A Dedicated Population for Reward Coding in the Hippocampus
Open accessAbstract
The hippocampus plays a critical role in goal-directed navigation. Across different environments, however, hippocampal maps are randomized, making it unclear how goal locations could be encoded consistently. To address this question, we developed a virtual reality task with shifting reward contingencies to distinguish place versus reward encoding. In mice performing the task, large-scale recordings in CA1 and subiculum revealed a small, specialized cell population that was only active near reward yet whose activity could not be explained by sensory cues or stereotyped reward anticipation behavior. Across different virtual environments, most cells remapped randomly, but reward encoding consistently arose from a single pool of cells, suggesting that they formed a dedicated channel for reward. These observations represent a significant departure from the current understanding of CA1 as a relatively homogeneous ensemble without fixed coding properties and provide a new candidate for the cellular basis of goal memory in the hippocampus.
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?
Place fields uniformly tiled the available space, with a slight over-representation of the reward's position and of prominent tactile cues on the belt.
“Place fields uniformly tiled the available space (Fig. 1c), with a slight over-representation of the reward’s position and of prominent tactile cues on the belt (see also refs. 39–41).”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [40]
The Results (Moving Reward Location Within One Environment; page unavailable) report approximately uniform spatial-field density across most of the track, with excess density near reward. They do not report over-representation at tactile cues on a belt; the Methods describe visual textures and towers along a virtual track instead. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe criteria used for PC identification are similar to those in the existing literature in both mammals and birds, for both electrophysiological and calcium imaging data.
“The criteria we use are similar to those in the existing literature in both mammals and birds, for both electrophysiological and calcium imaging data16,53.”
From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [53]
In STAR★METHODS, Quantification and Statistical Analysis (page unavailable), the paper gives criteria for identifying spatially modulated cells and place cells from calcium-imaging data in mice. It does not compare those criteria with criteria used in birds or establish their similarity to electrophysiological criteria. (LLM, conf=0.83)
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.
Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128 · see citing works
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
Daw, N. D., Niv, Y., & Dayan, P. (2005) · Nature Neuroscience · doi:10.1038/nn1560 · Cited by 2,533 · see citing works
The human hippocampus and spatial and episodic memory
Burgess, N., Maguire, E. A., & O'Keefe, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00830-9 · Cited by 2,401 · see citing works
Applications of the Morris water maze in the study of learning and memory
D’Hooge, R., & Deyn, P. P. D. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00067-4 · Cited by 2,035 · see citing works
Invariant visual representation by single neurons in the human brain
Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., & Fried, I. (2005) · Nature · doi:10.1038/nature03687 · Cited by 1,988 · see citing works
Advances in Neural Information Processing Systems 5
Zemel, R. S., Williams, C. K. I., & Mozer, M. C. (1993) · Cited by 1,896 · see citing works
Place units in the hippocampus of the freely moving rat
O'Keefe, J. (1976) · Experimental Neurology · doi:10.1016/0014-4886(76)90055-8 · Cited by 1,836 · 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
Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats
Ranck, J. B. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90290-2 · Cited by 1,322 · see citing works
Hippocampal place-cell sequences depict future paths to remembered goals
Pfeiffer, B. E., & Foster, D. J. (2013) · Nature · doi:10.1038/nature12112 · Cited by 1,216 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
McNaughton, B. L., Barnes, C. A., & O'Keefe, J. (1983) · Experimental Brain Research · doi:10.1007/bf00237147 · Cited by 1,071 · see citing works
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
Simultaneous Denoising, Deconvolution, and Demixing of Calcium Imaging Data
Pnevmatikakis, E. A., Soudry, D., Gao, Y., Machado, T. A., Merel, J., Pfau, D., Reardon, T. R., Mu, Y., Lacefield, C., Yang, W., et al. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.037 · Cited by 1,035 · see citing works
Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point
Johnson, A., & Redish, A. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3761-07.2007 · Cited by 1,003 · see citing works
The hippocampus as a predictive map
Stachenfeld, K. L., Botvinick, M. M., & Gershman, S. J. (2017) · Nature Neuroscience · doi:10.1038/nn.4650 · Cited by 1,000 · 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
Spatial firing patterns of hippocampal complex-spike cells in a fixed environment
Muller, R., Kubie, J., & Ranck, J. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01935.1987 · Cited by 898 · see citing works
