The subiculum is a patchwork of discrete subregions
Open accessAbstract
In the hippocampus, the classical pyramidal cell type of the subiculum acts as a primary output, conveying hippocampal signals to a diverse suite of downstream regions. Accumulating evidence suggests that the subiculum pyramidal cell population may actually be comprised of discrete subclasses. Here, we investigated the extent and organizational principles governing pyramidal cell heterogeneity throughout the mouse subiculum. Using single-cell RNA-seq, we find that the subiculum pyramidal cell population can be deconstructed into eight separable subclasses. These subclasses were mapped onto abutting spatial domains, ultimately producing a complex laminar and columnar organization with heterogeneity across classical dorsal-ventral, proximal-distal, and superficial-deep axes. We further show that these transcriptomically defined subclasses correspond to differential protein products and can be associated with specific projection targets. This work deconstructs the complex landscape of subiculum pyramidal cells into spatially segregated subclasses that may be observed, controlled, and interpreted in future experiments.
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?
Comparing this taxonomy with six previous studies, they found generally good but variable correspondences.
“Comparing this taxonomy with six previous studies (Cembrowski et al., 2018; Harris et al., 2018; Saunders et al., 2018; Tasic et al., 2018; Yao et al., 2020; Zeisel et al., 2018), we found generally good but variable correspondences”
From A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation (2021) · cites this paper as Cembrowski et al., 2018
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
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
(2008) · Journal of Machine Learning Research · Cited by 33,051 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322 · see citing works
Spatial reconstruction of single-cell gene expression data
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3192 · Cited by 7,055 · see citing works
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · 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
Functional organization of the hippocampal longitudinal axis
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3785 · Cited by 1,738 · see citing works
Leptin Action on GABAergic Neurons Prevents Obesity and Reduces Inhibitory Tone to POMC Neurons
Vong, L., Ye, C., Yang, Z., Choi, B. J., Chua, S. C., & Lowell, B. B. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.028 · Cited by 1,203 · see citing works
A Designer AAV Variant Permits Efficient Retrograde Access to Projection Neurons
Tervo, D. G. R., Hwang, B., Viswanathan, S., Gaj, T., Lavzin, M., Ritola, K., Lindo, S. E., Michael, S. C., Кулешова, Е. П., Ojala, D. S., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.021 · Cited by 1,170 · see citing works
Reduced fear expression after lesions of the ventral hippocampus
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152112399 · Cited by 912 · see citing works
Neuronal cell-type classification: challenges, opportunities and the path forward
Zeng, H., & Sanes, J. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.85 · Cited by 841 · see citing works
Div-Seq: Single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons
Habib, N., Li, Y., Heidenreich, M., Swiech, L., Avraham-Davidi, I., Trombetta, J. J., Hession, C., Zhang, F., & Regev, A. (2016) · Science · doi:10.1126/science.aad7038 · Cited by 601 · see citing works
Neunuebel, J. P., & Knierim, J. J. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.017 · Cited by 454 · see citing works
Knierim, J. J., Neunuebel, J. P., & Deshmukh, S. S. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0369 · Cited by 425 · see citing works
Hipposeq: a comprehensive RNA-seq database of gene expression in hippocampal principal neurons
Cembrowski, M. S., Wang, L., Sugino, K., Shields, B. C., & Spruston, N. (2016) · eLife · doi:10.7554/elife.14997 · Cited by 422 · see citing works
Genomic anatomy of the hippocampus
Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L., MacPherson, C. R., Mortrud, M. T., Cusick, A., Riley, Z. L., Sunkin, S. M., Bernard, A., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.12.008 · Cited by 403 · see citing works
Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells
Lee, S.-H., Marchionni, I., Bezaire, M., Varga, C., Danielson, N., Lovett-Barron, M., Losonczy, A., & Soltesz, I. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.034 · Cited by 358 · see citing works
CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus
Soltesz, I., & Losonczy, A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0118-0 · Cited by 333 · see citing works
Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons
Cembrowski, M. S., Bachman, J. L., Wang, L., Sugino, K., Shields, B. C., & Spruston, N. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.013 · Cited by 328 · 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
Knierim, J. J., Lee, I., & Hargreaves, E. L. (2006) · Hippocampus · doi:10.1002/hipo.20203 · Cited by 259 · see citing works
