CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus
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Hippocampal network operations supporting spatial navigation and declarative memory are traditionally interpreted in a framework where each hippocampal area, such as the dentate gyrus, CA3, and CA1, consists of homogeneous populations of functionally equivalent principal neurons. However, heterogeneity within hippocampal principal cell populations, in particular within pyramidal cells at the main CA1 output node, is increasingly recognized and includes developmental, molecular, anatomical, and functional differences. Here we review recent progress in the delineation of hippocampal principal cell subpopulations by focusing on radially defined subpopulations of CA1 pyramidal cells, and we consider how functional segregation of information streams, in parallel channels with nonuniform properties, could represent a general organizational principle of the hippocampus supporting diverse behaviors.
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CA1 pyramidal neurons show a high level of heterogeneity at the molecular, cellular, connectivity, and in-vivo properties.
“CA1 pyramidal neurons show a high level of heterogeneity at the molecular, cellular, connectivity, and in-vivo properties90–92.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [92]
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Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · 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
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · 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
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,462 · see citing works
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · see citing works
Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Memory systems of the brain: A brief history and current perspective
Squire, L. R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.06.005 · Cited by 2,269 · see citing works
Computing with Neural Circuits: A Model
Hopfield, J. J., & Tank, D. W. (1986) · Science · doi:10.1126/science.3755256 · Cited by 2,107 · see citing works
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
de Nó, R. L. (1934) · Cited by 1,974 · see citing works
Memory, navigation and theta rhythm in the hippocampal-entorhinal system
Buzsáki, G., & Moser, E. I. (2013) · Nature Neuroscience · doi:10.1038/nn.3304 · Cited by 1,847 · 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
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
Computational analysis of the role of the hippocampus in memory
Treves, A., & Rolls, E. T. (1994) · Hippocampus · doi:10.1002/hipo.450040319 · Cited by 1,272 · see citing works
Synaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,207 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
Neurogenesis in the adult hippocampus
Kempermann, G., Song, H., & Gage, F. H. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018812 · Cited by 1,072 · see citing works
The log-dynamic brain: how skewed distributions affect network operations
Buzsáki, G., & Mizuseki, K. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3687 · Cited by 964 · see citing works
Moser, E., Moser, M. ‐., & Andersen, P. N. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03916.1993 · Cited by 916 · see citing works
Bayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900107 · Cited by 913 · 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
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
Somogyi, P., Tamás, G., Luján, R., & Buhl, E. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00061-1 · Cited by 860 · see citing works
Preplay of future place cell sequences by hippocampal cellular assemblies
Dragoi, G., & Tonegawa, S. (2011) · Nature · doi:10.1038/nature09633 · Cited by 716 · see citing works
Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning
Donato, F., Rompani, S. B., & Caroni, P. (2013) · Nature · doi:10.1038/nature12866 · Cited by 703 · see citing works
Josselyn, S. A., Köhler, S., & Frankland, P. W. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4000 · Cited by 687 · see citing works
The Neuroscience of Mammalian Associative Learning
Fanselow, M. S., & Poulos, A. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070213 · Cited by 683 · see citing works
Shah, S., Lubeck, E., Zhou, W., & Cai, L. (2016) · Neuron · doi:10.1016/j.neuron.2016.10.001 · Cited by 671 · see citing works
Ventral CA1 neurons store social memory
Okuyama, T., Kitamura, T., Roy, D. S., Itohara, S., & Tonegawa, S. (2016) · Science · doi:10.1126/science.aaf7003 · Cited by 657 · see citing works