Functional imaging of hippocampal place cells at cellular resolution during virtual navigation
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., & Tank, D. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2648 · Cited by 873 · see citing works
Self-citationIntracellular dynamics of hippocampal place cells during virtual navigation
Harvey, C. D., Collman, F., Dombeck, D. A., & Tank, D. W. (2009) · Nature · doi:10.1038/nature08499 · Cited by 854 · see citing works
Self-citationThe neurobiological basis of spontaneous alternation
Lalonde, R. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00041-0 · Cited by 842 · see citing works
Single unit activity in the rat hippocampus during a spatial memory task
O'Keefe, J. M., & Speakman, A. (1987) · Experimental Brain Research · doi:10.1007/bf00255230 · Cited by 782 · see citing works
Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit
Aronov, D., Nevers, R., & Tank, D. W. (2017) · Nature · doi:10.1038/nature21692 · Cited by 773 · see citing works
Self-citationThe reorganization and reactivation of hippocampal maps predict spatial memory performance
Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010) · Nature Neuroscience · doi:10.1038/nn.2599 · Cited by 769 · see citing works
Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data
Mukamel, E. A., Nimmerjahn, A., & Schnitzer, M. J. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.009 · Cited by 711 · see citing works
Improving generalization for temporal difference learning: The successor representation
Dayan, P. (1993) · Neural Computation · doi:10.1162/neco.1993.5.4.613 · Cited by 693 · see citing works
Morris, R., Schenk, F., Tweedie, F., & Jarrard, L. E. (1990) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1990.tb00014.x · Cited by 661 · see citing works
An Information-Theoretic Approach to Deciphering the Hippocampal Code
Skaggs, W. E., McNaughton, B. L., & Gothard, K. M. (1992) · Cited by 536 · see citing works
Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task
Hollup, S., Molden, S., Donnett, J. G., Moser, M., & Moser, E. I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01635.2001 · Cited by 490 · see citing works
Gothard, K., Skaggs, W. E., Moore, K. L., & McNaughton, B. L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00823.1996 · Cited by 488 · see citing works
Hippocampus leads ventral striatum in replay of place-reward information
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., McNaughton, B. L., & Pennartz, C. M. A. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000173 · Cited by 400 · see citing works
A Scalable Population Code for Time in the Striatum
Mello, G. B. M. E., Soares, S., & Paton, J. J. (2015) · Current Biology · doi:10.1016/j.cub.2015.02.036 · Cited by 393 · see citing works
McKenzie, S., Frank, A. J., Kinsky, N. R., Porter, B., Rivière, P. D., & Eichenbaum, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.019 · Cited by 373 · see citing works
Selective information routing by ventral hippocampal CA1 projection neurons
Ciocchi, S., Passecker, J., Malagon‐Vina, H., Mikuš, N., & Klausberger, T. (2015) · Science · doi:10.1126/science.aaa3245 · Cited by 344 · see citing works
Memory without Feedback in a Neural Network
Goldman, M. S. (2009) · Neuron · doi:10.1016/j.neuron.2008.12.012 · Cited by 342 · see citing works
Vectorial representation of spatial goals in the hippocampus of bats
Sarel, A., Finkelstein, A., Las, L., & Ulanovsky, N. (2017) · Science · doi:10.1126/science.aak9589 · Cited by 330 · 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
Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields
Rickgauer, J. P., Deisseroth, K. A., & Tank, D. W. (2014) · Nature Neuroscience · doi:10.1038/nn.3866 · Cited by 323 · see citing works
Self-citationEngagement of Neural Circuits Underlying 2D Spatial Navigation in a Rodent Virtual Reality System
Aronov, D., & Tank, D. W. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.042 · Cited by 315 · see citing works
Self-citationMembrane 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
Self-citationRodrı́guez, F., López, J. C., Vargas, J. P., Broglio, C., Gómez, Y., & Salas, C. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00682-7 · Cited by 293 · see citing works
Reverse replay of hippocampal place cells is uniquely modulated by changing reward
Ambrose, R. E., Pfeiffer, B. E., & Foster, D. J. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.047 · Cited by 292 · see citing works
Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1
Danielson, N. B., Zaremba, J. D., Kaifosh, P., Bowler, J., Ladow, M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.020 · Cited by 288 · see citing works
Hippocampal ensemble dynamics timestamp events in long-term memory
Rubin, A., Geva, N., Sheintuch, L., & Ziv, Y. (2015) · eLife · doi:10.7554/elife.12247 · Cited by 266 · see citing works
Neuronal computations underlying the firing of place cells and their role in navigation
Burgess, N., & O'Keefe, J. M. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 240 · see citing works
Goal-Related Activity in Hippocampal Place Cells
Hok, V., Lenck‐Santini, P., Roux, S., Save, É., Muller, R. U., & Poucet, B. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2864-06.2007 · Cited by 232 · see citing works
Does the orbitofrontal cortex signal value?