Hippocampal—diencephalic—cingulate networks for memory and emotion: an anatomical guide
Bubb, E. J., Kinnavane, L., & Aggleton, J. P. (2017) · Brain and Neuroscience Advances · doi:10.1177/2398212817723443 · Cited by 234 · see citing works
Naber, P. A., & Witter, M. P. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980413)393:3 · Cited by 219 · see citing works
Dissociable Structural and Functional Hippocampal Outputs via Distinct Subiculum Cell Classes
Cembrowski, M. S., Phillips, M. G., DiLisio, S. F., Shields, B. C., Winnubst, J., Chandrashekar, J. V., Bas, E., & Spruston, N. (2018) · Cell · doi:10.1016/j.cell.2018.03.031 · Cited by 195 · see citing works
Lee, H., Wang, C., Deshmukh, S. S., & Knierim, J. J. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.012 · Cited by 164 · see citing works
Connections of the subiculum of the rat: Topography in relation to columnar and laminar organization
Witter, M. P. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.06.022 · Cited by 155 · see citing works
Laminar organization of the pyramidal cell layer of the subiculum in the rat
Ishizuka, N. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1195 · Cited by 144 · see citing works
O’Mara, S. M., Sanchez-Vives, M. V., Brotons‐Mas, J. R., & O‘Hare, E. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.03.040 · Cited by 137 · see citing works
Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus
Jarsky, T., Mady, R., Kennedy, B., & Spruston, N. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21564 · Cited by 130 · see citing works
Aggleton, J. P., & Christiansen, K. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.003 · Cited by 128 · see citing works
A manual method for the purification of fluorescently labeled neurons from the mammalian brain
Hempel, C. M., Sugino, K., & Nelson, S. B. (2007) · Nature Protocols · doi:10.1038/nprot.2007.416 · Cited by 124 · see citing works
Functional diversity along the transverse axis of hippocampal area CA1
Igarashi, K. M., Ito, H., Moser, E. I., & Moser, M. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.06.004 · Cited by 104 · see citing works
Kim, Y., & Spruston, N. (2011) · Hippocampus · doi:10.1002/hipo.20931 · Cited by 103 · see citing works
Noncanonical connections between the subiculum and hippocampal CA1
Xu, X., Sun, Y., Holmes, T. C., & López, A. J. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24024 · Cited by 88 · see citing works
Continuous Variation within Cell Types of the Nervous System
Cembrowski, M. S., & Menon, V. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.02.010 · Cited by 80 · see citing works
Yamawaki, N., Corcoran, K. A., Guedea, A. L., Shepherd, G. M., & Radulović, J. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy142 · Cited by 75 · see citing works
Mnemonic Functions for Nonlinear Dendritic Integration in Hippocampal Pyramidal Circuits
Kaifosh, P., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.019 · Cited by 74 · see citing works
Immunohistochemical investigation of the internal structure of the mouse subiculum
Ishihara, Y., & Fukuda, T. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.09.027 · Cited by 43 · see citing works
Routes to, from and within the subiculum
Böhm, C., Peng, Y., Geiger, J. R. P., & Schmitz, D. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2848-4 · Cited by 42 · see citing works
Dissociable Structural and Functional Hippocampal Outputs via Distinct Subiculum Cell Classes
Cembrowski, M. S., Phillips, M. G., DiLisio, S. F., Shields, B. C., Winnubst, J., Chandrashekar, J. V., Bas, E., & Spruston, N. (2018) · Cell · doi:10.1016/j.cell.2018.07.039 · Cited by 32 · see citing works
Integrating Results across Methodologies Is Essential for Producing Robust Neuronal Taxonomies
Cembrowski, M. S., & Spruston, N. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.023 · Cited by 17 · see citing works
Cembrowski, M. S. (2018) · Figshare · doi:10.6084/m9.figshare.7140350 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 46 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Paxinos G Franklin KBJ 2004 The Mouse Brain in Stereotaxic Coordinates, Compact Second edition Amsterdam; Boston Elsevier Academic Press
Cited by
Sorted by citations
Robust decomposition of cell type mixtures in spatial transcriptomics
Cable, D. M., Murray, E., Zou, L. S., Goeva, A., Macosko, E. Z., Chen, F., & Irizarry, R. A. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-00830-w · Cited by 1,487 · see citing works
A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation
Yao, Z., van Velthoven, C. T. J., Nguyen, T. N., Goldy, J., Sedeno-Cortes, A. E., Baftizadeh, F., Bertagnolli, D., Casper, T., Chiang, M., Crichton, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.021 · Cited by 1,065 · see citing works
Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
Winnubst, J., Bas, E., Ferreira, T. A., Wu, Z., Economo, M. N., Edson, P., Arthur, B. J., Bruns, C., Rokicki, K., Schauder, D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.07.042 · Cited by 538 · see citing works
What is a cell type and how to define it?
