{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T19:27:26Z","timestamp":1772306846922,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010256","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,7,15]],"date-time":"2022-07-15T00:00:00Z","timestamp":1657843200000}}],"reference-count":79,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T00:00:00Z","timestamp":1656979200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Stimulus presentation is believed to quench neural response variability as measured by fano-factor (FF). However, the relative contributions of within-trial spike irregularity and trial-to-trial rate variability to FF fluctuations have remained elusive. Here, we introduce a principled approach for accurate estimation of spiking irregularity and rate variability in time for doubly stochastic point processes. Consistent with previous evidence, analysis showed stimulus-induced reduction in rate variability across multiple cortical and subcortical areas. However, unlike what was previously thought, spiking irregularity, was not constant in time but could be enhanced due to factors such as bursting abating the quench in the post-stimulus FF. Simulations confirmed plausibility of a time varying spiking irregularity arising from within and between pool correlations of excitatory and inhibitory neural inputs. By accurate parsing of neural variability, our approach reveals previously unnoticed changes in neural response variability and constrains candidate mechanisms that give rise to observed rate variability and spiking irregularity within brain regions.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010256","type":"journal-article","created":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T14:18:57Z","timestamp":1657030737000},"page":"e1010256","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":16,"title":["Stimulus presentation can enhance spiking irregularity across subcortical and cortical regions"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5621-6199","authenticated-orcid":true,"given":"Saleh","family":"Fayaz","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7741-8689","authenticated-orcid":true,"given":"Mohammad Amin","family":"Fakharian","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3508-776X","authenticated-orcid":true,"given":"Ali","family":"Ghazizadeh","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,7,5]]},"reference":[{"key":"pcbi.1010256.ref001","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1038\/nn.3711","article-title":"Partitioning neuronal variability","volume":"17","author":"RLT Goris","year":"2014","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref002","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.1038\/nn.3247","article-title":"Two layers of neural variability","volume":"15","author":"MM Churchland","year":"2012","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref003","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1038\/nn.2501","article-title":"Stimulus onset quenches neural variability: A widespread cortical phenomenon","volume":"13","author":"MM Churchland","year":"2010","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref004","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1016\/j.neuron.2010.12.037","article-title":"Variance as a Signature of Neural Computations during Decision Making","volume":"69","author":"AK Churchland","year":"2011","journal-title":"Neuron"},{"key":"pcbi.1010256.ref005","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.1010256.ref006","doi-asserted-by":"crossref","first-page":"3697","DOI":"10.1523\/JNEUROSCI.3762-05.2006","article-title":"Neural variability in premotor cortex provides a signature of motor preparation","volume":"26","author":"MM Churchland","year":"2006","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref007","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1002395","article-title":"Neural network mechanisms underlying stimulus driven variability reduction","volume":"8","author":"G Deco","year":"2012","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010256.ref008","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1000106","article-title":"Increased brain signal variability accompanies lower behavioral variability in development","volume":"4","author":"AR McIntosh","year":"2008","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010256.ref009","doi-asserted-by":"crossref","first-page":"2667","DOI":"10.1152\/jn.00648.2010","article-title":"Brain noise is task dependent and region specific","volume":"104","author":"B Mi\u0161i\u0107","year":"2010","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref010","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1006527","article-title":"State dependence of stimulus-induced variability tuning in macaque MT","volume":"14","author":"JA