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These patterns are often described in terms of synchrony, oscillations, and phase relationships. Many methods have been proposed for the quantification of these collective states of dynamic neuronal organization. However, it is difficult to determine which method is best suited for which experimental setting and research question. This choice is further complicated by the fact that most methods are sensitive to a combination of synchrony, oscillations, and other factors; in addition, some of them display systematic biases that can complicate their interpretation. To address these challenges, we adopt a highly comparative approach, whereby spike trains are represented by a diverse library of measures. This enables unsupervised or supervised analysis in the space of measures, or in that of spike trains. We compile a battery of 122 measures of synchrony, oscillations, and phase relationships, complemented with 9 measures of spiking intensity and variability. We first apply them to sets of synthetic spike trains with known statistical properties, and show that all measures are confounded by extraneous factors such as firing rate or population frequency, but to different extents. Then, we analyze spike trains recorded in different species\u2014rat, mouse, and monkey\u2014and brain areas\u2014primary sensory cortices and hippocampus\u2014and show that our highly comparative approach provides a high-dimensional quantification of collective network activity that can be leveraged for both unsupervised and supervised characterization of firing patterns. Overall, the highly comparative approach provides a detailed description of the empirical properties of multineuron spike train analysis methods, including practical guidelines for their use in experimental settings, and advances our understanding of neuronal coordination and coding.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1013597","type":"journal-article","created":{"date-parts":[[2025,10,24]],"date-time":"2025-10-24T17:56:54Z","timestamp":1761328614000},"page":"e1013597","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Synchrony, oscillations, and phase relationships in collective neuronal activity: A highly comparative overview of 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cortex","volume":"16","author":"A Luczak","year":"2015","journal-title":"Nat Rev Neurosci"},{"issue":"5","key":"pcbi.1013597.ref003","doi-asserted-by":"crossref","first-page":"1698","DOI":"10.1073\/pnas.86.5.1698","article-title":"Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex","volume":"86","author":"CM Gray","year":"1989","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"pcbi.1013597.ref004","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/35086012","article-title":"Correlated neuronal activity and the flow of neural information","volume":"2","author":"E Salinas","year":"2001","journal-title":"Nat Rev Neurosci"},{"issue":"5974","key":"pcbi.1013597.ref005","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1126\/science.1183108","article-title":"Synchrony of thalamocortical inputs maximizes cortical reliability","volume":"328","author":"H-P Wang","year":"2010","journal-title":"Science"},{"issue":"6","key":"pcbi.1013597.ref006","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1038\/nrn3241","article-title":"The origin of extracellular fields and currents\u2014EEG, ECoG, LFP and spikes","volume":"13","author":"G Buzs\u00e1ki","year":"2012","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1013597.ref007","doi-asserted-by":"crossref","first-page":"101","DOI":"10.3389\/fncir.2016.00101","article-title":"Local field potentials: Myths and misunderstandings","volume":"10","author":"O Herreras","year":"2016","journal-title":"Front Neural Circuits"},{"issue":"2","key":"pcbi.1013597.ref008","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.neuroimage.2011.12.039","article-title":"Towards the utilization of EEG as a brain imaging tool","volume":"61","author":"CM Michel","year":"2012","journal-title":"Neuroimage"},{"issue":"5","key":"pcbi.1013597.ref009","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1016\/j.neuron.2013.10.017","article-title":"EEG and MEG: Relevance to neuroscience","volume":"80","author":"F Lopes da Silva","year":"2013","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1013597.ref010","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.tics.2005.08.011","article-title":"A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence","volume":"9","author":"P Fries","year":"2005","journal-title":"Trends Cogn Sci"},{"issue":"7","key":"pcbi.1013597.ref011","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1038\/nn.4569","article-title":"Flexible information routing by transient