Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning

Brandon, Mark P.; Bogaard, Andrew R.; Libby, Christopher P.; Connerney, Michael A.; Gupta, Kishan; Hasselmo, Michael E.

doi:10.1126/science.1201652

Cited by 407Memory and Neural MechanismsNeural dynamics and brain functionSpatial Cognition and Navigation

Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning

Open access

Brandon, Mark P., Bogaard, Andrew R., Libby, Christopher P., Connerney, Michael A., Gupta, Kishan, Hasselmo, Michael E.·2011·Science

DOI 10.1126/science.1201652PMC PMC3252766

Open this paper in CoChat — free account

Abstract

Inhibition of neuronal activity in the medial septum stops grid cells in the medial entorhinal cortex from firing in a grid.

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

Crossref · 10.1126/science.1201652

Cites

30 of 30 references verified0 citation errors · 0 not checkable

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?

Theta oscillations are not necessary for the emergence of the place code but play a major role in organizing place cell activity into temporal sequences that map available space and episodic events.
“Theta oscillations—although not necessary for the emergence of the place code21,22—play a major role in organizing place cell activity into temporal sequences that map the available space (and, similarly, episodic events4,23,24).”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [21]
The paper’s discussion (page not provided) says that companion findings showed spared hippocampal place-cell specificity during septal inactivation, and that the combined data suggest grid-cell periodicity is not essential for place-cell responses in familiar environments. That supports a narrower point than the attributed claim: it does not directly establish that theta is unnecessary for the emergence of a place code. The sentence’s separate claim about temporal sequences is attached to other citations, not this source. (LLM, conf=0.84)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809 · 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
Spatial representation in the entorhinal cortex
Fyhn, M., Molden, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2004) · Science · doi:10.1126/science.1099901 · Cited by 1,339 · see citing works
Representation of Geometric Borders in the Entorhinal Cortex
Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B., & Moser, E. I. (2008) · Science · doi:10.1126/science.1166466 · Cited by 1,213 · see citing works
Loss of Hippocampal Theta Rhythm Results in Spatial Memory Deficit in the Rat
Winson, J. (1978) · Science · doi:10.1126/science.663646 · Cited by 857 · see citing works
Boundary Vector Cells in the Subiculum of the Hippocampal Formation
Lever, C., Burton, S., Jeewajee, A., O'Keefe, J., & Burgess, N. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1319-09.2009 · Cited by 753 · 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
Development of the Spatial Representation System in the Rat
Langston, R. F., Ainge, J. A., Couey, J. J., Canto, C. B., Bjerknes, T. L., Witter, M. P., Moser, E. I., & Moser, M. (2010) · Science · doi:10.1126/science.1188210 · Cited by 667 · see citing works
Development of the Hippocampal Cognitive Map in Preweanling Rats
Wills, T. J., Cacucci, F., Burgess, N., & O'Keefe, J. (2010) · Science · doi:10.1126/science.1188224 · Cited by 616 · see citing works
Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells
O'Keefe, J. M., & Burgess, N. (2005) · Hippocampus · doi:10.1002/hipo.20115 · Cited by 547 · see citing works
Grid cells in pre- and parasubiculum
Boccara, C. N., Sargolini, F., Thoresen, V. H., Solstad, T., Witter, M. P., Moser, E. I., & Moser, M. (2010) · Nature Neuroscience · doi:10.1038/nn.2602 · Cited by 518 · 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
Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats
Mitchell, S., Rawlins, J. N. P., Steward, O., & Olton, D. S. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00292.1982 · Cited by 401 · see citing works
The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations
Koenig, J., Linder, A. N., Leutgeb, J. K., & Leutgeb, S. (2011) · Science · doi:10.1126/science.1201685 · Cited by 378 · see citing works
Temporal 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
Self-citation
Septo-hippocampal connections and the hippocampal theta rhythm
Rawlins, J. N. P., Feldon, J., & Gray, J. A. B. (1979) · Experimental Brain Research · doi:10.1007/bf01474253 · Cited by 228 · see citing works
Reversible inactivation of the medial septum differentially affects two forms of learning in rats
Mizumori, S. J. Y., Perez, G. M., Alvarado, M. C., Barnes, C. A., & McNaughton, B. L. (1990) · Brain Research · doi:10.1016/0006-8993(90)90188-h · Cited by 227 · see citing works
Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus
Mizumori, S., McNaughton, B. L., Barnes, C. A., & Fox, K. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03915.1989 · Cited by 223 · see citing works
A metric for space
Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20483 · Cited by 220 · see citing works
Grid cells and theta as oscillatory interference: Electrophysiological data from freely moving rats
Jeewajee, A., Barry, C., O'Keefe, J., & Burgess, N. (2008) · Hippocampus · doi:10.1002/hipo.20510 · Cited by 212 · see citing works
Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after‐spike dynamics
Navratilova, Z., Giocomo, L. M., Fellous, J., Hasselmo, M. E., & McNaughton, B. L. (2011) · Hippocampus · doi:10.1002/hipo.20939 · Cited by 160 · see citing works
Self-citation
Local modulation of basal forebrain: effects on working and reference memory
Givens, B. S., & Olton, D. S. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03578.1994 · Cited by 152 · see citing works
Theta Modulation in the Medial and the Lateral Entorhinal Cortices
Deshmukh, S. S., Yoganarasimha, D., Voicu, H., & Knierim, J. J. (2010) · Journal of Neurophysiology · doi:10.1152/jn.01141.2009 · Cited by 149 · see citing works
Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat
Chrobak, J. J., Stackman, R. W., & Walsh, T. J. (1989) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(89)90472-x · Cited by 148 · see citing works
Medial septal control of theta-correlated unit firing in the entorhinal cortex of awake rats
Jeffery, K. J., Donnett, J. G., & O'Keefe, J. M. (1995) · Neuroreport · doi:10.1097/00001756-199511000-00017 · Cited by 85 · see citing works
Interactions between 192-IgG saporin and intraseptal cholinergic and GABAergic drugs: Role of cholinergic medial septal neurons in spatial working memory.
Pang, K. C. H., & Nocera, R. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.2.265 · Cited by 63 · see citing works
Interactions between 192-IgG saporin and intraseptal cholinergic and GABAergic drugs: Role of cholinergic medial septal neurons in spatial working memory.
Pang, K. C. H., & Nocera, R. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.2.265 · Cited by 57 · see citing works
Medial septum lesions disrupt exploratory trip organization: Evidence for septohippocampal involvement in dead reckoning
Martin, M. M., Horn, K. L., Kusman, K. J., & Wallace, D. G. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.10.007 · Cited by 41 · see citing works
Untitled work
(1996) · doi:10.1002/(sici)1098-1063(1996)6:2

