{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,19]],"date-time":"2026-02-19T13:03:51Z","timestamp":1771506231332,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010027","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,25]],"date-time":"2022-04-25T00:00:00Z","timestamp":1650844800000}}],"reference-count":106,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2022,4,13]],"date-time":"2022-04-13T00:00:00Z","timestamp":1649808000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["Code 001"],"award-info":[{"award-number":["Code 001"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["442563-2016\/7"],"award-info":[{"award-number":["442563-2016\/7"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001807","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de S\u00e3o Paulo","doi-asserted-by":"publisher","award":["15\/24691-8"],"award-info":[{"award-number":["15\/24691-8"]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007384","name":"Instituto Nacional de Neuroci\u00eancia Translacional","doi-asserted-by":"crossref","award":["573604\/2008-8"],"award-info":[{"award-number":["573604\/2008-8"]}],"id":[{"id":"10.13039\/501100007384","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Universidad Nacional Aut\u00f3noma de Honduras","award":["CU-O-041-05-2014"],"award-info":[{"award-number":["CU-O-041-05-2014"]}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>The types of epileptiform activity occurring in the sclerotic hippocampus with highest incidence are interictal-like events (II) and periodic ictal spiking (PIS). These activities are classified according to their event rates, but it is still unclear if these rate differences are consequences of underlying physiological mechanisms. Identifying new and more specific information related to these two activities may bring insights to a better understanding about the epileptogenic process and new diagnosis. We applied Poincar\u00e9 map analysis and Recurrence Quantification Analysis (RQA) onto 35<jats:italic>in vitro<\/jats:italic>electrophysiological signals recorded from slices of 12 hippocampal tissues surgically resected from patients with pharmacoresistant temporal lobe epilepsy. These analyzes showed that the II activity is related to chaotic dynamics, whereas the PIS activity is related to deterministic periodic dynamics. Additionally, it indicates that their different rates are consequence of different endogenous dynamics. Finally, by using two computational models we were able to simulate the transition between II and PIS activities. The RQA was applied to different periods of these simulations to compare the recurrences between artificial and real signals, showing that different ranges of regularity-chaoticity can be directly associated with the generation of PIS and II activities.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010027","type":"journal-article","created":{"date-parts":[[2022,4,13]],"date-time":"2022-04-13T17:52:07Z","timestamp":1649872327000},"page":"e1010027","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Chaotic and stochastic dynamics of epileptiform-like activities in sclerotic hippocampus resected from patients with pharmacoresistant epilepsy"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7570-6866","authenticated-orcid":true,"given":"Noemi S.","family":"Ara\u00fajo","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8969-7953","authenticated-orcid":true,"given":"Selvin Z.","family":"Reyes-Garcia","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1266-5902","authenticated-orcid":true,"given":"Jo\u00e3o A. F.","family":"Brogin","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1783-0524","authenticated-orcid":true,"given":"Douglas D.","family":"Bueno","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0854-3582","authenticated-orcid":true,"given":"Esper A.","family":"Cavalheiro","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7810-4748","authenticated-orcid":true,"given":"Carla A.","family":"Scorza","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2129-8251","authenticated-orcid":true,"given":"Jean","family":"Faber","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,4,13]]},"reference":[{"key":"pcbi.1010027.ref001","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1001\/archneur.1964.00460150003001","article-title":"Etiology