Grid scale drives the scale and long-term stability of place maps
Open accessAbstract
Medial entorhinal cortex (MEC) grid cells fire at regular spatial intervals and project to the hippocampus, where place cells are active in spatially restricted locations. One feature of the grid population is the increase in grid spatial scale along the dorsal-ventral MEC axis. However, the difficulty in perturbing grid scale without impacting the properties of other functionally defined MEC cell types has obscured how grid scale influences hippocampal coding and spatial memory. Here we use a targeted viral approach to knock out HCN1 channels selectively in MEC, causing the grid scale to expand while leaving other MEC spatial and velocity signals intact. Grid scale expansion resulted in place scale expansion in fields located far from environmental boundaries, reduced long-term place field stability and impaired spatial learning. These observations, combined with simulations of a grid-to-place cell model and position decoding of place cells, illuminate how grid scale impacts place coding and spatial memory.
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?
If grid cell outputs are available, CSCG can use those as additional sensations, which would speed up learning in the middle portions of empty arenas where unique sensations are not available, and help stabilize the place fields away from the boundaries or other landmark cues.
“If grid cell outputs are available, CSCG can use those as additional sensations. This would speed up learning in the middle portions of empty arenas where unique sensations are not available, and it will also help stabilize the place fields away from the boundaries or other landmark cues (56, 57), consistent with the idea of grid cells providing an optional scaffolding for place cells (58).”
From Space is a latent sequence: A theory of the hippocampus (2024) · cites this paper as [56]
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
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
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
Path 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
The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells
Muller, R., & Kubie, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01951.1987 · Cited by 1,581 · 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
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
Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles
Leutgeb, S., Leutgeb, J. K., Barnes, C. A., Moser, E. I., McNaughton, B. L., & Moser, M. (2005) · Science · doi:10.1126/science.1114037 · Cited by 911 · 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
The entorhinal grid map is discretized
Stensola, H., Stensola, T., Solstad, T., Frøland, K., Moser, M., & Moser, E. I. (2012) · Nature · doi:10.1038/nature11649 · Cited by 706 · see citing works
Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus
Hargreaves, E. L., Rao, G., Lee, I., & Knierim, J. J. (2005) · Science · doi:10.1126/science.1110449 · Cited by 685 · see citing works
Speed cells in the medial entorhinal cortex
Kropff, E., Carmichael, J. E., Moser, M.-B., & Moser, E. I. (2015) · Nature · doi:10.1038/nature14622 · Cited by 668 · 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
Attractor Dynamics in the Hippocampal Representation of the Local Environment
Wills, T. J., Lever, C., Cacucci, F., Burgess, N., & O'Keefe, J. M. (2005) · Science · doi:10.1126/science.1108905 · Cited by 643 · see citing works
Quantitative measures of cluster quality for use in extracellular recordings
Schmitzer-Torbert, N. C., Jackson, J. C., Henze, D. A., Harris, K., & Redish, A. D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.09.066 · Cited by 642 · see citing works
A 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
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
Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry
Brun, V. H., Otnæss, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I. (2002) · Science · doi:10.1126/science.1071089 · Cited by 606 · see citing works
Anatomical organization of the parahippocampal-hippocampal network
WITTER, M. P., WOUTERLOOD, F. G., NABER, P. A., & VAN HAEFTEN, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06716.x · Cited by 567 · see citing works
Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons
Bittner, K. C., Grienberger, C., Vaidya, S. P., Milstein, A. D., Macklin, J. J., Suh, J., Tonegawa, S., & Magee, J. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4062 · Cited by 540 · see citing works
Chapter 1 Chapter Neurons, numbers and the hippocampal network
Amaral, D. G., Ishizuka, N., & Claiborne, B. J. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61237-6 · Cited by 523 · see citing works
From grid cells to place cells: A mathematical model
