The gamma cycle.
Abstract
Activated neuronal groups typically engage in rhythmic synchronization in the gamma-frequency range (30-100 Hz). Experimental and modeling studies demonstrate that each gamma cycle is framed by synchronized spiking of inhibitory interneurons. Here, we review evidence suggesting that the resulting rhythmic network inhibition interacts with excitatory input to pyramidal cells such that the more excited cells fire earlier in the gamma cycle. Thus, the amplitude of excitatory drive is recoded into phase values of discharges relative to the gamma cycle. This recoding enables transmission and read out of amplitude information within a single gamma cycle without requiring rate integration. Furthermore, variation of phase relations can be exploited to facilitate or inhibit exchange of information between oscillating cell assemblies. The gamma cycle could thus serve as a fundamental computational mechanism for the implementation of a temporal coding scheme that enables fast processing and flexible routing of activity, supporting fast selection and binding of distributed responses. This review is part of the INMED/TINS special issue Physiogenic and pathogenic oscillations: the beauty and the beast, based on presentations at the annual INMED/TINS symposium (http://inmednet.com).
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?
Neural synchrony plays a key role in coordinating brain functions.
“Neural synchrony thus appears to play a key role in coordinating brain functions.”
From Synchrony in Psychotherapy: A Review and an Integrative Framework for the Therapeutic Alliance (2016) · cites this paper as Fries et al., 2007
Cites
Gray, C. M., König, P., Engel, A. K., & Singer, W. (1989) · Nature · doi:10.1038/338334a0 · Cited by 4,183 · see citing works
Self-citationSpeed of processing in the human visual system
Thorpe, S., Fize, D., & Marlot, C. (1996) · Nature · doi:10.1038/381520a0 · Cited by 3,538 · see citing works
Impaired Electrical Signaling Disrupts Gamma Frequency Oscillations in Connexin 36-Deficient Mice
Hormuzdi, S. G., Pais, I., LeBeau, F. E. N., Towers, S. K., Rozov, A., Buhl, E. H., Whittington, M. A., & Monyer, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00387-7 · Cited by 522 · see citing works
Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells
Harris, K. D., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., Czurkó, A., & Buzsáki, G. (2002) · Nature · doi:10.1038/nature00808 · Cited by 398 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition
Jensen, O., & Mazaheri, A. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00186 · Cited by 3,237 · see citing works
Rhythms for cognition: communication through coherence
Fries, P. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.034 · Cited by 2,725 · see citing works
Self-citationDriving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
Network hubs in the human brain
van den Heuvel, M. P., & Sporns, O. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.09.012 · Cited by 2,123 · see citing works
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Control of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
Gamma frequency entrainment attenuates amyloid load and modifies microglia
Iaccarino, H. F., Singer, A. C., Martorell, A. J., Rudenko, A., Gao, F., Gillingham, T. Z., Mathys, H., Seo, J., Kritskiy, O., Abdurrob, F., et al. (2016) · Nature · doi:10.1038/nature20587 · Cited by 1,328 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
Cortical oscillations and sensory predictions
Arnal, L. H., & Giraud, A.-L. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.05.003 · Cited by 1,114 · see citing works
Manning, J. R., Jacobs, J., Fried, I., & Kahana, M. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2041-09.2009 · Cited by 973 · see citing works
EEG and MEG: Relevance to Neuroscience
Lopes da Silva, F. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.017 · Cited by 900 · see citing works
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.013 · Cited by 872 · see citing works
Ray, S., Crone, N. E., Niebur, E., Franaszczuk, P. J., & Hsiao, S. S. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2848-08.2008 · Cited by 722 · see citing works
Neural synchrony in cortical networks: history, concept and current status
Uhlhaas, P. (2009) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.017.2009 · Cited by 758 · see citing works
Power-Law Scaling in the Brain Surface Electric Potential
Miller, K. J., Sorensen, L. B., Ojemann, J. G., & den Nijs, M. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000609 · Cited by 742 · see citing works
Attentional stimulus selection through selective synchronization between monkey visual areas
Bosman, C. A., Schoffelen, J.-M., Brunet, N., Oostenveld, R., Bastos, A. M., Womelsdorf, T., Rubehn, B., Stieglitz, T., De Weerd, P., & Fries, P. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.037 · Cited by 720 · see citing works
Self-citationCarlén, M., Meletis, K., Siegle, J. H., Cardin, J. A., Futai, K., Vierling-Claassen, D., Rühlmann, C., Jones, S. R., Deisseroth, K., Sheng, M., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.31 · Cited by 669 · see citing works
Uhlhaas, P. J., Haenschel, C., Nikolic, D., & Singer, W. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn062 · Cited by 629 · see citing works
Self-citationKorotkova, T., Fuchs, E. C., Ponomarenko, A., von Engelhardt, J., & Monyer, H. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.017 · Cited by 480 · see citing works
Fries, P., Womelsdorf, T., Oostenveld, R., & Desimone, R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4499-07.2008 · Cited by 458 · see citing works
Self-citationCentral gain control in tinnitus and hyperacusis
Auerbach, B. D., Rodrigues, P. V., & Salvi, R. J. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00206 · Cited by 439 · see citing works
Synchrony in Psychotherapy: A Review and an Integrative Framework for the Therapeutic Alliance
Koole, S. L., & Tschacher, W. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00862 · Cited by 456 · see citing works
“Especially oscillatory rhythms in the beta/gamma range (20–80 Hz) may help facilitate communication between distributed neural functions (Varela et al., 2001; Fries et al., 2007; Uhlhaas et al., 2009).”
