{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,15]],"date-time":"2026-04-15T01:23:57Z","timestamp":1776216237299,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1013363","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,8,28]],"date-time":"2025-08-28T00:00:00Z","timestamp":1756339200000}}],"reference-count":64,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2025,8,13]],"date-time":"2025-08-13T00:00:00Z","timestamp":1755043200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00c3\u00b3n y Universidades","doi-asserted-by":"publisher","award":["PID2021-128158NB-C22"],"award-info":[{"award-number":["PID2021-128158NB-C22"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00c3\u00b3n y Universidades","doi-asserted-by":"publisher","award":["CEX2021-001164-M"],"award-info":[{"award-number":["CEX2021-001164-M"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00c3\u00b3n y Universidades","doi-asserted-by":"publisher","award":["PID2021-128158NB-C21"],"award-info":[{"award-number":["PID2021-128158NB-C21"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00c3\u00b3n y Universidades","doi-asserted-by":"publisher","award":["CEX2021-001165-S"],"award-info":[{"award-number":["CEX2021-001165-S"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Interactions among brain rhythms play a crucial role in organizing neuronal firing sequences during specific cognitive functions. In memory formation, the coupling between the phase of the theta rhythm and the amplitude of gamma oscillations has been extensively studied in the hippocampus. Prevailing perspectives suggest that the phase of the slower oscillation modulates the fast activity. However, recent metrics, such as Cross-Frequency Directionality (CFD), indicate that these electrophysiological interactions can be bidirectional. Using a computational model, we demonstrate that feedforward inhibition modeled by a theta-modulated ING (Interneuron Network Gamma) mechanism induces fast-to-slow interactions, while feedback inhibition through a theta-modulated PING (Pyramidal Interneuron Network Gamma) model drives slow-to-fast interactions. Importantly, in circuits combining both feedforward and feedback motifs, as commonly found experimentally, directionality is flexibly modulated by synaptic strength within biologically realistic ranges. A signature of this interaction is that fast-to-slow dominance in feedforward motifs is associated with gamma oscillations of higher frequency, and <jats:italic><jats:italic>vice versa<\/jats:italic><\/jats:italic>. Using previously acquired electrophysiological data from the hippocampus of rats freely navigating in a familiar environment or in a novel one, we show that CFD is dynamically regulated and linked to the frequency of the gamma band, as predicted by the model. Finally, the model attributes each theta-gamma interaction scheme, determined by the balance between feedforward and feedback inhibition, to distinct modes of information transmission and integration, adding computational flexibility. Our results offer a plausible neurobiological interpretation for cross-frequency directionality measurements associated with the activation of different underlying motifs that serve distinct computational needs.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1013363","type":"journal-article","created":{"date-parts":[[2025,8,13]],"date-time":"2025-08-13T18:40:21Z","timestamp":1755110421000},"page":"e1013363","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["The role of feedforward and feedback inhibition in modulating theta-gamma cross-frequency interactions in neural circuits"],"prefix":"10.1371","volume":"21","author":[{"given":"Dimitrios","family":"Chalkiadakis","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jaime","family":"S\u00e1nchez-Claros","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8234-7160","authenticated-orcid":true,"given":"V\u00edctor J.","family":"L\u00f3pez-Madrona","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Santiago","family":"Canals","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2980-7038","authenticated-orcid":true,"given":"Claudio R.","family":"Mirasso","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2025,8,13]]},"reference":[{"issue":"5679","key":"pcbi.1013363.ref001","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.1013363.ref002","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/S0165-0173(98)00056-3","article-title":"EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis","volume":"29","author":"W