"19","author":"S Seino","year":"2017","journal-title":"Diabetes, Obesity and Metabolism."},{"issue":"Suppl","key":"pcbi.1012130.ref004","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1002\/jcb.240550007","article-title":"Stimulus-secretion coupling in pancreatic beta cells","volume":"55","author":"FM Ashcroft","year":"1994","journal-title":"J Cell Biochem"},{"key":"pcbi.1012130.ref005","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1007\/978-3-030-12457-1_37","article-title":"Stimulus-Secretion Coupling in Beta-Cells: From Basic to Bedside","volume":"1131","author":"MS Islam","year":"2020","journal-title":"Adv Exp Med Biol"},{"key":"pcbi.1012130.ref006","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1152\/physrev.00008.2017","article-title":"Pancreatic \u03b2-Cell Electrical Activity and Insulin Secretion: Of Mice and Men","volume":"98","author":"P Rorsman","year":"2018","journal-title":"Physiological Reviews"},{"key":"pcbi.1012130.ref007","doi-asserted-by":"crossref","first-page":"2095","DOI":"10.1007\/s00125-020-05159-8","article-title":"Molecular and functional profiling of human islets: from heterogeneity to human phenotypes","volume":"63","author":"R Arrojo E Drigo","year":"2020","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref008","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1038\/s41574-021-00568-0","article-title":"The physiological role of \u03b2-cell heterogeneity in pancreatic islet function.","volume":"18","author":"RKP Benninger","year":"2022","journal-title":"Nat Rev Endocrinol"},{"key":"pcbi.1012130.ref009","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1080\/19382014.2017.1342022","article-title":"The triggering pathway to insulin secretion: Functional similarities and differences between the human and the mouse \u03b2 cells and their translational relevance.","volume":"9","author":"M Skelin Klemen","year":"2017","journal-title":"Islets."},{"key":"pcbi.1012130.ref010","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1152\/physiol.00044.2021","article-title":"Pulsatile Basal Insulin Secretion Is Driven by Glycolytic Oscillations.","volume":"37","author":"PA Fletcher","year":"2022","journal-title":"Physiology."},{"key":"pcbi.1012130.ref011","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1007\/s00125-020-05213-5","article-title":"Paracrine regulation of insulin secretion","volume":"63","author":"MO Huising","year":"2020","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref012","doi-asserted-by":"crossref","first-page":"5453","DOI":"10.1113\/jphysiol.2011.218909","article-title":"Gap junctions and other mechanisms of cell-cell communication regulate basal insulin secretion in the pancreatic islet","volume":"589","author":"RKP Benninger","year":"2011","journal-title":"The Journal of physiology"},{"key":"pcbi.1012130.ref013","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1016\/j.bpj.2023.01.039","article-title":"Functional characteristics of hub and wave-initiator cells in \u03b2 cell networks","volume":"122","author":"M \u0160terk","year":"2023","journal-title":"Biophys J"},{"key":"pcbi.1012130.ref014","doi-asserted-by":"crossref","first-page":"2723","DOI":"10.1016\/j.bpj.2014.10.048","article-title":"Intrinsic Islet Heterogeneity and Gap Junction Coupling Determine Spatiotemporal Ca2+ Wave Dynamics.","volume":"107","author":"RKP Benninger","year":"2014","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref015","doi-asserted-by":"crossref","first-page":"170709","DOI":"10.1016\/j.peptides.2021.170709","article-title":"Autonomic control of pancreatic beta cells: What is known on the regulation of insulin secretion and beta-cell proliferation in rodents and humans","volume":"148","author":"VS Moull\u00e9","year":"2022","journal-title":"Peptides"},{"key":"pcbi.1012130.ref016","doi-asserted-by":"crossref","first-page":"e54638","DOI":"10.1371\/journal.pone.0054638","article-title":"Glucose-Stimulated Calcium Dynamics in Islets of Langerhans in Acute Mouse Pancreas Tissue Slices.","volume":"8","author":"A Sto\u017eer","year":"2013","journal-title":"PLoS ONE."},{"key":"pcbi.1012130.ref017","doi-asserted-by":"crossref","first-page":"3152","DOI":"10.1007\/s00125-012-2727-6","article-title":"Islet nerves in focus\u2014defining their neurobiological and clinical role","volume":"55","author":"B. Ahr\u00e9n","year":"2012","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref018","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.biochi.2017.07.002","article-title":"Misunderstandings and controversies about the insulin-secreting properties of antidiabetic sulfonylureas","volume":"143","author":"J-C Henquin","year":"2017","journal-title":"Biochimie"},{"key":"pcbi.1012130.ref019","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1113\/JP276106","article-title":"Exendin-4 overcomes cytokine-induced decreases in gap junction coupling via protein kinase A and Epac2 in mouse and human islets","volume":"597","author":"NL Farnsworth","year":"2019","journal-title":"J Physiol"},{"key":"pcbi.1012130.ref020","doi-asserted-by":"crossref","first-page":"665537","DOI":"10.3389\/fendo.2021.665537","article-title":"The Insulin Response to Oral Glucose in GIP and GLP-1 Receptor Knockout Mice: Review of the Literature and Stepwise Glucose Dose Response Studies in Female Mice.","volume":"12","author":"B Ahr\u00e9n","year":"2021","journal-title":"Front Endocrinol"},{"key":"pcbi.1012130.ref021","doi-asserted-by":"crossref","first-page":"E716","DOI":"10.1152\/ajpendo.00649.2020","article-title":"Pancreatic \u03b2-cell heterogeneity in health and diabetes: classes, sources, and subtypes","volume":"320","author":"MA Miranda","year":"2021","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"pcbi.1012130.ref022","doi-asserted-by":"crossref","first-page":"R43","DOI":"10.1530\/JME-18-0011","article-title":"The role of beta cell heterogeneity in islet function and insulin release","volume":"61","author":"D Nasteska","year":"2018","journal-title":"J Mol Endocrinol"},{"key":"pcbi.1012130.ref023","doi-asserted-by":"crossref","first-page":"S7","DOI":"10.1016\/j.molmet.2019.06.015","article-title":"Heterogeneity of human pancreatic \u03b2-cells.","volume":"27S","author":"G Dominguez-Gutierrez","year":"2019","journal-title":"Mol Metab."