Schoenbaum, G., Takahashi, Y., Liu, T., & McDannald, M. A. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06210.x · Cited by 232 · see citing works
Influence of local objects on hippocampal representations: Landmark vectors and memory
Deshmukh, S. S., & Knierim, J. J. (2013) · Hippocampus · doi:10.1002/hipo.22101 · Cited by 217 · see citing works
van der Meer, M. A. A., Johnson, A. C., Schmitzer-Torbert, N. C., & Redish, A. D. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.023 · Cited by 210 · see citing works
Hippocampal Neurons Responding to First-Time Dislocation of a Target Object
Fyhn, M., Molden, S., Hollup, S., Moser, M., & Moser, E. I. (2002) · Neuron · doi:10.1016/s0896-6273(02)00784-5 · Cited by 202 · see citing works
Dynamic Grouping of Hippocampal Neural Activity During Cognitive Control of Two Spatial Frames
Kelemen, E., & Fenton, A. A. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000403 · Cited by 200 · see citing works
Awake hippocampal reactivations project onto orthogonal neuronal assemblies
Malvache, A., Reichinnek, S., Villette, V., Haimerl, C., & Cossart, R. (2016) · Science · doi:10.1126/science.aaf3319 · Cited by 163 · see citing works
Hetherington, P. A., & Shapiro, M. L. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.1.20 · Cited by 143 · see citing works
Low, R. J., Gu, Y., & Tank, D. W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421753111 · Cited by 141 · see citing works
Self-citationSharp, P. E. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(96)00165-9 · Cited by 134 · see citing works
McKenzie, S., Robinson, N. T. M., Herrera, L., Churchill, J. C., & Eichenbaum, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0879-13.2013 · Cited by 132 · see citing works
Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion
Zaremba, J. D., Diamantopoulou, A., Danielson, N., Grosmark, A., Kaifosh, P., Bowler, J. C., Liao, Z., Sparks, F. T., Gogos, J. A., & Losonczy, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4634 · Cited by 124 · see citing works
Differential but Complementary Mnemonic Functions of the Hippocampus and Subiculum
Deadwyler, S. A., & Hampson, R. E. (2004) · Neuron · doi:10.1016/s0896-6273(04)00195-3 · Cited by 123 · see citing works
Hippocampal map realignment and spatial learning
Rosenzweig, E. S., Redish, A. D., McNaughton, B. L., & Barnes, C. A. (2003) · Nature Neuroscience · doi:10.1038/nn1053 · Cited by 106 · see citing works
Kim, S. M., Ganguli, S., & Frank, L. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5942-11.2012 · Cited by 101 · see citing works
Atallah, H. E., McCool, A. D., Howe, M. W., & Graybiel, A. M. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.021 · Cited by 98 · see citing works
Neural encoding of the concept of nest in the mouse brain
Lin, L., Chen, G., Kuang, H., Wang, D., & Tsien, J. Z. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701106104 · Cited by 88 · see citing works
McKenzie, S., Keene, C. S., Farovik, A., Bladon, J. H., Place, R., Komorowski, R. W., & Eichenbaum, H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.12.008 · Cited by 53 · see citing works
Hippocampus-Dependent Goal Localization by Head-Fixed Mice in Virtual Reality
Sato, M., Kawano, M., Mizuta, K., Islam, T., Lee, M. G., & Hayashi, Y. (2017) · eNeuro · doi:10.1523/eneuro.0369-16.2017 · Cited by 45 · see citing works
Poucet, B., & Hok, V. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.06.003 · Cited by 40 · see citing works
Dynamic embedding of salience coding in hippocampal spatial mapsPreprint
Sato, M., Mizuta, K., Islam, T., Kawano, M., Takekawa, T., Gómez-Domínguez, D., Kim, K., Yamakawa, H., Ohkura, M., Fukai, T., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/266767 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior
Behrens, T. E. J., Muller, T. H., Whittington, J. C. R., Mark, S., Baram, A. B., Stachenfeld, K. L., & Kurth-Nelson, Z. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.002 · Cited by 1,055 · see citing works
Geometry of abstract learned knowledge in the hippocampus
Nieh, E. H., Schottdorf, M., Freeman, N. W., Low, R. J., Lewallen, S., Koay, S. A., Pinto, L., Gauthier, J. L., Brody, C. D., & Tank, D. W. (2021) · Nature · doi:10.1038/s41586-021-03652-7 · Cited by 321 · see citing works