Klimesch","year":"1999","journal-title":"Brain Res Brain Res Rev"},{"key":"pcbi.1013363.ref003","first-page":"4","article-title":"Shifts in Gamma Phase\u2013Amplitude Coupling Frequency from Theta to Alpha over Posterior Cortex during Visual Tasks","author":"B Voytek","year":"2010","journal-title":"Frontiers in Human Neuroscience"},{"issue":"8","key":"pcbi.1013363.ref004","first-page":"692","article-title":"Functional Interactions between Entorhinal Cortical Pathways Modulate Theta Activity in the Hippocampus","volume":"10","author":"VJ L\u00f3pez-Madrona","year":"2021","journal-title":"Biology (Basel)"},{"key":"pcbi.1013363.ref005","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 Res"},{"issue":"3","key":"pcbi.1013363.ref006","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1152\/physrev.00035.2008","article-title":"Neurophysiological and computational principles of cortical rhythms in cognition","volume":"90","author":"X-J Wang","year":"2010","journal-title":"Physiol Rev"},{"issue":"7","key":"pcbi.1013363.ref007","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1016\/j.neuron.2023.02.026","article-title":"Over and above frequency: Gamma oscillations as units of neural circuit operations","volume":"111","author":"A Fernandez-Ruiz","year":"2023","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1013363.ref008","doi-asserted-by":"crossref","first-page":"1849","DOI":"10.1038\/s41467-024-46012-5","article-title":"Gamma oscillatory complexity conveys behavioral information in hippocampal networks","volume":"15","author":"V Douchamps","year":"2024","journal-title":"Nat Commun"},{"issue":"11","key":"pcbi.1013363.ref009","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":"51","key":"pcbi.1013363.ref010","doi-asserted-by":"crossref","first-page":"20517","DOI":"10.1073\/pnas.0810524105","article-title":"Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task","volume":"105","author":"ABL Tort","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"49","key":"pcbi.1013363.ref011","doi-asserted-by":"crossref","first-page":"20942","DOI":"10.1073\/pnas.0911331106","article-title":"Theta-gamma coupling increases during the learning of item-context associations","volume":"106","author":"ABL Tort","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1013363.ref012","article-title":"Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks","volume":"9","author":"VJ L\u00f3pez-Madrona","year":"2020","journal-title":"Elife"},{"issue":"12","key":"pcbi.1013363.ref013","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1016\/j.tics.2016.09.007","article-title":"Oscillatory Dynamics of Prefrontal Cognitive Control","volume":"20","author":"RF Helfrich","year":"2016","journal-title":"Trends in Cognitive Sciences"},{"issue":"1","key":"pcbi.1013363.ref014","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":"6","key":"pcbi.1013363.ref015","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1016\/j.neuron.2013.03.007","article-title":"The theta-gamma neural code","volume":"77","author":"JE Lisman","year":"2013","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1013363.ref016","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1152\/jn.00957.2004","article-title":"Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network","volume":"94","author":"HG Rotstein","year":"2005","journal-title":"J Neurophysiol"},{"issue":"37","key":"pcbi.1013363.ref017","doi-asserted-by":"crossref","first-page":"13295","DOI":"10.1073\/pnas.0506259102","article-title":"Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus","volume":"102","author":"T Gloveli","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"pcbi.1013363.ref018","doi-asserted-by":"crossref","first-page":"2889","DOI":"10.1152\/jn.01233.2005","article-title":"Intrinsic and synaptic mechanisms determining the timing of neuron population activity during hippocampal theta oscillation","volume":"96","author":"G Orb\u00e1n","year":"2006","journal-title":"J Neurophysiol"},{"issue":"33","key":"pcbi.1013363.ref019","doi-asserted-by":"crossref","first-page":"13490","DOI":"10.1073\/pnas.0705708104","article-title":"On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus","volume":"104","author":"ABL Tort","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5","key":"pcbi.1013363.ref020","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1016\/j.neuron.2013.09.033","article-title":"Inhibition-induced theta resonance