},{"key":"pcbi.1012130.ref024","doi-asserted-by":"crossref","first-page":"777","DOI":"10.2337\/diab.41.7.777","article-title":"Heterogeneity in pancreatic beta-cell population","volume":"41","author":"DG Pipeleers","year":"1992","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref025","doi-asserted-by":"crossref","first-page":"5180","DOI":"10.1210\/en.2012-1257","article-title":"Subpopulations of GFP-marked mouse pancreatic \u03b2-cells differ in size, granularity, and insulin secretion","volume":"153","author":"H Katsuta","year":"2012","journal-title":"Endocrinology"},{"key":"pcbi.1012130.ref026","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1007\/s00125-008-1103-z","article-title":"Insulin secretion from human beta cells is heterogeneous and dependent on cell-to-cell contacts","volume":"51","author":"A Wojtusciszyn","year":"2008","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref027","doi-asserted-by":"crossref","first-page":"E305","DOI":"10.1152\/ajpendo.00043.2021","article-title":"Glucose-dependent activation, activity, and deactivation of beta cell networks in acute mouse pancreas tissue slices","volume":"321","author":"A Sto\u017eer","year":"2021","journal-title":"American Journal of Physiology-Endocrinology and Metabolism"},{"key":"pcbi.1012130.ref028","doi-asserted-by":"crossref","unstructured":"Kravets V, Dwulet JM, Schleicher WE, Hodson DJ, Davis AM, Pyle L, et al. Functional architecture of the pancreatic islets reveals first responder cells which drive the first-phase [Ca2+] response. bioRxiv. 2021; 2020.12.22.424082. doi: 10.1101\/2020.12.22.424082","DOI":"10.1101\/2020.12.22.424082"},{"key":"pcbi.1012130.ref029","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.3389\/fphys.2017.01106","article-title":"Critical and Supercritical Spatiotemporal Calcium Dynamics in Beta Cells.","volume":"8","author":"M Gosak","year":"2017","journal-title":"Frontiers in Physiology."},{"key":"pcbi.1012130.ref030","doi-asserted-by":"crossref","first-page":"E475","DOI":"10.1152\/ajpendo.00380.2018","article-title":"Calcium signaling and secretory granule pool dynamics underlie biphasic insulin secretion and its amplification by glucose: experiments and modeling","volume":"316","author":"MG Pedersen","year":"2019","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"pcbi.1012130.ref031","doi-asserted-by":"crossref","first-page":"102081","DOI":"10.1016\/j.ceca.2019.102081","article-title":"Intact pancreatic islets and dispersed beta-cells both generate intracellular calcium oscillations but differ in their responsiveness to glucose","volume":"83","author":"RT Scarl","year":"2019","journal-title":"Cell Calcium"},{"key":"pcbi.1012130.ref032","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1210\/endo-83-3-572","article-title":"Dynamics of insulin secretion by the perfused rat pancreas","volume":"83","author":"DL Curry","year":"1968","journal-title":"Endocrinology"},{"key":"pcbi.1012130.ref033","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fendo.2022.867663","article-title":"Glucose-Stimulated Calcium Dynamics in Beta Cells From Male C57BL\/6J, C57BL\/6N, and NMRI Mice: A Comparison of Activation, Activity, and Deactivation Properties in Tissue Slices.","volume":"13","author":"V Pohorec","year":"2022","journal-title":"Frontiers in Endocrinology"},{"key":"pcbi.1012130.ref034","doi-asserted-by":"crossref","first-page":"5048","DOI":"10.1529\/biophysj.108.140863","article-title":"Gap Junction Coupling and Calcium Waves in the Pancreatic Islet","volume":"95","author":"RKP Benninger","year":"2008","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref035","doi-asserted-by":"crossref","first-page":"105495","DOI":"10.1016\/j.cnsns.2020.105495","article-title":"Assessing the origin and velocity of Ca2+ waves in three-dimensional tissue: Insights from a mathematical model and confocal imaging in mouse pancreas tissue slices.","volume":"93","author":"M \u0160terk","year":"2021","journal-title":"Communications in Nonlinear Science and Numerical Simulation"},{"key":"pcbi.1012130.ref036","doi-asserted-by":"crossref","first-page":"27393","DOI":"10.3390\/s151127393","article-title":"Membrane Potential and Calcium Dynamics in Beta Cells from Mouse Pancreas Tissue Slices: Theory, Experimentation, and Analysis.","volume":"15","author":"J Dolen\u0161ek","year":"2015","journal-title":"Sensors."},{"key":"pcbi.1012130.ref037","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.2337\/db06-0232","article-title":"Cx36-mediated coupling reduces beta-cell heterogeneity, confines the stimulating glucose concentration range, and affects insulin release kinetics","volume":"56","author":"S Speier","year":"2007","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref038","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.bbamem.2017.03.005","article-title":"Gap junction proteins are key drivers of endocrine function","volume":"1860","author":"P. Meda","year":"2018","journal-title":"Biochim Biophys Acta Biomembr"},{"key":"pcbi.1012130.ref039","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1016\/j.diabres.2012.10.016","article-title":"Connexins and \u03b2-cell functions","volume":"99","author":"V Cigliola","year":"2013","journal-title":"Diabetes Res Clin Pract"},{"key":"pcbi.1012130.ref040","doi-asserted-by":"crossref","first-page":"1700","DOI":"10.2337\/db11-1312","article-title":"Connexin-36 gap junctions regulate in vivo first- and second-phase insulin secretion dynamics and glucose tolerance in the conscious mouse","volume":"61","author":"WS Head","year":"2012","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref041","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1016\/j.bpj.2017.07.021","article-title":"Spatially Organized \u03b2-Cell Subpopulations Control Electrical Dynamics across Islets of Langerhans","volume":"113","author":"MJ Westacott","year":"2017","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref042","doi-asserted-by":"crossref","first-page":"e64526","DOI":"10.7554\/eLife.64526","article-title":"Innervation modulates the functional connectivity between pancreatic endocrine cells.","volume":"11","author":"YHC Yang","year":"2022","journal-title":"eLife"},{"key":"pcbi.1012130.ref043","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1007\/s00109-020-01887-x","article-title":"Paracrine signaling in islet function and survival","volume":"98","author":"SM Hartig","year":"2020","journal-title":"J Mol Med (Berl)."