and pathogenesis of temporal lobe epilepsy","volume":"10","author":"MA Falconer","year":"1964","journal-title":"Arch Neurol"},{"key":"pcbi.1010027.ref002","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1111\/nan.12150","article-title":"Review: Hippocampal sclerosis in epilepsy: A neuropathology review","volume":"40","author":"M Thom","year":"2014","journal-title":"Neuropathol. Appl. Neurobiol"},{"key":"pcbi.1010027.ref003","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1056\/NEJMoa1703784","article-title":"Histopathological findings in brain tissue obtained during epilepsy surgery","volume":"377","author":"I Bl\u00fcmcke","year":"2017","journal-title":"N. Engl. J. Med"},{"key":"pcbi.1010027.ref004","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1016\/S0140-6736(11)60890-8","article-title":"The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: A cohort study","volume":"378","author":"J De Tisi","year":"2011","journal-title":"Lancet"},{"key":"pcbi.1010027.ref005","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1038\/nrneurol.2012.181","article-title":"Pharmacoresistance and the role of surgery in difficult to treat epilepsy","volume":"8","author":"S Wiebe","year":"2012","journal-title":"Nat. Rev. Neurol"},{"key":"pcbi.1010027.ref006","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.neurol.2015.01.563","article-title":"Hippocampus and epilepsy: Findings from human tissues","volume":"171","author":"G Huberfeld","year":"2015","journal-title":"Rev. Neurol"},{"key":"pcbi.1010027.ref007","doi-asserted-by":"crossref","first-page":"10416","DOI":"10.1523\/JNEUROSCI.2074-04.2004","article-title":"Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis","volume":"24","author":"S Gabriel","year":"2004","journal-title":"J. Neurosci"},{"key":"pcbi.1010027.ref008","doi-asserted-by":"crossref","first-page":"3290","DOI":"10.1093\/brain\/awl218","article-title":"Carbamazepine-resistance in the epileptic dentate gyrus of human hippocampal slices","volume":"129","author":"K Jandov\u00e1","year":"2006","journal-title":"Brain"},{"key":"pcbi.1010027.ref009","doi-asserted-by":"crossref","first-page":"S34","DOI":"10.1111\/j.1528-1157.2000.tb01532.x","article-title":"Nonlinear EEG analysis and its potential role in epileptology","volume":"41","author":"CE Elger","year":"2000","journal-title":"Epilepsia"},{"key":"pcbi.1010027.ref010","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1016\/j.crvi.2003.09.011","article-title":"Is there chaos in the brain? II. Experimental evidence and related models","volume":"326","author":"H Korn","year":"2003","journal-title":"C. R. Biol"},{"key":"pcbi.1010027.ref011","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/j.0013-9580.2003.12007.x","article-title":"Toward a neurodynamical understanding of ictogenesis","volume":"44","author":"MLV Quyen","year":"2003","journal-title":"Epilepsia"},{"key":"pcbi.1010027.ref012","doi-asserted-by":"crossref","first-page":"409","DOI":"10.3389\/fnhum.2017.00409","article-title":"Structure function revisited: a simple tool for complex analysis of neuronal activity","volume":"11","author":"F Nanni","year":"2017","journal-title":"Frontiers in human neuroscience"},{"issue":"2","key":"pcbi.1010027.ref013","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1177\/107385849600200213","article-title":"Chaos Theory and Epilepsy","volume":"2","author":"LD Iasemidis","year":"1996","journal-title":"The Neuroscientist"},{"key":"pcbi.1010027.