Zeng, H. (2022) · Cell · doi:10.1016/j.cell.2022.06.031 · Cited by 439 · see citing works
Heterogeneity within classical cell types is the rule: lessons from hippocampal pyramidal neurons
Cembrowski, M. S., & Spruston, N. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0125-5 · Cited by 258 · see citing works
Ayhan, F., Kulkarni, A., Berto, S., Sivaprakasam, K., Douglas, C., Lega, B. C., & Konopka, G. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.003 · Cited by 198 · see citing works
Hippocampus: Molecular, Cellular, and Circuit Features in Anxiety
Shi, H.-J., Wang, S., Wang, X.-P., Zhang, R.-X., & Zhu, L.-J. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01020-1 · Cited by 126 · see citing works
Propagation of hippocampal ripples to the neocortex by way of a subiculum-retrosplenial pathway
Nitzan, N., McKenzie, S., Beed, P. S., English, D. F., Oldani, S., Tukker, J. J., Buzsáki, G., & Schmitz, D. (2020) · Nature Communications · doi:10.1038/s41467-020-15787-8 · Cited by 129 · see citing works
Vector trace cells in the subiculum of the hippocampal formation
Poulter, S. L., Lee, S. A., Dachtler, J., Wills, T. J., & Lever, C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00761-w · Cited by 88 · see citing works
Hudson, R., Renard, J., Norris, C., Rushlow, W. J., & Laviolette, S. R. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0708-19.2019 · Cited by 86 · see citing works
Extensive and spatially variable within-cell-type heterogeneity across the basolateral amygdala
O’Leary, T. P., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2020) · eLife · doi:10.7554/elife.59003 · Cited by 75 · see citing works
Ding, S.-L., Yao, Z., Hirokawa, K. E., Nguyen, T. N., Graybuck, L. T., Fong, O., Bohn, P., Ngo, K., Smith, K. A., Koch, C., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107648 · Cited by 82 · see citing works
Erwin, S. R., Sun, W., Copeland, M., Lindo, S. E., Spruston, N., & Cembrowski, M. S. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107551 · Cited by 77 · see citing works
Sánchez-Bellot, C., Alsubaie, R., Mishchanchuk, K., Wee, R. W. S., & MacAskill, A. F. (2022) · Nature Communications · doi:10.1038/s41467-022-27977-7 · Cited by 64 · see citing works
Discrete subicular circuits control generalization of hippocampal seizures
Fei, F., Wang, X., Xu, C., Shi, J., Gong, Y., Cheng, H., Lai, N., Ruan, Y., Ding, Y., Wang, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32742-x · Cited by 62 · see citing works
Spatially patterned excitatory neuron subtypes and projections of the claustrum
Erwin, S. R., Bristow, B. N., Sullivan, K. E., Kendrick, R. M., Marriott, B. A., Wang, L., Clements, J., Lemire, A. L., Jackson, J., & Cembrowski, M. S. (2021) · eLife · doi:10.7554/elife.68967 · Cited by 61 · see citing works
Biased Connectivity of Brain-wide Inputs to Ventral Subiculum Output Neurons
Wee, R. W. S., & MacAskill, A. F. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.093 · Cited by 54 · see citing works
Time to retire the serial Papez circuit: Implications for space, memory, and attention
Aggleton, J. P., Nelson, A. J. D., & O’Mara, S. M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104813 · Cited by 56 · see citing works
Task-dependent mixed selectivity in the subiculum
Ledergerber, D., Battistin, C., Blackstad, J. S., Gardner, R. J., Witter, M. P., Moser, M., Roudi, Y., & Moser, E. I. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109175 · Cited by 49 · see citing works