},{"key":"pcbi.1012130.ref044","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2022.934775","article-title":"Alpha-cell paracrine signaling in the regulation of beta-cell insulin secretion","volume":"13","author":"MM Holter","year":"2022","journal-title":"Frontiers in Endocrinology"},{"key":"pcbi.1012130.ref045","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1007\/s00018-014-1755-4","article-title":"Beta cell connectivity in pancreatic islets: a type 2 diabetes target?","volume":"72","author":"GA Rutter","year":"2015","journal-title":"Cell Mol Life Sci"},{"key":"pcbi.1012130.ref046","first-page":"E1354","article-title":"Inhibition of connexin 36 hemichannels by glucose contributes to the stimulation of insulin secretion. AJP","volume":"306","author":"J Pizarro-Delgado","year":"2014","journal-title":"Endocrinology and Metabolism"},{"key":"pcbi.1012130.ref047","doi-asserted-by":"crossref","first-page":"151891","DOI":"10.1016\/j.aanat.2022.151891","article-title":"Early decrease in Cx36 is associated with increased cell adhesion molecules (CAMs) junctional content in mouse pancreatic islets after short-term high-fat diet feeding.","volume":"241","author":"C Martinez","year":"2022","journal-title":"Annals of Anatomy\u2014Anatomischer Anzeiger."},{"key":"pcbi.1012130.ref048","doi-asserted-by":"crossref","first-page":"E144","DOI":"10.1152\/ajpendo.00489.2011","article-title":"Impaired \u03b2-cell-\u03b2-cell coupling mediated by Cx36 gap junctions in prediabetic mice","volume":"303","author":"CPF Carvalho","year":"2012","journal-title":"American Journal of Physiology-Endocrinology and Metabolism"},{"key":"pcbi.1012130.ref049","doi-asserted-by":"crossref","first-page":"E709","DOI":"10.1152\/ajpendo.00132.2020","article-title":"Caloric restriction recovers impaired \u03b2-cell-\u03b2-cell gap junction coupling, calcium oscillation coordination, and insulin secretion in prediabetic mice","volume":"319","author":"ME Corezola do Amaral","year":"2020","journal-title":"American Journal of Physiology-Endocrinology and Metabolism"},{"key":"pcbi.1012130.ref050","doi-asserted-by":"crossref","unstructured":"Clair JRS, Westacott MJ, Miranda J, Farnsworth NL, Kravets V, Schleicher WE, et al. Restoring Connexin-36 Function in Diabetogenic Environments Precludes Mouse and Human Islet Dysfunction. bioRxiv; 2023. p. 2020.11.03.366179. doi: 10.1101\/2020.11.03.366179","DOI":"10.1101\/2020.11.03.366179"},{"key":"pcbi.1012130.ref051","doi-asserted-by":"crossref","first-page":"10268","DOI":"10.1038\/s41598-021-89333-x","article-title":"The effects of beta-cell mass and function, intercellular coupling, and islet synchrony on [Formula: see text] dynamics.","volume":"11","author":"M Saadati","year":"2021","journal-title":"Sci Rep"},{"key":"pcbi.1012130.ref052","doi-asserted-by":"crossref","first-page":"1798","DOI":"10.2337\/diabetes.54.6.1798","article-title":"Loss of Connexin36 Channels Alters -Cell Coupling, Islet Synchronization of Glucose-Induced Ca2+ and Insulin Oscillations, and Basal Insulin Release","volume":"54","author":"MA Ravier","year":"2005","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref053","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1007\/s12038-021-00251-6","article-title":"Do oscillations in pancreatic islets require pacemaker cells","volume":"47","author":"BE Peercy","year":"2022","journal-title":"J Biosci"},{"key":"pcbi.1012130.ref054","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.cmet.2016.06.020","article-title":"Beta Cell Hubs Dictate Pancreatic Islet Responses to Glucose.","volume":"24","author":"NR Johnston","year":"2016","journal-title":"Cell Metabolism"},{"key":"pcbi.1012130.ref055","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1038\/s42255-019-0075-2","article-title":"Leader \u03b2-cells coordinate Ca2+ dynamics across pancreatic islets in vivo","volume":"1","author":"V Salem","year":"2019","journal-title":"Nature Metabolism"},{"key":"pcbi.1012130.ref056","doi-asserted-by":"crossref","first-page":"922640","DOI":"10.3389\/fendo.2022.922640","article-title":"From Isles of K\u00f6nigsberg to Islets of Langerhans: Examining the Function of the Endocrine Pancreas Through Network Science.","volume":"13","author":"A Sto\u017eer","year":"2022","journal-title":"Front Endocrinol (Lausanne)."},{"key":"pcbi.1012130.ref057","doi-asserted-by":"crossref","first-page":"e3001761","DOI":"10.1371\/journal.pbio.3001761","article-title":"Functional architecture of pancreatic islets identifies a population of first responder cells that drive the first-phase calcium response","volume":"20","author":"V Kravets","year":"2022","journal-title":"PLoS Biol"},{"key":"pcbi.1012130.ref058","doi-asserted-by":"crossref","first-page":"2231609","DOI":"10.1080\/19382014.2023.2231609","article-title":"A primer on modelling pancreatic islets: from models of coupled \u03b2-cells to multicellular islet models.","volume":"15","author":"GJ F\u00e9lix-Mart\u00ednez","year":"2023","journal-title":"Islets"},{"key":"pcbi.1012130.ref059","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1080\/19382014.2018.1493316","article-title":"Beta-cell hubs maintain Ca 2+ oscillations in human and mouse islet simulations.","volume":"10","author":"C-L Lei","year":"2018","journal-title":"Islets"},{"key":"pcbi.1012130.ref060","doi-asserted-by":"crossref","first-page":"106247","DOI":"10.1016\/j.bpc.2019.106247","article-title":"Biophysical modeling of \u03b2-cells networks: Realistic architectures and heterogeneity effects","volume":"254","author":"A Loppini","year":"2019","journal-title":"Biophysical Chemistry"},{"key":"pcbi.1012130.ref061","doi-asserted-by":"crossref","first-page":"2584","DOI":"10.2337\/db22-0004","article-title":"Ca2+ Oscillations, Waves, and Networks in Islets From Human Donors With and Without Type 2","volume":"71","author":"M Gosak","year":"2022","journal-title":"Diabetes. Diabetes"},{"key":"pcbi.1012130.ref062","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1016\/S0006-3495(01)76096-1","article-title":"Excitation Wave Propagation as a Possible Mechanism for Signal Transmission in Pancreatic Islets of Langerhans","volume":"80","author":"OV Aslanidi","year":"2001","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref063","doi-asserted-by":"crossref","first-page":"121436","DOI":"10.1016\/j.lfs.2023.121436","article-title":"Molecular phenotyping of single pancreatic islet leader beta cells by \u201cFlash-Seq.