Solstad, T., Moser, E. I., & Einevoll, G. T. (2006) · Hippocampus · doi:10.1002/hipo.20244 · Cited by 477 · see citing works
A Behavioral Role for Dendritic Integration
Nolan, M. F., Malleret, G., Dudman, J. T., Buhl, D. L., Santoro, B., Gibbs, E., Vronskaya, S., Buzsáki, G., Siegelbaum, S. A., Kandel, E. R., et al. (2004) · Cell · doi:10.1016/j.cell.2004.11.020 · Cited by 472 · 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 cell symmetry is shaped by environmental geometry
Krupic, J., Bauža, M., Burton, S., Barry, C., & O'Keefe, J. M. (2015) · Nature · doi:10.1038/nature14153 · Cited by 374 · see citing works
Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex
Brun, V. H., Leutgeb, S., Wu, H., Schwarcz, R. M., Witter, M. P., Moser, E. I., & Moser, M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.034 · Cited by 364 · see citing works
Nolan, M. F., Malleret, G., Lee, K. H., Gibbs, E., Dudman, J. T., Santoro, B., Yin, D., Thompson, R. F., Siegelbaum, S. A., Kandel, E. R., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00884-5 · Cited by 320 · 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
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
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
Self-citationHippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts
Mankin, E. A., Diehl, G. W., Sparks, F. T., Leutgeb, S., & Leutgeb, J. K. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.001 · Cited by 279 · see citing works
What 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
Nolan, M. F., Malleret, G., Dudman, J. T., Buhl, D. L., Santoro, B., GIBBS, E., Vronskaya, S., Buzsáki, G., Siegelbaum, S. A., & Kandel, E. R. (2004) · Cell · doi:10.1016/s0092-8674(04)01055-4 · Cited by 274 · see citing works
Environmental Boundaries as an Error Correction Mechanism for Grid Cells
Hardcastle, K., Ganguli, S., & Giocomo, L. M. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.039 · Cited by 265 · see citing works
Self-citationOptogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity
Zhang, S., Ye, J., Miao, C., Tsao, A., Cerniauskas, I., Ledergerber, D., Moser, M., & Moser, E. I. (2013) · Science · doi:10.1126/science.1232627 · Cited by 256 · see citing works
Neuronal Tuning: To Sharpen or Broaden?
Zhang, K., & B, T. J. S. A. (1999) · Neural Computation · doi:10.1162/089976699300016809 · Cited by 253 · see citing works
Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior
Lee, D., Lin, B., & Lee, A. K. (2012) · Science · doi:10.1126/science.1221489 · Cited by 251 · see citing works
Shearing-induced asymmetry in entorhinal grid cells
Stensola, T., Stensola, H., Moser, M., & Moser, E. (2015) · Nature · doi:10.1038/nature14151 · Cited by 231 · see citing works
Grid cell firing patterns signal environmental novelty by expansion
Barry, C., Ginzberg, L. L., O'Keefe, J. M., & Burgess, N. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209918109 · Cited by 219 · see citing works
Diehl, G. W., Hon, O. J., Leutgeb, S., & Leutgeb, J. K. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.004 · Cited by 204 · 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
Connecting multiple spatial scales to decode the population activity of grid cells
Stemmler, M., Mathis, A., & Herz, A. V. M. (2015) · Science Advances · doi:10.1126/science.1500816 · Cited by 163 · see citing works
Grid Cells Use HCN1 Channels for Spatial Scaling
Giocomo, L. M., Hussaini, S. A., Fan, Z., Kandel, E. R., Moser, M., & Moser, E. I. (2011) · Cell · doi:10.1016/j.cell.2011.08.051 · Cited by 158 · see citing works
Self-citationBrandon, 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
Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex
Klink, R., & Alonso, Á. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:5 · Cited by 137 · see citing works
Hippocampal Remapping after Partial Inactivation of the Medial Entorhinal Cortex
Miao, C., Cao, Q., Ito, H., Yamahachi, H., Witter, M. P., Moser, M., & Moser, E. I. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.051 · Cited by 131 · 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
Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells
Sun, C., 北村, 貴., Yamamoto, J., Martin, J., Pignatelli, M., Kitch, L. J., Schnitzer, M. J., & Tonegawa, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511668112 · Cited by 121 · see citing works
Modular Realignment of Entorhinal Grid Cell Activity as a Basis for Hippocampal Remapping
Monaco, J. D., & Abbott, L. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1433-11.2011 · Cited by 117 · see citing works
Impaired Hippocampal Ripple-Associated Replay in a Mouse Model of Schizophrenia
Suh, J., Foster, D. J., Davoudi, H., Wilson, M. A., & Tonegawa, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.014 · Cited by 113 · see citing works
Tang, Q., Burgalossi, A., Ebbesen, C. L., Ray, S., Naumann, R. K., Schmidt, H., Spicher, D., & Brecht, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.009 · Cited by 102 · see citing works