Lombardo","year":"2018","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010256.ref011","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuron.2021.01.023","article-title":"Behavior needs neural variability","volume":"109","author":"L Waschke","year":"2021","journal-title":"Neuron"},{"key":"pcbi.1010256.ref012","doi-asserted-by":"crossref","first-page":"13257","DOI":"10.1523\/JNEUROSCI.2332-14.2015","article-title":"Age-related changes in 1\/f neural electrophysiological noise","volume":"35","author":"B Voytek","year":"2015","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref013","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.37102","article-title":"Cerebellar purkinje cells control eye movements with a rapid rate code that is invariant to spike irregularity","volume":"8","author":"HL Payne","year":"2019","journal-title":"Elife"},{"key":"pcbi.1010256.ref014","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1016\/j.neuron.2009.09.013","article-title":"Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4","volume":"63","author":"JF Mitchell","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1010256.ref015","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1523\/JNEUROSCI.4994-13.2015","article-title":"Cortical state determines global variability and correlations in visual cortex","volume":"35","author":"ML Sch\u00f6lvinck","year":"2015","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref016","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.neuron.2007.06.018","article-title":"Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4","volume":"55","author":"JF Mitchell","year":"2007","journal-title":"Neuron"},{"key":"pcbi.1010256.ref017","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-019-43934-9","article-title":"Thalamus exhibits less sensory variability quenching than cortex","volume":"9","author":"E Poland","year":"2019","journal-title":"Sci Rep"},{"key":"pcbi.1010256.ref018","doi-asserted-by":"crossref","first-page":"13870","DOI":"10.1523\/JNEUROSCI.5441-08.2009","article-title":"Dynamic encoding of movement direction in motor cortical neurons","volume":"29","author":"J Rickert","year":"2009","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref019","doi-asserted-by":"crossref","first-page":"2709","DOI":"10.1162\/NECO_a_00831","article-title":"Separating spike count correlation from firing rate correlation","volume":"28","author":"G Vinci","year":"2016","journal-title":"Neural Comput"},{"key":"pcbi.1010256.ref020","doi-asserted-by":"crossref","DOI":"10.3389\/fncom.2020.569049","article-title":"Fano Factor: A Potentially Useful Information","volume":"14","author":"K Rajdl","year":"2020","journal-title":"Front Comput Neurosci"},{"key":"pcbi.1010256.ref021","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/s00422-016-0690-x","article-title":"The Gamma renewal process as an output of the diffusion leaky integrate-and-fire neuronal model","volume":"110","author":"P Lansky","year":"2016","journal-title":"Biol Cybern"},{"key":"pcbi.1010256.ref022","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.biosystems.2004.09.023","article-title":"A measure of local variation of inter-spike intervals","volume":"79","author":"S Shinomoto","year":"2005","journal-title":"BioSystems"},{"key":"pcbi.1010256.ref023","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.jneumeth.2007.10.013","article-title":"Measurement of variability dynamics in cortical spike trains","volume":"169","author":"MP Nawrot","year":"2008","journal-title":"J Neurosci Methods"},{"key":"pcbi.1010256.ref024","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/s10827-009-0194-y","article-title":"A characterization of the time-rescaled gamma process as a model for spike trains","volume":"29","author":"T Shimokawa","year":"2010","journal-title":"J Comput Neurosci"},{"key":"pcbi.1010256.ref025","doi-asserted-by":"crossref","first-page":"3125","DOI":"10.1162\/NECO_a_00213","article-title":"Optimizing time histograms for non-Poissonian spike trains","volume":"23","author":"T Omi","year":"2011","journal-title":"Neural Comput"},{"key":"pcbi.1010256.ref026","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1152\/jn.00830.2010","article-title":"Interspike interval distributions of spiking neurons driven by fluctuating inputs","volume":"106","author":"S. Ostojic","year":"2011","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref027","doi-asserted-by":"crossref","first-page":"17332","DOI":"10.1523\/JNEUROSCI.6231-11.2012","article-title":"Channel noise from both slow adaptation currents and fast currents is required to explain spike-response variability in a sensory neuron","volume":"32","author":"K Fisch","year":"2012","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref028","doi-asserted-by":"crossref","first-page":"1123","DOI":"10.1162\/NECO_a_00432","article-title":"Impact of spike train autostructure on probability