Independent delta/theta rhythms in the human hippocampus and entorhinal cortex.
- Authors
- Mormann, Florian; Osterhage, Hannes; Andrzejak, Ralph G; Weber, Bernd; FernΓ‘ndez, GuillΓ©n; Fell, Juergen; Elger, Christian E; Lehnertz, Klaus
- Year
- 2008
- Journal
- Frontiers in human neuroscience
- PMID
- 18958204
- DOI
- 10.3389/neuro.09.003.2008
- PMCID
- PMC2525973
Theta oscillations in the medial temporal lobe (MTL) of mammals are involved in various functions such as spatial navigation, sensorimotor integration, and cognitive processing. While the theta rhythm was originally assumed to originate in the medial septum, more recent studies suggest autonomous theta generation in the MTL. Although coherence between entorhinal and hippocampal theta activity has been found to influence memory formation, it remains unclear whether these two structures can generate theta independently. In this study we analyzed intracranial electroencephalographic (EEG) recordings from 22 patients with unilateral hippocampal sclerosis undergoing presurgical evaluation prior to resection of the epileptic focus. Using a wavelet-based, frequency-band-specific measure of phase synchronization, we quantified synchrony between 10 different recording sites along the longitudinal axis of the hippocampal formation in the non-epileptic brain hemisphere. We compared EEG synchrony between adjacent recording sites (i) within the entorhinal cortex, (ii) within the hippocampus, and (iii) between the hippocampus and entorhinal cortex. We observed a significant interregional gap in synchrony for the delta and theta band, indicating the existence of independent delta/theta rhythms in different subregions of the human MTL. The interaction of these rhythms could represent the temporal basis for the information processing required for mnemonic encoding and retrieval.
Electrode implantation scheme. Longitudinal depth electrodes are placed with the anterior contacts located in the entorhinal cortex (EC) and the posterior contacts located in the hippocampus (Hi).
Exemplary results. (A) Exemplary traces of bandpass-filtered theta activity from two entorhinal (EC, channels 3 and 4) and two hippocampal (Hi, channels 5 and 6) recording sites. The average degree of synchrony R between these recording sites over time is color-coded and displayed in the synchronization matrix (upper right) for this EEG frequency band. In this schematic, only the three matrix entries for which the subsequent group statistics was performed are filled. (B) Synchronization matrices from the same patient for different EEG bands, including the theta matrix from (A), now with all entries filled.
Group statistics for 22 patients. Comparison of intra- and inter-regional synchrony within and between the entorhinal cortex and hippocampus for different frequency bands. Bars depict mean levels of synchrony across patients within the entorhinal cortex (ECβEC), between entorhinal cortex and hippocampus (ECβHi), and within the hippocampus (HiβHi), respectively, with error bars denoting the standard error. n.s. = not significant, * = p < 0.05, ** = p < 0.01, *** = p < 0.001 (two-sided Wilcoxon test; uncorrected p-values). Note that a statistically significant inter-regional gap in synchrony as defined in the methods section is observed only for the delta and theta band.