Self-citationReward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses
LeGates, T. A., Kvarta, M. D., Tooley, J. R., Francis, T. C., Lobo, M. K., Creed, M. C., & Thompson, S. M. (2018) · Nature · doi:10.1038/s41586-018-0740-8 · Cited by 290 · see citing works
The 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
Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior
Robinson, N. T. M., Descamps, L. A. L., Russell, L. E., Buchholz, M. O., Bicknell, B. A., Antonov, G. K., Lau, J. Y. N., Nutbrown, R., Schmidt-Hieber, C., & Häusser, M. (2020) · Cell · doi:10.1016/j.cell.2020.09.061 · Cited by 281 · see citing works
Whittington, J. C. R., McCaffary, D., Bakermans, J. J. W., & Behrens, T. E. J. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01153-y · Cited by 245 · see citing works
Bienkowski, M. S., Bowman, I., Song, M. Y., Gou, L., Ard, T., Cotter, K., Zhu, M., Benavidez, N. L., Yamashita, S., Abu-Jaber, J., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0241-y · Cited by 224 · see citing works
Turi, G. F., Li, W.-K., Chavlis, S., Pandi, I., O’Hare, J., Priestley, J. B., Grosmark, A. D., Liao, Z., Ladow, M., Zhang, J. F., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.009 · Cited by 218 · see citing works
Kaufman, A. M., Geiller, T., & Losonczy, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.029 · Cited by 193 · see citing works
Schafer, M., & Schiller, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.006 · Cited by 181 · see citing works
Entorhinal cortex directs learning-related changes in CA1 representations
Grienberger, C., & Magee, J. C. (2022) · Nature · doi:10.1038/s41586-022-05378-6 · Cited by 171 · see citing works
Hippocampal remapping as hidden state inference
Sanders, H., Wilson, M. A., & Gershman, S. J. (2020) · eLife · doi:10.7554/elife.51140 · Cited by 163 · 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
Contextual fear memory retrieval by correlated ensembles of ventral CA1 neurons
Jimenez, J., Berry, J. E., Lim, S. C., Ong, S. K., Kheirbek, M. A., & Hen, R. (2020) · Nature Communications · doi:10.1038/s41467-020-17270-w · Cited by 157 · 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
Hippocampal place cells have goal-oriented vector fields during navigation
Ormond, J., & O'Keefe, J. M. (2022) · Nature · doi:10.1038/s41586-022-04913-9 · Cited by 153 · see citing works
Sosa, M., & Giocomo, L. M. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00479-z · Cited by 142 · see citing works
Bidirectional synaptic plasticity rapidly modifies hippocampal representations
Milstein, A. D., Li, Y., Bittner, K. C., Grienberger, C., Soltesz, I., Magee, J. C., & Romani, S. (2021) · eLife · doi:10.7554/elife.73046 · Cited by 151 · see citing works
Fos ensembles encode and shape stable spatial maps in the hippocampus
Pettit, N. L., Yap, E.-L., Greenberg, M. E., & Harvey, C. D. (2022) · Nature · doi:10.1038/s41586-022-05113-1 · Cited by 146 · see citing works
Hippocampal neurons represent events as transferable units of experience
Sun, C., Yang, W., Martin, J., & Tonegawa, S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0614-x · Cited by 135 · see citing works
Guo, C., Blair, G. J., Sehgal, M., Jimka, F. N. S., Bellafard, A., Silva, A. J., Golshani, P., Basso, M. A., Blair, H. T., & Aharoni, D. B. (2023) · Science Advances · doi:10.1126/sciadv.adg3918 · Cited by 133 · see citing works
Lee, J. S., Briguglio, J. J., Cohen, J. D., Romani, S., & Lee, A. K. (2020) · Cell · doi:10.1016/j.cell.2020.09.024 · Cited by 132 · see citing works
Coarse Graining, Fixed Points, and Scaling in a Large Population of Neurons
Meshulam, L., Gauthier, J. L., Brody, C. D., Tank, D. W., & Bialek, W. (2019) · Physical Review Letters · doi:10.1103/physrevlett.123.178103 · Cited by 124 · see citing works
Self-citationHippocampal place codes are gated by behavioral engagement
Pettit, N. L., Yuan, X. C., & Harvey, C. D. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01050-4 · Cited by 119 · see citing works
Replay, the default mode network and the cascaded memory systems model
Kaefer, K., Stella, F., McNaughton, B. L., & Battaglia, F. P. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00620-6 · Cited by 124 · see citing works
Hippocampal astrocytes encode reward location