BackgroundLucid dreaming: a state of consciousness with features of both waking and non-lucid dreaming
Voss, U., Holzmann, R., Tuin, I., & Hobson, A. J. (2009) · Sleep · doi:10.1093/sleep/32.9.1191 · Cited by 445 · see citing works
Rapid Neocortical Dynamics: Cellular and Network Mechanisms
Haider, B., & McCormick, D. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.008 · Cited by 441 · see citing works
Critical-Period Plasticity in the Visual Cortex
Levelt, C. N., & Hübener, M. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113813 · Cited by 402 · see citing works
Dugué, L., Marque, P., & VanRullen, R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1161-11.2011 · Cited by 364 · see citing works
Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex
Spaak, E., Bonnefond, M., Maier, A., Leopold, D. A., & Jensen, O. (2012) · Current Biology · doi:10.1016/j.cub.2012.10.020 · Cited by 385 · see citing works
Role of myelin plasticity in oscillations and synchrony of neuronal activity
Pajevic, S., Basser, P. J., & Fields, R. D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.007 · Cited by 378 · see citing works
Key, B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1011 · Cited by 318 · see citing works
Kann, O., Papageorgiou, I. E., & Draguhn, A. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.104 · Cited by 295 · see citing works
Assessing transient cross-frequency coupling in EEG data
Cohen, M. X. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.10.012 · Cited by 262 · see citing works
Gandal, M. J., Edgar, J. C., Klook, K., & Siegel, S. J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.007 · Cited by 269 · see citing works
Oscillations and Filtering Networks Support Flexible Routing of Information
Akam, T., & Kullmann, D. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.019 · Cited by 245 · see citing works
Gaetz, W., Bloy, L., Wang, D. J., Port, R. G., Blaskey, L., Levy, S. E., & Roberts, T. P. L. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.068 · Cited by 267 · see citing works
Maier (2010) · Frontiers in System Neuroscience · doi:10.3389/fnsys.2010.00031 · Cited by 266 · see citing works
Steullet, P., Cabungcal, J. H., Monin, A., Dwir, D., O'Donnell, P., Cuenod, M., & Do, K. Q. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.021 · Cited by 262 · see citing works
Inhibitory Interneurons Regulate Temporal Precision and Correlations in Cortical Circuits
Cardin, J. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.07.015 · Cited by 254 · see citing works
Cortical gamma responses: Searching high and low
Crone, N. E., Korzeniewska, A., & Franaszczuk, P. J. (2011) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2010.10.013 · Cited by 201 · see citing works
Gamma-phase shifting in awake monkey visual cortex
Vinck, M., Lima, B., Womelsdorf, T., Oostenveld, R., Singer, W., Neuenschwander, S., & Fries, P. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1623-09.2010 · Cited by 189 · see citing works
Self-citationSteullet, P., Cabungcal, J.-H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T. P., Cuenod, M., & Do, K. Q. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3857-09.2010 · Cited by 202 · see citing works
Le Van Quyen, M., Staba, R., Bragin, A., Dickson, C., Valderrama, M., Fried, I., & Engel, J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5049-09.2010 · Cited by 189 · see citing works
Do, K. Q., Cuenod, M., & Hensch, T. K. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv065 · Cited by 158 · see citing works
Ketamine Disrupts Theta Modulation of Gamma in a Computer Model of Hippocampus
Neymotin, S. A., Lazarewicz, M. T., Sherif, M., Contreras, D., Finkel, L. H., & Lytton, W. W. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0501-11.2011 · Cited by 139 · see citing works
Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia
Grützner, C., Wibral, M., Sun, L., Rivolta, D., Singer, W., Maurer, K., & Uhlhaas, P. J. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00088 · Cited by 140 · see citing works
Self-citationWingert, J. C., & Sorg, B. A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.673210 · Cited by 129 · see citing works
Cognit activation: a mechanism enabling temporal integration in working memory
Fuster, J. M., & Bressler, S. L. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.03.005 · Cited by 139 · see citing works
Womelsdorf, T., Lima, B., Vinck, M., Oostenveld, R., Singer, W., Neuenschwander, S., & Fries, P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114223109 · Cited by 119 · see citing works
Self-citationMohan, U. R., Watrous, A. J., Miller, J. F., Lega, B. C., Sperling, M. R., Worrell, G. A., Gross, R. E., Zaghloul, K. A., Jobst, B. C., Davis, K. A., et al. (2020) · Brain Stimulation · doi:10.1016/j.brs.2020.05.009 · Cited by 120 · see citing works
Emotional Automaticity Is a Matter of Timing
Luo, Q., Holroyd, T., Majestic, C., Cheng, X., Schechter, J., & Blair, R. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.bc-5668-09.2010 · Cited by 118 · see citing works
Passie, T., Emrich, H. M., Karst, M., Brandt, S. D., & Halpern, J. H. (2012) · Drug Testing and Analysis · doi:10.1002/dta.1377 · Cited by 117 · see citing works
Sensory gating endophenotype based on its neural oscillatory pattern and heritability estimate
Hong, L. E., Summerfelt, A., Mitchell, B. D., McMahon, R. P., Wonodi, I., Buchanan, R. W., & Thaker, G. K. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.9.1008 · Cited by 115 · see citing works
Sommeijer, J.-P., & Levelt, C. N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035323 · Cited by 100 · see citing works
Burst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control
Womelsdorf, T., Ardid, S., Everling, S., & Valiante, T. A. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.046 · Cited by 113 · see citing works
Acute biphasic effects of ayahuasca.