| Name | Type |
|---|---|
| amygdala | anatomy |
| Anterior hippocampus | anatomy |
| anterior parahippocampal gyrus local | anatomy |
| Collateral sulcus local | anatomy |
| delta band | phenotype |
| diagonal band of Broca | anatomy |
| entorhinal cortex | anatomy |
| Entorhinal-hippocampal border local | anatomy |
| Entorhinal rhythm local | phenotype |
| epilepsy | phenotype |
| Focal epilepsy local | phenotype |
| Frequency band local | phenotype |
| gamma oscillations | phenotype |
| hippocampal CA1 region | anatomy |
| Hippocampal fissure local | anatomy |
| hippocampal formation | anatomy |
| Hippocampal rhythm local | phenotype |
| hippocampal sclerosis local | phenotype |
| hippocampus | anatomy |
| human MTL local | anatomy |
| humans | cohort |
| Inter-regional synchrony gap local | phenotype |
| learning/memory deficits local | phenotype |
| long term depression local | phenotype |
| long term potentiation local | phenotype |
| medial septum | anatomy |
| mediotemporal region local | anatomy |
| mediotemporal theta activity local | phenotype |
| memory | phenotype |
| Mnemonic processing local | phenotype |
| monkey cortex local | anatomy |
| Monkey cortex local | anatomy |
| MTL | anatomy |
| MTL subregions local | anatomy |
| neocortex | anatomy |
| original group of 40 patients local | cohort |
| parasubiculum | anatomy |
| patients | cohort |
| patients with temporal lobe epilepsy local | cohort |
| perirhinal cortex | anatomy |
| Pharmaco-refractory unilateral epilepsy local | phenotype |
| Pharmaco-refractory unilateral epilepsy cohort local | cohort |
| pharmacoresistant MTL epilepsy local | phenotype |
| Phase precession local | phenotype |
| rhinal cortex local | anatomy |
| rhinal-hippocampal theta coherence local | phenotype |
| rodent studies | cohort |
| seizure-free local | phenotype |
| Seizure-free interval local | phenotype |
| selected cohort of 22 patients local | cohort |
| Sensorimotor integration local | phenotype |
| Spatial navigation | phenotype |
| subregions of hippocampus local | anatomy |
| Sulcus semiannularis local | anatomy |
| Synchrony local | phenotype |
| temporal lobe | anatomy |
| temporal lobe epilepsy | anatomy |
| theta activity | phenotype |
| theta band | phenotype |
| Theta generators local | phenotype |
| theta oscillations | phenotype |
| theta phase reset local | phenotype |
| Unilateral MTL epilepsy cohort local | cohort |
| working memory | phenotype |
| Working memory task local | phenotype |
No uploaded files.
| Citation | PMID | DOI | Status |
|---|---|---|---|
| AckerC. D.KopellN.WhiteJ. A. (2003). Synchronization of strongly coupled excitatory neurons: relating network behavior to biophysics. J. Comput. Neurosci.15, 71β9010.1023/A:102447481951212843696 | β | β | β |
| AlonsoA.LlinasR. R. (1989). Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature342, 175β17710.1038/342175a02812013 | β | β | β |
| AxmacherN.MormannF.FernΓ‘ndezG.ElgerC. E.FellJ. (2006). Memory formation by neuronal synchronization. Brain Res. Brain Res. Rev.52, 170β18210.1016/j.brainresrev.2006.01.00716545463 | β | β | β |
| BraginA.JandΓ³G.NΓ‘dasdyZ.HetkeJ.WiseK.BuzsΓ‘kiG. (1995). Gamma (40β100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci.15, 47β60782315110.1523/JNEUROSCI.15-01-00047.1995PMC6578273 | β | β | β |
| BullockT. H.McCluneM. C.AchimowiczJ. Z.Iragui-MadozV. J.DuckrowR. B.SpencerS. S. (1995a). EEG coherence has structure in the millimeter domain: subdural and hippocampal recordings from epileptic patients. Electroencephalogr. Clin. Neurophysiol.95, 161β17710.1016/0013-4694(95)93347-A7555907 | β | β | β |
| BullockT. H.McCluneM. C.AchimowiczJ. Z.Iragui-MadozV. J.DuckrowR. B.SpencerS. S. (1995b). Temporal fluctuations in coherence of brain waves. Proc. Natl. Acad. Sci. USA92, 11568β1157210.1073/pnas.92.25.115688524805PMC40443 | β | β | β |