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-3-642-75545-3","volume-title":"Chaos in brain function","author":"E Ba\u015far","year":"1990"},{"key":"pcbi.1010027.ref015","doi-asserted-by":"crossref","DOI":"10.1142\/1857","volume-title":"Nonlinear Dynamical Analysis of the EEG","author":"BH Jansen","year":"1993"},{"issue":"01","key":"pcbi.1010027.ref016","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1142\/S0129065795000032","article-title":"Noise-enhanced performance in a cortical associative memory model","volume":"6","author":"HG Liljenstr\u00f6m","year":"1995","journal-title":"Int J Neural Syst"},{"key":"pcbi.1010027.ref017","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1002\/hipo.22657","article-title":"3-Hz subthreshold oscillations of CA2 neurons In vivo","volume":"26","author":"N Matsumoto","year":"2016","journal-title":"Hippocampus"},{"issue":"1","key":"pcbi.1010027.ref018","doi-asserted-by":"crossref","first-page":"S64","DOI":"10.1038\/sj.npp.1300137","article-title":"Neural stability and flexibility: a computational approach","volume":"28","author":"HG Liljenstr\u00f6m","year":"2003","journal-title":"Neuropsychopharmacol"},{"key":"pcbi.1010027.ref019","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/0006-8993(95)00485-9","article-title":"Chaotic responses of the hippocampal CA3 region to a mossy fiber stimulation in vitro","volume":"686","author":"H Hayashi","year":"1995","journal-title":"Brain Res"},{"issue":"3","key":"pcbi.1010027.ref020","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/0375-9601(85)90444-X","article-title":"Evidence of chaotic dynamics of brain activity during the sleep cycle","volume":"111","author":"A Babloyantz","year":"1985","journal-title":"Phys Lett A"},{"issue":"06","key":"pcbi.1010027.ref021","doi-asserted-by":"crossref","first-page":"1687","DOI":"10.1142\/S0218127410026769","article-title":"Brain dynamics at multiple scales: can one reconcile the apparent low-dimensional chaos of macroscopic variables with the seemingly stochastic behavior of single neurons?","volume":"20","author":"S El Boustani","year":"2010","journal-title":"Int J Bifurcat Chaos"},{"issue":"2","key":"pcbi.1010027.ref022","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1017\/S0140525X00047336","article-title":"How brains make chaos in order to make sense of the world","volume":"10","author":"CA Skarda","year":"1987","journal-title":"Behav Brain Sci"},{"issue":"4","key":"pcbi.1010027.ref023","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1172\/JCI117111","article-title":"Chaos and chaos control in biology","volume":"93","author":"JN Weiss","year":"1994","journal-title":"J Clin Invest"},{"issue":"2","key":"pcbi.1010027.ref024","first-page":"89","article-title":"Chaos in the neurosciences: cautionary tales from the frontier","volume":"40","author":"PE Rapp","year":"1993","journal-title":"Biologist"},{"issue":"7","key":"pcbi.1010027.ref025","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1109\/10.503182","article-title":"Detection of seizures from small samples using nonlinear dynamic system theory","volume":"43","author":"I Yaylali","year":"1996","journal-title":"IEEE Trans Biomed Eng"},{"issue":"5","key":"pcbi.1010027.ref026","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/0013-4694(94)00181-2","article-title":"Fractal analysis of electroencephalographic signals intracerebrally recorded during 35 epileptic seizures: evaluation of a new method for synoptic visualisation of ictal events","volume":"91","author":"ET Bullmore","year":"1994","journal-title":"Electroencephalogr Clin Neurophysiol"},{"issue":"9","key":"pcbi.1010027.ref027","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1016\/S0764-4469(01)01377-4","article-title":"Is there chaos in the brain? I. Concepts of nonlinear dynamics and methods of investigation","volume":"324","author":"P Faure","year":"2001","journal-title":"C R Seances Acad Sci III"},{"key":"pcbi.1010027.ref028","first-page":"1","article-title":"Different patterns of epileptiform-like activity are generated in the sclerotic hippocampus from patients with drug-resistant temporal lobe epilepsy","volume":"8","author":"SZ Reyes-Garcia","year":"2018","journal-title":"Sci Rep"},{"key":"pcbi.1010027.ref029","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/0013-4694(90)90031-E","article-title":"The Hans Berger lecture: Functional explorations of the human epileptic brain and their therapeutic implications","volume":"76","author":"J Engel","year":"1990","journal-title":"Electroencephalogr Clin Neurophysiol"},{"key":"pcbi.1010027.ref030","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1002\/ana.410380513","article-title":"Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy","volume":"38","author":"A