Flagged first, then by citations

Research works printed but not linked: 2

[5]O’Keefe J Recce ML Hippocampus 3 317 1993 8353611
[11]O’Keefe J Burgess N Hippocampus 15 853 2005 16145693 PMC2677681

Sorted by citations

Spatial representation in the hippocampal formation: a history
Moser, E. I., Moser, M.-B., & McNaughton, B. L. (2017) · Nature Neuroscience · doi:10.1038/nn.4653 · Cited by 560 · see citing works
Mechanisms and functions of theta rhythms
Colgin, L. L. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170330 · Cited by 559 · see citing works
A map of visual space in the primate entorhinal cortex
Killian, N. J., Jutras, M. J., & Buffalo, E. A. (2012) · Nature · doi:10.1038/nature11587 · Cited by 471 · see citing works
CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation
Neunuebel, J. P., & Knierim, J. J. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.017 · Cited by 454 · see citing works
Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex
Deshmukh, S. S., & Knierim, J. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00069 · Cited by 454 · see citing works
Grid cells without theta oscillations in the entorhinal cortex of bats
Yartsev, M. M., Witter, M. P., & Ulanovsky, N. (2011) · Nature · doi:10.1038/nature10583 · Cited by 391 · see citing works
Vestibular pathways involved in cognition.
Hitier, M., Besnard, S., & Smith, P. F. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00059 · Cited by 394 · see citing works
The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations
Koenig, J., Linder, A. N., Leutgeb, J. K., & Leutgeb, S. (2011) · Science · doi:10.1126/science.1201685 · Cited by 378 · see citing works
Grid cells and cortical representation
Moser, E. I., Roudi, Y., Witter, M. P., Kentros, C., Bonhoeffer, T., & Moser, M.-B. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3766 · Cited by 335 · see citing works
Grid cells require excitatory drive from the hippocampus
Bonnevie, T., Dunn, B. A., Fyhn, M., Hafting, T., Derdikman, D., Kubie, J. L., Roudi, Y., Moser, E. I., & Moser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3311 · Cited by 341 · see citing works
Theta sequences are essential for internally generated hippocampal firing fields
Wang, Y., Romani, S., Lustig, B. R., Leonardo, A. M., & Pastalkova, E. (2014) · Nature Neuroscience · doi:10.1038/nn.3904 · Cited by 314 · see citing works
Membrane potential dynamics of grid cells
Domnisoru, C., Kinkhabwala, A. A., & Tank, D. W. (2013) · Nature · doi:10.1038/nature11973 · Cited by 309 · see citing works
Specific evidence of low-dimensional continuous attractor dynamics in grid cells
Yoon, K., Buice, M. A., Barry, C., Hayman, R., Burgess, N., & Fiete, I. R. (2013) · Nature Neuroscience · doi:10.1038/nn.3450 · Cited by 296 · see citing works
Internally organized mechanisms of the head direction sense
Peyrache, A., Lacroix, M. M., Petersen, P. C., & Buzsáki, G. (2015) · Nature Neuroscience · doi:10.1038/nn.3968 · Cited by 274 · see citing works
Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields
Pastoll, H., Solanka, L., van Rossum, M. C. W., & Nolan, M. F. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.032 · Cited by 278 · see citing works
Cellular mechanisms of spatial navigation in the medial entorhinal cortex
Schmidt‐Hieber, C., & Häusser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3340 · Cited by 273 · see citing works
Tau Pathology Induces Excitatory Neuron Loss, Grid Cell Dysfunction, and Spatial Memory Deficits Reminiscent of Early Alzheimer’s Disease
Fu, H., Rodriguez, G. A., Herman, M., Emrani, S., Nahmani, E., Barrett, G., Figueroa, H. Y., Goldberg, E., Hussaini, S. A., & Duff, K. E. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.023 · Cited by 264 · see citing works
Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory
Jacobs, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0304 · Cited by 259 · see citing works
