Remembered reward locations restructure entorhinal spatial maps
Open accessAbstract
Reward and the map in the brain: Recent findings suggest a more complex role of grid cells in the brain than simply coding for space. The grid map in the entorhinal cortex, which is responsible for encoding spatial information, is not as rigid as originally thought and can be distorted by environmental modifications (see the Perspective by Quian Quiroga). Butler et al. compared grid cell coding during a free-foraging task and a spatial memory task in rats. They discovered that entorhinal spatial maps restructure to incorporate the location of a learned reward. Boccara et al. tested the influence of behaviorally relevant information on the cognitive map that emerges from grid cell firing in the rat medial entorhinal cortex. They found that grid cells participate in neural coding of the goal locality, not the whole environment. Science , this issue p. 1447 , p. 1443 ; see also p. 1388
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Neurons in navigational brain regions change their firing patterns ('remap') in response to changing contextual factors such as environmental cues, task conditions, and behavioral states.
“These cells also change their firing patterns (‘remap’) in response to changing contextual factors such as environmental cues, task conditions, and behavioral states, which influence neural activity throughout the brain.”
From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as Butler et al., 2019
The supplied passages (section labeled Abstract; page unavailable) report that medial entorhinal cells remapped between environments with different cues and task demands. They do not establish remapping in response to behavioral states specifically, or show that these factors influence neural activity throughout the brain. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMedial entorhinal cortex neurons change their firing rates and shift their spatial firing positions (remap) under a variety of circumstances, even when navigational cues remain stable.
“At the same time, these neurons change their firing rates and shift their spatial firing positions—or ‘remap’—under a variety of circumstances, even when navigational cues remain stable (Bant et al., 2020; Boccara et al., 2019; Butler et al., 2019; Campbell et al., 2021; Campbell et al., 2018; Hardcastle et al., 2017b; Low et al., 2021).”
From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as Butler et al., 2019
The paper reports changes in MEC firing rates and spatial patterns, including remapping between task environments (passages labeled Abstract; page unavailable). But its two environments differed in wall color and scent, so this study does not establish that the changes occurred while navigational cues remained stable. It also studies a particular task change rather than a variety of circumstances. (LLM, conf=0.88)
Experimental — accuracy not yet measuredNeurons in navigational brain regions change their firing rates and shift their spatial firing positions, or remap, under a variety of circumstances even when navigational cues remain stable.
“At the same time, these neurons change their firing rates and shift their spatial firing positions-or “remap”-under a variety of circumstances, even when navigational cues remain stable.[6][7][8][23][24][25][26]”
From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as [7]
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Cites
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
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
Trajectory Encoding in the Hippocampus and Entorhinal Cortex
Frank, L. M., Brown, E. N., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00018-0 · Cited by 731 · 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
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
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
Stephens, D. W., & Krebs, J. R. (1987) · Princeton University Press eBooks · doi:10.1515/9780691206790 · Cited by 621 · see citing works
Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory
Kentros, C. G., Agnihotri, N. T., Streater, S., Hawkins, R. D., & Kandel, E. R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00192-8 · Cited by 537 · 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 398 · 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
Using Grid Cells for Navigation
Bush, D., Barry, C., Manson, D., & Burgess, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.006 · Cited by 334 · see citing works
Heterogeneous Modulation of Place Cell Firing by Changes in Context
Anderson, M. I., & Jeffery, K. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-26-08827.2003 · Cited by 328 · 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-citationThe entorhinal cognitive map is attracted to goals
Boccara, C. N., Nardin, M., Stella, F., O’Neill, J., & Csicsvari, J. (2019) · Science · doi:10.1126/science.aav4837 · Cited by 288 · 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
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