distribution of joint spike events","volume":"25","author":"G Pipa","year":"2013","journal-title":"Neural Comput"},{"key":"pcbi.1010256.ref029","doi-asserted-by":"crossref","first-page":"63","DOI":"10.3934\/mbe.2014.11.63","article-title":"The effect of interspike interval statistics on the information gain under the rate coding hypothesis","volume":"11","author":"S Koyama","year":"2014","journal-title":"Math Biosci Eng"},{"key":"pcbi.1010256.ref030","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1007\/s10827-009-0158-2","article-title":"Comparison of local measures of spike time irregularity and relating variability to firing rate in motor cortical neurons","volume":"29","author":"A Ponce-Alvarez","year":"2010","journal-title":"J Comput Neurosci"},{"key":"pcbi.1010256.ref031","doi-asserted-by":"crossref","first-page":"13802","DOI":"10.1523\/JNEUROSCI.2452-07.2007","article-title":"Balanced excitatory and inhibitory inputs to cortical neurons decouple firing irregularity from rate modulations","volume":"27","author":"K Miura","year":"2007","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref032","unstructured":"Pachitariu M, Brody C, Jun P, Holmes P. Probabilistic models for spike trains of single neurons. Marius Pachitariu. Citeseer. 2015. http:\/\/www.gatsby.ucl.ac.uk\/~marius\/papers\/SpikTrainStats.pdf"},{"key":"pcbi.1010256.ref033","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1152\/jn.1996.75.5.1806","article-title":"Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons","volume":"75","author":"GR Holt","year":"1996","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref034","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1162\/neco.2007.19.6.1503","article-title":"A method for selecting the bin size of a time histogram","volume":"19","author":"H Shimazaki","year":"2007","journal-title":"Neural Comput"},{"key":"pcbi.1010256.ref035","doi-asserted-by":"crossref","first-page":"6820","DOI":"10.1523\/JNEUROSCI.6491-10.2011","article-title":"Roles of Nucleus Accumbens Core and Shell in Incentive-Cue Responding and Behavioral Inhibition","volume":"31","author":"F Ambroggi","year":"2011","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref036","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1016\/j.tins.2008.06.002","article-title":"Reliability, synchrony and noise","volume":"31","author":"GB Ermentrout","year":"2008","journal-title":"Trends Neurosci"},{"key":"pcbi.1010256.ref037","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1038\/s41598-018-33064-z","article-title":"Mathematical Modeling and Analyses of Interspike-Intervals of Spontaneous Activity in Afferent Neurons of the Zebrafish Lateral Line","volume":"8","author":"S Song","year":"2018","journal-title":"Sci Rep"},{"key":"pcbi.1010256.ref038","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1287\/ijoc.1080.0316","article-title":"Transforming renewal processes for simulation of nonstationary arrival processes","volume":"21","author":"I Gerhardt","year":"2009","journal-title":"INFORMS J Comput"},{"key":"pcbi.1010256.ref039","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1016\/S0896-6273(00)80379-7","article-title":"Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration","volume":"19","author":"M H\u00e4usser","year":"1997","journal-title":"Neuron"},{"key":"pcbi.1010256.ref040","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.28132","article-title":"Dynamic modulation of activity in cerebellar nuclei neurons during pavlovian eyeblink conditioning in mice","volume":"6","author":"MM ten Brinke","year":"2017","journal-title":"Elife"},{"key":"pcbi.1010256.ref041","first-page":"1","article-title":"Regular patterns in cerebellar Purkinje cell simple spike trains","volume":"2","author":"SL Shin","year":"2007","journal-title":"PLoS One"},{"key":"pcbi.1010256.ref042","doi-asserted-by":"crossref","first-page":"eabe0693","DOI":"10.1126\/sciadv.abe0693","article-title":"Common coding of expected value and value uncertainty memories in the prefrontal cortex and basal ganglia output","volume":"7","author":"A Ghazizadeh","year":"2021","journal-title":"Sci Adv"},{"key":"pcbi.1010256.ref043","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1016\/j.neuron.2015.07.026","article-title":"Coordinated Neuronal Activity Enhances Corticocortical Communication","volume":"87","author":"A Zandvakili","year":"2015","journal-title":"Neuron"},{"key":"pcbi.1010256.ref044","first-page":"1","article-title":"Prefrontal Cortex Represents Long-Term Memory of Object Values for Months","author":"A Ghazizadeh","year":"2018","journal-title":"Curr Biol"},{"key":"pcbi.1010256.ref045","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1016\/j.neuron.2016.06.028","article-title":"Bottom-Up and Top-Down Input Augment the Variability of Cortical Neurons","volume":"91","author":"C