{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T20:01:09Z","timestamp":1787169669900,"version":"build-2736575974"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1012628","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T00:00:00Z","timestamp":1733961600000}}],"reference-count":78,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2024,12,2]],"date-time":"2024-12-02T00:00:00Z","timestamp":1733097600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100019185","name":"HORIZON EUROPE Global Challenges and European Industrial Competitiveness","doi-asserted-by":"publisher","award":["101071178"],"award-info":[{"award-number":["101071178"]}],"id":[{"id":"10.13039\/100019185","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Theta-band oscillations (3\u20138 Hz) in the mammalian hippocampus organize the temporal structure of cortical inputs, resulting in a phase code that enables rhythmic input sampling for episodic memory formation and spatial navigation. However, it remains unclear what evolutionary pressures might have driven the selection of theta over higher-frequency bands that could potentially provide increased input sampling resolution. Here, we address this question by introducing a theoretical framework that combines the efficient coding and neural oscillatory sampling hypotheses, focusing on the information rate (bits\/s) of phase coding neurons. We demonstrate that physiologically realistic noise levels create a trade-off between the speed of input sampling, determined by oscillation frequency, and encoding precision in rodent hippocampal neurons. This speed-precision trade-off results in a maximum information rate of \u223c1\u20132 bits\/s within the theta frequency band, thus confining the optimal oscillation frequency to the low end of the spectrum. We also show that this framework accounts for key hippocampal features, such as the preservation of the theta band along the dorsoventral axis despite physiological gradients, and the modulation of theta frequency and amplitude by running speed. Extending the analysis beyond the hippocampus, we propose that theta oscillations could also support efficient stimulus encoding in the visual cortex and olfactory bulb. More broadly, our framework lays the foundation for studying how system features, such as noise, constrain the optimal sampling frequencies in both biological and artificial brains.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1012628","type":"journal-article","created":{"date-parts":[[2024,12,2]],"date-time":"2024-12-02T14:03:31Z","timestamp":1733148211000},"page":"e1012628","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":11,"title":["Theta oscillations optimize a speed-precision trade-off in phase coding neurons"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7164-4597","authenticated-orcid":true,"given":"Adri\u00e1n F.","family":"Amil","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Albert","family":"Albesa-Gonz\u00e1lez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul F. M. J.","family":"Verschure","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,12,2]]},"reference":[{"issue":"1","key":"pcbi.1012628.ref001","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/0014-4886(76)90055-8","article-title":"Place units in the hippocampus of the freely moving rat","volume":"51","author":"J O\u2019Keefe","year":"1976","journal-title":"Experimental neurology"},{"issue":"3","key":"pcbi.1012628.ref002","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1002\/hipo.450030307","article-title":"Phase relationship between hippocampal place units and the EEG theta rhythm","volume":"3","author":"J O\u2019Keefe","year":"1993","journal-title":"Hippocampus"},{"issue":"5","key":"pcbi.1012628.ref003","doi-asserted-by":"crossref","first-page":"2602","DOI":"10.1152\/jn.2000.83.5.2602","article-title":"Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding","volume":"83","author":"O Jensen","year":"2000","journal-title":"Journal of neurophysiology"},{"issue":"7","key":"pcbi.1012628.ref004","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1002\/hipo.20121","article-title":"The theta\/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme","volume":"15","author":"J Lisman","year":"2005","journal-title":"Hippocampus"},{"issue":"6890","key":"pcbi.1012628.ref005","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/nature00807","article-title":"Role of experience and oscillations in transforming a rate code into a temporal code","volume":"417","author":"M Mehta","year":"2002","journal-title":"Nature"},{"issue":"4","key":"pcbi.1012628.ref006","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1113\/jphysiol.2008.164111","article-title":"Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information","volume":"587","author":"D McLelland","year":"2009","journal-title":"The Journal of physiology"},{"issue":"6682","key":"pcbi.1012628.ref007","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1126\/science.adk2456","article-title":"Local activation of CA1 pyramidal cells induces theta-phase precession","volume":"383","author":"HE