| BuzsakiG.LeungL. W.VanderwolfC. H. (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Res.287, 139β171635735610.1016/0165-0173(83)90037-1 | β | β | β |
| BuzsΓ‘kiG. (2002). Theta oscillations in the hippocampus. Neuron33, 325β34010.1016/S0896-6273(02)00586-X11832222 | β | β | β |
| BuzsΓ‘kiG. (2005). Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus15, 827β84010.1002/hipo.2011316149082 | β | β | β |
| BuzsΓ‘kiG. (2006). Rhythms of the Brain. Oxford University Press, New York. | β | β | β |
| CanoltyR. T.EdwardsE.DalalS. S.SoltaniM.NagarajanS. S.KirschH. E.BergerM. S.BarbaroN. M.KnightR. T. (2006). High gamma power is phase-locked to theta oscillations in human neocortex. Science313, 1626β162810.1126/science.112811516973878PMC2628289 | β | β | β |
| ChrobakJ. J.BuzsΓ‘kiG. (1998). Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci.18, 388β398941251510.1523/JNEUROSCI.18-01-00388.1998PMC6793397 | β | β | β |
| DemiralpT.BayraktarogluZ.LenzD.JungeS.BuschN. A.MaessB.ErgenM.HerrmannC. S. (2007). Gamma amplitudes are coupled to theta phase in human EEG during visual perception. Int. J. Psychophysiol.64, 24β3010.1016/j.ijpsycho.2006.07.00516956685 | β | β | β |
| DiehlB.LudersH. O. (2000). Temporal lobe epilepsy: when are invasive recordings needed?Epilepsia41, S61βS7410.1111/j.1528-1157.2000.tb01536.x11001338 | β | β | β |
| EkstromA.SuthanaN.BehnkeE.SalamonN.BookheimerS.FriedI. (2008). High-resolution depth electrode localization and imaging in patients with pharmacologically intractable epilepsy. J. Neurosurg.108, 812β81510.3171/JNS/2008/108/4/081218377264PMC2628813 | β | β | β |
| FellJ.KlaverP.ElfadilH.SchallerC.ElgerC. E.FernΓ‘ndezG. (2003). Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization?Eur. J. Neurosci.17, 1082β108810.1046/j.1460-9568.2003.02522.x12653984 | β | β | β |
| FriedI.MacDonaldK. A.WilsonC. L. (1997). Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron18, 753β76510.1016/S0896-6273(00)80315-39182800 | β | β | β |
| GilliesM. J.TraubR. D.LeBeauF. E. N.DaviesC. H.GloveliT.BuhlE. H.WhittingtonM. A. (2002). A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J. Physiol.543, 779β79310.1113/jphysiol.2002.02458812231638PMC2290530 | β | β | β |
| GiocomoL. M.ZilliE. A.FransenE.HasselmoM. E. (2007). Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science315, 1719β172210.1126/science.113920717379810PMC2950607 | β | β | β |
| GivensB. (1996). Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport8, 159β163905177210.1097/00001756-199612200-00032 | β | β | β |
| GlasgowS. D.ChapmanC. A. (2007). Local generation of theta-frequency EEG activity in the parasubiculum. J. Neurophysiol.97, 3868β387910.1152/jn.01306.200617392407 | β | β | β |
| GrunwaldT.ElgerC. E.LehnertzK.Van RoostD.HeinzeH. J. (1995). Alterations of intrahippocampal cognitive potentials in temporal lobe epilepsy. Electroencephalogr. Clin. Neurophysiol.95, 53β6210.1016/0013-4694(95)00015-Q7621772 | β | β | β |
| HasselmoM. E.BodelonC.WybleB. P. (2002). A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput.14, 793β81710.1162/08997660231731896511936962 | β | β | β |
| HolscherC.AnwylR.RowanM. J. (1997). Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J. Neurosci.17, 6470β6477923625410.1523/JNEUROSCI.17-16-06470.1997PMC6568346 | β | β | β |
| HuertaP. T.LismanJ. E. (1995). Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron15, 1053β106310.1016/0896-6273(95)90094-27576649 | β | β | β |
| HuxterJ.BurgessN.O'KeefeJ. (2003). Independent rate and temporal coding in hippocampal pyramidal cells. Nature425, 828β83210.1038/nature0205814574410PMC2677642 | β | β | β |
| HymanJ. M.WybleB. P.GoyalV.RossiC. A.HasselmoM. E. (2003). Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J. Neurosci.23, 11725β117311468487410.1523/JNEUROSCI.23-37-11725.2003PMC6740943 | β | β | β |