Campbell, M. G., Ocko, S. A., Mallory, C. S., Low, I. I. C., Ganguli, S., & Giocomo, L. M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0189-y · Cited by 187 · see citing works
Self-citationImpaired 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
Bassett, J. P., Tullman, M. L., & Taube, J. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0268-07.2007 · Cited by 127 · see citing works
Grid Cells Encode Local Positional Information
Ismakov, R., Barak, O., Jeffery, K. J., & Derdikman, D. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.034 · Cited by 68 · see citing works
Purely Translational Realignment in Grid Cell Firing Patterns Following Nonmetric Context Change
Marozzi, E., Ginzberg, L. L., Alenda, A., & Jeffery, K. J. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv120 · Cited by 53 · see citing works
Grid scale drives the scale and long-term stability of place maps
Mallory, C. S., Hardcastle, K., Bant, J. S., & Giocomo, L. M. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0055-3 · Cited by 46 · see citing works
Self-citationMeng, L. K., Kramer, M. A. M., Middleton, S. J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085269 · Cited by 21 · see citing works
A multistage mathematical approach to automated clustering of high-dimensional noisy data
Friedman, A., Keselman, M. D., Gibb, L., & Graybiel, A. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503940112 · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- [26]Hardcastle K, Maheswaranathan N, Ganguli S, Giocomo LM, A multiplexed, heterogeneous, and adaptive code for navigation in medial entorhinal cortex. Neuron 94, 375– 387 (2017). 28392071 PMC5498174
- [28]Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI, Representation of geometric borders in the entorhinal cortex. Science 322, 1865– 1868 (2008). 19095945
- [30]Kropff E, Carmichael JE, Moser MB, Moser EI, Speed cells in the medial entorhinal cortex. Nature 523, 419– 424 (2015). 26176924
- [34]Stensola H, The entorhinal map is discretized. Nature 492, 72– 78 (2012). 23222610
- [35]Stensola T, Stensola H, Moser MB, Moser EI, Shearing-induced asymmetry in entorhinal grid cells. Nature 518, 207– 212 (2015). 25673414
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Whittington, J. C. R., Muller, T. H., Mark, S., Chen, G., Barry, C., Burgess, N., & Behrens, T. E. J. (2020) · Cell · doi:10.1016/j.cell.2020.10.024 · Cited by 660 · see citing works
Toroidal topology of population activity in grid cells
Gardner, R. J., Hermansen, E., Pachitariu, M., Burak, Y., Baas, N. A., Dunn, B. A., Moser, M.-B., & Moser, E. I. (2022) · Nature · doi:10.1038/s41586-021-04268-7 · Cited by 428 · see citing works
Learning structures: Predictive representations, replay, and generalization
Momennejad, I. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.02.017 · Cited by 159 · see citing works
Spatial goal coding in the hippocampal formation
Nyberg, N., Duvelle, É., Barry, C., & Spiers, H. J. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.012 · Cited by 141 · 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-citationTopography 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-citationKloc, M. L., Chen, Y., Daglian, J. M., Holmes, G. L., Baram, T. Z., & Barry, J. M. (2023) · Hippocampus · doi:10.1002/hipo.23541 · Cited by 21 · see citing works
Remapping in a recurrent neural network model of navigation and context inference
Low, I. I., Giocomo, L. M., & Williams, A. H. (2023) · eLife · doi:10.7554/elife.86943 · Cited by 15 · see citing works
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Quiroga, R. Q. (2019) · Science · doi:10.1126/science.aaw8829 · Cited by 14 · see citing works
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Low, I. I. C., Giocomo, L. M., & Williams, A. H. (2023) · doi:10.1101/2023.01.25.525596 · Cited by 3 · see citing works
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Self-citation
- Authors
- Butler, W. N., Hardcastle, K., & Giocomo, L. M.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Butler, William N.
- Hardcastle, Kiah
- Giocomo, Lisa M.
- Venue
- Science
- Published
- 2019-03-29
- Volume
- 363
- Issue
- 6434
- Pages
- 1447-1452
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC6516752
- OpenAlex
- W2924737142
- Cited by
- 232
- References
- 31
- Citations by year
- 2026: 27 · 2025: 49 · 2024: 25 · 2023: 41 · 2022: 26 · 2021: 25 · 2020: 22 · 2019: 17
- FWCI
- 13.08
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Office of Naval Research (N000141812690)
- National Institute of Mental Health (NIMH MH106475)
- National Institute on Drug Abuse (NIDA DA042012)
- James S. McDonnell Foundation
- Esther A. and Joseph Klingenstein Fund
- New York Stem Cell Foundation
- Stanford University (Interdisciplinary Graduate Fellowship)
- 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, entorhinal cortex, spatial maps, reward location, spatial memory, cognitive maps, rats, neural coding
- MeSH terms
- Grid Cells, Animals, Brain Mapping, Male, Mental Recall, Reward, Entorhinal Cortex, Head Movements, Rats, Spatial Navigation
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