Sloin","year":"2024","journal-title":"Science"},{"key":"pcbi.1012628.ref008","first-page":"2023","article-title":"Hippocampal Theta Phase Precession Supports Memory Formation and Retrieval of Naturalistic Experience in Humans","author":"J Zheng","year":"2023","journal-title":"bioRxiv"},{"issue":"2","key":"pcbi.1012628.ref009","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1113\/jphysiol.2002.031245","article-title":"Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system","volume":"546","author":"TW Margrie","year":"2003","journal-title":"The Journal of physiology"},{"issue":"11","key":"pcbi.1012628.ref010","doi-asserted-by":"crossref","first-page":"e1002211","DOI":"10.1371\/journal.pcbi.1002211","article-title":"Neural dynamics as sampling: a model for stochastic computation in recurrent networks of spiking neurons","volume":"7","author":"L Buesing","year":"2011","journal-title":"PLoS computational biology"},{"issue":"2","key":"pcbi.1012628.ref011","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1038\/nn.2727","article-title":"Ephaptic coupling of cortical neurons","volume":"14","author":"CA Anastassiou","year":"2011","journal-title":"Nature neuroscience"},{"issue":"2","key":"pcbi.1012628.ref012","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.neuron.2009.08.037","article-title":"Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop","volume":"64","author":"K Mizuseki","year":"2009","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1012628.ref013","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.neuron.2015.09.034","article-title":"Rhythms for cognition: communication through coherence","volume":"88","author":"P Fries","year":"2015","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1012628.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.tins.2004.10.010","article-title":"Spike times make sense","volume":"28","author":"R VanRullen","year":"2005","journal-title":"Trends in neurosciences"},{"issue":"10","key":"pcbi.1012628.ref015","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1016\/j.tics.2016.07.006","article-title":"Perceptual cycles","volume":"20","author":"R VanRullen","year":"2016","journal-title":"Trends in cognitive sciences"},{"issue":"3","key":"pcbi.1012628.ref016","doi-asserted-by":"crossref","first-page":"e1009753","DOI":"10.1371\/journal.pcbi.1009753","article-title":"Cortical oscillations support sampling-based computations in spiking neural networks","volume":"18","author":"A Korcsak-Gorzo","year":"2022","journal-title":"PLoS computational biology"},{"key":"pcbi.1012628.ref017","article-title":"Rhythmic information sampling in the brain during visual recognition","author":"L Caplette","year":"2022","journal-title":"bioRxiv"},{"key":"pcbi.1012628.ref018","article-title":"Discrete sampling in perception via neuronal oscillations\u2014Evidence from rhythmic, non-invasive brain stimulation","author":"FH Kasten","year":"2020","journal-title":"European Journal of Neuroscience"},{"issue":"7373","key":"pcbi.1012628.ref019","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1038\/nature10521","article-title":"Perception of sniff phase in mouse olfaction","volume":"479","author":"M Smear","year":"2011","journal-title":"Nature"},{"issue":"2","key":"pcbi.1012628.ref020","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1093\/chemse\/bjj016","article-title":"The sniff as a unit of olfactory processing","volume":"31","author":"A Kepecs","year":"2006","journal-title":"Chemical senses"},{"issue":"01","key":"pcbi.1012628.ref021","article-title":"Possible principles underlying the transformation of sensory messages","volume":"1","author":"HB Barlow","year":"1961","journal-title":"Sensory communication"},{"issue":"3","key":"pcbi.1012628.ref022","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1016\/j.neuron.2013.10.002","article-title":"Scaling brain size, keeping timing: evolutionary preservation of brain rhythms","volume":"80","author":"G Buzs\u00e1ki","year":"2013","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1012628.ref023","doi-asserted-by":"crossref","first-page":"4839","DOI":"10.1038\/s41467-021-25150-0","article-title":"Theta-phase dependent neuronal coding during sequence learning in human single neurons","volume":"12","author":"L Reddy","year":"2021","journal-title":"Nature communications"},{"issue":"5","key":"pcbi.1012628.ref024","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.cub.2008.02.023","article-title":"Phase-of-firing coding of natural visual stimuli in primary visual cortex","volume":"18","author":"MA Montemurro","year":"2008","journal-title":"Current biology"},{"issue":"4","key":"pcbi.1012628.ref025","doi-asserted-by":"crossref","first-page":"1119","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":"2","key":"pcbi.1012628.ref026","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/s00422-006-0082-8","article-title":"A review of the integrate-and-fire neuron model: II. Inhomogeneous synaptic input and network properties","volume":"95","author":"AN Burkitt","year":"2006","journal-title":"Biological