Grid cells and theta as oscillatory interference: Electrophysiological data from freely moving rats
Open accessAbstract
The oscillatory interference model (Burgess et al. (2007) Hippocampus 17:801–812) explains the generation of spatially stable, regular firing patterns by medial entorhinal cortical (mEC) grid cells in terms of the interference between velocity‐controlled oscillators (VCOs) with different preferred directions. This model predicts specific relationships between the intrinsic firing frequency and spatial scale of grid cell firing, the EEG theta frequency, and running speed (Burgess,2008). Here, we use spectral analyses of EEG and of spike autocorrelograms to estimate the intrinsic firing frequency of grid cells, and the concurrent theta frequency, in mEC Layer II in freely moving rats. The intrinsic firing frequency of grid cells increased with running speed and decreased with grid scale, according to the quantitative prediction of the model. Similarly, theta frequency increased with running speed, which was also predicted by the model. An alternative Moiré interference model (Blair et al.,2007) predicts a direction‐dependent variation in intrinsic firing frequency, which was not found. Our results suggest that interference between VCOs generates the spatial firing patterns of entorhinal grid cells according to the oscillatory interference model. They also provide specific constraints on this model of grid cell firing and have more general implications for viewing neuronal processing in terms of interfering oscillatory processes. © 2008 Wiley‐Liss, Inc.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The dependence of directional modulation on running speed is consistent with the effects of speed on the firing rate and apparent spatial organisation of grid cells.
“The dependence of directional modulation on running speed is consistent with the effects of speed on the firing rate6,10 and apparent spatial organisation (Fig. 1d) of grid cells”
From Evidence for grid cells in a human memory network (2010) · cites this paper as [10]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Phase relationship between hippocampal place units and the EEG theta rhythm
O'Keefe, J. M., & Recce, M. L. (1993) · Hippocampus · doi:10.1002/hipo.450030307 · Cited by 2,561 · see citing works
Self-citationPath integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M.-B., & Moser, E. I. (2006) · Science · doi:10.1126/science.1125572 · Cited by 1,485 · see citing works
Geometric determinants of the place fields of hippocampal neurons
O'Keefe, J., & Burgess, N. (1996) · Nature · doi:10.1038/381425a0 · Cited by 1,166 · see citing works
Self-citationKramis, R., Vanderwolf, C. H., & Bland, B. H. (1975) · Experimental Neurology · doi:10.1016/0014-4886(75)90195-8 · Cited by 791 · see citing works
Hippocampal remapping and grid realignment in entorhinal cortex
Fyhn, M., Hafting, T., Treves, A., Moser, M.-B., & Moser, E. I. (2007) · Nature · doi:10.1038/nature05601 · Cited by 749 · see citing works
An oscillatory interference model of grid cell firing
Burgess, N., Barry, C., & O'Keefe, J. M. (2007) · Hippocampus · doi:10.1002/hipo.20327 · Cited by 688 · see citing works
Self-citationA Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex
Fuhs, M. C., & Touretzky, D. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4353-05.2006 · Cited by 628 · see citing works
O'Keefe, J. M., & Burgess, N. (2005) · Hippocampus · doi:10.1002/hipo.20115 · Cited by 547 · see citing works
Self-citationExperience-dependent rescaling of entorhinal grids
Barry, C., Hayman, R. M. A., Burgess, N., & Jeffery, K. J. (2007) · Nature Neuroscience · doi:10.1038/nn1905 · Cited by 532 · see citing works
Self-citationWhishaw, I. Q., & Vanderwolf, C. H. (1973) · Behavioral Biology · doi:10.1016/s0091-6773(73)80041-0 · Cited by 508 · see citing works
Hippocampus-independent phase precession in entorhinal grid cells
Hafting, T., Fyhn, M., Bonnevie, T., Moser, M., & Moser, E. I. (2008) · Nature · doi:10.1038/nature06957 · Cited by 471 · see citing works
Alonso, A., & Klink, R. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.128 · Cited by 421 · see citing works
The Boundary Vector Cell Model of Place Cell Firing and Spatial Memory
Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O'Keefe, J., Jeffery, K., & Burgess, Ν. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.71 · Cited by 401 · see citing works
Self-citationA model of hippocampal function
Burgess, N., Recce, M., & O'Keefe, J. (1994) · Neural Networks · doi:10.1016/s0893-6080(05)80159-5 · Cited by 393 · see citing works
Self-citationTemporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing
Giocomo, L. M., Zilli, E. A., Fransén, E., & Hasselmo, M. E. (2007) · Science · doi:10.1126/science.1139207 · Cited by 377 · see citing works
Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex
Brun, V. H., Solstad, T., Kjelstrup, K. B., Fyhn, M., Witter, M. P., Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20504 · Cited by 315 · see citing works
Jensen, O. B., & Lisman, J. E. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2602 · Cited by 312 · see citing works
Maurer, A. P., VanRhoads, S. R., Sutherland, G. R., Lipa, P., & McNaughton, B. L. (2005) · Hippocampus · doi:10.1002/hipo.20114 · Cited by 308 · see citing works
Grid cells and theta as oscillatory interference: Theory and predictions
Burgess, N. (2008) · Hippocampus · doi:10.1002/hipo.20518 · Cited by 292 · see citing works
Self-citationWhat Grid Cells Convey about Rat Location
Fiete, I., Burak, Y., & Brookings, T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5684-07.2008 · Cited by 276 · see citing works
