Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG
Abstract
Although previous studies have established that successful memory encoding is associated with increased synchronization of theta-band and gamma-band oscillations, it is unclear if there is a functional relationship between oscillations in these frequency bands. Using scalp-recorded EEG in healthy human participants, we demonstrate that cross-frequency coupling between frontal theta phase and posterior gamma power is enhanced during the encoding of visual stimuli which participants later on remember versus items which participants subsequently forget ("subsequent memory effect," SME). Conventional wavelet analyses and source localizations revealed SMEs in spectral power of theta-, alpha-, and gamma-band. Successful compared to unsuccessful encoding was reflected in increased theta-band activity in right frontal cortex as well as increased gamma-band activity in parietal-occipital regions. Moreover, decreased alpha-band activity in prefrontal and occipital cortex was also related to successful encoding. Overall, these findings support the idea that during the formation of new memories frontal cortex regions interact with cortical representations in posterior areas.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Theta/gamma coupling is functionally relevant for long-term memory processes and contributes to recall of stored information in rats and humans.
“The theta/gamma coupling has been shown to be functionally relevant for long-term memory processes (Tort et al., 2009) contributing to the recall of stored information both in rats (Shirvalkar et al., 2010) and in humans (Friese et al., 2013).”
From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Friese et al., 2013
Theta/gamma coupling occurs between frontal theta and posterior gamma oscillations.
“However, these studies revealed that the coupling occurs between the frontal theta and the posterior gamma oscillations (Friese et al., 2013).”
From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Friese et al., 2013
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Delorme, A., & Makeig, S. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.10.009 · Cited by 24,371 · see citing works
EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis
Klimesch, W. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00056-3 · Cited by 6,889 · see citing works
The brainweb: phase synchronization and large-scale integration
Varela, F., Lachaux, J.-P., Rodriguez, E., & Martinerie, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35067550 · Cited by 4,761 · see citing works
Tulving, E. (1985) · Canadian Psychology / Psychologie canadienne · doi:10.1037/h0080017 · Cited by 4,638 · see citing works
Dynamic predictions: Oscillations and synchrony in top–down processing
Engel, A. K., Fries, P., & Singer, W. (2001) · Nature Reviews Neuroscience · doi:10.1038/35094565 · Cited by 3,454 · see citing works
High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex
Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., Berger, M. S., Barbaro, N. M., & Knight, R. T. (2006) · Science · doi:10.1126/science.1128115 · Cited by 2,650 · see citing works
The functional role of cross-frequency coupling
Canolty, R. T., & Knight, R. T. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.09.001 · Cited by 2,101 · see citing works
Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., & Schroeder, C. E. (2008) · Science · doi:10.1126/science.1154735 · Cited by 1,719 · see citing works
The role of phase synchronization in memory processes
Fell, J., & Axmacher, N. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2979 · Cited by 1,620 · see citing works
Storage of 7 +/- 2 short-term memories in oscillatory subcycles
Lisman, J. E., & Idiart, M. A. P. (1995) · Science · doi:10.1126/science.7878473 · Cited by 1,471 · see citing works
Measuring Phase-Amplitude Coupling Between Neuronal Oscillations of Different Frequencies
Tort, A. B. L., Komorowski, R. W., Eichenbaum, H., & Kopell, N. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00106.2010 · Cited by 1,365 · see citing works
New vistas for α-frequency band oscillations
Palva, S., & Palva, J. M. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.02.001 · Cited by 1,339 · see citing works
Lakatos, P., Shah, A. S., Knuth, K. H., Ulbert, I., Karmos, G., & Schroeder, C. E. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00263.2005 · Cited by 1,241 · see citing works
Human gamma-frequency oscillations associated with attention and memory
Jensen, O. B., Kaiser, J., & Lachaux, J.-P. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.001 · Cited by 1,239 · see citing works
Cross-frequency coupling between neuronal oscillations