cybernetics"},{"issue":"2","key":"pcbi.1012628.ref027","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s10827-006-8527-6","article-title":"The parameters of the stochastic leaky integrate-and-fire neuronal model","volume":"21","author":"P Lansky","year":"2006","journal-title":"Journal of Computational Neuroscience"},{"issue":"10","key":"pcbi.1012628.ref028","doi-asserted-by":"crossref","first-page":"2186","DOI":"10.1103\/PhysRevLett.86.2186","article-title":"Effects of synaptic noise and filtering on the frequency response of spiking neurons","volume":"86","author":"N Brunel","year":"2001","journal-title":"Physical Review Letters"},{"issue":"12","key":"pcbi.1012628.ref029","doi-asserted-by":"crossref","first-page":"1782","DOI":"10.1109\/TCSI.2002.805707","article-title":"Phase noise and timing jitter in oscillators with colored-noise sources","volume":"49","author":"A Demir","year":"2002","journal-title":"IEEE Transactions on Circuits and Systems I: Fundamental Theory and Applications"},{"key":"pcbi.1012628.ref030","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s10827-015-0560-x","article-title":"Statistical structure of neural spiking under non-Poissonian or other non-white stimulation","volume":"39","author":"T Schwalger","year":"2015","journal-title":"Journal of computational neuroscience"},{"issue":"6695","key":"pcbi.1012628.ref031","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1038\/29528","article-title":"Signal-dependent noise determines motor planning","volume":"394","author":"CM Harris","year":"1998","journal-title":"Nature"},{"issue":"3","key":"pcbi.1012628.ref032","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1152\/jn.2002.88.3.1533","article-title":"Sources of signal-dependent noise during isometric force production","volume":"88","author":"KE Jones","year":"2002","journal-title":"Journal of neurophysiology"},{"key":"pcbi.1012628.ref033","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1007\/s10827-018-0682-z","article-title":"Spike timing precision of neuronal circuits","volume":"44","author":"D Kilinc","year":"2018","journal-title":"Journal of computational neuroscience"},{"key":"pcbi.1012628.ref034","volume-title":"Analysis and simulation of noise in nonlinear electronic circuits and systems","author":"A Demir","year":"2012"},{"key":"pcbi.1012628.ref035","unstructured":"Lahiri S, Sohl-Dickstein J, Ganguli S. A universal tradeoff between power, precision and speed in physical communication. arXiv preprint arXiv:160307758. 2016;."},{"issue":"4","key":"pcbi.1012628.ref036","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1038\/s41593-018-0118-0","article-title":"CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus","volume":"21","author":"I Soltesz","year":"2018","journal-title":"Nature neuroscience"},{"issue":"1","key":"pcbi.1012628.ref037","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1749-6632.2000.tb06716.x","article-title":"Anatomical organization of the parahippocampal-hippocampal network","volume":"911","author":"MP Witter","year":"2000","journal-title":"Annals of the New York Academy of Sciences"},{"issue":"3","key":"pcbi.1012628.ref038","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/hipo.22526","article-title":"Mapping the electrophysiological and morphological properties of CA 1 pyramidal neurons along the longitudinal hippocampal axis","volume":"26","author":"R Malik","year":"2016","journal-title":"Hippocampus"},{"issue":"3","key":"pcbi.1012628.ref039","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1016\/j.neuron.2012.07.015","article-title":"Traveling theta waves along the entire septotemporal axis of the hippocampus","volume":"75","author":"J Patel","year":"2012","journal-title":"Neuron"},{"issue":"22","key":"pcbi.1012628.ref040","doi-asserted-by":"crossref","first-page":"5707","DOI":"10.1113\/jphysiol.2012.242693","article-title":"Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus","volume":"590","author":"KA Dougherty","year":"2012","journal-title":"The Journal of physiology"},{"issue":"6","key":"pcbi.1012628.ref041","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1002\/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7","article-title":"Functional differentiation in the hippocampus","volume":"8","author":"MB Moser","year":"1998","journal-title":"Hippocampus"},{"key":"pcbi.1012628.ref042","article-title":"Theta oscillations in the human hippocampus normalize the information content of episodic memory","author":"D Pata","year":"2022","journal-title":"bioRxiv"},{"key":"pcbi.1012628.ref043","article-title":"Speed modulation of hippocampal theta frequency and power predicts water maze learning","author":"CK Young","year":"2020","journal-title":"BioRxiv"},{"issue":"1-2","key":"pcbi.1012628.ref044","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/S0006-8993(98)00390-4","article-title":"The frequency of rat\u2019s hippocampal theta rhythm is related to the speed of locomotion","volume":"796","author":"U S\u0142awi\u0144ska","year":"1998","journal-title":"Brain research"},{"issue":"1","key":"pcbi.1012628.ref045","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1037\/h0076177","article-title":"Relationship