Williamson","year":"1995","journal-title":"Ann Neurol"},{"key":"pcbi.1010027.ref031","doi-asserted-by":"crossref","first-page":"3513","DOI":"10.1073\/pnas.83.10.3513","article-title":"Low-dimensional chaos in an instance of epilepsy","volume":"83","author":"A Babloyantz","year":"1986","journal-title":"Proc Natl Acad Sci. USA"},{"key":"pcbi.1010027.ref032","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1126\/science.7770778","article-title":"Reliability of spike timing in neocortical neurons","volume":"268","author":"ZF Mainen","year":"1995","journal-title":"Science"},{"key":"pcbi.1010027.ref033","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1126\/science.274.5293.1724","article-title":"Chaos in neuronal networks with balanced excitatory and inhibitory activity","volume":"274","author":"C Van Vreeswijk","year":"1996","journal-title":"Science"},{"key":"pcbi.1010027.ref034","first-page":"3401","article-title":"Unstable periodic orbits in human epileptic activity","volume":"56","author":"M Le Van Quyen","year":"1997","journal-title":"Phys Rev F"},{"key":"pcbi.1010027.ref035","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/S0167-8760(99)00043-4","article-title":"Non-linear time series analysis of intracranial EEG recordings in patients with epilepsy: An overview","volume":"34","author":"K Lehnertz","year":"1999","journal-title":"Int J Psychophysiol"},{"key":"pcbi.1010027.ref036","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1142\/S0219519412400155","article-title":"Nonlinear analysis of physiological signals: A review","volume":"12","author":"O Faust","year":"2012","journal-title":"J Mech Med Biol"},{"key":"pcbi.1010027.ref037","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.physrep.2006.11.001","article-title":"Recurrence plots for the analysis of complex systems","volume":"438","author":"N Marwan","year":"2007","journal-title":"Phys Rep"},{"issue":"1","key":"pcbi.1010027.ref038","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1140\/epjst\/e2008-00829-1","article-title":"A historical review of recurrence plots","volume":"164","author":"N Marwan","year":"2008","journal-title":"Eur Phys J Spec Top"},{"key":"pcbi.1010027.ref039","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-3-319-07155-8_1","volume-title":"Recurrence Quantification Analysis","author":"N Marwan","year":"2015"},{"issue":"1222","key":"pcbi.1010027.ref040","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1098\/rspb.1984.0024","article-title":"A model of neuronal bursting using three coupled first order differential equations","volume":"221","author":"JL Hindmarsh","year":"1984","journal-title":"P Roy Soc Lond B Bio"},{"issue":"6","key":"pcbi.1010027.ref041","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1109\/TNN.2003.820440","article-title":"Simple model of spiking neurons","volume":"14","author":"EM Izhikevich","year":"2003","journal-title":"IEEE T Neural Networ"},{"issue":"1","key":"pcbi.1010027.ref042","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.jneumeth.2008.11.004","article-title":"sigTOOL: A MATLAB-based environment for sharing laboratory-developed software to analyze biological signals","volume":"178","author":"M Lidierth","year":"2009","journal-title":"J. Neurosci Methods"},{"key":"pcbi.1010027.ref043","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v008.i18","article-title":"Evaluating Kolmogorov\u2019s Distribution","volume":"8","author":"G Marsaglia","year":"2003","journal-title":"J Stat Soft"},{"key":"pcbi.1010027.ref044","doi-asserted-by":"crossref","first-page":"R45","DOI":"10.1016\/j.cub.2011.11.005","article-title":"Spike sorting","volume":"22","author":"RQ Quiroga","year":"2012","journal-title":"Curr Biol"},{"key":"pcbi.1010027.ref045","volume-title":"Pattern Recognition","author":"S Theodoridis","year":"2009"},{"key":"pcbi.1010027.ref046","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4614-7375-6","volume-title":"Poincar\u00e9 plot methods for heart rate variability analysis","author":"AH Khandoker","year":"2013"},{"key":"pcbi.1010027.ref047","first-page":"H244","article-title":"Quantitative beat-to-beat analysis of heart