\u201d","volume":"316","author":"P Chabosseau","year":"2023","journal-title":"Life Sci"},{"key":"pcbi.1012130.ref064","first-page":"14","article-title":"Editorial: The pancreatic islet\u2013a multifaceted hub of inter-cellular communication.","author":"Q Zhang","year":"2023","journal-title":"Front Endocrinol."},{"key":"pcbi.1012130.ref065","doi-asserted-by":"crossref","first-page":"830","DOI":"10.2337\/dbi19-0012","article-title":"\u201cTake Me To Your Leader\u201d: An Electrophysiological Appraisal of the Role of Hub Cells in Pancreatic Islets.","volume":"69","author":"LS Satin","year":"2020","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref066","doi-asserted-by":"crossref","first-page":"830","DOI":"10.2337\/dbi19-0012","article-title":"\u201cTake Me To Your Leader\u201d: An Electrophysiological Appraisal of the Role of Hub Cells in Pancreatic Islets.","volume":"69","author":"GA Rutter","year":"2020","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref067","doi-asserted-by":"crossref","first-page":"830","DOI":"10.2337\/dbi19-0012","article-title":"Response to Comment on Satin et al. \u201cTake Me To Your Leader\u201d: An Electrophysiological Appraisal of the Role of Hub Cells in Pancreatic Islets.","volume":"69","author":"LS Satin","year":"2020","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref068","doi-asserted-by":"crossref","first-page":"053103","DOI":"10.1063\/1.4949020","article-title":"Heterogeneity and nearest-neighbor coupling can explain small-worldness and wave properties in pancreatic islets.","volume":"26","author":"G Cappon","year":"2016","journal-title":"Chaos: An Interdisciplinary Journal of Nonlinear Science."},{"key":"pcbi.1012130.ref069","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.plrev.2017.11.003","article-title":"Network science of biological systems at different scales: A review","volume":"24","author":"M Gosak","year":"2018","journal-title":"Physics of Life Reviews"},{"key":"pcbi.1012130.ref070","doi-asserted-by":"crossref","first-page":"e83147","DOI":"10.7554\/eLife.83147","article-title":"Beta-cell intrinsic dynamics rather than gap junction structure dictates subpopulations in the islet functional network","volume":"12","author":"JK Briggs","year":"2023","journal-title":"eLife"},{"key":"pcbi.1012130.ref071","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2023.1315520","article-title":"Exendin-4 affects calcium signalling predominantly during activation and activity of beta cell networks in acute mouse pancreas tissue slices","volume":"14","author":"E Paradi\u017e Leitgeb","year":"2024","journal-title":"Front Endocrinol"},{"key":"pcbi.1012130.ref072","doi-asserted-by":"crossref","first-page":"7845","DOI":"10.1038\/srep07845","article-title":"Progressive glucose stimulation of islet beta cells reveals a transition from segregated to integrated modular functional connectivity patterns.","volume":"5","author":"R Markovi\u010d","year":"2015","journal-title":"Scientific Reports"},{"key":"pcbi.1012130.ref073","doi-asserted-by":"crossref","first-page":"1790","DOI":"10.2337\/db07-1615","article-title":"Glucose Metabolism In Vivo in Four Commonly Used Inbred Mouse Strains","volume":"57","author":"ED Berglund","year":"2008","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref074","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1530\/JOE-16-0377","article-title":"High fat feeding unmasks variable insulin responses in male C57BL\/6 mouse substrains","volume":"233","author":"RL Hull","year":"2017","journal-title":"Journal of Endocrinology"},{"key":"pcbi.1012130.ref075","doi-asserted-by":"crossref","first-page":"25","DOI":"10.2337\/db15-0982","article-title":"Attention to Background Strain Is Essential for Metabolic Research: C57BL\/6 and the International Knockout Mouse Consortium","volume":"65","author":"DA Fontaine","year":"2016","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref076","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.88189.3","article-title":"Novel regulators of islet function identified from genetic variation in mouse islet Ca2+ oscillations.","volume":"12","author":"CH Emfinger","year":"2023","journal-title":"eLife"},{"key":"pcbi.1012130.ref077","doi-asserted-by":"crossref","first-page":"781581","DOI":"10.3389\/fphys.2021.781581","article-title":"Symbiosis of Electrical and Metabolic Oscillations in Pancreatic \u03b2-Cells","volume":"12","author":"I Marinelli","year":"2021","journal-title":"Front Physiol"},{"key":"pcbi.1012130.ref078","doi-asserted-by":"crossref","first-page":"054409","DOI":"10.1103\/PhysRevE.108.054409","article-title":"Both electrical and metabolic coupling shape the collective multimodal activity and functional connectivity patterns in beta cell collectives: A computational model perspective","volume":"108","author":"M \u0160terk","year":"2023","journal-title":"Phys Rev E"},{"key":"pcbi.1012130.ref079","doi-asserted-by":"crossref","first-page":"1264395","DOI":"10.3389\/fnetp.2023.1264395","article-title":"Multilevel synchronization of human \u03b2-cells networks.","volume":"3","author":"N Luchetti","year":"2023","journal-title":"Front Netw Physiol"},{"key":"pcbi.1012130.ref080","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.jtbi.2018.06.017","article-title":"Transitions between bursting modes in the integrated oscillator model for pancreatic \u03b2-cells","volume":"454","author":"I Marinelli","year":"2018","journal-title":"J Theor Biol"},{"key":"pcbi.1012130.ref081","doi-asserted-by":"crossref","first-page":"351","DOI":"10.2337\/dbi17-0004","article-title":"Closing