| InsaustiR.JuottonenK.SoininenH.InsaustiA. M.PartanenK.VainioP.LaaksoM. P.PitkanenA. (1998). MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. AJNR. Am. J. Neuroradiol.19, 659β6719576651PMC8337393 | β | β | β |
| JacobsJ.KahanaM. J.EkstromA. D.FriedI. (2007). Brain oscillations control timing of single-neuron activity in humans. J. Neurosci.27, 3839β384410.1523/JNEUROSCI.4636-06.200717409248PMC6672400 | β | β | β |
| JensenO.LismanJ. E. (1998). An oscillatory short-term memory buffer model can account for data on the Sternberg task. J. Neurosci.18, 10688β10699985260410.1523/JNEUROSCI.18-24-10688.1998PMC6793327 | β | β | β |
| KamondiA.AcsΓ‘dyL.WangX. J.BuzsΓ‘kiG. (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus8, 244β26110.1002/(SICI)1098-1063(1998)8:3<244::AID-HIPO7>3.0.CO;2-J9662139 | β | β | β |
| KocsisB.BraginA.BuzsΓ‘kiG. (1999). Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J. Neurosci.19, 6200β62121040705610.1523/JNEUROSCI.19-14-06200.1999PMC6783086 | β | β | β |
| LogothetisN. K.KayserC.OeltermannA. (2007). In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron55, 809β82310.1016/j.neuron.2007.07.02717785187 | β | β | β |
| McCartneyH.JohnsonA. D.WeilZ. M.GivensB. (2004). Theta reset produces optimal conditions for long-term potentiation. Hippocampus14, 684β68710.1002/hipo.2001915318327 | β | β | β |
| MormannF.FellJ.AxmacherN.WeberB.LehnertzK.ElgerC. E.FernΓ‘ndezG. (2005). Phase/amplitude reset and thetaβgamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus15, 890β90010.1002/hipo.2011716114010 | β | β | β |
| MormannF.LehnertzK.DavidP.ElgerC. E. (2000). Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D144, 358β36910.1016/S0167-2789(00)00087-7 | β | β | β |
| O'KeefeJ.RecceM. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus3, 317β33010.1002/hipo.4500303078353611 | β | β | β |
| OlivierA.MarchandE.PetersT.TylerJ. (1987). Depth electrode implantation at the Montreal Neurological Institute and Hospital. In Surgical Treatment of the Epilepsies, EngelJ.Jr, ed. (New York, NY, Raven Press), pp. 595β601 | β | β | β |
| OsterhageH.MormannF.WagnerT.LehnertzK. (2007). Measuring the directionality of coupling: phase versus state space dynamics and application to EEG time series. Int. J. Neural Syst.17, 139β14810.1142/S012906570700101917640095 | β | β | β |
| PavlidesC.GreensteinY. J.GrudmanM.WinsonJ. (1988). Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res.439, 383β38710.1016/0006-8993(88)91499-03359196 | β | β | β |
| PetscheH.StumpfC.GogolakG. (1962). The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroencephalogr. Clin. Neurophysiol.14, 202β21110.1016/0013-4694(62)90030-514038334 | β | β | β |
| RaghavachariS.LismanJ. E.TullyM.MadsenJ. R.BromfieldE. B.KahanaM. J. (2006). Theta oscillations in human cortex during a working-memory task: evidence for local generators. J. Neurophysiol.95, 1630β163810.1152/jn.00409.200516207788 | β | β | β |
| RizzutoD. S.MadsenJ. R.BromfieldE. B.Schulze-BonhageA.KahanaM. J. (2006). Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. Neuroimage31, 1352β135810.1016/j.neuroimage.2006.01.00916542856 | β | β | β |
| RotsteinH. G.PervouchineD. D.AckerC. D.GilliesM. J.WhiteJ. A.BuhlE. H.WhittingtonM. A.KopellN. (2005). Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. J. Neurophysiol.94, 1509β151810.1152/jn.00957.200415857967 | β | β | β |
| SiapasA. G.LubenovE. V.WilsonM. A. (2005). Prefrontal phase locking to hippocampal theta oscillations. Neuron46, 141β15110.1016/j.neuron.2005.02.02815820700 | β | β | β |
| SkaggsW. E.McNaughtonB. L.WilsonM. A.BarnesC. A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus6, 149β17210.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K8797016 | β | β | β |
| SpencerD. D. (1987). Depth electrode implantation at Yale University. In: Surgical Treatment of the Epilepsies, EngelJ.Jr, ed. (New York, NY, Raven Press), pp. 603β608 | β | β | β |
| TaylorC. P.DudekF. E. (1984). Excitation of hippocampal pyramidal cells by an electrical field effect. J. Neurophysiol.52, 126β142608685310.1152/jn.1984.52.1.126 | β | β | β |
| TorrenceC.CompoG. P. (1998). A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc.79, 61β7810.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2 | β | β | β |
| Van RoostD.SolymosiL.SchrammJ.van OosterwyckB.ElgerC. E. (1998). Depth electrode implantation in the length axis of the hippocampus for the presurgical evaluation of medial temporal lobe epilepsy: a computed tomography-based stereotactic insertion technique and its accuracy. Neurosurgery43, 819β82610.1097/00006123-199810000-000589766309 | β | β | β |
| VertesR. P.KocsisB. (1997). Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience81, 893β926933035510.1016/s0306-4522(97)00239-x | β | β | β |
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| Title | Authors | Journal | Year | Link |
|---|---|---|---|---|
| Improving working memory by electrical stimulation and cross-frequency coupling. | Al Qasem W et al. | β | 2024 | β |
| Theta-gamma-coupling as predictor of working memory performance in young and elderly healthy people. | Abubaker M et al. | β | 2024 | β |
| Effects of inhaling essential oils of Citrus limonum L., Santalum album, and Cinnamomum camphora on human brain activity. | Ueda K et al. | β | 2023 | β |
| Hippocampal non-theta state: The "Janus face" of information processing. | Mysin I et al. | β | 2023 | β |
| Predicting Alcohol-Related Memory Problems in Older Adults: A Machine Learning Study with Multi-Domain Features. | Kamarajan C et al. | β | 2023 | β |
| The Usefulness of Quantitative Electroencephalography in Diagnosis and Severity Evaluation of Delirium: A Retrospective Study. | Kim SB et al. | β | 2023 | β |
| Cognitive and Emotional Mapping With SEEG. | Drane DL et al. | β | 2021 | β |
| DΓ©jΓ vu experiences in anxiety. | Wells CE et al. | β | 2021 | β |
| Chemosensory Event-Related Potentials and Power Spectrum could be A Possible Biomarker in 3M Syndrome Infants? | Invitto S et al. | β | 2020 | β |
| Hippocampal theta coordinates memory processing during visual exploration. | Kragel JE et al. | β | 2020 | β |
| Interpretation of the Intracranial Stereoelectroencephalography Signal. | Kokkinos V | β | 2020 | β |
| Intracranial-EEG evidence for medial temporal pole driving amygdala activity induced by multi-modal emotional stimuli. | Sonkusare S et al. | β | 2020 | β |
| Characterizing hippocampal dynamics with MEG: A systematic review and evidence-based guidelines. | Ruzich E et al. | β | 2019 | β |
| Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation. | Chen D et al. | β | 2018 | β |
| Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation. | Miller J et al. | β | 2018 | β |
| Phase-tuned neuronal firing encodes human contextual representations for navigational goals. | Watrous AJ et al. | β | 2018 | β |
| Carbachol-induced network oscillations in an in vitro limbic system brain slice. | LΓ©vesque M et al. | β | 2017 | β |
| Decomposing Multifractal Crossovers. | Nagy Z et al. | β | 2017 | β |
| Dorsal vs. ventral differences in fast Up-state-associated oscillations in the medial prefrontal cortex of the urethane-anesthetized rat. | Gretenkord S et al. | β | 2017 | β |
| Phase-tuned neuronal firing encodes human contextual representations for navigational goals | Watrous AJ et al. | β | 2017 | β |
| Spontaneous dynamics of neural networks in deep layers of prefrontal cortex. | Blaeser AS et al. | β | 2017 | β |
| Verbal memory decline from hippocampal depth electrodes in temporal lobe surgery for epilepsy. | Ljung H et al. | β | 2017 | β |
| Hippocampal pattern completion is linked to gamma power increases and alpha power decreases during recollection. | Staresina BP et al. | β | 2016 | β |
| Making Waves in the Brain: What Are Oscillations, and Why Modulating Them Makes Sense for Brain Injury. | Pevzner A et al. | β | 2016 | β |
| Assessing directionality and strength of coupling through symbolic analysis: an application to epilepsy patients. | Lehnertz K et al. | β | 2015 | β |
| Distinguishing cognitive state with multifractal complexity of hippocampal interspike interval sequences. | Fetterhoff D et al. | β | 2015 | β |
| Neurocognitive stages of spatial cognitive mapping measured during free exploration of a large-scale virtual environment. | Plank M et al. | β | 2015 | β |
| Can spurious indications for phase synchronization due to superimposed signals be avoided? | Porz S et al. | β | 2014 | β |
| Emergence of semiology in epileptic seizures. | Chauvel P et al. | β | 2014 | β |
| Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory. | Jacobs J | β | 2014 | β |
| The spectro-contextual encoding and retrieval theory of episodic memory. | Watrous AJ et al. | β | 2014 | β |
| A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. | Watrous AJ et al. | β | 2013 | β |
| A neocortical delta rhythm facilitates reciprocal interlaminar interactions via nested theta rhythms. | Carracedo LM et al. | β | 2013 | β |
| Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. | Watrous AJ et al. | β | 2013 | β |
| Incidental and intentional learning of verbal episodic material differentially modifies functional brain networks. | Kuhnert MT et al. | β | 2013 | β |
| Increased mesiotemporal delta activity characterizes virtual navigation in humans. | Clemens Z et al. | β | 2013 | β |
| Modifications of EEG power spectra in mesial temporal lobe during n-back tasks of increasing difficulty. A sLORETA study. | Imperatori C et al. | β | 2013 | β |
| DΓ©jΓ experiences in temporal lobe epilepsy. | Illman NA et al. | β | 2012 | β |
| Distinct contributions of human hippocampal theta to spatial cognition and anxiety. | Cornwell BR et al. | β | 2012 | β |
| High-frequency neural activity and human cognition: past, present and possible future of intracranial EEG research. | Lachaux JP et al. | β | 2012 | β |
| Rhinal-hippocampal interactions during dΓ©jΓ vu. | Bartolomei F et al. | β | 2012 | β |
| Slow EEG rhythms and inter-hemispheric synchronization across sleep and wakefulness in the human hippocampus. | Moroni F et al. | β | 2012 | β |
| Assessing directed interactions from neurophysiological signals--an overview. | Lehnertz K | β | 2011 | β |
| Behavioral correlates of human hippocampal delta and theta oscillations during navigation. | Watrous AJ et al. | β | 2011 | β |
| Using bivariate signal analysis to characterize the epileptic focus: the benefit of surrogates. | Andrzejak RG et al. | β | 2011 | β |
| A comparison of sleeplike slow oscillations in the hippocampus under ketamine and urethane anesthesia. | Sharma AV et al. | β | 2010 | β |
| Cross-frequency coupling supports multi-item working memory in the human hippocampus. | Axmacher N et al. | β | 2010 | β |
| Neurophysiological and computational principles of cortical rhythms in cognition. | Wang XJ | β | 2010 | β |
| Selective theta-synchronization of choice-relevant information subserves goal-directed behavior. | Womelsdorf T et al. | β | 2010 | β |
| Synchronous neural activity and memory formation. | Jutras MJ et al. | β | 2010 | β |
| Theta oscillations during holeboard training in rats: different learning strategies entail different context-dependent modulations in the hippocampus. | Woldeit ML et al. | β | 2010 | β |
| Dynamic Causal Models for phase coupling. | Penny WD et al. | β | 2009 | β |
| Phase coupling between rhythmic slow activity and gamma characterizes mesiotemporal rapid-eye-movement sleep in humans. | Clemens Z et al. | β | 2009 | β |
| Brain rhythms in the human medial temporal lobe. | Heinze HJ | β | 2008 | β |