Cenquizca, L. A., & Swanson, L. W. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.002 · Cited by 640 · see citing works
Memory Engram Cells Have Come of Age
Tonegawa, S., Liu, X., Ramirez, S., & Redondo, R. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.002 · Cited by 613 · 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
Dense Inhibitory Connectivity in Neocortex
Fino, E., & Yuste, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.025 · Cited by 532 · see citing works
Cell type–specific genetic and optogenetic tools reveal hippocampal CA2 circuits
Kohara, K., Pignatelli, M., Rivest, A. J., Jung, H.-Y., Kitamura, T., Suh, J., Frank, D., Kajikawa, K., Mise, N., Obata, Y., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3614 · Cited by 528 · see citing works
D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949
Morris, R. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00182-3 · Cited by 520 · see citing works
Packer, A. M., & Yuste, R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3131-11.2011 · Cited by 506 · see citing works
Space in the brain: How the hippocampal formation supports spatial cognition
Hartley, T., Lever, C., Burgess, N., & O'Keefe, J. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0510 · Cited by 495 · 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 478 · see citing works
Hippocampal CA1 pyramidal cells form functionally distinct sublayers
Mizuseki, K., Diba, K., Pastalkova, E., & Buzsáki, G. (2011) · Nature Neuroscience · doi:10.1038/nn.2894 · Cited by 473 · see citing works
Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations
Stark, E., Roux, L., Eichler, R., Senzai, Y., Royer, S., & Buzsáki, G. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.023 · Cited by 459 · see citing works
Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs
Sotres-Bayón, F., Sierra‐Mercado, D., Pardilla‐Delgado, E., & Quirk, G. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.028 · Cited by 451 · see citing works
Understanding memory through hippocampal remapping
Colgin, L. L., Moser, E. I., & Moser, M.-B. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.06.008 · Cited by 450 · see citing works
Coordination of entorhinal–hippocampal ensemble activity during associative learning
Igarashi, K. M., Lu, L., Colgin, L. L., Moser, M., & Moser, E. I. (2014) · Nature · doi:10.1038/nature13162 · Cited by 435 · 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
Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., Harmin, D. A., & Greenberg, M. E. (2014) · Cell · doi:10.1016/j.cell.2014.03.058 · Cited by 416 · 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
Lisman, J. E., & Otmakhova, N. A. (2001) · Hippocampus · doi:10.1002/hipo.1071 · Cited by 402 · see citing works
What is memory? The present state of the engram
Poo, M.-M., Pignatelli, M., Ryan, T. J., Tonegawa, S., Bonhoeffer, T., Martin, K. C., Rudenko, A., Tsai, L., Tsien, R. W., Fishell, G., et al. (2016) · BMC Biology · doi:10.1186/s12915-016-0261-6 · Cited by 391 · see citing works
Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity
Yoshimura, Y., & Callaway, E. M. (2005) · Nature Neuroscience · doi:10.1038/nn1565 · Cited by 390 · see citing works
Bezaire, M. J., & Soltesz, I. (2013) · Hippocampus · doi:10.1002/hipo.22141 · Cited by 373 · see citing works
Self-citationDiversity in neural firing dynamics supports both rigid and learned hippocampal sequences
Grosmark, A. D., & Buzsáki, G. (2016) · Science · doi:10.1126/science.aad1935 · Cited by 367 · see citing works
Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways
Gittis, A. H., Nelson, A., Thwin, M. T., Palop, J. J., & Kreitzer, A. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4870-09.2010 · Cited by 364 · see citing works
Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1
Dong, H., Swanson, L. W., Chen, L., Fanselow, M. S., & Toga, A. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812608106 · Cited by 361 · 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
Self-citationA computational theory of hippocampal function, and tests of the theory: New developments
Kesner, R. P., & Rolls, E. T. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.009 · Cited by 347 · 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
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
Bodor, Á. L., Katona, I., Nyíri, G., Mackie, K., Ledent, C., Hájos, N., & Freund, T. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0442-05.2005 · Cited by 325 · see citing works
The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition
Bloodgood, B. L., Sharma, N., Browne, H. A., Trepman, A. Z., & Greenberg, M. E. (2013) · Nature · doi:10.1038/nature12743 · Cited by 310 · see citing works
The time of origin of neurons in the hippocampal region of the rhesus monkey
RAKIC, P. T., & Nowakowski, R. S. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901960109 · Cited by 305 · see citing works
Specific synapses develop preferentially among sister excitatory neurons in the neocortex
Yu, Y.-C., Bultje, R. S., Wang, X., & Shi, S.-H. (2009) · Nature · doi:10.1038/nature07722 · Cited by 305 · 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
Self-citationDistinct Hippocampal Pathways Mediate Dissociable Roles of Context in Memory Retrieval
Xu, C., Krabbe, S., Gründemann, J., Botta, P., Fadok, J. P., Osakada, F., Saur, D., Grewe, B. F., Schnitzer, M. J., Callaway, E. M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.051 · Cited by 277 · see citing works
Behavior-dependent specialization of identified hippocampal interneurons
Lapray, D., Lasztóczi, B., Lagler, M., Viney, T. J., Katona, L., Valenti, O., Hartwich, K., Borhegyi, Z., Somogyi, P., & Klausberger, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3176 · Cited by 262 · see citing works
GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus
Klausberger, T. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06913.x · Cited by 260 · see citing works
Spatial Representation along the Proximodistal Axis of CA1
Henriksen, E. J., Colgin, L. L., Barnes, C. A., Witter, M. P., Moser, M., & Moser, E. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.042 · Cited by 260 · see citing works
Knierim, J. J., Lee, I., & Hargreaves, E. L. (2006) · Hippocampus · doi:10.1002/hipo.20203 · Cited by 259 · see citing works
Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples
Valero, M., Cid, E., Averkin, R. G., Aguilar, J., Sánchez-Aguilera, A., Viney, T. J., Gómez-Domínguez, D., Bellistri, E., & de la Prida, L. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4074 · Cited by 259 · see citing works
Varga, C., Golshani, P., & Soltesz, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210929109 · Cited by 253 · see citing works
Self-citationFunctional and structural underpinnings of neuronal assembly formation in learning
Holtmaat, A., & Caroni, P. (2016) · Nature Neuroscience · doi:10.1038/nn.4418 · Cited by 239 · 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
Clonally related visual cortical neurons show similar stimulus feature selectivity
Li, Y., Lü, H., Cheng, P., Ge, S., Xu, H., Shi, S., & Dan, Y. (2012) · Nature · doi:10.1038/nature11110 · Cited by 223 · see citing works
Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly
Yu, Y.-C., He, S., Chen, S., Fu, Y., Brown, K. N., Yao, X.-H., Ma, J., Gao, K. P., Sosinsky, G. E., Huang, K., et al. (2012) · Nature · doi:10.1038/nature10958 · Cited by 219 · see citing works
Target-selective GABAergic control of entorhinal cortex output
Varga, C., Lee, S. Y., & Soltesz, I. (2010) · Nature Neuroscience · doi:10.1038/nn.2570 · Cited by 219 · see citing works
Role of Hippocampal CA2 Region in Triggering Sharp-Wave Ripples
Oliva, A., Fernández‐Ruiz, A., Buzsáki, G., & Berényi, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.008 · Cited by 217 · see citing works
A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning
Li, Y., Xu, J., Liu, Y., Zhu, J., Liu, N., Zeng, W., Huang, N., Rasch, M. J., Jiang, H., Gu, X., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4517 · Cited by 210 · see citing works
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010303 · Cited by 198 · see citing works
Cannabinoid Control of Learning and Memory through HCN Channels
Maroso, M., Szabo, G. G., Kim, H. K., Alexander, A., Bui, A. D., Lee, S.-H., Lutz, B., & Soltész, I. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.023 · Cited by 186 · see citing works
Large environments reveal the statistical structure governing hippocampal representations
Rich, P. D., Liaw, H.-P., & Lee, A. K. (2014) · Science · doi:10.1126/science.1255635 · Cited by 177 · see citing works
Structured Synaptic Connectivity between Hippocampal Regions
Druckmann, S., Feng, L., Lee, B., Yook, C., Zhao, T., Magee, J. C., & Kim, J. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.026 · Cited by 177 · see citing works
Katona, L., Lapray, D., Viney, T. J., Oulhaj, A., Borhegyi, Z., Micklem, B. R., Klausberger, T., & Somogyi, P. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.007 · Cited by 169 · see citing works
Place cells are more strongly tied to landmarks in deep than in superficial CA1
Geiller, T., Fattahi, M., Choi, J.-S., & Royer, S. (2017) · Nature Communications · doi:10.1038/ncomms14531 · Cited by 163 · see citing works
Molinari, S., Battini, R., Ferrari, S., Pozzi, L., Killcross, S., Robbins, T. W., Jouvenceau, A., Billard, J., Dutar, P., Lamour, Y. A., et al. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.8028 · Cited by 160 · see citing works
Donato, F., Chowdhury, A., Lahr, M., & Caroni, P. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.011 · Cited by 159 · see citing works
Somogyi, P., Katona, L., Klausberger, T., Lasztóczi, B., & Viney, T. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0518 · Cited by 159 · see citing works
Sun, Q., Sotayo, A. O., Cazzulino, A. S., Snyder, A. M., Denny, C. A., & Siegelbaum, S. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.012 · Cited by 159 · see citing works
Dynamic Reconfiguration of Hippocampal Interneuron Circuits during Spatial Learning
Dupret, D., O’Neill, J., & Csicsvari, J. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.033 · Cited by 158 · see citing works
Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus
Deguchi, Y., Donato, F., Galimberti, I., Cabuy, E., & Caroni, P. (2011) · Nature Neuroscience · doi:10.1038/nn.2768 · Cited by 157 · see citing works
Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: I. Branching patterns
Bannister, N. J., & Larkman, A. U. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600111 · Cited by 156 · see citing works
Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo
Viney, T. J., Lasztóczi, B., Katona, L., Crump, M., Tukker, J. J., Klausberger, T., & Somogyi, P. (2013) · Nature Neuroscience · doi:10.1038/nn.3550 · Cited by 155 · see citing works
Hippocampal pyramidal cells: the reemergence of cortical lamination
Slomianka, L., Amrein, I., Knuesel, I., Sørensen, J. C. H., & Wolfer, D. P. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0322-0 · Cited by 152 · see citing works
How we remember: brain mechanisms of episodic memory
(2012) · Choice Reviews Online · doi:10.5860/choice.49-5040 · Cited by 147 · see citing works
Shah, S., Lubeck, E., Zhou, W., & Cai, L. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.008 · Cited by 146 · see citing works
Masurkar, A. V., Srinivas, K. V., Brann, D. H., Warren, R., Lowes, D. C., & Siegelbaum, S. A. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.012 · Cited by 137 · see citing works
Postmitotic neurons migrate tangentially in the cortical ventricular zone
O’Rourke, N. A., Chenn, A., & McConnell, S. K. (1997) · Development · doi:10.1242/dev.124.5.997 · Cited by 135 · see citing works
Bliss, T. V. P., & Lømo, T. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010273 · Cited by 135 · 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
The influence of objects on place field expression and size in distal hippocampal CA1
Burke, S. N., Maurer, A. P., Nematollahi, S., Uprety, A. R., Wallace, J. L., & Barnes, C. A. (2011) · Hippocampus · doi:10.1002/hipo.20929 · Cited by 130 · see citing works
Functional fission of parvalbumin interneuron classes during fast network events
Varga, C., Oijala, M., Lish, J., Szabo, G. G., Bezaire, M., Marchionni, I., Golshani, P., & Soltesz, I. (2014) · eLife · doi:10.7554/elife.04006 · Cited by 130 · see citing works
Fariñas, I., & DeFelipe, J. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040106 · Cited by 129 · see citing works
Neunuebel, J. P., Yoganarasimha, D., Rao, G., & Knierim, J. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0946-13.2013 · Cited by 126 · see citing works
Valero, M., Averkin, R. G., Fernández‐Lamo, I., Aguilar, J., Lopez‐Pigozzi, D., Brotons‐Mas, J. R., Cid, E., Tamás, G., & de la Prida, L. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.032 · Cited by 126 · see citing works
The hippocampal rate code: anatomy, physiology and theory
Ahmed, O. J., & Mehta, M. R. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.009 · Cited by 116 · see citing works
Fariñas, I., & DeFelipe, J. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040105 · Cited by 113 · see citing works
Spatial coding and physiological properties of hippocampal neurons in the Cornu Ammonis subregions
Oliva, A., Fernández‐Ruiz, A., Buzsáki, G., & Berényi, A. (2016) · Hippocampus · doi:10.1002/hipo.22659 · Cited by 113 · see citing works
Similarity of Visual Selectivity among Clonally Related Neurons in Visual Cortex
Ohtsuki, G., Nishiyama, M., Yoshida, T., Murakami, T., Histed, M. H., Lois, C., & Ohki, K. (2012) · Neuron · doi:10.1016/j.neuron.2012.05.023 · Cited by 112 · 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