Theta rhythm and the encoding and retrieval of space and time
Hasselmo, M. E., & Stern, C. E. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.022 · Cited by 261 · see citing works
Self-citation
Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation
Geva‐Sagiv, M., Las, L., Yovel, Y., & Ulanovsky, N. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3888 · Cited by 262 · see citing works
Direct Electrical Stimulation of the Human Entorhinal Region and Hippocampus Impairs Memory
Jacobs, J., Miller, J. F., Lee, S. A., Coffey, T., Watrous, A. J., Sperling, M. R., Sharan, A. D., Worrell, G. A., Berry, B. M., Lega, B. C., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.10.062 · Cited by 244 · see citing works
Disruption of the head direction cell network impairs the parahippocampal grid cell signal
Winter, S. S., Clark, B. J., & Taube, J. S. (2015) · Science · doi:10.1126/science.1259591 · Cited by 247 · see citing works
The representation of space in the brain
Grieves, R. M., & Jeffery, K. J. (2016) · Behavioural Processes · doi:10.1016/j.beproc.2016.12.012 · Cited by 230 · see citing works
Computational Models of Grid Cells
Giocomo, L. M., Moser, M., & Moser, E. I. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.023 · Cited by 231 · see citing works
Attractor Dynamics of Spatially Correlated Neural Activity in the Limbic System
Knierim, J. J., & Zhang, K. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150351 · Cited by 222 · see citing works
Specific basal forebrain-cortical cholinergic circuits coordinate cognitive operations
Záborszky, L., Gombkoto, P., Varsanyi, P., Gielow, M. R., Poe, G., Role, L. W., Ananth, M., Rajebhosale, P., Talmage, D. A., Hasselmo, M. E., et al. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1676-18.2018 · Cited by 202 · see citing works
Self-citation
Egocentric boundary vector tuning of the retrosplenial cortex
Alexander, A. S., Carstensen, L. C., Hinman, J. R., Raudies, F., Chapman, G. W., & Hasselmo, M. E. (2020) · Science Advances · doi:10.1126/sciadv.aaz2322 · Cited by 197 · see citing works
Self-citation
Ventral Midline Thalamus Is Critical for Hippocampal-Prefrontal Synchrony and Spatial Working Memory
Hallock, H. L., Wang, A., & Griffin, A. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0991-16.2016 · Cited by 197 · see citing works
Our sense of direction: progress, controversies and challenges
Cullen, K., & Taube, J. (2017) · Nature Neuroscience · doi:10.1038/nn.4658 · Cited by 196 · see citing works
A Unified Mathematical Framework for Coding Time, Space, and Sequences in the Hippocampal Region
Howard, M. W., MacDonald, C. J., Tiganj, Z., Shankar, K. H., Du, Q., Hasselmo, M. E., & Eichenbaum, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5808-12.2014 · Cited by 195 · see citing works
Self-citation
Impaired path integration in mice with disrupted grid cell firing
Gil, M., Ancau, M., Schlesiger, M. I., Neitz, A., Allen, K., De Marco, R. J., & Monyer, H. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0039-3 · Cited by 174 · see citing works
Models of place and grid cell firing and theta rhythmicity
Burgess, N., & O'Keefe, J. M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.07.002 · Cited by 193 · see citing works
Cholinergic modulation of cognitive processing: insights drawn from computational models
Newman, E. L., Gupta, K., Climer, J. R., Monaghan, C. K., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00024 · Cited by 185 · see citing works
Self-citation
Grid-Layout and Theta-Modulation of Layer 2 Pyramidal Neurons in Medial Entorhinal Cortex
Ray, S., Naumann, R. K., Burgalossi, A., Tang, Q., Schmidt, H., & Brecht, M. (2014) · Science · doi:10.1126/science.1243028 · Cited by 179 · see citing works
Local and Distant Input Controlling Excitation in Layer II of the Medial Entorhinal Cortex
Fuchs, E. C., Neitz, A., Pinna, R., Melzer, S., Caputi, A., & Monyer, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.029 · Cited by 179 · see citing works