synchrony","volume":"20","author":"A Palmigiano","year":"2017","journal-title":"Nat 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Fries","year":"2001","journal-title":"Science"},{"issue":"1","key":"pcbi.1013597.ref015","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1073\/pnas.0605643104","article-title":"Sequential structure of neocortical spontaneous activity in vivo","volume":"104","author":"A Luczak","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"pcbi.1013597.ref016","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1016\/j.neuron.2008.04.025","article-title":"A precisely timed asynchronous pattern of ON and OFF retinal ganglion cell activity during propagation of retinal waves","volume":"58","author":"D Kerschensteiner","year":"2008","journal-title":"Neuron"},{"issue":"23","key":"pcbi.1013597.ref017","doi-asserted-by":"crossref","first-page":"8570","DOI":"10.1523\/JNEUROSCI.2817-10.2011","article-title":"Synchrony makes neurons fire in sequence, and stimulus properties determine who is ahead","volume":"31","author":"MN Havenith","year":"2011","journal-title":"J Neurosci"},{"key":"pcbi.1013597.ref018","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/S0079-6123(08)60556-7","article-title":"Oscillatory and non-oscillatory synchronizations in the visual cortex and their possible roles in associations of visual features","volume":"102","author":"R Eckhorn","year":"1994","journal-title":"Prog Brain Res"},{"issue":"1","key":"pcbi.1013597.ref019","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1073\/pnas.92.1.290","article-title":"Relation between oscillatory activity and long-range synchronization in cat visual cortex","volume":"92","author":"P K\u00f6nig","year":"1995","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"pcbi.1013597.ref020","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/0013-4694(69)90092-3","article-title":"Hippocampal electrical activity and voluntary movement in the rat","volume":"26","author":"CH Vanderwolf","year":"1969","journal-title":"Electroencephalogr Clin Neurophysiol"},{"key":"pcbi.1013597.ref021","unstructured":"O\u2019Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford: Clarendon Press; 1978."},{"issue":"7","key":"pcbi.1013597.ref022","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1002\/hipo.20109","article-title":"Human hippocampal theta activity during virtual navigation","volume":"15","author":"AD Ekstrom","year":"2005","journal-title":"Hippocampus"},{"issue":"46","key":"pcbi.1013597.ref023","doi-asserted-by":"crossref","first-page":"12297","DOI":"10.1073\/pnas.1708716114","article-title":"Human hippocampal theta power indicates movement onset and distance travelled","volume":"114","author":"D Bush","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"12","key":"pcbi.1013597.ref024","doi-asserted-by":"crossref","DOI":"10.1016\/j.cell.2021.04.017","article-title":"Phase precession in the human hippocampus and entorhinal cortex","volume":"184","author":"SE Qasim","year":"2021","journal-title":"Cell"},{"issue":"4","key":"pcbi.1013597.ref025","doi-asserted-by":"crossref","DOI":"10.1016\/j.cell.2018.09.017","article-title":"Nonoscillatory phase coding and synchronization in the bat hippocampal formation","volume":"175","author":"T Eliav","year":"2018","journal-title":"Cell"},{"issue":"83","key":"pcbi.1013597.ref026","doi-asserted-by":"crossref","first-page":"20130048","DOI":"10.1098\/rsif.2013.0048","article-title":"Highly comparative time-series analysis: The empirical structure of time series and their methods","volume":"10","author":"BD Fulcher","year":"2013","journal-title":"J R Soc Interface"},{"issue":"12","key":"pcbi.1013597.ref027","doi-asserted-by":"crossref","first-page":"3026","DOI":"10.1109\/TKDE.2014.2316504","article-title":"Highly comparative feature-based time-series classification","volume":"26","author":"BD Fulcher","year":"2014","journal-title":"IEEE Trans Knowl Data Eng"},{"issue":"10","key":"pcbi.1013597.ref028","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1038\/s43588-023-00519-x","article-title":"Unifying pairwise interactions in complex dynamics","volume":"3","author":"OM Cliff","year":"2023","journal-title":"Nat Comput Sci"},{"issue":"4","key":"pcbi.1013597.ref029","doi-asserted-by":"crossref","first-page":"100227","DOI":"10.1016\/j.patter.2021.100227","article-title":"HCGA: Highly comparative graph analysis for network phenotyping","volume":"2","author":"RL Peach","year":"2021","journal-title":"Patterns (N Y)"},{"key":"pcbi.1013597.ref030","doi-asserted-by":"crossref","first-page":"761826","DOI":"10.3389\/fnins.2021.761826","article-title":"Theoretical relationship between two measures of spike synchrony: Correlation index and vector strength","volume":"15","author":"D Kessler","year":"2021","journal-title":"Front