Jensen, O., & Colgin, L. L. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.05.003 · Cited by 991 · see citing works
Cross-frequency coupling supports multi-item working memory in the human hippocampus
Axmacher, N., Henseler, M. M., Jensen, O. B., Weinreich, I., Elger, C. E., & Fell, J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911531107 · Cited by 929 · see citing works
Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans
Tallon‐Baudry, C., Bertrand, O., Delpuech, C., & Pernier, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00722.1997 · Cited by 926 · see citing works
Theta-gamma coupling increases during the learning of item-context associations
Tort, A. B. L., Komorowski, R. W., Manns, J. R., Kopell, N. J., & Eichenbaum, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911331106 · Cited by 919 · see citing works
Observing the transformation of experience into memory
Paller, K. A., & Wagner, A. D. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01845-3 · Cited by 852 · see citing works
Tort, A. B. L., Kramer, M., Thorn, C. A., Gibson, D. J., Kubota, Y., Graybiel, A. M., & Kopell, N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810524105 · Cited by 842 · see citing works
Transient induced gamma-band response in EEG as a manifestation of miniature saccades
Yuval-Greenberg, S., Tomer, O., Keren, A. S., Nelken, I., & Deouell, L. Y. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.027 · Cited by 776 · see citing works
Theta and gamma oscillations during encoding predict subsequent recall
Sederberg, P. B., Kahana, M. J., Howard, M. W., Donner, E. J., & Madsen, J. R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10809.2003 · Cited by 750 · see citing works
Brain Oscillatory Substrates of Visual Short-Term Memory Capacity
Sauseng, P., Klimesch, W., Heise, K.-F., Gruber, W. R., Holz, E. M., Karim, A. A., Glennon, M., Gerloff, C. P., Birbaumer, N., & Hummel, F. C. (2009) · Current Biology · doi:10.1016/j.cub.2009.08.062 · Cited by 707 · see citing works
Theta and gamma oscillations predict encoding and retrieval of declarative memory
Osipova, D., Takashima, A., Oostenveld, R., Fernández, G., Maris, E., & Jensen, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1948-06.2006 · Cited by 671 · see citing works
Phase Synchrony among Neuronal Oscillations in the Human Cortex
Palva, J. M., Palva, S., & Kaila, K. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4250-04.2005 · Cited by 663 · see citing works
Blumenfeld, R., & Ranganath, C. (2007) · The Neuroscientist · doi:10.1177/1073858407299290 · Cited by 634 · see citing works
Statistical control of artifacts in dense array EEG/MEG studies
Junghöfer, M., Elbert, T. R., Tucker, D. M., & Rockstroh, B. S. (2000) · Psychophysiology · doi:10.1111/1469-8986.3740523 · Cited by 577 · see citing works
Functional role of gamma and theta oscillations in episodic memory
Nyhus, E., & Curran, T. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.12.014 · Cited by 564 · see citing works
Theta band power in the human scalp EEG and the encoding of new information
Klimesch, W., Doppelmayr, M., Russegger, H., & Pachinger, T. (1996) · NeuroReport · doi:10.1097/00001756-199605170-00002 · Cited by 422 · see citing works
Mormann, F., Fell, J., Axmacher, N., Weber, B., Lehnertz, K., Elger, C. E., & Fernández, G. (2005) · Hippocampus · doi:10.1002/hipo.20117 · Cited by 403 · see citing works
Brain oscillations and human memory: EEG correlates in the upper alpha and theta band
Klimesch, W., Doppelmayr, M. M., Pachinger, T., & Ripper, B. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00771-4 · Cited by 346 · see citing works
Gamma Power Is Phase-Locked to Posterior Alpha Activity
Osipova, D. V., Hermes, D., & Jensen, O. B. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003990 · Cited by 329 · see citing works
Brain Oscillations Dissociate between Semantic and Nonsemantic Encoding of Episodic Memories
Hanslmayr, S., Spitzer, B., & Bäuml, K. T. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn197 · Cited by 303 · see citing works
Gamma amplitudes are coupled to theta phase in human EEG during visual perception
Demıralp, T., Bayraktaroğlu, Z., Lenz, D., Junge, S., Busch, N. A., Maeß, B., Ergen, M., & Herrmann, C. S. (2006) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2006.07.005 · Cited by 214 · see citing works
Cross-frequency phase synchronization: A brain mechanism of memory matching and attention
Sauseng, P., Klimesch, W., Gruber, W. R., & Birbaumer, N. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.11.032 · Cited by 205 · see citing works
Oscillatory Event-Related Brain Dynamics
Pantev, C., Elbert, T. R., & Lütkenhöner, B. (1994) · Springer eBooks · doi:10.1007/978-1-4899-1307-4 · Cited by 198 · see citing works