in on the Mechanisms of Pulsatile Insulin Secretion","volume":"67","author":"R Bertram","year":"2018","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref082","doi-asserted-by":"crossref","first-page":"e13701","DOI":"10.1371\/journal.pone.0013701","article-title":"Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory.","volume":"5","author":"Stam CJ Wijk BCM van","year":"2010","journal-title":"Daffertshofer A.PLOS ONE"},{"key":"pcbi.1012130.ref083","doi-asserted-by":"crossref","first-page":"20130521","DOI":"10.1098\/rstb.2013.0521","article-title":"Graph analysis of functional brain networks: practical issues in translational neuroscience. Philosophical Transactions of the Royal Society B","volume":"369","author":"F De Vico Fallani","year":"2014","journal-title":"Biological Sciences"},{"key":"pcbi.1012130.ref084","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1089\/brain.2022.0082","article-title":"Threshold Selection for Brain Connectomes.","volume":"13","author":"N Theis","year":"2023","journal-title":"Brain Connect"},{"key":"pcbi.1012130.ref085","doi-asserted-by":"crossref","first-page":"e53199","DOI":"10.1371\/journal.pone.0053199","article-title":"The Problem of Thresholding in Small-World Network Analysis.","volume":"8","author":"N Langer","year":"2013","journal-title":"PLOS ONE."},{"key":"pcbi.1012130.ref086","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/j.neuroimage.2017.02.005","article-title":"Proportional thresholding in resting-state fMRI functional connectivity networks and consequences for patient-control connectome studies: Issues and recommendations.","volume":"152","author":"MP van den Heuvel","year":"2017","journal-title":"Neuroimage."},{"key":"pcbi.1012130.ref087","doi-asserted-by":"crossref","first-page":"e35673","DOI":"10.1371\/journal.pone.0035673","article-title":"EEG-based functional brain networks: does the network size matter?","volume":"7","author":"A Joudaki","year":"2012","journal-title":"PLoS One"},{"key":"pcbi.1012130.ref088","doi-asserted-by":"crossref","first-page":"e105041","DOI":"10.1371\/journal.pone.0105041","article-title":"EEG source connectivity analysis: from dense array recordings to brain networks","volume":"9","author":"M Hassan","year":"2014","journal-title":"PLoS One"},{"key":"pcbi.1012130.ref089","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/gigascience\/gix004","article-title":"Multilayer modeling and analysis of human brain networks","volume":"6","author":"M. De Domenico","year":"2017","journal-title":"Gigascience"},{"key":"pcbi.1012130.ref090","doi-asserted-by":"crossref","first-page":"2964","DOI":"10.1038\/s41598-023-29321-5","article-title":"Frequency-specific brain network architecture in resting-state fMRI","volume":"13","author":"S Kajimura","year":"2023","journal-title":"Sci Rep"},{"key":"pcbi.1012130.ref091","first-page":"14","article-title":"The effect of forskolin and the role of Epac2A during activation, activity, and deactivation of beta cell networks","author":"M Skelin Klemen","year":"2023","journal-title":"Frontiers in Endocrinology"},{"key":"pcbi.1012130.ref092","doi-asserted-by":"crossref","first-page":"20713","DOI":"10.1016\/S0021-9258(19)36744-4","article-title":"Influence of membrane potential changes on cytoplasmic Ca2+ concentration in an electrically excitable cell, the insulin-secreting pancreatic B-cell","volume":"267","author":"P Gilon","year":"1992","journal-title":"Journal of Biological Chemistry"},{"key":"pcbi.1012130.ref093","doi-asserted-by":"crossref","first-page":"22265","DOI":"10.1016\/S0021-9258(18)41522-0","article-title":"Oscillations of secretion driven by oscillations of cytoplasmic Ca2+ as evidences in single pancreatic islets","volume":"268","author":"P Gilon","year":"1993","journal-title":"The Journal of biological chemistry"},{"key":"pcbi.1012130.ref094","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.mam.2015.01.003","article-title":"Pulsatile insulin secretion, impaired glucose tolerance and type 2 diabetes","volume":"42","author":"LS Satin","year":"2015","journal-title":"Molecular Aspects of Medicine"},{"key":"pcbi.1012130.ref095","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1007\/BF00581418","article-title":"Cyclic variations of glucose-induced electrical activity in pancreatic B cells","volume":"393","author":"JC Henquin","year":"1982","journal-title":"Pflugers Arch"},{"key":"pcbi.1012130.ref096","doi-asserted-by":"crossref","first-page":"337","DOI":"10.3389\/fphys.2021.612233","article-title":"Assessing Different Temporal Scales of Calcium Dynamics in Networks of Beta Cell Populations.","volume":"12","author":"J Zmazek","year":"2021","journal-title":"Frontiers in Physiology"},{"key":"pcbi.1012130.ref097","first-page":"171","article-title":"Role of oscillations in membrane potential, cytoplasmic Ca2+, and metabolism for plasma insulin oscillations","author":"P. Bergsten","year":"2002","journal-title":"Diabetes. American Diabetes Association Inc."},{"key":"pcbi.1012130.ref098","doi-asserted-by":"crossref","first-page":"2082","DOI":"10.1529\/biophysj.106.087296","article-title":"Glucose modulates [Ca2+]i oscillations in pancreatic islets via ionic and glycolytic mechanisms","volume":"91","author":"CS Nunemaker","year":"2006","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref099","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1007\/BF00400464","article-title":"Culture duration and conditions affect the oscillations of cytoplasmic calcium concentration induced by glucose in mouse pancreatic islets","volume":"37","author":"P Gilon","year":"1994","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref100","doi-asserted-by":"crossref","first-page":"2852","DOI":"10.1016\/S0006-3495(03)70014-9","article-title":"The Ca2+ Dynamics of Isolated Mouse \u03b2-Cells and Islets: Implications for Mathematical Models","volume":"84","author":"M Zhang","year":"2003","journal-title":"Biophysical Journal"},{"key":"pcbi.1012130.ref101","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1111\/j.1469-7793.1999.00839.x","article-title":"Influence of cell number on the