in cortical circuits","volume":"80","author":"E Stark","year":"2013","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1013363.ref021","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1016\/j.neuron.2014.08.051","article-title":"Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks","volume":"84","author":"EW Schomburg","year":"2014","journal-title":"Neuron"},{"issue":"5","key":"pcbi.1013363.ref022","doi-asserted-by":"crossref","DOI":"10.1016\/j.neuron.2017.02.017","article-title":"Entorhinal-CA3 dual-input control of spike timing in the hippocampus by theta-gamma coupling","volume":"93","author":"A Fern\u00e1ndez-Ruiz","year":"2017","journal-title":"Neuron"},{"issue":"6537","key":"pcbi.1013363.ref023","doi-asserted-by":"crossref","DOI":"10.1126\/science.abf3119","article-title":"Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies","volume":"372","author":"A Fern\u00e1ndez-Ruiz","year":"2021","journal-title":"Science"},{"issue":"1","key":"pcbi.1013363.ref024","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.neuron.2013.09.046","article-title":"Theta-gamma-modulated synaptic currents in hippocampal granule cells in vivo define a mechanism for network oscillations","volume":"81","author":"AJ Pern\u00eda-Andrade","year":"2014","journal-title":"Neuron"},{"issue":"11","key":"pcbi.1013363.ref025","doi-asserted-by":"crossref","first-page":"105457","DOI":"10.1016\/j.isci.2022.105457","article-title":"Theta dominates cross-frequency coupling in hippocampal-medial entorhinal circuit during awake-behavior in rats","volume":"25","author":"Y Zhou","year":"2022","journal-title":"iScience"},{"issue":"5","key":"pcbi.1013363.ref026","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1016\/j.neuron.2014.01.021","article-title":"Layer-specific GABAergic control of distinct gamma oscillations in the CA1 hippocampus","volume":"81","author":"B Laszt\u00f3czi","year":"2014","journal-title":"Neuron"},{"issue":"3","key":"pcbi.1013363.ref027","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1152\/jn.00263.2005","article-title":"An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex","volume":"94","author":"P Lakatos","year":"2005","journal-title":"J Neurophysiol"},{"key":"pcbi.1013363.ref028","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1016\/j.neuroscience.2015.09.054","article-title":"New uses of LFPs: Pathway-specific threads obtained through spatial discrimination","volume":"310","author":"O Herreras","year":"2015","journal-title":"Neuroscience"},{"key":"pcbi.1013363.ref029","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.neuroimage.2015.05.044","article-title":"Measuring directionality between neuronal oscillations of different frequencies","volume":"118","author":"H Jiang","year":"2015","journal-title":"Neuroimage"},{"issue":"45","key":"pcbi.1013363.ref030","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2313304121","article-title":"Differential neural mechanisms underlie cortical gating of visual spatial attention mediated by alpha-band oscillations","volume":"121","author":"X Yang","year":"2024","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"12","key":"pcbi.1013363.ref031","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1005893","article-title":"Non-linear auto-regressive models for cross-frequency coupling in neural time series","volume":"13","author":"T Dupr\u00e9 la Tour","year":"2017","journal-title":"PLoS Comput Biol"},{"issue":"32","key":"pcbi.1013363.ref032","doi-asserted-by":"crossref","first-page":"11733","DOI":"10.1523\/JNEUROSCI.0501-11.2011","article-title":"Ketamine disrupts \u03b8 modulation of \u03b3 in a computer model of hippocampus","volume":"31","author":"SA Neymotin","year":"2011","journal-title":"J Neurosci"},{"issue":"20","key":"pcbi.1013363.ref033","doi-asserted-by":"crossref","first-page":"6402","DOI":"10.1523\/JNEUROSCI.16-20-06402.1996","article-title":"Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model","volume":"16","author":"XJ Wang","year":"1996","journal-title":"J Neurosci"},{"issue":"14","key":"pcbi.1013363.ref034","doi-asserted-by":"crossref","first-page":"8128","DOI":"10.1073\/pnas.100124097","article-title":"Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm","volume":"97","author":"JA White","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"pcbi.1013363.ref035","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1162\/089976603321192059","article-title":"Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity","volume":"15","author":"C