rate dynamics during exercise","volume":"271","author":"MP Tulppo","year":"1996","journal-title":"Am J Physiol"},{"key":"pcbi.1010027.ref048","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1109\/10.959330","article-title":"Do existing measures of Poincar\u00e9 plot geometry reflect nonlinear features of heart rate variability?","volume":"48","author":"M Brennan","year":"2001","journal-title":"IEEE Trans Biomed Eng"},{"key":"pcbi.1010027.ref049","doi-asserted-by":"crossref","first-page":"391","DOI":"10.2307\/2987742","article-title":"Measuring Skewness and Kurtosis","volume":"33","author":"RA Groeneveld","year":"1984","journal-title":"The Statistician"},{"key":"pcbi.1010027.ref050","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1080\/00031305.1988.10475539","article-title":"Kurtosis: A Critical Review","volume":"42","author":"KP Balanda","year":"1988","journal-title":"Am Stat"},{"key":"pcbi.1010027.ref051","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1080\/00031305.2014.917055","article-title":"Kurtosis as Peakedness, 1905\u20142014","volume":"68","author":"PH Westfall","year":"2014","journal-title":"R.I.P. Am Stat"},{"key":"pcbi.1010027.ref052","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/0375-9601(92)90426-M","article-title":"Embeddings and delays as derived from quantification of recurrence plots","volume":"171","author":"JP Zbilut","year":"1992","journal-title":"Phys Lett. A"},{"key":"pcbi.1010027.ref053","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-07155-8","volume-title":"Recurrence quantification analysis: Theory and best practices","author":"CL Webber","year":"2015"},{"key":"pcbi.1010027.ref054","volume-title":"Practical biomedical signal analysis using MATLAB","author":"KJ Blinowska","year":"2012"},{"key":"pcbi.1010027.ref055","volume-title":"Dynamical Systems and Turbulence","author":"F Takens","year":"1981"},{"key":"pcbi.1010027.ref056","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1209\/0295-5075\/4\/9\/004","article-title":"Recurrence plots of dynamical systems","volume":"4","author":"JP Eckmann","year":"1987","journal-title":"Europhys Lett"},{"key":"pcbi.1010027.ref057","doi-asserted-by":"crossref","first-page":"2427","DOI":"10.1103\/PhysRevA.34.2427","article-title":"Spurious dimension from correlation algorithms applied to limited time-series data","volume":"34","author":"J Theiler","year":"1986","journal-title":"Phys Rev A Gen Phys"},{"key":"pcbi.1010027.ref058","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0173776","article-title":"A neural mass model of cross frequency coupling","volume":"12","author":"M Chehelcheraghi","year":"2017","journal-title":"PLoS One"},{"key":"pcbi.1010027.ref059","doi-asserted-by":"crossref","first-page":"3178","DOI":"10.1103\/PhysRevLett.83.3178","article-title":"Recurrence Time Statistics for Chaotic Systems and Their Applications","volume":"83","author":"JB Gao","year":"1999","journal-title":"Phys Rev Lett"},{"key":"pcbi.1010027.ref060","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1142\/S0218127411029008","article-title":"How to avoid potential pitfalls in recurrence plot based data analysis","volume":"21","author":"N Marwan","year":"2011","journal-title":"Int J Bifurcat Chaos"},{"key":"pcbi.1010027.ref061","first-page":"3","volume-title":"Data Handling in Science and Technology","author":"JM Amigo","year":"2020"},{"key":"pcbi.1010027.ref062","doi-asserted-by":"crossref","DOI":"10.1201\/9781482295412","volume-title":"Chaos theory tamed","author":"G Williams","year":"1997"},{"key":"pcbi.1010027.ref063","volume-title":"Stochastic processes: a survey of the mathematical theory","author":"J Lamperti","year":"2012"},{"key":"pcbi.1010027.ref064","article-title":"Cardiac and Autonomic Dysfunctions Assessed Through Recurrence Quantitative Analysis of Electrocardiogram Signals and an Application to the 6-Hydroxydopamine Parkinson\u2019s Disease Animal Model","volume":"1919","author":"L Shinoda","year":"2021","journal-title":"Frontiers in physiology"},{"key":"pcbi.1010027.ref065","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0370-1573(99)00096-4","article-title":"The control of chaos: theory and