The medial entorhinal cortex is necessary for temporal organization of hippocampal neuronal activity
Schlesiger, M. I., Cannova, C. C., Boublil, B. L., Hales, J. B., Mankin, E. A., Brandon, M. P., Leutgeb, J. K., Leibold, C., & Leutgeb, S. (2015) · Nature Neuroscience · doi:10.1038/nn.4056 · Cited by 165 · see citing works
Self-citation
Neural Mechanisms of Self-Location
Barry, C., & Burgess, N. (2014) · Current Biology · doi:10.1016/j.cub.2014.02.049 · Cited by 168 · see citing works
Reconciling the different faces of hippocampal theta: The role of theta oscillations in cognitive, emotional and innate behaviors
Korotkova, T. M., Ponomarenko, A. A., Monaghan, C. K., Poulter, S. L., Cacucci, F., Wills, T. J., Hasselmo, M. E., & Lever, C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.004 · Cited by 159 · see citing works
Self-citation
Optogenetic Activation of Septal Glutamatergic Neurons Drive Hippocampal Theta Rhythms
Robinson, J. C., Manseau, F., Ducharme, G., Amilhon, B., Vigneault, É., Mestikawy, S. E., & Williams, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2141-15.2016 · Cited by 159 · see citing works
Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus
Somogyi, P., Katona, L., Klausberger, T., Lasztóczi, B., & Viney, T. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0518 · Cited by 158 · see citing works
Multiple Running Speed Signals in Medial Entorhinal Cortex
Hinman, J. R., Brandon, M. P., Climer, J. R., Chapman, G. W., & Hasselmo, M. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.027 · Cited by 156 · see citing works
Self-citation
New and Distinct Hippocampal Place Codes Are Generated in a New Environment during Septal Inactivation
Brandon, M. P., Koenig, J., Leutgeb, J. K., & Leutgeb, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.013 · Cited by 145 · see citing works
Self-citation
What do grid cells contribute to place cell firing?
Bush, D., Barry, C., & Burgess, N. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2013.12.003 · Cited by 156 · see citing works
Synaptic Targets of Medial Septal Projections in the Hippocampus and Extrahippocampal Cortices of the Mouse
Ünal, G., Joshi, A., Viney, T. J., Kis, V., & Somogyi, P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2639-15.2015 · Cited by 149 · see citing works
Acetylcholine Release in Prefrontal Cortex Promotes Gamma Oscillations and Theta–Gamma Coupling during Cue Detection
Howe, W. M., Gritton, H. J., Lusk, N. A., Roberts, E. A., Hetrick, V. L., Berke, J. D., & Sarter, M. F. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2737-16.2017 · Cited by 147 · see citing works
A Framework for Intelligence and Cortical Function Based on Grid Cells in the Neocortex
Hawkins, J., Lewis, M., Klukas, M., Purdy, S., & Ahmad, S. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00121 · Cited by 144 · see citing works
Cholinergic modulation of spatial learning, memory and navigation
Solari, N., & Hangya, B. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14089 · Cited by 139 · see citing works
Complementary Functional Organization of Neuronal Activity Patterns in the Perirhinal, Lateral Entorhinal, and Medial Entorhinal Cortices
Keene, C. S., Bladon, J. H., McKenzie, S., Liu, C. D., O'Keefe, J., & Eichenbaum, H. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4368-15.2016 · Cited by 131 · see citing works
A Hybrid Oscillatory Interference/Continuous Attractor Network Model of Grid Cell Firing
Bush, D., & Burgess, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4017-13.2014 · Cited by 138 · see citing works
A novel somatosensory spatial navigation system outside the hippocampal formation
Long, X., & Zhang, S. (2021) · Cell Research · doi:10.1038/s41422-020-00448-8 · Cited by 136 · see citing works
Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference
Welday, A. C., Shlifer, I. G., Bloom, M. L., Zhang, K., & Blair, H. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0712-11.2011 · Cited by 134 · see citing works