B\u00f6rgers","year":"2003","journal-title":"Neural Comput"},{"issue":"3","key":"pcbi.1013363.ref036","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1162\/0899766053019908","article-title":"Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons","volume":"17","author":"C B\u00f6rgers","year":"2005","journal-title":"Neural Comput"},{"issue":"1","key":"pcbi.1013363.ref037","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1146\/annurev-neuro-062111-150444","volume":"35","author":"G Buzs\u00e1ki","year":"2012","journal-title":"Annual Review of Neuroscience"},{"key":"pcbi.1013363.ref038","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-51171-9","volume-title":"An introduction to modeling neuronal dynamics","author":"C B\u00f6rgers","year":"2017"},{"key":"pcbi.1013363.ref039","volume-title":"Neural Dynamics and Information Transmission: From Cortical Circuits to the Hippocampal Modelling [Ph. D. thesis]","author":"J S\u00e1nchez Claros","year":"2024"},{"key":"pcbi.1013363.ref040","doi-asserted-by":"crossref","first-page":"65","DOI":"10.3389\/fncom.2016.00065","article-title":"Computational Modeling of Single Neuron Extracellular Electric Potentials and Network Local Field Potentials using LFPsim","volume":"10","author":"H Parasuram","year":"2016","journal-title":"Front Comput Neurosci"},{"issue":"5961","key":"pcbi.1013363.ref041","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1126\/science.1177876","article-title":"Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons","volume":"327","author":"H Hu","year":"2010","journal-title":"Science"},{"issue":"9","key":"pcbi.1013363.ref042","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1038\/78800","article-title":"Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons","volume":"3","author":"JC Magee","year":"2000","journal-title":"Nat Neurosci"},{"issue":"2","key":"pcbi.1013363.ref043","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1152\/jn.01145.2004","article-title":"Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression","volume":"94","author":"S Canals","year":"2005","journal-title":"J Neurophysiol"},{"issue":"6","key":"pcbi.1013363.ref044","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1162\/neco.1997.9.6.1179","article-title":"The NEURON simulation environment","volume":"9","author":"ML Hines","year":"1997","journal-title":"Neural Comput"},{"issue":"5793","key":"pcbi.1013363.ref045","doi-asserted-by":"crossref","first-page":"1626","DOI":"10.1126\/science.1128115","article-title":"High gamma power is phase-locked to theta oscillations in human neocortex","volume":"313","author":"RT Canolty","year":"2006","journal-title":"Science"},{"key":"pcbi.1013363.ref046","first-page":"2825","article-title":"Scikit-learn: Machine Learning in Python","volume":"12","author":"F Pedregosa","year":"2011","journal-title":"Journal of Machine Learning Research"},{"key":"pcbi.1013363.ref047","doi-asserted-by":"crossref","first-page":"87","DOI":"10.3389\/fncom.2016.00087","article-title":"Neuronal Oscillations with Non-sinusoidal Morphology Produce Spurious Phase-to-Amplitude Coupling and Directionality","volume":"10","author":"D Lozano-Soldevilla","year":"2016","journal-title":"Front Comput Neurosci"},{"key":"pcbi.1013363.ref048","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1113\/jphysiol.1996.sp021397","article-title":"Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo","author":"RD Traub","year":"1996","journal-title":"J Physiol"},{"issue":"5532","key":"pcbi.1013363.ref049","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1126\/science.1060342","article-title":"Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition","volume":"293","author":"F Pouille","year":"2001","journal-title":"Science"},{"issue":"5","key":"pcbi.1013363.ref050","doi-asserted-by":"crossref","first-page":"2382","DOI":"10.1093\/cercor\/bhaa359","article-title":"The Entorhinal Cortical Alvear Pathway Differentially Excites Pyramidal Cells and Interneuron Subtypes in Hippocampal CA1","volume":"31","author":"KA Bell","year":"2021","journal-title":"Cereb Cortex"},{"issue":"12","key":"pcbi.1013363.ref051","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1038\/nn.2441","article-title":"Input normalization by global feedforward inhibition expands cortical dynamic range","volume":"12","author":"F Pouille","year":"2009","journal-title":"Nat