Schenberg, E. E., Alexandre, J. F. M., Filev, R., Cravo, A. M., Sato, J. R., Muthukumaraswamy, S. D., Yonamine, M., Waguespack, M., Lomnicka, I., Barker, S. A., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137202 · Cited by 111 · see citing works
Glutamate receptor dysfunction and drug targets across models of autism spectrum disorders
Carlson, G. C. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.02.003 · Cited by 102 · see citing works
Yanagi, M., Joho, R. H., Southcott, S. A., Shukla, A. A., Ghose, S., & Tamminga, C. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.49 · Cited by 102 · see citing works
Hippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
Lucid dreaming: an age-dependent brain dissociation.
VOSS, U., FRENZEL, C., KOPPEHELE‐GOSSEL, J., & HOBSON, A. (2012) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2012.01022.x · Cited by 76 · see citing works
Advances in Electrophysiological Research
Kamarajan, C. (2015) · Alcohol Research: Current Reviews · doi:10.35946/arcr.v37.1.05 · Cited by 72 · see citing works
Sturman, D. A., & Moghaddam, B. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4210-10.2011 · Cited by 69 · see citing works
Christian, E. P., Snyder, D. H., Song, W., Gurley, D. A., Smolka, J., Maier, D. L., Ding, M., Gharahdaghi, F., Liu, X. F., Chopra, M., et al. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00539.2013 · Cited by 68 · see citing works
Steullet, P., Cabungcal, J.-H., Cuénod, M., & Do, K. Q. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00244 · Cited by 49 · see citing works
Herman, P. A., Lundqvist, M., & Lansner, A. (2013) · Brain Research · doi:10.1016/j.brainres.2013.08.002 · Cited by 47 · see citing works
McNally, J. M., McCarley, R. W., & Brown, R. E. (2013) · Current Psychiatry Reports · doi:10.1007/s11920-012-0346-z · Cited by 47 · see citing works
Craddock, T. J. A., Priel, A., & Tuszynski, J. A. (2014) · Journal of Integrative Neuroscience · doi:10.1142/s0219635214400019 · Cited by 38 · see citing works
Cohen, M. X., David, N., Vogeley, K., & Elger, C. E. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00724.x · Cited by 31 · see citing works
Coupling of gamma band activity to sleep spindle oscillations - a combined EEG/MEG study
Weber, F. D., Supp, G. G., Klinzing, J. G., Mölle, M., Engel, A. K., & Born, J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2020.117452 · Cited by 29 · see citing works
Ripple band phase precession of place cell firing during replay
Bush, D., Ólafsdóttir, H. F., Barry, C., & Burgess, N. (2022) · Current Biology · doi:10.1016/j.cub.2021.10.033 · Cited by 20 · see citing works
Electrophysiology of Schizophrenia
Winterer, G., & McCarley, R. W. (2010) · Schizophrenia · doi:10.1002/9781444327298.ch15 · Cited by 23 · see citing works
- Authors
- Fries, P., Nikolić, D., & Singer, W.
- Affiliations
- Radboud University Nijmegen (NL)
- Goethe University Frankfurt (DE)
- Corresponding author
- Fries, Pascal
- Venue
- Trends in Neurosciences
- Publisher
- Elsevier BV
- Published
- 2007-07
- Volume
- 30
- Issue
- 7
- Pages
- 309-316
- ISSN
- 0166-2236 (ISSN-L)
- OpenAlex
- W2116356678
- Cited by
- 1,044
- References
- 4
- Citations by year
- 2026: 17 · 2025: 25 · 2024: 32 · 2023: 32 · 2022: 43 · 2021: 50 · 2020: 55 · 2019: 43 · 2018: 50 · 2017: 56 · 2016: 54 · 2015: 49 · 2014: 60 · 2013: 75 · 2012: 79
- FWCI
- 5.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Neurosciences (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- European Science Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- gamma oscillations, neuronal synchronization, inhibitory interneurons, excitatory drive, phase coding, temporal coding, pyramidal neurons, neural oscillations
- MeSH terms
- Action Potentials, Animals, Brain, Humans, Interneurons, Models, Neurological, Periodicity, Reaction Time, Neural Networks, Computer, Pyramidal Cells
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