A Developmental Switch in Place Cell Accuracy Coincides with Grid Cell Maturation
Muessig, L., Hauser, J., Wills, T. J., & Cacucci, F. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.011 · Cited by 130 · see citing works
Segregation of cortical head direction cell assemblies on alternating theta cycles
Brandon, M. P., Bogaard, A. R., Schultheiss, N. W., & Hasselmo, M. E. (2013) · Nature Neuroscience · doi:10.1038/nn.3383 · Cited by 124 · see citing works
Self-citation
Medial Entorhinal Cortex Selectively Supports Temporal Coding by Hippocampal Neurons
Robinson, N. T. M., Priestley, J. B., Rueckemann, J. W., Garcia, A. D., Smeglin, V. A., Marino, F., & Eichenbaum, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.003 · Cited by 119 · see citing works
Neural circuits underlying the generation of theta oscillations
Pignatelli, M., Beyeler, A., & Leinekugel, X. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.09.007 · Cited by 124 · see citing works
Frequency of theta rhythm is controlled by acceleration, but not speed, in running rats
Kropff, E., Carmichael, J. E., Moser, E. I., & Moser, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.017 · Cited by 125 · see citing works
DC-shifts in amplitude in-field generated by an oscillatory interference model of grid cell firing
Onslow, A. C. E., Hasselmo, M. E., & Newman, E. L. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00001 · Cited by 123 · see citing works
Self-citation
How You Get There From Here: Interaction of Visual Landmarks and Path Integration in Human Navigation
Zhao, M., & Warren, W. H. (2015) · Psychological Science · doi:10.1177/0956797615574952 · Cited by 112 · see citing works
Novelty and Anxiolytic Drugs Dissociate Two Components of Hippocampal Theta in Behaving Rats
Wells, C. E., Amos, D. P., Jeewajee, A., Douchamps, V., Rodgers, J., O'Keefe, J. M., Burgess, N., & Lever, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5040-12.2013 · Cited by 116 · see citing works
Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum
Howe, M. W., Atallah, H. E., McCool, A. D., Gibson, D. J., & Graybiel, A. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113158108 · Cited by 116 · see citing works
Human hippocampal theta power indicates movement onset and distance travelled
Bush, D., Bisby, J. A., Bird, C. M., Gollwitzer, S., Rodionov, R., Diehl, B., McEvoy, A. W., Walker, M. C., & Burgess, N. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708716114 · Cited by 112 · see citing works
Locally ordered representation of 3D space in the entorhinal cortex
Ginosar, G., Aljadeff, J., Burak, Y., Sompolinsky, H., Las, L., & Ulanovsky, N. (2021) · Nature · doi:10.1038/s41586-021-03783-x · Cited by 111 · see citing works
A Model of Grid Cell Development through Spatial Exploration and Spike Time-Dependent Plasticity
Widloski, J., & Fiete, I. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.018 · Cited by 106 · see citing works
Specific Impairment of “What-Where-When” Episodic-Like Memory in Experimental Models of Temporal Lobe Epilepsy
Inostroza, M., Brotons‐Mas, J. R., Laurent, F., Cid, E., & de la Prida, L. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0957-13.2013 · Cited by 101 · see citing works
Transgenically Targeted Rabies Virus Demonstrates a Major Monosynaptic Projection from Hippocampal Area CA2 to Medial Entorhinal Layer II Neurons
Rowland, D. C., Weible, A. P., Wickersham, I. R., Wu, H., Mayford, M., Witter, M. P., & Kentros, C. G. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1046-13.2013 · Cited by 101 · see citing works
Hippocampal Neural Circuits Respond to Optogenetic Pacing of Theta Frequencies by Generating Accelerated Oscillation Frequencies
Zutshi, I., Brandon, M. P., Fu, M. L., Donegan, M. L., Leutgeb, J. K., & Leutgeb, S. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.061 · Cited by 103 · see citing works