Precise spatial coding is preserved along the longitudinal hippocampal axis
Keinath, A., Wang, M. E., Wann, E. G., Yuan, R. K., Dudman, J. T., & Muzzio, I. A. (2014) · Hippocampus · doi:10.1002/hipo.22333 · Cited by 101 · see citing works
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
Increased Size and Stability of CA1 and CA3 Place Fields in HCN1 Knockout Mice
Hussaini, S. A., Kempadoo, K. A., Thuault, S., Siegelbaum, S. A., & Kandel, E. R. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.007 · Cited by 86 · see citing works
A three‐plane architectonic atlas of the rat hippocampal region
Boccara, C. N., Kjønigsen, L. J., Hammer, I. M., Bjaalie, J. G., Leergaard, T. B., & Witter, M. P. (2014) · Hippocampus · doi:10.1002/hipo.22407 · Cited by 80 · see citing works
Hippocampal global remapping for different sensory modalities in flying bats
Geva‐Sagiv, M., Romani, S., Las, L., & Ulanovsky, N. (2016) · Nature Neuroscience · doi:10.1038/nn.4310 · Cited by 80 · see citing works
Rueckemann, J. W., DiMauro, A., Rangel, L. M., Han, X., Boyden, E. S., & Eichenbaum, H. (2015) · Hippocampus · doi:10.1002/hipo.22519 · Cited by 60 · see citing works
The structure of networks that produce the transformation from grid cells to place cells
Cheng, S., & Frank, L. M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.002 · Cited by 55 · see citing works
Ormond, J., & McNaughton, B. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421963112 · Cited by 52 · see citing works
Lyttle, D. N., Gereke, B. J., Lin, K., & Fellous, J. (2013) · Hippocampus · doi:10.1002/hipo.22132 · Cited by 33 · see citing works
Pastoll, H., White, M. D., & Nolan, M. F. (2012) · Journal of Visualized Experiments · doi:10.3791/3802 · Cited by 28 · see citing works
Hyperpolarization‐activated cyclic nucleotide‐gated 1 independent grid cell‐phase precession in mice
Eggink, H. M., Mertens, P. E. C., Storm, E., & Giocomo, L. M. (2013) · Hippocampus · doi:10.1002/hipo.22231 · Cited by 22 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Perineuronal nets stabilize the grid cell network
Christensen, A. C., Lensjø, K. K., Lepperød, M. E., Dragly, S.-A., Sutterud, H., Blackstad, J. S., Fyhn, M., & Hafting, T. (2021) · Nature Communications · doi:10.1038/s41467-020-20241-w · Cited by 1,865 · see citing works
Remembered reward locations restructure entorhinal spatial maps
Butler, W. N., Hardcastle, K., & Giocomo, L. M. (2019) · Science · doi:10.1126/science.aav5297 · Cited by 232 · see citing works
Self-citationShin, J. D., Tang, W., & Jadhav, S. P. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.012 · Cited by 199 · see citing works
Santoro, B., & Shah, M. M. (2020) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010919-023356 · Cited by 108 · see citing works
Savelli, F., & Knierim, J. J. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.188912 · Cited by 93 · see citing works
Dynamic and reversible remapping of network representations in an unchanging environment
Low, I. I. C., Williams, A. H., Campbell, M. G., Linderman, S. W., & Giocomo, L. M. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.005 · Cited by 70 · see citing works
Self-citationSpace is a latent sequence: A theory of the hippocampus
Raju, R. V., Guntupalli, J. S., Zhou, G., Wendelken, C., Lázaro-Gredilla, M., & George, D. (2024) · Science Advances · doi:10.1126/sciadv.adm8470 · Cited by 25 · see citing works
Topography in the bursting dynamics of entorhinal neurons
Bant, J. S., Hardcastle, K., Ocko, S. A., & Giocomo, L. M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.057 · Cited by 25 · see citing works
Self-citation
- Authors
- Mallory, C. S., Hardcastle, K., Bant, J. S., & Giocomo, L. M.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Mallory, Caitlin S.
- Giocomo, Lisa M.
- Venue
- Nature Neuroscience
- Published
- 2018-01-15
- Volume
- 21
- Issue
- 2
- Pages
- 270-282
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5823610
- OpenAlex
- W2782629502
- Cited by
- 46
- References
- 65
- Citations by year
- 2025: 6 · 2024: 8 · 2023: 4 · 2022: 2 · 2021: 6 · 2020: 7 · 2019: 9 · 2018: 4
- FWCI
- 3.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH106475, R56MH106475)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- grid cells, place cells, medial entorhinal cortex, grid scale, HCN1 channels, spatial memory, spatial learning, position decoding
- MeSH terms
- Place Cells, Grid Cells, Action Potentials, Animals, Animals, Newborn, Brain Mapping, Electroencephalography, Female, Hippocampus, Male, Mice, Inbred C57BL, Mice, Transgenic, Models, Neurological, Neural Pathways, Phosphopyruvate Hydratase, Space Perception, Potassium Channels, Entorhinal Cortex, Green Fluorescent Proteins, Mice, Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
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