Doron, A., Rubin, A., Benmelech-Chovav, A., Benaim, N., Carmi, T., Refaeli, R., Novick, N., Kreisel, T., Ziv, Y., & Goshen, I. (2022) · Nature · doi:10.1038/s41586-022-05146-6 · Cited by 122 · see citing works
Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences
Priestley, J. B., Bowler, J. C., Rolotti, S. V., Fusi, S., & Losonczy, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.026 · Cited by 122 · see citing works
Local Feedback Inhibition Tightly Controls Rapid Formation of Hippocampal Place Fields
Rolotti, S. V., Ahmed, M. S., Szoboszlay, M., Geiller, T., Negrean, A., Blockus, H., Gonzalez, K. C., Sparks, F. T., Canales, A. S. S., Tuttman, A. L., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.12.003 · Cited by 114 · see citing works
Representation of visual landmarks in retrosplenial cortex
Fischer, L. F., Soto-Albors, R. M., Buck, F., & Harnett, M. T. (2020) · eLife · doi:10.7554/elife.51458 · Cited by 104 · see citing works
George, D., Rikhye, R. V., Gothoskar, N., Guntupalli, J. S., Dedieu, A., & Lázaro-Gredilla, M. (2021) · Nature Communications · doi:10.1038/s41467-021-22559-5 · Cited by 109 · see citing works
Neural dynamics underlying associative learning in the dorsal and ventral hippocampus
Biane, J. S., Ladow, M. A., Stefanini, F., Boddu, S. P., Fan, A., Hassan, S., Dundar, N., Apodaca-Montano, D. L., Zhou, L. Z., Fayner, V., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01296-6 · Cited by 95 · see citing works
Contributions of adult neurogenesis to dentate gyrus network activity and computations
Tuncdemir, S. N., Lacefield, C., & Hen, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112112 · Cited by 97 · see citing works
Gulli, R. A., Duong, L., Corrigan, B. W., Doucet, G., Williams, S., Fusi, S., & Martínez-Trujillo, J. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0548-3 · Cited by 96 · see citing works
Krishnan, S., Heer, C. M., Cherian, C., & Sheffield, M. E. J. (2022) · Nature Communications · doi:10.1038/s41467-022-34465-5 · Cited by 97 · see citing works
The role of the hippocampus in the consolidation of emotional memories during sleep
Pronier, É., Morici, J. F., & Girardeau, G. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.003 · Cited by 96 · 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
Insensitivity of place cells to the value of spatial goals in a two-choice flexible navigation task
Duvelle, É., Grieves, R. M., Hok, V., Poucet, B., Arleo, A., Jeffery, K. J., & Save, É. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1578-18.2018 · Cited by 91 · see citing works
Robust information routing by dorsal subiculum neurons
Kitanishi, T., Umaba, R., & Mizuseki, K. (2021) · Science Advances · doi:10.1126/sciadv.abf1913 · Cited by 88 · see citing works
Mapping sequence structure in the human lateral entorhinal cortex
Bellmund, J. L. S., Deuker, L., & Doeller, C. F. (2019) · eLife · doi:10.7554/elife.45333 · Cited by 93 · see citing works
Maier, A., Gieling, C., Heinen-Ludwig, L., Stefan, V., Schultz, J., Güntürkün, O., Becker, B., Hurlemann, R., & Scheele, D. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19020212 · Cited by 87 · see citing works
Zhao, X., Hsu, C.-L., & Spruston, N. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.003 · Cited by 82 · see citing works
Dynamic control of hippocampal spatial coding resolution by local visual cues
Bourboulou, R., Marti, G., Michon, F.-X., Feghaly, E. E., Nouguier, M., Robbe, D., Koenig, J., & Epsztein, J. (2019) · eLife · doi:10.7554/elife.44487 · Cited by 76 · see citing works
Distinct Mechanisms of Over-Representation of Landmarks and Rewards in the Hippocampus
Sato, M., Mizuta, K., Islam, T., Kawano, M., Sekine, Y., Takekawa, T., Gómez-Domínguez, D., Schmidt, A., Wolf, F., Kim, K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107864 · Cited by 78 · see citing works
Hippocampal cells segregate positive and negative engrams
Shpokayte, M., McKissick, O. P., Guan, X., Yuan, B., Rahsepar, B., Fernandez, F. R., Ruesch, E. A., Grella, S. L., White, J. A., Liu, X. S., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03906-8 · Cited by 75 · see citing works
Barcoding of episodic memories in the hippocampus of a food-caching bird