Self-citation
Hippocampal Remapping and Its Entorhinal Origin
Latuske, P., Kornienko, O., Kohler, L., & Allen, K. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00253 · Cited by 102 · see citing works
A Novel Mechanism for the Grid-to-Place Cell Transformation Revealed by Transgenic Depolarization of Medial Entorhinal Cortex Layer II
Kanter, B. R., Lykken, C. M., Avesar, D., Weible, A. P., Dickinson, J. R., Dunn, B. A., Borgesius, N. Z., Roudi, Y., & Kentros, C. G. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.001 · Cited by 100 · see citing works
Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies
Petersen, P., & Buzsáki, G. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.023 · Cited by 92 · see citing works
Origin and role of path integration in the cognitive representations of the hippocampus: computational insights into open questions
Savelli, F., & Knierim, J. J. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.188912 · Cited by 93 · see citing works
Diversity and function of corticopetal and corticofugal GABAergic projection neurons
Melzer, S., & Monyer, H. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0344-9 · Cited by 94 · see citing works
Vestibular control of entorhinal cortex activity in spatial navigation
Jacob, P.-Y., Poucet, B., Liberge, M., Save, É., & Sargolini, F. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00038 · Cited by 93 · see citing works
Grid Cells and Place Cells: An Integrated View of their Navigational and Memory Function
Sanders, H., Rennó‐Costa, C., Idiart, M., & Lisman, J. E. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.10.004 · Cited by 88 · see citing works
The role of replay and theta sequences in mediating hippocampal‐prefrontal interactions for memory and cognition
Zielinski, M. C., Tang, W., & Jadhav, S. P. (2017) · Hippocampus · doi:10.1002/hipo.22821 · Cited by 95 · see citing works
Functional properties of stellate cells in medial entorhinal cortex layer II
Rowland, D. C., Obenhaus, H. A., Skytøen, E. R., Zhang, Q., Kentros, C. G., Moser, E. I., & Moser, M. (2018) · eLife · doi:10.7554/elife.36664 · Cited by 90 · see citing works
First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus)
Mayer, U., Salva, O. R., & Vallortígara, G. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.031 · Cited by 80 · see citing works
Transient inactivation of the thalamic nucleus reuniens and rhomboid nucleus produces deficits of a working-memory dependent tactile-visual conditional discrimination task.
Hallock, H. L., Wang, A., Shaw, C. L., & Griffin, A. L. (2013) · Behavioral Neuroscience · doi:10.1037/a0034653 · Cited by 85 · see citing works
Transformation of the head-direction signal into a spatial code
Peyrache, A., Schieferstein, N., & Buzsáki, G. (2017) · Nature Communications · doi:10.1038/s41467-017-01908-3 · Cited by 83 · see citing works
A Canonical Circuit for Generating Phase-Amplitude Coupling
Onslow, A. C. E., Jones, M. W., & Bogacz, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102591 · Cited by 83 · see citing works
Passive Transport Disrupts Grid Signals in the Parahippocampal Cortex
Winter, S. S., Mehlman, M. L., Clark, B. J., & Taube, J. S. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.034 · Cited by 81 · see citing works
GABAergic Projections from the Medial Septum Selectively Inhibit Interneurons in the Medial Entorhinal Cortex
Gonzalez‐Sulser, A., Parthier, D., Candela, A., McClure, C., Pastoll, H., Garden, D. L. F., Sürmeli, G., & Nolan, M. F. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1612-14.2014 · Cited by 81 · see citing works
Phase coding by grid cells in unconstrained environments: two‐dimensional phase precession
Climer, J. R., Newman, E. L., & Hasselmo, M. E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12256 · Cited by 78 · see citing works
Self-citation
How the Brain’s Navigation System Shapes Our Visual Experience