Hanslmayr, S., Volberg, G., Wimber, M., Raabe, M., Greenlee, M. W., & Bäuml, K. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3140-11.2011 · Cited by 193 · see citing works
Induced gamma band responses: an early marker of memory encoding and retrieval
Gruber, T., Tsivilis, D., Montaldi, D., & Müller, M. M. (2004) · Neuroreport · doi:10.1097/01.wnr.0000137077.26010.12 · Cited by 174 · see citing works
Self-citationKlimesch, W., Schimke, H., Doppelmayr, M., Ripper, B., Schwaiger, J., & Pfurtscheller, G. (1996) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(96)00054-2 · Cited by 149 · see citing works
EEG theta synchronization conjoined with alpha desynchronization indicate intentional encoding
Mölle, M., Marshall, L., Fehm, H. L., & Born, J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01921.x · Cited by 114 · see citing works
Brain oscillatory correlates of working memory constraints
Freunberger, R., Werkle‐Bergner, M., Griesmayr, B., Lindenberger, U., & Klimesch, W. (2010) · Brain Research · doi:10.1016/j.brainres.2010.12.048 · Cited by 114 · see citing works
Gruber, T., Trujillo‐Barreto, N. J., Giabbiconi, C., et al. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.004 · Cited by 87 · see citing works
Self-citationInduced gamma band responses in human EEG after the control of miniature saccadic artifacts
Hassler, U., Trujillo‐Barreto, N. J., & Gruber, T. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.062 · Cited by 82 · see citing works
Self-citationShort-term memory capacity (7+/−2) predicted by theta to gamma cycle length ratio
Kamiński, J., Brzezicka, A., & Wróbel, A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.10.001 · Cited by 82 · see citing works
Multiple comparison procedures within experimental research.
Davis, C. A., & Gaito, J. (1984) · Canadian Psychology/Psychologie canadienne · doi:10.1037/h0080769 · Cited by 76 · see citing works
Magnetoencephalographic gamma-band responses to illusory triangles in humans
Kaiser, J., Fauth‐Bühler, M., & Lutzenberger, W. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.06.033 · Cited by 76 · see citing works
Bertrand, O., & Pantev, C. (1994) · Springer eBooks · doi:10.1007/978-1-4899-1307-4_17 · Cited by 70 · see citing works
Friese, U., Supp, G. G., Hipp, J. F., Engel, A. K., & Gruber, T. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.073 · Cited by 38 · see citing works
Self-citationTsunada, J., Baker, A. E., Christison-Lagay, K. L., Davis, S. J., & Cohen, Y. E. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00217 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Episodic sequence memory is supported by a theta-gamma phase code
Heusser, A. C., Poeppel, D., Ezzyat, Y., & Davachi, L. (2016) · Nature Neuroscience · doi:10.1038/nn.4374 · Cited by 290 · see citing works
The Functional Role of Dreaming in Emotional Processes
Scarpelli, S., Bartolacci, C., D'Atri, A., Gorgoni, M., & De Gennaro, L. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00459 · Cited by 190 · see citing works
Ahnaou, A., Moechars, D., Raeymaekers, L., Biermans, R., Manyakov, N. V., Bottelbergs, A., Wintmolders, C., Van Kolen, K., Van De Casteele, T., Kemp, J. A., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-13839-6 · Cited by 98 · see citing works
Mental Sleep Activity and Disturbing Dreams in the Lifespan
Scarpelli, S., Bartolacci, C., D’Atri, A., Gorgoni, M., & De Gennaro, L. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16193658 · Cited by 41 · see citing works
“Specifically, the so-called theta / gamma coupling seems to be particularly involved in long-term memory encoding [158], also promoting the retrieval of stored mnestic traces in animals as well as in humans [159].”
Amer, T., & Davachi, L. (2022) · doi:10.31234/osf.io/32egy · Cited by 3 · see citing works
- Authors
- Friese, U., Köster, M., Hassler, U., Martens, U., Trujillo-Barreto, N., & Gruber, T.
- Affiliations
- Osnabrück University (DE)
- Corresponding author
- Friese, Uwe
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 66
- Pages
- 642-647
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2046550948
- Cited by
- 233
- References
- 50
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 14 · 2023: 18 · 2022: 22 · 2021: 21 · 2020: 19 · 2019: 15 · 2018: 18 · 2017: 34 · 2016: 25 · 2015: 9 · 2014: 13 · 2013: 6
- FWCI
- 4.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- German Research Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- memory encoding, cross-frequency coupling, theta oscillations, gamma oscillations, subsequent memory effect, frontal cortex, alpha band, EEG source localization, visual memory, neuronal synchronization
- MeSH terms
- Brain, Cortical Synchronization, Electroencephalography, Female, Humans, Male, Memory, Scalp, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review