Hippocampal place cell assemblies are speed-controlled oscillators
Geisler, C. E., Robbe, D., Zugaro, M., Sirota, A., & Buzsáki, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610121104 · Cited by 273 · see citing works
Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20483 · Cited by 220 · see citing works
Hasselmo, M. E. (2008) · Hippocampus · doi:10.1002/hipo.20512 · Cited by 209 · see citing works
Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus
Huxter, J. R., Senior, T. J., Allen, K. L., & Csicsvari, J. (2008) · Nature Neuroscience · doi:10.1038/nn.2106 · Cited by 206 · see citing works
The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion
Sławińska, U., & Kasicki, S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00390-4 · Cited by 201 · see citing works
Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing
Lengyel, M., Szatmáry, Z., & Érdi, P. (2003) · Hippocampus · doi:10.1002/hipo.10116 · Cited by 162 · see citing works
Rivas, J. L. M., Gaztelu, J. M., & Garc�a-Austt, E. (1996) · Experimental Brain Research · doi:10.1007/bf00242908 · Cited by 144 · see citing works
Blair, H. T., Welday, A. C., & Zhang, K. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4724-06.2007 · Cited by 133 · see citing works
Blair, H. T., Gupta, K., & Zhang, K. (2008) · Hippocampus · doi:10.1002/hipo.20509 · Cited by 126 · see citing works
Hippocampal Neurophysiology in the Behaving Animal
O'Keefe, J. M. (2006) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195100273.003.0011 · Cited by 116 · see citing works
Self-citationComputation by oscillations: Implications of experimental data for theoretical models of grid cells
Giocomo, L. M., & Hasselmo, M. E. (2008) · Hippocampus · doi:10.1002/hipo.20501 · Cited by 72 · see citing works
Discharge Properties of Hippocampal Neurons during Performance of a Jump Avoidance Task
Lenck‐Santini, P., Fenton, A. A., & Muller, R. U. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5329-07.2008 · Cited by 50 · see citing works
Nerad, L., & Bilkey, D. K. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00199.2004 · Cited by 30 · see citing works
Episodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Flagged first, then by citations
Cited by
Sorted by citations
Evidence for grid cells in a human memory network
Doeller, C. F., Barry, C., & Burgess, N. (2010) · Nature · doi:10.1038/nature08704 · Cited by 828 · see citing works
Self-citationMizuseki, K., Sirota, A., Pastalkova, E., & Buzsáki, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.037 · Cited by 718 · see citing works
Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning
Brandon, M. P., Bogaard, A. R., Libby, C. P., Connerney, M. A., Gupta, K., & Hasselmo, M. E. (2011) · Science · doi:10.1126/science.1201652 · Cited by 407 · see citing works
A Multiplexed, Heterogeneous, and Adaptive Code for Navigation in Medial Entorhinal Cortex
Hardcastle, K., Maheswaranathan, N., Ganguli, S., & Giocomo, L. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.025 · Cited by 312 · see citing works
Pang, D. S. J., Robledo, C. J., Carr, D. R., Gent, T. C., Vyssotski, A. L., Caley, A., Zecharia, A. Y., Wisden, W., Brickley, S. G., & Franks, N. P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907228106 · Cited by 97 · see citing works
Do hippocampal pyramidal cells respond to nonspatial stimuli?
O’Keefe, J., & Krupic, J. (2021) · Physiological Reviews · doi:10.1152/physrev.00014.2020 · Cited by 93 · see citing works
Self-citationSavelli, F., & Knierim, J. J. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.188912 · Cited by 93 · see citing works
Glutamatergic synaptic integration of locomotion speed via septoentorhinal projections
Justus, D., Dalügge, D., Bothe, S., Fuhrmann, F., Hannes, C., Kaneko, H., Friedrichs, D., Sosulina, L., Schwarz, I., Elliott, D. A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4447 · Cited by 82 · see citing works
Recurrent circuits within medial entorhinal cortex superficial layers support grid cell firing
Zutshi, I., Fu, M. L., Lilascharoen, V., Leutgeb, J. K., Lim, B. K., & Leutgeb, S. (2018) · Nature Communications · doi:10.1038/s41467-018-06104-5 · Cited by 57 · see citing works
Altered Hippocampal-Prefrontal Neural Dynamics in Mouse Models of Down Syndrome
Chang, P., Bush, D., Schorge, S., Good, M., Canonica, T., Shing, N., Noy, S., Wiseman, F. K., Burgess, N., Tybulewicz, V. L. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.065 · Cited by 47 · see citing works
Self-citation
- Authors
- Jeewajee, A., Barry, C., O'Keefe, J., & Burgess, N.
- Affiliations
- University College London (GB)
- UCL Queen Square Institute of Neurology (GB)
- Corresponding author
- Burgess, N.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2008-11-19
- Volume
- 18
- Issue
- 12
- Pages
- 1175-1185
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC3173868
- OpenAlex
- W2006952639
- Cited by
- 212
- References
- 38
- Citations by year
- 2025: 12 · 2024: 8 · 2023: 9 · 2022: 6 · 2021: 8 · 2020: 16 · 2019: 28 · 2018: 10 · 2017: 10 · 2016: 10 · 2015: 13 · 2014: 13 · 2013: 19 · 2012: 16
- FWCI
- 5.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- grid cells, theta oscillations, medial entorhinal cortex, grid scale, running speed, spatial firing patterns, freely moving rats, EEG spectral analysis
- MeSH terms
- Action Potentials, Animals, Biological Clocks, Computer Simulation, Electroencephalography, Locomotion, Male, Membrane Potentials, Nerve Net, Synaptic Transmission, Neurons, Orientation, Running, Signal Processing, Computer-Assisted, Theta Rhythm, Entorhinal Cortex, Rats, Long-Evans, Rats
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