Nau, M., Julian, J. B., & Doeller, C. F. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.06.008 · Cited by 79 · see citing works
Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells
Barry, C., Heys, J. G., & Hasselmo, M. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00005 · Cited by 79 · see citing works
Self-citation
The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation
Butler, W. N., Smith, K. S., van der Meer, M. A. A., & Taube, J. S. (2017) · Current Biology · doi:10.1016/j.cub.2017.03.033 · Cited by 77 · see citing works
Anatomical organization of presubicular head-direction circuits
Preston‐Ferrer, P., Coletta, S., Frey, M., & Burgalossi, A. (2016) · eLife · doi:10.7554/elife.14592 · Cited by 74 · see citing works
Spatial and memory circuits in the medial entorhinal cortex
Sasaki, T., Leutgeb, S., & Leutgeb, J. K. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.10.008 · Cited by 73 · see citing works
Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome
Cha, Y., Chakrapani, S., Craig, A. B., & Baloh, R. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049560 · Cited by 72 · see citing works
Head direction is coded more strongly than movement direction in a population of entorhinal neurons
Raudies, F., Brandon, M. P., Chapman, G. W., & Hasselmo, M. E. (2014) · Brain Research · doi:10.1016/j.brainres.2014.10.053 · Cited by 71 · see citing works
Self-citation
Human brain dynamics in active spatial navigation
Do, T., Lin, C., & Gramann, K. (2021) · Scientific Reports · doi:10.1038/s41598-021-92246-4 · Cited by 72 · see citing works
Path integration in normal aging and Alzheimer’s disease
Segen, V., Ying, J., Morgan, E., Brandon, M. P., & Wolbers, T. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.11.001 · Cited by 66 · see citing works
Self-citation
Medial septum regulates the hippocampal spatial representation
Mamad, O., McNamara, H. M., Reilly, R. B., & Tsanov, M. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00166 · Cited by 69 · see citing works
All Layers of Medial Entorhinal Cortex Receive Presubicular and Parasubicular Inputs
Canto, C. B., Koganezawa, N., Beed, P. S., Moser, E. I., & Witter, M. P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3526-12.2012 · Cited by 71 · see citing works
Differential Representation of Landmark and Self-Motion Information along the CA1 Radial Axis: Self-Motion Generated Place Fields Shift toward Landmarks during Septal Inactivation
Fattahi, M., Sharif, F., Geiller, T. C., & Royer, S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3211-17.2018 · Cited by 69 · see citing works
Irregular distribution of grid cell firing fields in rats exploring a 3D volumetric space
Grieves, R. M., Jedidi-Ayoub, S., Mishchanchuk, K., Liu, A., Renaudineau, S., Duvelle, É., & Jeffery, K. J. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00907-4 · Cited by 69 · see citing works
Target selectivity of septal cholinergic neurons in the medial and lateral entorhinal cortex
Desikan, S., Koser, D. E., Neitz, A., & Monyer, H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716531115 · Cited by 69 · see citing works
Grid-like hexadirectional modulation of human entorhinal theta oscillations
Maidenbaum, S., Miller, J. F., Stein, J. M., & Jacobs, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1805007115 · Cited by 71 · see citing works
Neurons in Primate Entorhinal Cortex Represent Gaze Position in Multiple Spatial Reference Frames
Meister, M. L. R., & Buffalo, E. A. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2432-17.2018 · Cited by 68 · see citing works
Network mechanisms of grid cells
Moser, E. I., Moser, M., & Roudi, Y. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0511 · Cited by 65 · see citing works
Thalamocortical interactions in cognition and disease: The mediodorsal and anterior thalamic nuclei
Perry, B. A. L., Lomi, E., & Mitchell, A. S. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.032 · Cited by 62 · see citing works