Chettih, S. N., Mackevicius, E. L., Hale, S., & Aronov, D. (2024) · Cell · doi:10.1016/j.cell.2024.02.032 · Cited by 74 · see citing works
Eliwa, H., Brizard, B., Guisquet, A. L., Hen, R., Belzung, C., & Surget, A. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105097 · Cited by 73 · see citing works
Arbitration of Approach-Avoidance Conflict by Ventral Hippocampus
Bryant, K. G., & Barker, J. M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.615337 · Cited by 72 · see citing works
Different encoding of reward location in dorsal and intermediate hippocampus
Jarzębowski, P., Hay, Y. A., Grewe, B. F., & Paulsen, O. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.024 · Cited by 71 · see citing works
Single-Neuron Representations of Spatial Targets in Humans
Tsitsiklis, M., Miller, J. F., Qasim, S. E., Inman, C. S., Gross, R. E., Willie, J. T., Smith, E. H., Sheth, S. A., Schevon, C. A., Sperling, M. R., et al. (2020) · Current Biology · doi:10.1016/j.cub.2019.11.048 · Cited by 74 · see citing works
Liu, X., Ren, C., Lu, Y., Liu, Y., Kim, J., Leutgeb, S., Komiyama, T., & Kuzum, D. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00841-5 · Cited by 64 · see citing works
Linking hippocampal multiplexed tuning, Hebbian plasticity and navigation
Moore, J. J., Cushman, J. D., Acharya, L., Popeney, B., & Mehta, M. R. (2021) · Nature · doi:10.1038/s41586-021-03989-z · Cited by 69 · see citing works
Prioritized experience replays on a hippocampal predictive map for learning
Igata, H., Ikegaya, Y., & Sasaki, T. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2011266118 · Cited by 75 · see citing works
Dopamine signals as temporal difference errors: recent advances
Starkweather, C. K., & Uchida, N. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.08.014 · Cited by 67 · see citing works
Behavior determines the hippocampal spatial mapping of a multisensory environment
Radvansky, B. A., Oh, J. Y., Climer, J. R., & Dombeck, D. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109444 · Cited by 60 · see citing works
The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization
Jordan, J. T. (2019) · Hippocampus · doi:10.1002/hipo.23188 · Cited by 66 · see citing works
Complementary encoding of spatial information in hippocampal astrocytes
Curreli, S., Bonato, J., Romanzi, S., Panzeri, S., & Fellin, T. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001530 · Cited by 66 · see citing works
The evolving view of replay and its functions in wake and sleep
Findlay, G., Tononi, G., & Cirelli, C. (2020) · SLEEP Advances · doi:10.1093/sleepadvances/zpab002 · Cited by 61 · see citing works
Rapid learning of predictive maps with STDP and theta phase precession
George, T. M., de Cothi, W., Stachenfeld, K., & Barry, C. (2023) · eLife · doi:10.7554/elife.80663 · Cited by 74 · see citing works
Zhou, J., Montesinos-Cartagena, M., Wikenheiser, A. M., Gardner, M., Niv, Y., & Schoenbaum, G. M. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.040 · Cited by 65 · see citing works
Membrane potential dynamics underlying context-dependent sensory responses in the hippocampus
Zhao, X., Wang, Y., Spruston, N., & Magee, J. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0646-2 · Cited by 61 · see citing works
Five Decades of Hippocampal Place Cells and EEG Rhythms in Behaving Rats
Colgin, L. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0741-19.2019 · Cited by 61 · see citing works
Differential encoding of place value between the dorsal and intermediate hippocampus
Jin, S., & Lee, I. (2021) · Current Biology · doi:10.1016/j.cub.2021.04.073 · Cited by 60 · see citing works
Differences in reward biased spatial representations in the lateral septum and hippocampus
Wirtshafter, H. S., & Wilson, M. A. (2020) · eLife · doi:10.7554/elife.55252 · Cited by 62 · see citing works
Kinkhabwala, A. A., Gu, Y., Aronov, D., & Tank, D. W. (2020) · eLife · doi:10.7554/elife.43140 · Cited by 52 · see citing works
Self-citationIntegrating new memories into the hippocampal network activity space
Gava, G. P., McHugh, S. B., Lefèvre, L., Lopes‐dos‐Santos, V., Trouche, S. G., El-Gaby, M., Schultz, S. R., & Dupret, D. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00804-w · Cited by 58 · see citing works