characteristics and synchrony of Ca 2+ oscillations in clusters of mouse pancreatic islet cells","volume":"520","author":"FC Jonkers","year":"1999","journal-title":"The Journal of Physiology"},{"key":"pcbi.1012130.ref102","doi-asserted-by":"crossref","first-page":"e14101","DOI":"10.14814\/phy2.14101","article-title":"Beta-cell excitability and excitability-driven diabetes in adult Zebrafish islets","volume":"7","author":"CH Emfinger","year":"2019","journal-title":"Physiol Rep"},{"key":"pcbi.1012130.ref103","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/0014-5793(89)81484-X","article-title":"Glucose-induced oscillations of intracellular Ca2+ concentration resembling bursting electrical activity in single mouse islets of Langerhans","volume":"259","author":"M Valdeolmillos","year":"1989","journal-title":"FEBS Letters"},{"key":"pcbi.1012130.ref104","doi-asserted-by":"crossref","first-page":"4655","DOI":"10.1210\/en.2006-0424","article-title":"Oscillatory Membrane Potential Response to Glucose in Islet \u03b2-Cells: A Comparison of Islet-Cell Electrical Activity in Mouse and Rat","volume":"147","author":"JE Manning Fox","year":"2006","journal-title":"Endocrinology"},{"key":"pcbi.1012130.ref105","doi-asserted-by":"crossref","first-page":"2028","DOI":"10.2337\/diabetes.49.12.2028","article-title":"Differential patterns of glucose-induced electrical activity and intracellular calcium responses in single mouse and rat pancreatic islets","volume":"49","author":"CM Antunes","year":"2000","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref106","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.ygcen.2008.12.017","article-title":"Glucose-dependent and -independent electrical activity in islets of Langerhans of Psammomys obesus, an animal model of nutritionally induced obesity and diabetes","volume":"161","author":"CL Zimliki","year":"2009","journal-title":"Gen Comp Endocrinol"},{"key":"pcbi.1012130.ref107","doi-asserted-by":"crossref","first-page":"2552","DOI":"10.2337\/diabetes.51.8.2552","article-title":"Increased glucose sensitivity of stimulus-secretion coupling in islets from Psammomys obesus after diet induction of diabetes","volume":"51","author":"JAG Pertusa","year":"2002","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref108","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/0014-5793(95)01422-5","article-title":"Intercellular Ca2+ waves sustain coordinate insulin secretion in pig islets of Langerhans","volume":"379","author":"F Bertuzzi","year":"1996","journal-title":"FEBS Lett"},{"key":"pcbi.1012130.ref109","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1177\/096368979900800616","article-title":"Lessons from in vitro perifusion of pancreatic islets isolated from 80 human pancreases","volume":"8","author":"F Bertuzzi","year":"1999","journal-title":"Cell Transplant"},{"key":"pcbi.1012130.ref110","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/S0143-4160(96)90003-2","article-title":"[Ca*+], oscillations pancreatic islets","volume":"20","author":"F Martin","year":"1996","journal-title":"Cell Calcium"},{"key":"pcbi.1012130.ref111","doi-asserted-by":"crossref","first-page":"e82374","DOI":"10.1371\/journal.pone.0082374","article-title":"The Relationship between Membrane Potential and Calcium Dynamics in Glucose-Stimulated Beta Cell Syncytium in Acute Mouse Pancreas Tissue Slices.","volume":"8","author":"J Dolen\u0161ek","year":"2013","journal-title":"PLoS ONE"},{"key":"pcbi.1012130.ref112","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1007\/s004240050334","article-title":"Regulation of pancreatic \u03b2-cell electrical activity and insulin release by physiological amino acid concentrations.","volume":"433","author":"S Bolea","year":"1997","journal-title":"Pfl\u00fcgers Arch"},{"key":"pcbi.1012130.ref113","doi-asserted-by":"crossref","first-page":"878","DOI":"10.2337\/db20-0214","article-title":"Dynamic Uni- and Multicellular Patterns Encode Biphasic Activity in Pancreatic Islets","volume":"70","author":"M Jaffredo","year":"2021","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref114","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s00424-003-1097-9","article-title":"A novel approach to in situ characterization of pancreatic \u03b2-cells.","volume":"446","author":"S Speier","year":"2003","journal-title":"Pfl\u00fcgers Archiv"},{"key":"pcbi.1012130.ref115","doi-asserted-by":"crossref","first-page":"59","DOI":"10.3727\/096368912X659880","article-title":"Pancreatic islet basement membrane loss and remodeling after mouse islet isolation and transplantation: impact for allograft rejection","volume":"23","author":"HF Irving-Rodgers","year":"2014","journal-title":"Cell Transplant"},{"key":"pcbi.1012130.ref116","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1007\/BF03035309","article-title":"Absence of effect of culture duration on glucose-activated alterations in intracellular calcium concentration in mouse pancreatic islets","volume":"38","author":"MW Roe","year":"1995","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref117","first-page":"32","article-title":"Evidence for the existence and potential roles of intra-islet glucagon-like peptide-1.","volume":"13","author":"SA Campbell","year":"2021"},{"key":"pcbi.1012130.ref118","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1111\/j.1469-7793.1998.471bq.x","article-title":"Origin of slow and fast oscillations of Ca 2+ in mouse pancreatic islets","volume":"508","author":"Y-J Liu","year":"1998","journal-title":"The Journal of Physiology"},{"key":"pcbi.1012130.ref119","doi-asserted-by":"crossref","first-page":"1741","DOI":"10.1111\/dom.14747","article-title":"Liraglutide increases islet Ca2+ oscillation frequency and insulin secretion by activating hyperpolarization-activated cyclic nucleotide-gated channels","volume":"24","author":"KE Zaborska","year":"2022","journal-title":"Diabetes Obes Metab"},{"key":"pcbi.1012130.ref120","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1007\/s00125-006-0536-5","article-title":"Changes in gene expression in beta cells after islet isolation and transplantation using laser-capture microdissection","volume":"50","author":"YB