Witter, M. P., & Amaral, D. G. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24983 · Cited by 49 · see citing works
Thompson, J. R., Nelson, E. D., Tippani, M., Ramnauth, A. D., Divecha, H. R., Miller, R. A., Eagles, N. J., Pattie, E. A., Kwon, S., Bach, S. V., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-02022-0 · Cited by 51 · see citing works
Dunn, A. R., & Kaczorowski, C. C. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107069 · Cited by 42 · see citing works
Internal-state-dependent control of feeding behavior via hippocampal ghrelin signaling
Wee, R. W. S., Mishchanchuk, K., AlSubaie, R., Church, T. W., Gold, M. G., & MacAskill, A. F. (2023) · Neuron · doi:10.1016/j.neuron.2023.10.016 · Cited by 50 · see citing works
Lin, X., Amalraj, M., Blanton, C., Avila, B., Holmes, T. C., Nitz, D. A., & Xu, X. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001127 · Cited by 48 · see citing works
Neuronal cell types, projections, and spatial organization of the central amygdala
O’Leary, T. P., Kendrick, R. M., Bristow, B. N., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2022) · iScience · doi:10.1016/j.isci.2022.105497 · Cited by 38 · see citing works
Single-cell transcriptomics as a framework and roadmap for understanding the brain
Cembrowski, M. S. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.108353 · Cited by 32 · see citing works
Wang, W. X., & Lefebvre, J. L. (2022) · Nature Communications · doi:10.1038/s41467-022-30977-2 · Cited by 32 · see citing works
Kupferschmidt, D. A., Cummings, K. A., Joffe, M. E., MacAskill, A. F., Malik, R., Sánchez-Bellot, C., Tejeda, H. A., & Yarur, H. E. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1136-22.2022 · Cited by 29 · see citing works
Dissecting the role of subiculum in epilepsy: Research update and translational potential
Fei, F., Wang, X., Wang, Y., & Chen, Z. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102029 · Cited by 28 · see citing works
Dopamine D1–D2 signalling in hippocampus arbitrates approach and avoidance
Godino, A., Salery, M., Minier-Toribio, A. M., Patel, V., Fullard, J. F., Kondev, V., Parise, E. M., Martínez-Rivera, F. J., Morel, C., Roussos, P., et al. (2025) · Nature · doi:10.1038/s41586-025-08957-5 · Cited by 26 · see citing works
Parvalbumin interneuron loss mediates repeated anesthesia-induced memory deficits in mice
Roque, P. S., Pérez, C. T., Hooshmandi, M., Wong, C., Eslamizade, M. J., Heshmati, S., Brown, N., Sharma, V. K., Lister, K. C., Goyon, V., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci159344 · Cited by 22 · see citing works
Sharp cell-type-identity changes differentiate the retrosplenial cortex from the neocortex
Sullivan, K. E., Kraus, L., Kapustina, M., Wang, L., Stach, T. R., Lemire, A. L., Clements, J., & Cembrowski, M. S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112206 · Cited by 19 · see citing works
Amaral, D. G., Lavenex, P., & Insausti, R. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0003 · Cited by 19 · see citing works
The subiculum and its role in focal epileptic disorders
Lévesque, M., & Avoli, M. (2020) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0091 · Cited by 18 · see citing works
Activity‐regulated gene expression across cell types of the mouse hippocampus
Nelson, E. D., Maynard, K. R., Nicholas, K. R., Tran, M. N., Divecha, H. R., Collado‐Torres, L., Hicks, S. C., & Martinowich, K. (2023) · Hippocampus · doi:10.1002/hipo.23548 · Cited by 15 · see citing works
scDLC: a deep learning framework to classify large sample single-cell RNA-seq data
Zhou, Y., Peng, M., Yang, B., Tong, T., Zhang, B., & Tang, N. (2022) · BMC Genomics · doi:10.1186/s12864-022-08715-1 · Cited by 15 · see citing works
Atypical hippocampal excitatory neurons express and govern object memory
Kinman, A. I., Merryweather, D. N., Erwin, S. R., Campbell, R. E., Sullivan, K. E., Kraus, L., Kapustina, M., Bristow, B. N., Zhang, M. Y., Elder, M. W., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56260-8 · Cited by 17 · see citing works
A model for mapping between the human and rodent cerebral cortex
Swanson, L. W., & Hof, P. R. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24708 · Cited by 15 · see citing works
KCNQ3 is the principal target of retigabine in CA1 and subicular excitatory neurons
Varghese, N., Lauritano, A., Taglialatela, M., & Tzingounis, A. V. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00564.2020 · Cited by 14 · see citing works
Subicular neurons represent multiple variables of a hippocampal-dependent task by using theta rhythm
Lee, S., Seol, J.-M., & Lee, I. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001546 · Cited by 13 · see citing works
Heterogeneous expression patterns of fibronectin in the mouse subiculum
Kashima, T., Noguchi, A., Ikegaya, Y., & Matsumoto, N. (2019) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2019.04.010 · Cited by 13 · see citing works
Linking axon morphology to gene expression: a strategy for neuronal cell-type classification
Winnubst, J., Spruston, N., & Harris, J. A. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.006 · Cited by 14 · see citing works
Elucidating memory in the brain via single‐cell transcriptomics
Sullivan, K. E., Kendrick, R. M., & Cembrowski, M. S. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15250 · Cited by 11 · see citing works
Franz, J., Barheier, N., Wilms, H., Tulke, S., Haas, C. A., & Häussler, U. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1142507 · Cited by 12 · see citing works
Aversive Contexts Reduce Activity in the Ventral Subiculum- BNST Pathway
Urien, L., Cohen, S., Howard, S., Yakimov, A., Nordlicht, R., & Bauer, E. P. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.019 · Cited by 10 · see citing works
Structural and Functional Properties of Hippocampal Neurons
Spruston, N., Piskorowski, R. A., Chevaleyre, V., Eyre, M. D., McBain, C. J., & Bartos, M. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0005 · Cited by 11 · see citing works
Laminar organization of pyramidal neuron cell types defines distinct CA1 hippocampal subregions
Pachicano, M., Mehta, S., Hurtado, A. H., Ard, T. D., Stanis, J., Breningstall, B. M., & Bienkowski, M. S. (2025) · Nature Communications · doi:10.1038/s41467-025-66613-y · Cited by 13 · see citing works
Aydın, A. G., Lemenze, A. D., & Bieszczad, K. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-74732-7 · Cited by 10 · see citing works
Data-driven fine-grained region discovery in the mouse brain with transformers
Lee, A. J., Dubuc, A., Kunst, M., Yao, S., Lusk, N. A., Ng, L., Zeng, H., Tasic, B., & Abbasi-Asl, R. (2025) · Nature Communications · doi:10.1038/s41467-025-64259-4 · Cited by 13 · see citing works
Hippocampal transcriptomic responses to enzyme‐mediated cellular dissociation
Harris, R. M., Kao, H., Alarcón, J. M., Hofmann, H. A., & Fenton, A. A. (2019) · Hippocampus · doi:10.1002/hipo.23095 · Cited by 10 · see citing works
The subiculum role on learning and memory tasks using rats and mice: A scoping review
de Melo, M. B., Daldegan‐Bueno, D., Favaro, V. M., & Oliveira, M. G. M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105460 · Cited by 9 · see citing works
Maliković, J., Amrein, I., Vinciguerra, L., Lalošević, D., Wolfer, D. P., & Slomianka, L. (2023) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2022.1070035 · Cited by 8 · see citing works
Probing subicular inputs to the medial prefrontal cortex
Beerens, S., Vroman, R., Webster, J. F., & Wozny, C. (2021) · iScience · doi:10.1016/j.isci.2021.102856 · Cited by 7 · see citing works
Task-dependent mixed selectivity in the subiculumPreprint
Ledergerber, D., Battistin, C., Blackstad, J. S., Gardner, R. J., Witter, M. P., Moser, M., Roudi, Y., & Moser, E. I. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.06.129221 · Cited by 7 · see citing works
Murphy, T. R., Amidon, R. F., Donohue, J. D., Li, L., & Anderson, G. R. (2024) · iScience · doi:10.1016/j.isci.2024.108799 · Cited by 6 · see citing works
Flaive, A., Cabelguen, J., & Ryczko, D. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00179.2020 · Cited by 5 · see citing works
Parvalbumin expression identifies subicular principal cells with high projection specificity
Baccini, G., Foggetti, A., Wernet, N., Engelhardt, K.-A., Steinecke, C.-S., Edelmann, E., Balueva, K., Kronenbitter, K., Michels, J., Kulik, Á., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116004 · Cited by 4 · see citing works
Lin, X., Amalraj, M., Blanton, C., Avila, B., Holmes, T. C., Nitz, D. A., & Xu, X. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.01.429124 · Cited by 5 · see citing works
In Vivo Quantification of White Matter Pathways in the Human Hippocampus
Gumus, M., Bourganos, A., & Mack, M. L. (2025) · Human Brain Mapping · doi:10.1002/hbm.70417 · Cited by 4 · see citing works
Hu, G., Zheng, Y., Zhang, B., Zhao, C. N., Xu, L., Wei, J., Jing, J., Liu, Y., Zeng, T., & Zhou, Y. (2024) · Molecular Biology of the Cell · doi:10.1091/mbc.e23-12-0492 · Cited by 4 · see citing works
Potenza, M. L., Blankvoort, S., Carvalho, M. M., Grimstvedt, J. S., Maria, V. D., Moan, K., Nair, R. R., Flatset, M. S., Zhang, Q., Thomas, L. F., et al. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1274174 · Cited by 4 · see citing works
Organization and development of hippocampal circuits
Pignatelli, M., & Rockland, K. S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814411-4.00009-3 · Cited by 4 · see citing works
A specific olfactory bulb interneuron subtype Tpbg/5T4 generated at embryonic and neonatal stages
Tsuboi, A. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1427378 · Cited by 3 · see citing works
Olkhova, E. A., Smith, L. A., Dennis, B. H., Ng, Y. S., LeBeau, F. E. N., & Gorman, G. S. (2024) · Biochemical Society Transactions · doi:10.1042/bst20230191 · Cited by 3 · see citing works
Lopez, K. M., Mancero-Montalvo, R., Iturralde-Carrillo, A., Feng, A., Shaver, T. L., Choi, H., Jaiswal, N., Roman, J. K., Bhakta, P. A., Chavez, G. J., et al. (2025) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2025.2529503 · Cited by 3 · see citing works
Sex Differences in the Ventral Subiculum's Microcircuitry and Function
Miller, C. N., & Aoto, J. N. (2025) · Hippocampus · doi:10.1002/hipo.70054 · Cited by 3 · see citing works
Propagation of Hippocampal Ripples to the Neocortex by Way of a Subiculum-Retrospleanial PathwayPreprint
Nitzan, N., McKenzie, S., English, D., Beed, P., Oldani, S., Tukker, J. J., Buzsáki, G., & Schmitz, D. (2019) · Social Science Research Network · doi:10.2139/ssrn.3381954
Control of Innate Olfactory Valence by Segregated Cortical Amygdala CircuitsPreprint
Howe, J., Chan, C. L., Lee, D., Blanquart, M., Romero, H. K., Zadina, A. N., Lemieux, M., Mills, F., Desplats, P., Tye, K. M., et al. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4884646 · Cited by 3 · see citing works
Neuronal Heterogeneity in the Medial Septum and Diagonal Band of Broca: Classes and ContinuaPreprint
Kuhn, F., Mocellin, P., Pupe, S., Wang, L., Lemire, A. L., Sosulina, L., Barnstedt, O., Spruston, N., Cembrowski, M. S., & Remy, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.27.609593 · Cited by 4 · see citing works
Distinct molecular mechanisms of stress habituation in the mouse hippocampusPreprint
Waag, R., von Ziegler, L., Sturman, O., Sonder, E., Leonardi, J., Frei, S., Gapp, K., Germain, P., & Bohacek, J. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.04.641433 · Cited by 3 · see citing works
Wang, W. X., & Lefebvre, J. L. (2020) · doi:10.1101/2020.02.29.971366
Prenatal alcohol damages the subiculum, a key region for learning and memory: A narrative review
Lopez, K. M., Shaver, T. L., & Valenzuela, C. F. (2026) · Alcohol · doi:10.1016/j.alcohol.2026.03.008 · Cited by 2 · see citing works
Structural diversity inside the mouse subiculum revealed by a new marker protein fibronectin 1
Ishihara, Y., Miyamoto, Y., Esumi, S., & Fukuda, T. (2024) · Anatomical Science International · doi:10.1007/s12565-024-00803-4 · Cited by 2 · see citing works
Single-cell map of the female brain across reproductive transitionsPreprint
Demarchi, L., Tickerhoof, M. C., Kameshwar, A. K. S., Rocks, D., Ouldibbat, L., Milosevic, A., Suzuki, M., & Kundaković, M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.03.697507 · Cited by 2 · see citing works
Ishihara, Y., Sato, F., Guinet, A., Grosser, S., Vida, I., Kubota, Y., & Takayama, C. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2024.12.048 · Cited by 1 · see citing works
Direct excitatory loop and theta resonance in the anterior cingulate-mediodorsal thalamic circuit
Yoshimoto, A., Morikawa, S., Takeuchi, H., & Ikegaya, Y. (2025) · Communications Biology · doi:10.1038/s42003-025-08431-y · Cited by 1 · see citing works
Exercise for brain health: From cells to circuits
Vivar, C., Orihuela, L. P., & Apostol, G. (2025) · Progress in brain research · doi:10.1016/bs.pbr.2025.05.006 · Cited by 1 · see citing works
Chen, J., Chen, T., Zhu, X., Dai, X., Fang, Z., Sun, Y., Zhao, Q., Zheng, B., Xu, S., Wang, Y., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-09204-3 · Cited by 1 · see citing works
Ventral subicular pyramidal neurons contribute to epileptogenesis via anterior thalamic circuit
Gong, Y., Zhang, S., Fei, F., Huang, L., Guo, X., Li, M., Yang, Y., Liu, Y., Wang, Y., Chen, Z., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-09402-z · Cited by 1 · see citing works
Spatial Organization of Morpho‐Electric Subtypes of Pyramidal Neuron in the Subiculum
Guinet, A., Behr, J., Vida, I., & Grosser, S. (2026) · Hippocampus · doi:10.1002/hipo.70081 · Cited by 1 · see citing works
Divergent hippocampal output via covariant local and long-range neuronal structure
Campbell, R., Zhang, M. Y., Merryweather, D. N., & Cembrowski, M. S. (2026) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2026.102893 · Cited by 2 · see citing works
Subiculum Encodes Environmental Structure
Place, R., Xu, E., Sun, Y., Olson, J. M., & Nitz, D. A. (2026) · Hippocampus · doi:10.1002/hipo.70086 · Cited by 1 · see citing works
The subiculum: cell-type-specific composition, computation, and function
Kinman, A. I., Kraus, L., & Cembrowski, M. S. (2026) · Trends in Neurosciences · doi:10.1016/j.tins.2026.02.004 · Cited by 1 · see citing works
Fei, F., Shi, J., Xi, J., Xu, Y., Ying, S., Fan, X., Lu, W., Li, Z., Li, M., Wang, Y., et al. (2026) · Advanced Science · doi:10.1002/advs.202516399 · Cited by 1 · see citing works
Martin, S. K., Aggleton, J. P., & O’Mara, S. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.07.415125
Lee, S., Seol, J.-M., & Lee, I. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.11.456028
Lewis, S. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0106-0
Genetically distinct parallel projection populations from ventral hippocampus to prefrontal cortexPreprint
Sánchez-Bellot, C., & MacAskill, A. F. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.18.529052
Santos‐Silva, T. (2023) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2023.tde-10112023-160657
Role of the Subiculum in Focal Epilepsy
Evstratova, A., Díaz-Fernández, B., Lévesque, M., Avoli, M., & Huberfeld, G. (2024) · Oxford University Press eBooks · doi:10.1093/med/9780197549469.003.0010 · Cited by 1 · see citing works
Goodman, A. M., Schellinger, E. D., Kahn, J. B., Takano, H., Coulter, D. A., & Joksimovic, S. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.12.675815
Essential function of Nr4a2 in subicular development and social novelty
Liu, X.-Y., Tao, Y., Zhang, Q., Liu, W., Zhao, L., Hu, Z., Zhou, B.-Y., Li, Z.-X., Qi, C., Zhang, L., et al. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.12.014
Zhou, Y., Peng, M., Yang, B., Tong, T., Zhang, B., & Tang, N. (2022) · Figshare · doi:10.6084/m9.figshare.20306725
Bassett, T. E., Wang, Y., Wood, E. M., Zhang, H., Petrovic, Z., Prifti, V., Jovasevic, V., Yamawaki, N., Ren, L. Y., Khalatyan, N., et al. (2026) · iScience · doi:10.1016/j.isci.2026.115317 · Cited by 1 · see citing works
Synaptic connectivity and head-direction signal integration in the mouse presubiculum
Richevaux, L. (2021) · theses.fr (ABES) · doi:10.70675/8b297dc9zb72bz4762z951dz9ab52c80ce77
GABAergic projection from the subiculum to the medial entorhinal cortex in mice and ratsPreprint
Aimi, T., Shibuya, T., Umeno, H., Karasawa, K., Tsutsui, K., Ohara, S., & Kitanishi, T. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.06.730551
GABAergic subiculum–medial entorhinal projection in mice and rats
Aimi, T., Shibuya, T., Umeno, H., Karasawa, K., TSUTSUI, K.-I., Ohara, S., & Kitanishi, T. (2026) · Cerebral Cortex · doi:10.1093/cercor/bhag177
- Authors
- Cembrowski, M. S., Wang, L., Lemire, A. L., Copeland, M., DiLisio, S. F., Clements, J., & Spruston, N.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Cembrowski, Mark S
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-10-30
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6226292
- OpenAlex
- W2899509757
- Cited by
- 98
- References
- 46
- Citations by year
- 2026: 10 · 2025: 19 · 2024: 10 · 2023: 9 · 2022: 12 · 2021: 13 · 2020: 14 · 2019: 9 · 2018: 2
- FWCI
- 3.38
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- subiculum, pyramidal neurons, neuronal heterogeneity, hippocampal output, laminar organization, columnar organization, dorsal-ventral axis, single-cell transcriptomics, mice
- MeSH terms
- Animals, Gene Expression Regulation, Hippocampus, Male, Mice, Transgenic, S100 Proteins, Reproducibility of Results, Sequence Analysis, RNA, Pyramidal Cells, Gene Expression Profiling, CA1 Region, Hippocampal, Single-Cell Analysis, Transcriptome
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