applications","volume":"329","author":"S Boccaletti","year":"2000","journal-title":"Physics reports"},{"key":"pcbi.1010027.ref066","doi-asserted-by":"crossref","DOI":"10.1515\/9781400858156","volume-title":"Chaos","author":"AV Holden","year":"1986"},{"key":"pcbi.1010027.ref067","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/0375-9601(93)90994-B","article-title":"A new method for computing Lyapunov exponents","volume":"175","author":"G Barna","year":"1993","journal-title":"Physics Letters A"},{"key":"pcbi.1010027.ref068","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1086\/318732","article-title":"A comparison between methods to compute Lyapunov exponents","volume":"121","author":"G Tancredi","year":"2001","journal-title":"The Astronomical Journal"},{"key":"pcbi.1010027.ref069","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1002\/1097-0193(200009)11:1<46::AID-HBM40>3.0.CO;2-5","article-title":"Measuring the complexity of time series: an application to neurophysiological signals","volume":"11","author":"SL Gonzalez Andino","year":"2000","journal-title":"Human brain mapping"},{"key":"pcbi.1010027.ref070","doi-asserted-by":"crossref","first-page":"062114","DOI":"10.1103\/PhysRevE.95.062114","article-title":"Entropy measures, entropy estimators, and their performance in quantifying complex dynamics: Effects of artifacts, nonstationarity, and long-range correlations","volume":"95","author":"W Xiong","year":"2017","journal-title":"Physical Review E"},{"issue":"3","key":"pcbi.1010027.ref071","doi-asserted-by":"crossref","first-page":"033128","DOI":"10.1063\/1.2975967","article-title":"The Hindmarsh\u2013Rose neuron model: bifurcation analysis and piecewise-linear approximations","volume":"18","author":"M Storace","year":"2008","journal-title":"Chaos"},{"issue":"9","key":"pcbi.1010027.ref072","doi-asserted-by":"crossref","first-page":"e0138919","DOI":"10.1371\/journal.pone.0138919","article-title":"Analysis of chaotic resonance in Izhikevich neuron model","volume":"10","author":"S Nobukawa","year":"2015","journal-title":"PloS one"},{"issue":"8","key":"pcbi.1010027.ref073","doi-asserted-by":"crossref","first-page":"2210","DOI":"10.1093\/brain\/awu133","article-title":"On the nature of seizure dynamics","volume":"137","author":"V. K. Jirsa","year":"2014","journal-title":"Brain"},{"key":"pcbi.1010027.ref074","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1016\/S0140-6736(06)68735-7","article-title":"Deceleration capacity of heart rate as a predictor of mortality after myocardial infarction: cohort study","volume":"367","author":"A Bauer","year":"2006","journal-title":"Lancet"},{"key":"pcbi.1010027.ref075","first-page":"1","article-title":"Deceleration and acceleration capacities of heart rate associated with heart failure with high discriminating performance","author":"W Hu","year":"2016","journal-title":"Sci Rep"},{"key":"pcbi.1010027.ref076","first-page":"23","article-title":"What is physiologic complexity and how does it change with aging and disease? Neurobiol","volume":"23","author":"AL Goldberger","year":"2002","journal-title":"Aging"},{"key":"pcbi.1010027.ref077","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/0002-8703(92)90510-3","article-title":"Patterns of beat-to-beat heart rate variability in advanced heart failure","volume":"123","author":"MA Woo","year":"1992","journal-title":"Am Heart J"},{"key":"pcbi.1010027.ref078","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/0735-1097(94)90737-4","article-title":"Complex heart rate variability and serum norepinephrine levels in patients with advanced heart failure","volume":"23","author":"MA Woo","year":"1994","journal-title":"J Am Coll Cardiol"},{"key":"pcbi.1010027.ref079","first-page":"1","article-title":"Geometric patterns of time-delay plots from different cardiac rhythms and arrhythmias using short-term EKG signals","volume":"37","author":"RA Borracci","year":"2017","journal-title":"Clin Physiol Funct Imaging"},{"key":"pcbi.1010027.ref080","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1046\/j.1475-097X.2003.00466.x","article-title":"Poincar\u00e9 plot indexes of heart rate variability capture dynamic adaptations after haemodialysis