Bowler, J. C., & Losonczy, A. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.013 · Cited by 55 · see citing works
The Basis of Navigation Across Species
Freas, C. A., & Cheng, K. (2021) · Annual Review of Psychology · doi:10.1146/annurev-psych-020821-111311 · Cited by 56 · see citing works
Predicting the Future with Multi-scale Successor RepresentationsPreprint
Momennejad, I., & Howard, M. W. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/449470 · Cited by 59 · see citing works
Neural representation of goal direction in the monarch butterfly brain
Beetz, M. J., Kraus, C., & el Jundi, B. (2023) · Nature Communications · doi:10.1038/s41467-023-41526-w · Cited by 60 · see citing works
The Integration of Goal-Directed Signals onto Spatial Maps of Hippocampal Place Cells
Aoki, Y., Igata, H., Ikegaya, Y., & Sasaki, T. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.002 · Cited by 54 · see citing works
Remapping revisited: how the hippocampus represents different spaces
Fenton, A. A. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00817-x · Cited by 56 · see citing works
Hippocampal neuronal activity is aligned with action plans
Zutshi, I., Apostolelli, A., Yang, W., Zheng, Z. S., Dohi, T., Balzani, E., Williams, A. H., Savin, C., & Buzsáki, G. (2025) · Nature · doi:10.1038/s41586-024-08397-7 · Cited by 59 · see citing works
Goal-seeking compresses neural codes for space in the human hippocampus and orbitofrontal cortex
Muhle-Karbe, P. S., Sheahan, H., Pezzulo, G., Spiers, H. J., Chien, S., Schuck, N. W., & Summerfield, C. (2023) · Neuron · doi:10.1016/j.neuron.2023.08.021 · Cited by 50 · see citing works
The Hippocampal Horizon: Constructing and Segmenting Experience for Episodic Memory
Ross, T. W., & Easton, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.038 · Cited by 49 · see citing works
Two Functionally Distinct Serotonergic Projections into Hippocampus
Luchetti, A., Bota, A., Weitemier, A. Z., Mizuta, K., Sato, M., Islam, T., McHugh, T. J., Tashiro, A., & Hayashi, Y. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2724-19.2020 · Cited by 49 · see citing works
Contextual and pure time coding for self and other in the hippocampus
Omer, D. B., Las, L., & Ulanovsky, N. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01226-y · Cited by 47 · see citing works
Silva, A., & Martínez, M. C. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1082158 · Cited by 47 · see citing works
Constructing future behavior in the hippocampal formation through composition and replay
Bakermans, J. J. W., Warren, J., Whittington, J. C. R., & Behrens, T. E. J. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01908-3 · Cited by 67 · see citing works
Formation of an expanding memory representation in the hippocampus
Vaidya, S. P., Li, G., Chitwood, R. A., Li, Y., & Magee, J. C. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01986-3 · Cited by 53 · see citing works
A flexible hippocampal population code for experience relative to reward
Sosa, M., Plitt, M. H., & Giocomo, L. M. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01985-4 · Cited by 49 · see citing works
Structured inhibitory activity dynamics in new virtual environments
Arriaga, M. A., & Han, E. B. (2019) · eLife · doi:10.7554/elife.47611 · Cited by 48 · see citing works
Kong, E., Lee, K.-H., Do, J., Kim, P., & Lee, D. (2023) · Nature Communications · doi:10.1038/s41467-023-38338-3 · Cited by 46 · see citing works
Memory retrieval modulates spatial tuning of single neurons in the human entorhinal cortex
Qasim, S. E., Miller, J. F., Inman, C. S., Gross, R. E., Willie, J. T., Lega, B. C., Lin, J.-J., Sharan, A. D., Wu, C., Sperling, M. R., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0523-z · Cited by 46 · see citing works
Takamiya, S., Shiotani, K., Ohnuki, T., Osako, Y., Tanisumi, Y., Yuki, S., Manabe, H., Hirokawa, J., & Sakurai, Y. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.718619 · Cited by 44 · see citing works
Reorganization of CA1 dendritic dynamics by hippocampal sharp-wave ripples during learning
Rolotti, S. V., Blockus, H., Sparks, F. T., Priestley, J. B., & Losonczy, A. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.017 · Cited by 50 · see citing works
Abstract Representation of Prospective Reward in the Hippocampus