G\u00f3mez-Laberge","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1010256.ref046","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/0959-4388(94)90059-0","article-title":"Noise, neural codes and cortical organization","volume":"4","author":"MN Shadlen","year":"1994","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1010256.ref047","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1523\/JNEUROSCI.13-01-00334.1993","article-title":"The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs","volume":"13","author":"WR Softky","year":"1993","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref048","doi-asserted-by":"crossref","first-page":"11903","DOI":"10.1103\/PhysRevE.82.011903","article-title":"Stimulus-dependent suppression of chaos in recurrent neural networks","volume":"82","author":"K Rajan","year":"2010","journal-title":"Phys Rev E\u2014Stat Nonlinear, Soft Matter Phys"},{"key":"pcbi.1010256.ref049","doi-asserted-by":"crossref","first-page":"6193","DOI":"10.1523\/JNEUROSCI.20-16-06193.2000","article-title":"Impact of correlated synaptic input on output firing rate and variability in simple neuronal models","volume":"20","author":"E Salinas","year":"2000","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref050","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fncir.2014.00012","article-title":"Comparison of the dynamics of neural interactions between current-based and conductance-based integrate-and-fire recurrent networks","volume":"8","author":"S Cavallari","year":"2014","journal-title":"Front Neural Circuits"},{"key":"pcbi.1010256.ref051","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1038\/nn.3220","article-title":"Slow dynamics and high variability in balanced cortical networks with clustered connections","volume":"15","author":"A Litwin-Kumar","year":"2012","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref052","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/nn.4242","article-title":"The mechanics of state-dependent neural correlations","volume":"19","author":"B Doiron","year":"2016","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref053","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1038\/nn.4243","article-title":"Efficient codes and balanced networks","volume":"19","author":"S Den\u00e8ve","year":"2016","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref054","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1038\/nn.2105","article-title":"Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities","volume":"11","author":"M Okun","year":"2008","journal-title":"Nat Neurosci"},{"key":"pcbi.1010256.ref055","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"},{"key":"pcbi.1010256.ref056","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1126\/science.1179850","article-title":"The asynchronous state in cortical circuits","volume":"327","author":"A Renart","year":"2010","journal-title":"Science (80-)"},{"key":"pcbi.1010256.ref057","first-page":"5422","article-title":"Spatial and temporal scales of neuronal correlation in visual area V4","volume":"158","author":"MA Smith","year":"2013","journal-title":"Ann Intern Med"},{"key":"pcbi.1010256.ref058","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/0006-8993(74)90438-7","article-title":"Neuronal variability: non-stationary responses to identical visual stimuli","volume":"79","author":"GJ Tomko","year":"1974","journal-title":"Brain Res"},{"key":"pcbi.1010256.ref059","doi-asserted-by":"crossref","first-page":"e264","DOI":"10.1371\/journal.pbio.0020264","article-title":"Amplification of trial-to-trial response variability by neurons in visual cortex","volume":"2","author":"M. Carandini","year":"2004","journal-title":"PLoS Biol"},{"key":"pcbi.1010256.ref060","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1523\/JNEUROSCI.19-04-01203.1999","article-title":"The photovoltage of macaque cone photoreceptors: Adaptation, noise, and kinetics","volume":"19","author":"DM Schneeweis","year":"1999","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref061","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1038\/nrn3025","article-title":"From the stochasticity of molecular processes to the variability of synaptic transmission","volume":"12","author":"C Ribrault","year":"2011","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1010256.ref062","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1146\/annurev.neuro.051508.135516","article-title":"Synaptic mechanisms for plasticity in neocortex","volume":"32","author":"DE Feldman","year":"2009","journal-title":"Annu Rev Neurosci"},{"key":"pcbi.1010256.ref063","doi-asserted-by":"crossref","first-page":"3125","DOI":"10.1016\/j.visres.2007.08.023","article-title":"Visual adaptation: Neural, psychological and computational aspects","volume":"47","author":"CWG Clifford","year":"2007","journal-title":"Vision