between hippocampal theta activity and running speed in the rat","volume":"88","author":"WL McFarland","year":"1975","journal-title":"Journal of comparative and physiological psychology"},{"issue":"1","key":"pcbi.1012628.ref046","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-020-15670-6","article-title":"Functionally distinct high and low theta oscillations in the human hippocampus","volume":"11","author":"A Goyal","year":"2020","journal-title":"Nature communications"},{"issue":"21","key":"pcbi.1012628.ref047","doi-asserted-by":"crossref","first-page":"4326","DOI":"10.1523\/JNEUROSCI.0987-21.2022","article-title":"A direct comparison of theta power and frequency to speed and acceleration","volume":"42","author":"JP Kennedy","year":"2022","journal-title":"Journal of Neuroscience"},{"issue":"19","key":"pcbi.1012628.ref048","doi-asserted-by":"crossref","first-page":"8149","DOI":"10.1073\/pnas.0610121104","article-title":"Hippocampal place cell assemblies are speed-controlled oscillators","volume":"104","author":"C Geisler","year":"2007","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1012628.ref049","first-page":"37","article-title":"Theta variation and spatiotemporal scaling along the septotemporal axis of the hippocampus","volume":"9","author":"LL Long","year":"2015","journal-title":"Frontiers in systems neuroscience"},{"issue":"19","key":"pcbi.1012628.ref050","doi-asserted-by":"crossref","first-page":"3811","DOI":"10.1016\/j.cub.2020.07.006","article-title":"Mouse visual cortex is modulated by distance traveled and by theta oscillations","volume":"30","author":"J Fournier","year":"2020","journal-title":"Current Biology"},{"issue":"43","key":"pcbi.1012628.ref051","doi-asserted-by":"crossref","first-page":"10408","DOI":"10.1523\/JNEUROSCI.0923-17.2017","article-title":"The timing of reward-seeking action tracks visually cued theta oscillations in primary visual cortex","volume":"37","author":"JM Levy","year":"2017","journal-title":"Journal of Neuroscience"},{"issue":"8","key":"pcbi.1012628.ref052","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2020.108415","article-title":"Somatostatin neurons govern theta oscillations induced by salient visual signals","volume":"33","author":"P Huang","year":"2020","journal-title":"Cell Reports"},{"issue":"1","key":"pcbi.1012628.ref053","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.neuron.2004.12.025","article-title":"Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex","volume":"45","author":"H Lee","year":"2005","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1012628.ref054","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.cub.2020.10.091","article-title":"Theta, but not gamma oscillations in area V4 depend on input from primary visual cortex","volume":"31","author":"R Kienitz","year":"2021","journal-title":"Current Biology"},{"issue":"24","key":"pcbi.1012628.ref055","doi-asserted-by":"crossref","first-page":"E5614","DOI":"10.1073\/pnas.1719433115","article-title":"A theta rhythm in macaque visual cortex and its attentional modulation","volume":"115","author":"G Spyropoulos","year":"2018","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1012628.ref056","doi-asserted-by":"crossref","first-page":"e52583","DOI":"10.7554\/eLife.52583","article-title":"Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb","volume":"9","author":"J Losacco","year":"2020","journal-title":"elife"},{"issue":"9","key":"pcbi.1012628.ref057","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1038\/nn.3760","article-title":"Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb","volume":"17","author":"I Fukunaga","year":"2014","journal-title":"Nature neuroscience"},{"issue":"1","key":"pcbi.1012628.ref058","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1038\/s41467-017-02717-4","article-title":"Generalized leaky integrate-and-fire models classify multiple neuron types","volume":"9","author":"C Teeter","year":"2018","journal-title":"Nature communications"},{"key":"pcbi.1012628.ref059","unstructured":"Zheng J, Meister M. The Unbearable Slowness of Being. arXiv preprint arXiv:240810234. 2024;."},{"issue":"5885","key":"pcbi.1012628.ref060","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1126\/science.1157086","article-title":"Finite scale of spatial representation in the hippocampus","volume":"321","author":"KB Kjelstrup","year":"2008","journal-title":"Science"},{"issue":"12","key":"pcbi.1012628.ref061","doi-asserted-by":"crossref","first-page":"2743","DOI":"10.1162\/089976601317098510","article-title":"Information transfer between rhythmically coupled networks: reading the hippocampal phase code","volume":"13","author":"O Jensen","year":"2001","journal-title":"Neural computation"},{"issue":"2","key":"pcbi.1012628.ref062","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/0013-4694(62)90030-5","article-title":"The significance of the rabbit\u2019s septum as a relay station between the midbrain and the hippocampus I. The control of hippocampus arousal activity by the septum cells","volume":"14","author":"H