Neurosci"},{"key":"pcbi.1013597.ref031","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.62116","article-title":"Topographic gradients of intrinsic dynamics across neocortex","volume":"9","author":"G Shafiei","year":"2020","journal-title":"Elife"},{"key":"pcbi.1013597.ref032","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.sleep.2022.06.013","article-title":"Beyond traditional sleep scoring: Massive feature extraction and data-driven clustering of sleep time series","volume":"98","author":"N Decat","year":"2022","journal-title":"Sleep Med"},{"issue":"1","key":"pcbi.1013597.ref033","doi-asserted-by":"crossref","first-page":"6000","DOI":"10.1038\/s41467-023-41689-6","article-title":"Neurophysiological signatures of cortical micro-architecture","volume":"14","author":"G Shafiei","year":"2023","journal-title":"Nat Commun"},{"key":"pcbi.1013597.ref034","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.neunet.2023.12.007","article-title":"Uncovering a stability signature of brain dynamics associated with meditation experience using massive time-series feature extraction","volume":"171","author":"NW Bailey","year":"2024","journal-title":"Neural Netw"},{"issue":"12","key":"pcbi.1013597.ref035","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1012692","article-title":"Extracting interpretable signatures of whole-brain dynamics through systematic comparison","volume":"20","author":"AG Bryant","year":"2024","journal-title":"PLoS Comput Biol"},{"issue":"7","key":"pcbi.1013597.ref036","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1038\/s41592-025-02704-4","article-title":"Benchmarking methods for mapping functional connectivity in the brain","volume":"22","author":"Z-Q Liu","year":"2025","journal-title":"Nat Methods"},{"issue":"7","key":"pcbi.1013597.ref037","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.3003217","article-title":"Wakefulness can be distinguished from general anesthesia and sleep in flies using a massive library of univariate time series analyses","volume":"23","author":"A Leung","year":"2025","journal-title":"PLoS Biol"},{"key":"pcbi.1013597.ref038","unstructured":"Cox DR, Isham V. Point Processes. CRC Press. 1980."},{"issue":"4","key":"pcbi.1013597.ref039","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/S0006-3495(67)86596-2","article-title":"Neuronal spike trains and stochastic point processes. I. The single spike train","volume":"7","author":"DH Perkel","year":"1967","journal-title":"Biophys J"},{"issue":"4","key":"pcbi.1013597.ref040","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1016\/S0006-3495(67)86597-4","article-title":"Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains","volume":"7","author":"DH Perkel","year":"1967","journal-title":"Biophys J"},{"key":"pcbi.1013597.ref041","unstructured":"Dayan P, Abbott LF. Theoretical neuroscience: Computational and mathematical modeling of neural systems. Cambridge, MA: MIT Press; 2001."},{"issue":"10","key":"pcbi.1013597.ref042","doi-asserted-by":"crossref","first-page":"3870","DOI":"10.1523\/JNEUROSCI.18-10-03870.1998","article-title":"The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding","volume":"18","author":"MN Shadlen","year":"1998","journal-title":"J Neurosci"},{"key":"pcbi.1013597.ref043","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.jphysparis.2009.11.007","article-title":"Spike timing-dependent plasticity is affected by the interplay of intrinsic and network oscillations","volume":"104","author":"F Baroni","year":"2010","journal-title":"J Physiol Paris"},{"issue":"2","key":"pcbi.1013597.ref044","article-title":"Delay selection by spike-timing-dependent plasticity in recurrent networks of spiking neurons receiving oscillatory inputs","volume":"9","author":"RR Kerr","year":"2013","journal-title":"PLoS Comput 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competition in cortical interneuron networks","volume":"16","author":"PHE Tiesinga","year":"2004","journal-title":"Neural Comput"},{"issue":"6","key":"pcbi.1013597.ref049","doi-asserted-by":"crossref","first-page":"4810","DOI":"10.1103\/PhysRevE.48.4810","article-title":"Dynamics of globally coupled inhibitory neurons with heterogeneity","volume":"48","author":"D Golomb","year":"1993","journal-title":"Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics"},{"issue":"9","key":"pcbi.1013597.ref050","doi-asserted-by":"crossref","first-page":"3432","DOI":"10.1152\/jn.00848.2014","article-title":"SPIKY: A graphical user interface for monitoring spike train synchrony","volume":"113","author":"T Kreuz","year":"2015","journal-title":"J Neurophysiol"},{"issue":"4","key":"pcbi.1013597.ref051","doi-asserted-by":"crossref","first-page":"043028","DOI":"10.1088\/1367-2630\/aa68c3","article-title":"Leaders and followers: quantifying consistency in spatio-temporal