The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations
Koenig, J., Linder, A. N., Leutgeb, J. K., & Leutgeb, S. (2011) · Science · doi:10.1126/science.1201685 · Cited by 378 · see citing works
How reduction of theta rhythm by medial septum inactivation may covary with disruption of entorhinal grid cell responses due to reduced cholinergic transmission
Pilly, P. K., & Grossberg, S. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00173 · Cited by 11 · see citing works
Segregation of cortical head direction cell assemblies on alternating theta cycles
Br, M. P., Bogaard, A. R., Schultheiss, N. W., & Michael, E. (2016)
Self-citation
Reviewed by:
Pilly, P. K., Grossberg, S., & Williams, S. (2013)
Theta oscillations, timing and cholinergic modulation in the rodent hippocampal circuit
Climer, J. R. (2016) · OpenBU (Boston University)

Authors: Brandon, M. P., Bogaard, A. R., Libby, C. P., Connerney, M. A., Gupta, K., & Hasselmo, M. E.
Affiliations: Boston University (US)
Corresponding author: Brandon, Mark P.
Hasselmo, Michael E.
ORCID: Brandon, Mark P.
Bogaard, Andrew R.
Libby, Christopher P.
Connerney, Michael A.
Gupta, Kishan
Hasselmo, Michael E.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2011-04-29
Volume: 332
Issue: 6029
Pages: 595-599
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1201652
PMC: PMC3252766
OpenAlex: W2037343688
Cited by: 407
References: 29
Citations by year: 2026: 12 · 2025: 19 · 2024: 25 · 2023: 17 · 2022: 19 · 2021: 24 · 2020: 22 · 2019: 18 · 2018: 30 · 2017: 36 · 2016: 21 · 2015: 34 · 2014: 45 · 2013: 43 · 2012: 25
FWCI: 21.10
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.sciencemag.org/site/feature/contribinfo/prep/license.xhtml (vor)
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Office of Naval Research (N00014-10-1-0936)
National Institute of Mental Health (R01 MH60013, MH61492)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
Keywords: grid cells, theta oscillations, medial entorhinal cortex, medial septum, muscimol inactivation, head direction cells, spatial periodicity, directional tuning, spatial coding, rhythmicity, rats
MeSH terms: Animals, Male, Membrane Potentials, Motor Activity, Muscimol, Nerve Net, Neural Pathways, Neurons, Periodicity, Septum Pellucidum, Space Perception, 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

Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks