Kentros, C. G., Agnihotri, N. T., Streater, S., Hawkins, R. D. & Kandel, E. R. Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42, 283–295 (2004).
Ziv, Y. et al. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 16, 264–266 (2013).
Driscoll, L. N., Duncker, L. & Harvey, C. D. Representational drift: emerging theories for continual learning and experimental future directions. Curr. Opin. Neurobiol. 76, 102609 (2022).
Rubin, A., Geva, N., Sheintuch, L. & Ziv, Y. Hippocampal ensemble dynamics timestamp events in long-term memory. eLife 4, e12247 (2015).
Dupret, D., O’Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995–1002 (2010).
Sadeh, S. & Clopath, C. Contribution of behavioural variability to representational drift. eLife 11, e77907 (2022).
Liberti, W. A., Schmid, T. A., Forli, A., Snyder, M. & Yartsev, M. M. A stable hippocampal code in freely flying bats. Nature 604, 98–103 (2022).
Thompson, L. T. & Best, P. J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 509, 299–308 (1990).
Hainmueller, T. & Bartos, M. Parallel emergence of stable and dynamic memory engrams in the hippocampus. Nature 558, 292–296 (2018).
Dong, C., Madar, A. D. & Sheffield, M. E. J. Distinct place cell dynamics in CA1 and CA3 encode experience in new environments. Nat. Commun. 12, 2977 (2021).
Sheintuch, L., Geva, N., Deitch, D., Rubin, A. & Ziv, Y. Organization of hippocampal CA3 into correlated cell blockemblies supports a stable spatial code. Cell Rep. 42, 112119 (2023).
Geva, N., Deitch, D., Rubin, A. & Ziv, Y. Time and experience differentially affect distinct aspects of hippocampal representational drift. Neuron 111, 2357–2366.e5 (2023).
Rule, M. E. et al. Stable task information from an unstable neural population. eLife 9, e51121 (2020).
Aitken, F. & Kok, P. Hippocampal representations switch from errors to predictions during acquisition of predictive blockociations. Nat. Commun. 13, 3294 (2022).
Mblocket, P., Qin, S. & Zavatone-Veth, J. A. Drifting neuronal representations: bug or feature? Biol. Cybern. 116, 253–266 (2022).
Mallory, C. S., Hardcastle, K., Bant, J. S. & Giocomo, L. M. Grid scale drives the scale and long-term stability of place maps. Nat. Neurosci. 21, 270–282 (2018).
McNaughton, B. L., Barnes, C. A. & O’Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52, 41–49 (1983).
Tchernichovski, O., Benjamini, Y. & Golani, I. The dynamics of long-term exploration in the rat: Part I. A phase-plane blockysis of the relationship between location and velocity. Biol. Cybern. 78, 423–432 (1998).
Moreno, M. M. et al. Olfactory perceptual learning requires adult neurogenesis. Proc. Natl Acad. Sci. USA 106, 17980–17985 (2009).
Trinh, K. & Storm, D. R. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6, 519–525 (2003).
Zou, J. et al. Targeted deletion of ERK5 MAP kinase in the developing nervous system impairs development of GABAergic interneurons in the main olfactory bulb and behavioral discrimination between structurally similar odorants. J. Neurosci. 32, 4118–4132 (2012).
Radvansky, B. A. & Dombeck, D. A. An olfactory virtual reality system for mice. Nat. Commun. 9, 839 (2018).
Radvansky, B. A., Oh, J. Y., Climer, J. R. & Dombeck, D. A. Behavior determines the hippocampal spatial mapping of a multisensory environment. Cell Rep. 36, 109444 (2021).
Ryan, T. J. & Frankland, P. W. Forgetting as a form of adaptive engram cell plasticity. Nat. Rev. Neurosci. 23, 173–186 (2022).
Keinath, A. T., Mosser, C.-A. & Brandon, M. P. The representation of context in mouse hippocampus is preserved despite neural drift. Nat. Commun. 13, 2415 (2022).
Khatib, D. et al. Active experience, not time, determines within-day representational drift in dorsal CA1. Neuron 111, 2348–2356.e5 (2023).
Krishnan, S. & Sheffield, M. E. J. Reward expectation reduces representational drift in the hippocampus. Preprint at bioRxiv (2023).
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L. & Tank, D. W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13, 1433–1440 (2010).
Sheffield, M. E. J., Adoff, M. D. & Dombeck, D. A. Increased prevalence of calcium transients across the dendritic arbor during place field formation. Neuron 96, 490–504.e5 (2017).
Rechavi, Y., Rubin, A., Yizhar, O. & Ziv, Y. Exercise increases information content and affects long-term stability of hippocampal place codes. Cell Rep. 41, 111695 (2022).
de Snoo, M. L., Miller, A. M. P., Ramsaran, A. I., Josselyn, S. A. & Frankland, P. W. Exercise accelerates place cell representational drift. Curr. Biol. 33, R96–R97 (2023).
Priestley, J. B., Bowler, J. C., Rolotti, S. V., Fusi, S. & Losonczy, A. Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences. Neuron 110, 1978–1992.e6 (2022).
Gauthier, J. L. & Tank, D. W. A dedicated population for reward coding in the hippocampus. Neuron 99, 179–193.e7 (2018).
Pettit, N. L., Yuan, X. C. & Harvey, C. D. Hippocampal place codes are gated by behavioral engagement. Nat. Neurosci. 25, 561–566 (2022).
Katlowitz, K. A., Picardo, M. A. & Long, M. A. Stable sequential activity underlying the maintenance of a precisely executed skilled behavior. Neuron 98, 1133–1140.e3 (2018).
Liberti, W. A. et al. Unstable neurons underlie a stable learned behavior. Nat. Neurosci. 19, 1665–1671 (2016).
Benavides-Piccione, R. et al. Differential structure of hippocampal CA1 pyramidal neurons in the human and mouse. Cereb. Cortex 30, 730–752 (2020).
Climer, J. R. & Dombeck, D. A. Information theoretic approaches to deciphering the neural code with functional fluorescence imaging. eNeuro (2021).
Dewan, A. et al. Single olfactory receptors set odor detection thresholds. Nat. Commun. 9, 2887 (2018).
Anderson, M. I. & Jeffery, K. J. Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827–8835 (2003).
Zhang, S. & Manahan-Vaughan, D. Spatial olfactory learning contributes to place field formation in the hippocampus. Cereb. Cortex 25, 423–432 (2015).
Save, E., Nerad, L. & Poucet, B. Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10, 64–76 (2000).
Muller, R. U. & Kubie, J. L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987).
Bostock, E., Muller, R. U. & Kubie, J. L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193–205 (1991).
Dozio, N., Maggioni, E., Pittera, D., Gallace, A. & Obrist, M. May I smell your attention: exploration of smell and sound for visuospatial attention in virtual reality. Front. Psychol. 12, 671470 (2021).
Stefanini, F. et al. A distributed neural code in the dentate gyrus and in CA1. Neuron 107, 703–716.e4 (2020).
Rubin, A. et al. Revealing neural correlates of behavior without behavioral measurements. Nat. Commun. 10, 4745 (2019).
Snyder, M. C., Qi, K. K. & Yartsev, M. M. Neural representation of human experimenters in the bat hippocampus. Nat. Neurosci. 27, 1675–1679 (2024).
Chiu, Y., Dong, C., Krishnan, S. & Sheffield, M. E. J. The precision of place fields governs their fate across epochs of experience. eNeuro (2023).
Aikath, D., Weible, A. P., Rowland, D. C. & Kentros, C. G. Role of self-generated odor cues in contextual representation. Hippocampus 24, 1039–1051 (2014).
Wood, E. R., Dudchenko, P. A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).
Epsztein, J., Brecht, M. & Lee, A. K. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70, 109–120 (2011).
Bittner, K. C. et al. Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons. Nat. Neurosci. 18, 1133–1142 (2015).
Delamare, G., Zaki, Y., Cai, D. J. & Clopath, C. Drift of neural ensembles driven by slow fluctuations of intrinsic excitability. eLife 12, RP88053 (2024).
Cai, D. J. et al. A shared neural ensemble links distinct contextual memories encoded close in time. Nature 534, 115–118 (2016).
Oh, M. M., Oliveira, F. A. & Disterhoft, J. F. Learning and aging related changes in intrinsic neuronal excitability. Front. Ageing Neurosci. (2010).
Las, L. & Ulanovsky, N. in Space, Time and Memory in the Hippocampal Formation (eds Derdikman, D. & Knierim, J. J.) 431–461 (2014).
Heys, J. G., MacLeod, K. M., Moss, C. F. & Hblockelmo, M. E. Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science 340, 363–367 (2013).
Jensen, K., Harpaz, N., Dhawale, A., Wolff, S. & Ölveczky, B. Long-term stability of single neuron activity in the motor system. Nat. Neurosci. 25, 1664–1674 (2022).
Schoonover, C. E., Ohashi, S. N., Axel, R. & Fink, A. J. P. Representational drift in primary olfactory cortex. Nature 594, 541–546 (2021).
Driscoll, L. N., Pettit, N. L., Minderer, M., Chettih, S. N. & Harvey, C. D. Dynamic reorganization of neuronal activity patterns in parietal cortex. Cell 170, 986–999.e16 (2017).
Dhawale, A. K., Wolff, S. B. E., Ko, R. & Ölveczky, B. P. The basal ganglia control the detailed kinematics of learned motor skills. Nat. Neurosci. 24, 1256–1269 (2021).
Zhang, Y. et al. Fast and sensitive GCaMP calcium indicators for imaging neural populations. Nature 615, 884–891 (2023).
Aronov, D. & Tank, D. W. Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 84, 442–456 (2014).
Pachitariu M. et al. Suite2p: beyond 10,000 neurons with standard two-photon microscopy. Preprint at bioRxiv (2017).
Dombeck, D. A., Khabbaz, A. N., Collman, F., Adelman, T. L. & Tank, D. W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43–57 (2007).
Sheintuch, L. et al. Tracking the same neurons across multiple days in Ca2+ imaging data. Cell Rep. 21, 1102–1115 (2017).
Zhang, K., Ginzburg, I., McNaughton, B. L. & Sejnowski, T. J. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79, 1017–1044 (1998).
Belkin, M. & Niyogi, P. Laplacian Eigenmaps for dimensionality reduction and data representation. Neural Comput. 15, 1373–1396 (2003).
Buzsáki, G. & Mizuseki, K. The log-dynamic brain: how skewed distributions affect network operations. Nat. Rev. Neurosci. 15, 264–278 (2014).
Zou, H. & Hastie, T. Regularization and variable selection via the elastic net. J. R. Stat. Soc. B 67, 301–320 (2005).
Climer, J., Davoudi, H., Oh, J. & Dombeck, D. Hippocampal representations drift in stable multisensory environments (1.0) [Data set]. Zenodo (2025).