Ahn","year":"2007","journal-title":"Diabetologia"},{"key":"pcbi.1012130.ref121","doi-asserted-by":"crossref","first-page":"e30415","DOI":"10.1371\/journal.pone.0030415","article-title":"Analysis of Beta-Cell Gene Expression Reveals Inflammatory Signaling and Evidence of Dedifferentiation following Human Islet Isolation and Culture","volume":"7","author":"S Negi","year":"2012","journal-title":"PLOS ONE"},{"key":"pcbi.1012130.ref122","article-title":"Confocal Laser Scanning Microscopy of Calcium Dynamics in Acute Mouse Pancreatic Tissue Slices","author":"A Sto\u017eer","year":"2021","journal-title":"Journal of Visualized Experiments"},{"key":"pcbi.1012130.ref123","doi-asserted-by":"crossref","first-page":"2809","DOI":"10.1038\/nprot.2014.195","article-title":"Using pancreas tissue slices for in situ studies of islet of Langerhans and acinar cell biology","volume":"9","author":"A Marciniak","year":"2014","journal-title":"Nat Protoc"},{"key":"pcbi.1012130.ref124","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1007\/BF00550880","article-title":"Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets","volume":"418","author":"RM Santos","year":"1991","journal-title":"Pfl\u00fcgers Archiv\u2014European Journal of Physiology"},{"key":"pcbi.1012130.ref125","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1113\/jphysiol.1995.sp020804","article-title":"The electrical activity of mouse pancreatic beta-cells recorded in vivo shows glucose-dependent oscillations","volume":"486","author":"JV S\u00e1nchez-Andr\u00e9s","year":"1995","journal-title":"The Journal of Physiology"},{"key":"pcbi.1012130.ref126","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/S0014-5793(00)01631-8","article-title":"Synchronous glucose-dependent [Ca 2+] i oscillations in mouse pancreatic islets of Langerhans recorded in vivo","volume":"477","author":"J Fernandez","year":"2000","journal-title":"FEBS Letters"},{"key":"pcbi.1012130.ref127","doi-asserted-by":"crossref","first-page":"2676","DOI":"10.2337\/db15-1718","article-title":"Alterations in \u03b2-Cell Calcium Dynamics and Efficacy Outweigh Islet Mass Adaptation in Compensation of Insulin Resistance and Prediabetes Onset","volume":"65","author":"C Chen","year":"2016","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref128","doi-asserted-by":"crossref","first-page":"416","DOI":"10.2337\/diab.38.4.416","article-title":"Tolbutamide as Mimic of Glucose on \u03b2-Cell Electrical Activity: ATP-Sensitive K+ Channels as Common Pathway for Both Stimuli","volume":"38","author":"DL Cook","year":"1989","journal-title":"Diabetes"},{"key":"pcbi.1012130.ref129","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1007\/BF00586918","article-title":"Membrane potential of beta-cells in pancreatic islets","volume":"351","author":"HP Meissner","year":"1974","journal-title":"Pfl\u00fcgers Archiv\u2014European Journal of Physiology"},{"key":"pcbi.1012130.ref130","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1210\/endo.131.1.1611991","article-title":"Adenosine triphosphate-sensitive K+ channels may not be the sole regulators of glucose-induced electrical activity in pancreatic B-cells","volume":"131","author":"JC Henquin","year":"1992","journal-title":"Endocrinology"},{"key":"pcbi.1012130.ref131","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1038\/nrn.2016.182","article-title":"Micro-connectomics: probing the organization of neuronal networks at the cellular scale.","volume":"18","author":"M Schr\u00f6ter","year":"2017","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1012130.ref132","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1038\/ncomms1612","article-title":"Existence of long-lasting experience-dependent plasticity in endocrine cell networks","volume":"3","author":"DJ Hodson","year":"2012","journal-title":"Nat Commun"},{"key":"pcbi.1012130.ref133","doi-asserted-by":"crossref","first-page":"936160","DOI":"10.3389\/fendo.2022.936160","article-title":"Network Properties of Electrically Coupled Bursting Pituitary Cells.","volume":"13","author":"M Fazli","year":"2022","journal-title":"Front Endocrinol (Lausanne)."},{"key":"pcbi.1012130.ref134","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.jtbi.2014.04.024","article-title":"Modeling the functional network of primary intercellular Ca2+ wave propagation in astrocytes and its application to study drug effects","volume":"356","author":"M Pires","year":"2014","journal-title":"J Theor Biol"},{"key":"pcbi.1012130.ref135","doi-asserted-by":"crossref","first-page":"e2010075118","DOI":"10.1073\/pnas.2010075118","article-title":"Intercellular communication induces glycolytic synchronization waves between individually oscillating cells","volume":"118","author":"M Mojica-Benavides","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1012130.ref136","doi-asserted-by":"crossref","first-page":"e0143781","DOI":"10.1371\/journal.pone.0143781","article-title":"The Analysis of Intracellular and Intercellular Calcium Signaling in Human Anterior Lens Capsule Epithelial Cells with Regard to Different Types and Stages of the Cataract.","volume":"10","author":"M Gosak","year":"2015","journal-title":"PLoS One."},{"key":"pcbi.1012130.ref137","doi-asserted-by":"crossref","first-page":"26822","DOI":"10.1073\/pnas.2016905117","article-title":"Multiscale imaging of basal cell dynamics in the functionally mature mammary gland","volume":"117","author":"AJ Stevenson","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1012130.ref138","doi-asserted-by":"crossref","first-page":"e0268644","DOI":"10.1371\/journal.pone.0268644","article-title":"Calcium imaging in intact mouse acinar cells in acute pancreas tissue slices","volume":"17","author":"U Marolt","year":"2022","journal-title":"PLoS One"},{"key":"pcbi.1012130.ref139","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.3389\/fphys.2018.01377","article-title":"Causality Analysis and Cell Network Modeling of Spatial Calcium Signaling Patterns in Liver Lobules.","volume":"9","author":"A Verma","year":"2018","journal-title":"Front Physiol"},{"key":"pcbi.1012130.ref140","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.physrep.2014.07.001","article-title":"The