in chronic renal failure patients","volume":"23","author":"C Lerma","year":"2003","journal-title":"Clin Physiol Func Im"},{"key":"pcbi.1010027.ref081","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.jelectrocard.2015.11.004","article-title":"Heart rate variability analysed by Poincar\u00e9 plot in patients with metabolic syndrome","volume":"49","author":"A Kubi\u010dkov\u00e1","year":"2016","journal-title":"J Electrocardiol"},{"key":"pcbi.1010027.ref082","first-page":"1332","article-title":"Characterization and classification of patients with different levels of cardiac death risk by using Poincar\u00e9 plot analysis","author":"J Rodriguez","year":"2017","journal-title":"Conf Proc IEEE Eng Med Biol Soc"},{"key":"pcbi.1010027.ref083","doi-asserted-by":"crossref","first-page":"1921","DOI":"10.1007\/s11517-016-1486-9","article-title":"Do the deceleration\/acceleration capacities of heart rate reflect cardiac sympathetic or vagal activity? A model study","volume":"54","author":"Q Pan","year":"2016","journal-title":"Med Biol Eng Comput"},{"key":"pcbi.1010027.ref084","doi-asserted-by":"crossref","first-page":"1170","DOI":"10.1016\/j.neuron.2016.07.039","article-title":"Virtual Cortical Resection Reveals Push-Pull Network Control Preceding Seizure Evolution","volume":"91","author":"AN Khambhati","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1010027.ref085","doi-asserted-by":"crossref","first-page":"1926","DOI":"10.1126\/science.1099745","article-title":"Neuronal oscillations in cortical networks","volume":"304","author":"G Buzs\u00e1ki","year":"2004","journal-title":"Science"},{"key":"pcbi.1010027.ref086","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1016\/j.tins.2015.09.001","article-title":"Neural Cross-Frequency Coupling: Connecting Architectures, Mechanisms, and Functions","volume":"38","author":"A Hyafil","year":"2015","journal-title":"Trends Neurosci"},{"issue":"11","key":"pcbi.1010027.ref087","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1038\/3305","article-title":"Neurogenesis in the adult human hippocampus","volume":"4","author":"PS Eriksson","year":"1998","journal-title":"Nat Med"},{"issue":"10","key":"pcbi.1010027.ref088","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1002\/hipo.22616","volume":"26","author":"H Eichenbaum","year":"2016","journal-title":"Hippocampus"},{"key":"pcbi.1010027.ref089","doi-asserted-by":"crossref","DOI":"10.1093\/acprof:oso\/9780195100273.001.0001","volume-title":"The hippocampus book","author":"P Andersen","year":"2006"},{"issue":"4","key":"pcbi.1010027.ref090","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1111\/j.1535-7511.2005.00049.x","article-title":"The role of the subiculum in epilepsy and epileptogenesis","volume":"5","author":"C. E Stafstrom","year":"2005","journal-title":"Epilepsy Curr"},{"issue":"3","key":"pcbi.1010027.ref091","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.yebeh.2009.12.023","article-title":"Stimulation-based anticipation and control of state transitions in the epileptic brain","volume":"17","author":"S. N. Kalitzin","year":"2010","journal-title":"Epilepsy Behav"},{"key":"pcbi.1010027.ref092","doi-asserted-by":"crossref","first-page":"S102","DOI":"10.1016\/j.yebeh.2011.08.017","article-title":"Computational model prospective on the observation of proictal states in epileptic neuronal systems","volume":"22","author":"S. Kalitzin","year":"2011","journal-title":"Epilepsy Behav"},{"issue":"3","key":"pcbi.1010027.ref093","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1109\/TBME.2005.869800","article-title":"Dynamics of epileptic phenomena determined from statistics of ictal transitions","volume":"53","author":"P. Suffczynski","year":"2006","journal-title":"IEEE Trans. Biomed. Eng."