propagation patterns","volume":"19","author":"T Kreuz","year":"2017","journal-title":"New J Phys"},{"key":"pcbi.1013597.ref052","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.jneumeth.2017.09.008","article-title":"Spike-contrast: A novel time scale independent and multivariate measure of spike train synchrony","volume":"293","author":"M Ciba","year":"2018","journal-title":"J Neurosci Methods"},{"key":"pcbi.1013597.ref053","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/S0167-2789(00)00087-7","article-title":"Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients","volume":"144","author":"F Mormann","year":"2000","journal-title":"Phys D: Nonlin Phenom"},{"issue":"43","key":"pcbi.1013597.ref054","doi-asserted-by":"crossref","first-page":"14288","DOI":"10.1523\/JNEUROSCI.2767-14.2014","article-title":"Detecting pairwise correlations in spike trains: An objective comparison of methods and application to the study of retinal waves","volume":"34","author":"CS Cutts","year":"2014","journal-title":"J Neurosci"},{"issue":"5","key":"pcbi.1013597.ref055","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1016\/0896-6273(93)90122-8","article-title":"Transient period of correlated bursting activity during development of the mammalian retina","volume":"11","author":"RO Wong","year":"1993","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1013597.ref056","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.jneumeth.2007.05.031","article-title":"Measuring spike train synchrony","volume":"165","author":"T Kreuz","year":"2007","journal-title":"J Neurosci Methods"},{"issue":"1","key":"pcbi.1013597.ref057","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.jneumeth.2010.11.020","article-title":"Time-resolved and time-scale adaptive measures of spike train synchrony","volume":"195","author":"T Kreuz","year":"2011","journal-title":"J Neurosci 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Neurophysiol"},{"issue":"4","key":"pcbi.1013597.ref061","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1162\/089976601300014321","article-title":"A novel spike distance","volume":"13","author":"MC van Rossum","year":"2001","journal-title":"Neural Comput"},{"key":"pcbi.1013597.ref062","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.jneumeth.2006.02.023","article-title":"Measuring spike pattern reliability with the Lempel-Ziv-distance","volume":"156","author":"M Christen","year":"2006","journal-title":"J Neurosci Methods"},{"key":"pcbi.1013597.ref063","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/S0925-2312(02)00838-X","article-title":"A new correlation-based measure of spike timing reliability","author":"S Schreiber","year":"2003","journal-title":"Neurocomputing (Amst)"},{"issue":"21","key":"pcbi.1013597.ref064","doi-asserted-by":"crossref","first-page":"3997","DOI":"10.1002\/sim.2946","article-title":"A binless correlation measure reduces 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Neurophysiol"},{"issue":"12","key":"pcbi.1013597.ref071","doi-asserted-by":"crossref","first-page":"2823","DOI":"10.1162\/089976603322518759","article-title":"Differences in spiking patterns among cortical neurons","volume":"15","author":"S Shinomoto","year":"2003","journal-title":"Neural Comput"},{"issue":"7","key":"pcbi.1013597.ref072","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1000433","article-title":"Relating neuronal firing patterns to functional differentiation of cerebral cortex","volume":"5","author":"S Shinomoto","year":"2009","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"pcbi.1013597.ref073","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1152\/jn.01030.2005","article-title":"Measurement of time-dependent changes in the irregularity of neural spiking","volume":"96","author":"RM Davies","year":"2006","journal-title":"J Neurophysiol"},{"key":"pcbi.1013597.ref074","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1113\/jphysiol.2003.053264","article-title":"Measuring spike coding in the rat supraoptic nucleus","volume":"555","author":"GS Bhumbra","year":"2004","journal-title":"J Physiol"},{"issue":"10","key":"pcbi.1013597.ref075","doi-asserted-by":"crossref","first-page":"2359","DOI":"10.1162\/neco.2006.18.10.2359","article-title":"Estimating spiking irregularities under changing environments","volume":"18","author":"K Miura","year":"2006","journal-title":"Neural Comput"},{"key":"pcbi.1013597.ref076","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1007\/BF01009349","article-title":"Statistical macrodynamics of large dynamical systems. Case of a phase transition in oscillator communities","volume":"49","author":"Y Kuramoto","year":"1987","journal-title":"J Stat Phys"},{"key":"pcbi.1013597.ref077","doi-asserted-by":"crossref","unstructured":"Brockwell PJ, Davis RA. Time series: Theory and methods. Springer New York; 1991. https:\/\/doi.org\/10.1007\/978-1-4419-0320-4","DOI":"10.1007\/978-1-4419-0320-4"},{"issue":"4","key":"pcbi.1013597.ref078","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/nn1036","article-title":"Single auditory neurons rapidly discriminate conspecific communication signals","volume":"6","author":"CK Machens","year":"2003","journal-title":"Nat Neurosci"},{"issue":"1","key":"pcbi.1013597.ref079","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1152\/jn.01257.2005","article-title":"Distinct time scales in cortical discrimination of natural sounds in songbirds","volume":"96","author":"R Narayan","year":"2006","journal-title":"J Neurophysiol"},{"issue":"3","key":"pcbi.1013597.ref080","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.tins.2009.12.001","article-title":"Sensory neural codes using multiplexed temporal scales","volume":"33","author":"S Panzeri","year":"2010","journal-title":"Trends Neurosci"},{"issue":"11","key":"pcbi.1013597.ref081","article-title":"Rate, not selectivity, determines neuronal population coding accuracy in auditory cortex","volume":"15","author":"W Sun","year":"2017","journal-title":"PLoS Biol"},{"issue":"7665","key":"pcbi.1013597.ref082","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/nature23020","article-title":"Distinct timescales of population coding across cortex","volume":"548","author":"CA Runyan","year":"2017","journal-title":"Nature"},{"key":"pcbi.1013597.ref083","article-title":"Coordinated neuronal ensembles in primary auditory cortical columns","volume":"7","author":"JZ See","year":"2018","journal-title":"Elife"},{"key":"pcbi.1013597.ref084","article-title":"High-density extracellular recordings from the primary auditory cortex in anesthetized rats listening to dynamic broadband stimuli","author":"JZ See","year":"2018","journal-title":"CRCNS.org"},{"issue":"1","key":"pcbi.1013597.ref085","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1038\/s41597-022-01244-2","article-title":"Calcium Imaging and electrophysiology of hippocampal activity under anesthesia and natural sleep in mice","volume":"9","author":"A Formozov","year":"2022","journal-title":"Sci Data"},{"key":"pcbi.1013597.ref086","article-title":"Calcium imaging and electrophysiology of hippocampal activity under anesthesia and natural sleep in mice","author":"A Formozov","year":"2022","journal-title":"G-Node"},{"issue":"48","key":"pcbi.1013597.ref087","doi-asserted-by":"crossref","first-page":"12591","DOI":"10.1523\/JNEUROSCI.2929-08.2008","article-title":"Spatial and temporal scales of neuronal correlation in primary visual cortex","volume":"28","author":"MA Smith","year":"2008","journal-title":"J Neurosci"},{"key":"pcbi.1013597.ref088","unstructured":"Kohn A, Smith MA. Utah array extracellular recordings of spontaneous and visually evoked activity from anesthetized macaque primary visual cortex (V1). CRCNS.org. https:\/\/crcns.org\/data-sets\/v1\/utah-array-extracellular-recordings. 2016."},{"issue":"3","key":"pcbi.1013597.ref089","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1097\/00001756-199303000-00004","article-title":"High frequency (60-90 Hz) oscillations in primary visual cortex of awake monkey","volume":"4","author":"R Eckhorn","year":"1993","journal-title":"Neuroreport"},{"issue":"6689","key":"pcbi.1013597.ref090","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/28179","article-title":"Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro","volume":"394","author":"A Fisahn","year":"1998","journal-title":"Nature"},{"issue":"8","key":"pcbi.1013597.ref091","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1038\/nn1292","article-title":"Multiplexing using synchrony in the zebrafish olfactory bulb","volume":"7","author":"RW Friedrich","year":"2004","journal-title":"Nat Neurosci"},{"key":"pcbi.1013597.ref092","doi-asserted-by":"crossref","first-page":"5177","DOI":"10.1113\/jphysiol.2009.178384","article-title":"Flexible spike timing of layer 5 neurons during dynamic beta oscillation shifts in rat prefrontal cortex","volume":"587","author":"KI van Aerde","year":"2009","journal-title":"J Physiol"},{"issue":"1","key":"pcbi.1013597.ref093","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0085109","article-title":"Spike firing and IPSPs in layer V pyramidal neurons during beta oscillations in rat primary motor cortex (M1) in vitro","volume":"9","author":"MG Lacey","year":"2014","journal-title":"PLoS One"},{"issue":"4","key":"pcbi.1013597.ref094","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.3001146","article-title":"Anesthetics fragment hippocampal network activity, alter spine dynamics, and affect memory consolidation","volume":"19","author":"W Yang","year":"2021","journal-title":"PLoS