structure and dynamics of multilayer networks","volume":"544","author":"S Boccaletti","year":"2014","journal-title":"Phys Rep"},{"key":"pcbi.1012130.ref141","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1093\/comnet\/cnu016","article-title":"Multilayer networks.","volume":"2","author":"M Kivel\u00e4","year":"2014","journal-title":"Journal of Complex Networks"},{"key":"pcbi.1012130.ref142","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.physrep.2020.05.004","article-title":"Networks beyond pairwise interactions: Structure and dynamics","volume":"874","author":"F Battiston","year":"2020","journal-title":"Physics Reports"},{"key":"pcbi.1012130.ref143","doi-asserted-by":"crossref","first-page":"20220043","DOI":"10.1098\/rsif.2022.0043","article-title":"Dynamics on higher-order networks: a review","volume":"19","author":"S Majhi","year":"2022","journal-title":"Journal of The Royal Society Interface"},{"key":"pcbi.1012130.ref144","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1109\/JPROC.2015.2476824","article-title":"Wiener\u2013Granger Causality in Network Physiology With Applications to Cardiovascular Control and Neuroscience","volume":"104","author":"A Porta","year":"2016","journal-title":"Proceedings of the IEEE"},{"key":"pcbi.1012130.ref145","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1038\/s41593-019-0510-4","article-title":"Advancing functional connectivity research from association to causation","volume":"22","author":"AT Reid","year":"2019","journal-title":"Nat Neurosci"},{"key":"pcbi.1012130.ref146","doi-asserted-by":"crossref","first-page":"108506","DOI":"10.1016\/j.jneumeth.2019.108506","article-title":"DeepFMRI: End-to-end deep learning for functional connectivity and classification of ADHD using fMRI","volume":"335","author":"A Riaz","year":"2020","journal-title":"J Neurosci Methods"},{"key":"pcbi.1012130.ref147","doi-asserted-by":"crossref","first-page":"12804","DOI":"10.1038\/s41598-021-91878-w","article-title":"Unraveling hidden interactions in complex systems with deep learning.","volume":"11","author":"S Ha","year":"2021","journal-title":"Sci Rep"},{"key":"pcbi.1012130.ref148","doi-asserted-by":"crossref","first-page":"041001","DOI":"10.1088\/1478-3975\/abffbe","article-title":"Emerging machine learning approaches to phenotyping cellular motility and morphodynamics.","volume":"18","author":"HJ Choi","year":"2021","journal-title":"Phys Biol"},{"key":"pcbi.1012130.ref149","doi-asserted-by":"crossref","first-page":"1667","DOI":"10.1038\/s41467-023-37318-x","article-title":"Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice","volume":"14","author":"Y Printz","year":"2023","journal-title":"Nat Commun"},{"key":"pcbi.1012130.ref150","doi-asserted-by":"crossref","first-page":"e2202204119","DOI":"10.1073\/pnas.2202204119","article-title":"Temporal signals drive the emergence of multicellular information networks","volume":"119","author":"G Li","year":"2022","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1012130.ref151","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis.","volume":"9","author":"J Schindelin","year":"2012","journal-title":"Nat Methods"},{"key":"pcbi.1012130.ref152","doi-asserted-by":"crossref","first-page":"E477","DOI":"10.1152\/ajpendo.00030.2023","article-title":"Ca2+ release or Ca2+ entry, that is the question: what governs Ca2+ oscillations in pancreatic \u03b2 cells?","volume":"324","author":"PA Fletcher","year":"2023","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"pcbi.1012130.ref153","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1038\/s41593-021-00804-w","article-title":"Integrating new memories into the hippocampal network activity space","volume":"24","author":"GP Gava","year":"2021","journal-title":"Nat Neurosci"},{"key":"pcbi.1012130.ref154","first-page":"719","article-title":"A Measure of Concurrent Neural Firing Activity Based on Mutual Information. Neuroinformatics.","volume":"19","author":"G Mijatovic","year":"2021"},{"key":"pcbi.1012130.ref155","doi-asserted-by":"crossref","DOI":"10.1002\/0471200611","author":"TM Cover","year":"2001","journal-title":"Elements of Information Theory"},{"key":"pcbi.1012130.ref156","doi-asserted-by":"crossref","first-page":"3503","DOI":"10.1098\/rsta.2008.0110","article-title":"Cell coupling in mouse pancreatic -Cells measured in intact islets of Langerhans","volume":"366","author":"Q Zhang","year":"2008","journal-title":"Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences."},{"key":"pcbi.1012130.ref157","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1090\/S0002-9939-1956-0078686-7","article-title":"On the shortest spanning subtree of a graph and the traveling salesman problem","author":"JB Kruskal","year":"1956","journal-title":"Proceedings of the American Mathematical Society"},{"key":"pcbi.1012130.ref158","doi-asserted-by":"crossref","first-page":"1389","DOI":"10.1002\/j.1538-7305.1957.tb01515.x","article-title":"Shortest connection networks and some generalizations","volume":"36","author":"RC Prim","year":"1957","journal-title":"The Bell System Technical Journal"},{"key":"pcbi.1012130.ref159","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.physrep.2005.10.009","article-title":"Complex networks: Structure and dynamics","volume":"424","author":"S Boccaletti","year":"2006","journal-title":"Physics Reports"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1012130","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,23]],"date-time":"2024-05-23T00:00:00Z","timestamp":1716422400000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012130","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,23]],"date-time":"2024-05-23T18:12:19Z","timestamp":1716487939000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012130"}},"subtitle":[],"editor":[{"given":"Jonathan","family":"Rubin","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,5,13]]},"references-count":159,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,5,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1012130","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1012130","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,13]]}}}