},{"issue":"1","key":"pcbi.1010027.ref094","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.yebeh.2009.02.033","article-title":"Neuropathology of focal epilepsies: a critical review","volume":"15","author":"I Bl\u00fcmcke","year":"2009","journal-title":"Epilepsy Behav"},{"key":"pcbi.1010027.ref095","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1038\/nrneurol.2013.173","article-title":"Epilepsy: hippocampal sclerosis\u2014are we speaking the same language?","volume":"9","author":"GD Jackson","year":"2013","journal-title":"Nat Rev Neurol"},{"key":"pcbi.1010027.ref096","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1002\/hipo.450040213","article-title":"Electrophysiological characterization of CA2 pyramidal cells from epileptic humans","volume":"4","author":"A Williamson","year":"1994","journal-title":"Hippocampus"},{"issue":"5","key":"pcbi.1010027.ref097","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1152\/jn.00232.2012","article-title":"Seizures as imbalanced up states: excitatory and inhibitory conductances during seizure-like events","volume":"109","author":"J \u017diburkus","year":"2013","journal-title":"J Neurophysiol"},{"issue":"5885","key":"pcbi.1010027.ref098","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1126\/science.1149381","article-title":"Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations","volume":"321","author":"T Klausberger","year":"2008","journal-title":"Science"},{"issue":"3","key":"pcbi.1010027.ref099","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/S0959-4388(00)00091-X","article-title":"Hebb and homeostasis in neuronal plasticity","volume":"10","author":"GG Turrigiano","year":"2000","journal-title":"Curr Opin Neurobiol"},{"issue":"7363","key":"pcbi.1010027.ref100","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nature10360","article-title":"Neocortical excitation\/inhibition balance in information processing and social dysfunction","volume":"477","author":"O Yizhar","year":"2011","journal-title":"Nature"},{"issue":"5","key":"pcbi.1010027.ref101","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1016\/j.neuron.2016.10.027","article-title":"The impact of structural heterogeneity on excitation-inhibition balance in cortical networks","volume":"92","author":"ID Landau","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1010027.ref102","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1152\/jn.1988.59.1.259","article-title":"Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice","volume":"59","author":"SF Traynelis","year":"1988","journal-title":"J Neurophysiol"},{"key":"pcbi.1010027.ref103","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.eplepsyres.2011.07.008","article-title":"Progressive, potassium-sensitive epileptiform activity in hippocampal area CA3 of pilocarpine-treated rats with recurrent seizures","volume":"97","author":"DP McCloskey","year":"2011","journal-title":"Epilepsy Res"},{"key":"pcbi.1010027.ref104","doi-asserted-by":"crossref","first-page":"2130","DOI":"10.1152\/jn.1999.82.5.2130","article-title":"Seizure-like events in disinhibited ventral slices of adult rat hippocampus","volume":"82","author":"C Borck","year":"1999","journal-title":"J Neurophysiol"},{"key":"pcbi.1010027.ref105","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1152\/jn.00914.2009","article-title":"Neuronal density determines network connectivity and spontaneous activity in cultured hippocampus","volume":"104","author":"M Ivenshitz","year":"2010","journal-title":"J Neurophysiol"},{"key":"pcbi.1010027.ref106","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1002\/cne.901820508","article-title":"A Golgi study of cell types in the hilar region of the hippocampus in the rat","volume":"182","author":"DG Amaral","year":"1978","journal-title":"J Comp Neurol"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1010027","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,25]],"date-time":"2022-04-25T00:00:00Z","timestamp":1650844800000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010027","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,22]],"date-time":"2024-09-22T05:44:04Z","timestamp":1726983844000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010027"}},"subtitle":[],"editor":[{"given":"Peter Neal","family":"Taylor","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,4,13]]},"references-count":106,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,4,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010027","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1010027","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,13]]}}}