Neurosci"},{"issue":"1","key":"pcbi.1013363.ref052","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1523\/JNEUROSCI.19-01-00274.1999","article-title":"Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat","volume":"19","author":"J Csicsvari","year":"1999","journal-title":"J Neurosci"},{"issue":"1","key":"pcbi.1013363.ref053","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1111\/j.1460-9568.2009.07042.x","article-title":"Qualitatively different modes of perirhinal-hippocampal engagement when rats explore novel vs. familiar objects as revealed by c-Fos imaging","volume":"31","author":"MM Albasser","year":"2010","journal-title":"Eur J Neurosci"},{"issue":"4","key":"pcbi.1013363.ref054","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1162\/089976602317318965","article-title":"A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning","volume":"14","author":"ME Hasselmo","year":"2002","journal-title":"Neural Comput"},{"issue":"20","key":"pcbi.1013363.ref055","doi-asserted-by":"crossref","first-page":"8689","DOI":"10.1523\/JNEUROSCI.4483-12.2013","article-title":"Evidence for encoding versus retrieval scheduling in the hippocampus by theta phase and acetylcholine","volume":"33","author":"V Douchamps","year":"2013","journal-title":"J Neurosci"},{"issue":"1","key":"pcbi.1013363.ref056","doi-asserted-by":"crossref","first-page":"14413","DOI":"10.1038\/ncomms14413","article-title":"Amygdala- Hippocampal Dynamics during Salient Information Processing","volume":"8","author":"J Zheng","year":"2017","journal-title":"Nature Communications"},{"issue":"3","key":"pcbi.1013363.ref057","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.2004274","article-title":"Dynamic Frontotemporal Systems Process Space and Time in Working Memory","volume":"16","author":"EL Johnson","year":"2018","journal-title":"PLOS Biology"},{"issue":"10","key":"pcbi.1013363.ref058","first-page":"2070","article-title":"Distinct Directional Couplings between Slow and Fast Gamma Power to the Phase of Theta Oscillations in the Rat Hippocampus. European","volume":"51","author":"H Jiang","year":"2020","journal-title":"Journal of Neuroscience"},{"key":"pcbi.1013363.ref059","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.18566","article-title":"Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit","volume":"5","author":"MJ Bezaire","year":"2016","journal-title":"Elife"},{"issue":"1","key":"pcbi.1013363.ref060","doi-asserted-by":"crossref","first-page":"3664","DOI":"10.1038\/s41467-019-11537-7","article-title":"Challenging the point neuron dogma: FS basket cells as 2-stage nonlinear integrators","volume":"10","author":"A Tzilivaki","year":"2019","journal-title":"Nat Commun"},{"issue":"1","key":"pcbi.1013363.ref061","doi-asserted-by":"crossref","first-page":"111962","DOI":"10.1016\/j.celrep.2022.111962","article-title":"Lateral entorhinal cortex inputs modulate hippocampal dendritic excitability by recruiting a local disinhibitory microcircuit","volume":"42","author":"OM Bilash","year":"2023","journal-title":"Cell Rep"},{"key":"pcbi.1013363.ref062","article-title":"Hippocampal GABAergic Interneurons and Memory","author":"A Tzilivaki","year":"2023","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1013363.ref063","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.neuron.2016.12.018","article-title":"Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal Ripple Oscillations in Awake Mice In Vivo","volume":"93","author":"J Gan","year":"2017","journal-title":"Neuron"},{"issue":"4","key":"pcbi.1013363.ref064","doi-asserted-by":"crossref","DOI":"10.1016\/j.neuron.2021.11.015","article-title":"Extrinsic control and intrinsic computation in the hippocampal CA1 circuit","volume":"110","author":"I Zutshi","year":"2022","journal-title":"Neuron"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1013363","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,8,28]],"date-time":"2025-08-28T00:00:00Z","timestamp":1756339200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013363","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,8,28]],"date-time":"2025-08-28T17:46:04Z","timestamp":1756403164000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1013363"}},"subtitle":[],"editor":[{"given":"Lyle J.","family":"Graham","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2025,8,13]]},"references-count":64,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2025,8,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1013363","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1013363","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,13]]}}}