Biol"},{"issue":"1","key":"pcbi.1013597.ref095","doi-asserted-by":"crossref","first-page":"12140","DOI":"10.1038\/s41598-017-11873-y","article-title":"Estimating the intrinsic dimension of datasets by a minimal neighborhood information","volume":"7","author":"E Facco","year":"2017","journal-title":"Sci Rep"},{"issue":"1","key":"pcbi.1013597.ref096","doi-asserted-by":"crossref","first-page":"20005","DOI":"10.1038\/s41598-022-20991-1","article-title":"The generalized ratios intrinsic dimension estimator","volume":"12","author":"F Denti","year":"2022","journal-title":"Sci Rep"},{"issue":"10","key":"pcbi.1013597.ref097","doi-asserted-by":"crossref","first-page":"100589","DOI":"10.1016\/j.patter.2022.100589","article-title":"DADApy: Distance-based analysis of data-manifolds in Python","volume":"3","author":"A Glielmo","year":"2022","journal-title":"Patterns (N Y)"},{"key":"pcbi.1013597.ref098","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3389\/fphys.2012.00015","article-title":"Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis","volume":"3","author":"E Tagliazucchi","year":"2012","journal-title":"Front Physiol"},{"issue":"5","key":"pcbi.1013597.ref099","doi-asserted-by":"crossref","first-page":"1457","DOI":"10.1152\/jn.00873.2012","article-title":"Monitoring spike train synchrony","volume":"109","author":"T Kreuz","year":"2013","journal-title":"J Neurophysiol"},{"key":"pcbi.1013597.ref100","doi-asserted-by":"crossref","unstructured":"Pinsky PF, Rinzel J. Synchrony Measures for Biological Neural Networks. Biological Cybernetics. 1995 ;73(2):129\u2013137. https:\/\/doi.org\/10.1007\/BF00204051.","DOI":"10.1007\/s004220050169"},{"issue":"1","key":"pcbi.1013597.ref101","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.physd.2006.09.039","article-title":"Measuring synchronization in coupled model systems: A comparison of different approaches","volume":"225","author":"T Kreuz","year":"2007","journal-title":"Physica D: Nonlinear Phenomena"},{"key":"pcbi.1013597.ref102","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.jneumeth.2018.02.009","article-title":"Which spike train distance is most suitable for distinguishing rate and temporal coding?","volume":"299","author":"E Satuvuori","year":"2018","journal-title":"J Neurosci Methods"},{"issue":"5","key":"pcbi.1013597.ref103","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1162\/neco_a_01277","article-title":"Comparison of different spike train synchrony measures regarding their robustness to erroneous data from bicuculline-induced epileptiform activity","volume":"32","author":"M Ciba","year":"2020","journal-title":"Neural Comput"},{"key":"pcbi.1013597.ref104","doi-asserted-by":"crossref","first-page":"117415","DOI":"10.1016\/j.neuroimage.2020.117415","article-title":"Modulation of cortical slow oscillations and complexity across anesthesia levels","volume":"224","author":"M Dasilva","year":"2021","journal-title":"Neuroimage"},{"issue":"11","key":"pcbi.1013597.ref105","doi-asserted-by":"crossref","first-page":"3529","DOI":"10.1073\/pnas.1410509112","article-title":"Stochastic transitions into silence cause noise correlations in cortical circuits","volume":"112","author":"G Mochol","year":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013597.ref106","doi-asserted-by":"crossref","unstructured":"Meskaldji D-E, Morgenthaler S, Van De Ville D. New measures of brain functional connectivity by temporal analysis of extreme events. In: 2015 IEEE 12th international symposium on biomedical imaging (ISBI); 2015. p. 26\u20139. https:\/\/doi.org\/10.1109\/isbi.2015.7163808","DOI":"10.1109\/ISBI.2015.7163808"},{"issue":"2","key":"pcbi.1013597.ref107","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.tics.2016.12.008","article-title":"Brain oscillations and the importance of waveform shape","volume":"21","author":"SR Cole","year":"2017","journal-title":"Trends Cogn Sci"},{"issue":"1","key":"pcbi.1013597.ref108","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/s41597-020-0553-0","article-title":"A self-organizing, living library of time-series data","volume":"7","author":"BD Fulcher","year":"2020","journal-title":"Sci Data"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1013597","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T00:00:00Z","timestamp":1761782400000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013597","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T17:57:11Z","timestamp":1761847031000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013597"}},"subtitle":[],"editor":[{"given":"Daniel","family":"Bush","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2025,10,24]]},"references-count":108,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,10,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1013597","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,24]]}}}