Res"},{"key":"pcbi.1010256.ref064","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1146\/annurev-neuro-060909-153238","article-title":"Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement","volume":"34","author":"G. Turrigiano","year":"2011","journal-title":"Annu Rev Neurosci"},{"key":"pcbi.1010256.ref065","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1152\/jn.90592.2008","article-title":"Behavioral states, network states, and sensory response variability","volume":"100","author":"A Fontanini","year":"2008","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref066","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuron.2012.09.010","article-title":"Neuromodulation of Neuronal Circuits: Back to the Future","volume":"76","author":"E. Marder","year":"2012","journal-title":"Neuron"},{"key":"pcbi.1010256.ref067","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fncom.2018.00048","article-title":"Neural coding with bursts\u2014current state and future perspectives","volume":"12","author":"F Zeldenrust","year":"2018","journal-title":"Front Comput Neurosci"},{"key":"pcbi.1010256.ref068","unstructured":"Buzs\u00e1ki G, Llin\u00e1s R, Singer W, Berthoz A, Christen Y. Temporal coding in the brain. Springer Science & Business Media; 2012."},{"key":"pcbi.1010256.ref069","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.conb.2020.03.003","article-title":"Cell assemblies, sequences and temporal coding in the hippocampus","volume":"64","author":"G. Dragoi","year":"2020","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1010256.ref070","doi-asserted-by":"crossref","first-page":"6191","DOI":"10.1523\/JNEUROSCI.19-14-06191.1999","article-title":"Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat","volume":"19","author":"G Dragoi","year":"1999","journal-title":"J Neurosci"},{"key":"pcbi.1010256.ref071","doi-asserted-by":"crossref","first-page":"a021683","DOI":"10.1101\/cshperspect.a021683","article-title":"Motor learning and the cerebellum","volume":"7","author":"CI De Zeeuw","year":"2015","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"pcbi.1010256.ref072","doi-asserted-by":"crossref","unstructured":"Yin TCT. Neural mechanisms of encoding binaural localization cues in the auditory brainstem. Integrative functions in the mammalian auditory pathway. Springer; 2002. pp. 99\u2013159.","DOI":"10.1007\/978-1-4757-3654-0_4"},{"key":"pcbi.1010256.ref073","doi-asserted-by":"crossref","first-page":"1700","DOI":"10.1152\/jn.2001.86.4.1700","article-title":"Excess synchrony in motor cortical neurons provides redundant direction information with that from coarse temporal measures","volume":"86","author":"MW Oram","year":"2001","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref074","doi-asserted-by":"crossref","first-page":"2928","DOI":"10.1152\/jn.00644.2004","article-title":"Trial-to-trial variability and its effect on time-varying dependency between two neurons","volume":"94","author":"V Ventura","year":"2005","journal-title":"J Neurophysiol"},{"key":"pcbi.1010256.ref075","first-page":"8","article-title":"Effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons","volume":"69","author":"MJE Richardson","year":"2004","journal-title":"Phys Rev E\u2014Stat Physics, Plasmas, Fluids, Relat Interdiscip Top"},{"key":"pcbi.1010256.ref076","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.1010256.ref077","unstructured":"Zandvakili A, Kohn A. Simultaneous V1-V2 neuronal population recordings in anesthetized macaque monkeys. 2019. http:\/\/dx.doi.org\/10.6080\/K0B27SHN"},{"key":"pcbi.1010256.ref078","article-title":"Stimulus presentation can enhance spiking irregularity across subcortical and cortical regions\u2014Code and Data","author":"S Fayaz","year":"2022","journal-title":"Dryad, Data"},{"key":"pcbi.1010256.ref079","doi-asserted-by":"crossref","unstructured":"ten Brinke MM, Heiney SA, Wang X, Proietti-Onori M, Boele H-J, Bakermans J, et al. Eyelid behavior and spike activity of cerebellar interpositus nucleus neurons during eyeblink conditioning in awake behaving mice. 2017. http:\/\/dx.doi.org\/10.6080\/K0B85697","DOI":"10.7554\/eLife.28132"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1010256","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,7,15]],"date-time":"2022-07-15T00:00:00Z","timestamp":1657843200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010256","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,15]],"date-time":"2022-07-15T13:40:02Z","timestamp":1657892402000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010256"}},"subtitle":[],"editor":[{"given":"Alireza","family":"Soltani","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,7,5]]},"references-count":79,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7,5]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010256","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.03.27.437321","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,5]]}}}