Zeithamová, D., Gelman, B. D., Frank, L. E., & Preston, A. R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0719-18.2018 · Cited by 39 · see citing works
Goal-oriented representations in the human hippocampus during planning and navigation
Crivelli-Decker, J. E., Clarke, A., Park, S. A., Huffman, D. J., Boorman, E. D., & Ranganath, C. (2023) · Nature Communications · doi:10.1038/s41467-023-35967-6 · Cited by 40 · see citing works
Divergence in Population Coding for Space between Dorsal and Ventral CA1
Chockanathan, U., & Padmanabhan, K. (2021) · eNeuro · doi:10.1523/eneuro.0211-21.2021 · Cited by 42 · see citing works
Hazon, O., Minces, V. H., Tomàs, D. P., Ganguli, S., Schnitzer, M. J., & Jercog, P. E. (2022) · Nature Communications · doi:10.1038/s41467-022-31254-y · Cited by 47 · see citing works
Lateral entorhinal cortex subpopulations represent experiential epochs surrounding reward
Issa, J. B., Radvansky, B. A., Xuan, F., & Dombeck, D. A. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01557-4 · Cited by 44 · see citing works
Morrell, M. C., Sederberg, A., & Nemenman, I. M. (2021) · Physical Review Letters · doi:10.1103/physrevlett.126.118302 · Cited by 40 · see citing works
Jeong, N., & Singer, A. C. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102604 · Cited by 40 · see citing works
Mystery of the memory engram: History, current knowledge, and unanswered questions
Lopez, M. R., Wasberg, S. M., Gagliardi, C. M., Normandin, M. E., & Muzzio, I. A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105574 · Cited by 39 · see citing works
A neural code for egocentric spatial maps in the human medial temporal lobePreprint
Kunz, L., Brandt, A., Reinacher, P. C., Staresina, B. P., Reifenstein, E. T., Weidemann, C. T., Herweg, N. A., Tsitsiklis, M., Kempter, R., Kahana, M. J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.03.973131 · Cited by 38 · see citing works
A population code for spatial representation in the zebrafish telencephalon
Yang, C., Mammen, L., Kim, B., Li, M., Robson, D. N., & Li, J. M. (2024) · Nature · doi:10.1038/s41586-024-07867-2 · Cited by 38 · see citing works
“The criteria we use are similar to those in the existing literature in both mammals and birds, for both electrophysiological and calcium imaging data 16,53 .”
MATRIEX imaging: multiarea two-photon real-time in vivo explorer
Yang, M., Zhou, Z., Zhang, J., Jia, S., Li, T., Guan, J., Liao, X., Leng, B., Lyu, J., Zhang, K., et al. (2019) · Light Science & Applications · doi:10.1038/s41377-019-0219-x · Cited by 37 · see citing works
Interactions between the hippocampus and the auditory pathway
Zhang, L., Wang, J., Sun, H., Feng, G., & Gao, Z. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107589 · Cited by 36 · see citing works
Pfeiffer, B. E. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2479-21.2022 · Cited by 36 · see citing works
Potential factors influencing replay across CA1 during sharp-wave ripples
de la Prida, L. M. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0236 · Cited by 36 · see citing works
Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
Beeler, J. A., & Dreyer, J. K. (2019) · eNeuro · doi:10.1523/eneuro.0345-18.2019 · Cited by 31 · see citing works
- Authors
- Gauthier, J. L., & Tank, D. W.
- Affiliations
- Princeton University (US)
- Corresponding author
- Gauthier, Jeffrey L.
- Tank, David W.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-07
- Volume
- 99
- Issue
- 1
- Pages
- 179-193.e7
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC7023678
- OpenAlex
- W2811470308
- Cited by
- 394
- References
- 68
- Citations by year
- 2026: 44 · 2025: 50 · 2024: 62 · 2023: 50 · 2022: 49 · 2021: 51 · 2020: 42 · 2019: 31 · 2018: 15
- FWCI
- 20.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH NRSA (1F32NS077840-01A1)
- NIH NIMH (R01 2R01MH083686-06)
- NIH (R37NS081242-06)
- 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
- reward coding, hippocampus, CA1, subiculum, place cells, goal-directed navigation, virtual reality navigation, reward anticipation
- MeSH terms
- Virtual Reality, Animals, Hippocampus, Motivation, Neurons, Reward, Task Performance and Analysis, Mice, CA1 Region, Hippocampal, Optical Imaging, Spatial Navigation
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