Petsche","year":"1962","journal-title":"Electroencephalography and clinical neurophysiology"},{"issue":"3","key":"pcbi.1012628.ref063","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S0896-6273(02)00586-X","article-title":"Theta oscillations in the hippocampus","volume":"33","author":"G Buzs\u00e1ki","year":"2002","journal-title":"Neuron"},{"issue":"3-4","key":"pcbi.1012628.ref064","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.jphysparis.2011.09.007","article-title":"Neural circuits underlying the generation of theta oscillations","volume":"106","author":"M Pignatelli","year":"2012","journal-title":"Journal of Physiology-Paris"},{"issue":"5","key":"pcbi.1012628.ref065","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1016\/j.neuron.2015.05.001","article-title":"Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit","volume":"86","author":"F Fuhrmann","year":"2015","journal-title":"Neuron"},{"key":"pcbi.1012628.ref066","doi-asserted-by":"crossref","first-page":"67","DOI":"10.3389\/fnsys.2017.00067","article-title":"Speed and oscillations: medial septum integration of attention and navigation","volume":"11","author":"M Tsanov","year":"2017","journal-title":"Frontiers in systems neuroscience"},{"issue":"4","key":"pcbi.1012628.ref067","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1016\/j.neuron.2020.05.023","article-title":"Cooling of medial septum reveals theta phase lag coordination of hippocampal cell assemblies","volume":"107","author":"PC Petersen","year":"2020","journal-title":"Neuron"},{"issue":"10","key":"pcbi.1012628.ref068","doi-asserted-by":"crossref","first-page":"e2021238118","DOI":"10.1073\/pnas.2021238118","article-title":"Volitional learning promotes theta phase coding in the human hippocampus","volume":"118","author":"D Pacheco Estefan","year":"2021","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1012628.ref069","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/0014-4886(75)90195-8","article-title":"Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital","volume":"49","author":"R Kramis","year":"1975","journal-title":"Experimental neurology"},{"key":"pcbi.1012628.ref070","article-title":"Training spiking neural networks using lessons from deep learning","author":"JK Eshraghian","year":"2023","journal-title":"Proceedings of the IEEE"},{"issue":"6","key":"pcbi.1012628.ref071","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1109\/MSP.2019.2931595","article-title":"Surrogate gradient learning in spiking neural networks: Bringing the power of gradient-based optimization to spiking neural networks","volume":"36","author":"EO Neftci","year":"2019","journal-title":"IEEE Signal Processing Magazine"},{"key":"pcbi.1012628.ref072","unstructured":"Zhu RJ, Zhao Q, Li G, Eshraghian JK. Spikegpt: Generative pre-trained language model with spiking neural networks. arXiv preprint arXiv:230213939. 2023;."},{"key":"pcbi.1012628.ref073","unstructured":"Zhu RJ, Wang Z, Gilpin L, Eshraghian JK. Autonomous Driving with Spiking Neural Networks. arXiv preprint arXiv:240519687. 2024;."},{"key":"pcbi.1012628.ref074","unstructured":"Bybee C, Frady EP, Sommer FT. Deep learning in spiking phasor neural networks. arXiv preprint arXiv:220400507. 2022;."},{"issue":"1","key":"pcbi.1012628.ref075","doi-asserted-by":"crossref","first-page":"014004","DOI":"10.1088\/2634-4386\/ad2373","article-title":"Exploiting deep learning accelerators for neuromorphic workloads","volume":"4","author":"PSV Sun","year":"2024","journal-title":"Neuromorphic Computing and Engineering"},{"key":"pcbi.1012628.ref076","first-page":"2023","article-title":"Oscillations in an Artificial Neural Network Convert Competing Inputs into a Temporal Code","author":"K Duecker","year":"2023","journal-title":"bioRxiv"},{"issue":"2","key":"pcbi.1012628.ref077","doi-asserted-by":"crossref","first-page":"e1011852","DOI":"10.1371\/journal.pcbi.1011852","article-title":"Trained recurrent neural networks develop phase-locked limit cycles in a working memory task","volume":"20","author":"M Pals","year":"2024","journal-title":"PLOS Computational Biology"},{"issue":"6960","key":"pcbi.1012628.ref078","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1038\/nature02058","article-title":"Independent rate and temporal coding in hippocampal pyramidal cells","volume":"425","author":"J Huxter","year":"2003","journal-title":"Nature"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1012628","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T00:00:00Z","timestamp":1733961600000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012628","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T13:55:40Z","timestamp":1734011740000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1012628"}},"subtitle":[],"editor":[{"given":"Daniel","family":"Bush","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,12,2]]},"references-count":78,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12,2]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1012628","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.12.08.519523","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,2]]}}}