Nakamura, N. H., Flasbeck, V., Maingret, N., Kitsukawa, T., & Sauvage, M. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4480-12.2013 · Cited by 103 · see citing works
Otsuka, T., & Kawaguchi, Y. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2219-09.2009 · Cited by 99 · see citing works
Selection of preconfigured cell assemblies for representation of novel spatial experiences
Dragoi, G., & Tonegawa, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0522 · Cited by 94 · see citing works
Kowalski, J., Gan, J., Jónás, P., & Pernía‐Andrade, A. J. (2015) · Hippocampus · doi:10.1002/hipo.22550 · Cited by 85 · see citing works
Leonardo, E. D., Richardson-Jones, J. W., Sibille, E. L., Kottman, A., & Hen, R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.082 · Cited by 84 · see citing works
Distinct Lineage-Dependent Structural and Functional Organization of the Hippocampus
Xu, H.-T., Han, Z., Gao, P., He, S., Li, Z., Shi, W., Kodish, O., Shao, W., Brown, K. N., Huang, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.067 · Cited by 80 · see citing works
Marissal, T., Bonifazi, P., Picardo, M. A., Nardou, R., Petit, L. F., Baude, A., Fishell, G., Ben‐Ari, Y., & Cossart, R. (2012) · Nature Communications · doi:10.1038/ncomms2318 · Cited by 79 · see citing works
Functional division of hippocampal area CA1 via modulatory gating of entorhinal cortical inputs
Ito, H., & Schuman, E. M. (2011) · Hippocampus · doi:10.1002/hipo.20909 · Cited by 79 · see citing works
Quantitative estimate of the information relayed by the Schaffer collaterals
Treves, A. (1995) · Journal of Computational Neuroscience · doi:10.1007/bf00961437 · Cited by 77 · see citing works
Nielsen, J. V., Nielsen, F. H., Ismail, R., Noraberg, J., & Jensen, N. A. (2007) · Development · doi:10.1242/dev.000265 · Cited by 76 · see citing works
Cellular dynamics of neuronal migration in the hippocampus
Hayashi, K., Kubo, K., Kitazawa, A., & Nakajima, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00135 · Cited by 74 · 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
Self-citationKitazawa, A., Kubo, K., Hayashi, K., Matsunaga, Y., Ishii, K., & Nakajima, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2254-13.2014 · Cited by 73 · see citing works
Three axonal projection routes of individual pyramidal cells in the ventral CA1 hippocampus
Arszovszki, A., Borhegyi, Z., & Klausberger, T. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00053 · Cited by 73 · see citing works
Memory retrieval along the proximodistal axis of CA1
Nakazawa, Y., Pevzner, A., Tanaka, K. Z., & Wiltgen, B. J. (2016) · Hippocampus · doi:10.1002/hipo.22596 · Cited by 73 · see citing works
Nielsen, J. V., Blom, J. B., Noraberg, J., & Jensen, N. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp261 · Cited by 67 · see citing works
Computational Modeling of Entorhinal Cortex
Hasselmo, M. E., Fransén, E. A., Dickson, C. T., & Alonso, A. A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06741.x · Cited by 63 · see citing works
New dimensions of interneuronal specialization unmasked by principal cell heterogeneity
Krook-Magnuson, E., Varga, C., Lee, S.-H., & Soltesz, I. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.005 · Cited by 63 · see citing works
Hartzell, A. L., Burke, S. N., Hoang, L. T., Lister, J. P., Rodriguez, C. N., & Barnes, C. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4727-12.2013 · Cited by 55 · see citing works
Inhibitory microcircuit modules in hippocampal learning
Caroni, P. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.06.010 · Cited by 48 · see citing works
Distinct memory circuits composing the hippocampal region
Granger, R., Wiebe, S. P., Taketani, M., & LYNCH, G. S. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 45 · see citing works
Mapping memory function in the medial temporal lobe with the immediate-early gene Arc
Sauvage, M. M., Nakamura, N. H., & Beer, Z. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.048 · Cited by 41 · see citing works
Neural Activity Patterns Underlying Spatial Coding in the Hippocampus
Sosa, M., Gillespie, A. K., & Frank, L. M. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_462 · Cited by 41 · see citing works
Hasselmo, M. E. (2011) · The MIT Press eBooks · doi:10.7551/mitpress/9780262016353.001.0001 · Cited by 40 · see citing works
Graves, A. R., Moore, S. J., Spruston, N., Tryba, A. K., & Kaczorowski, C. C. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00186.2016 · Cited by 29 · see citing works
Regulation of hippocampus‐dependent memory by the zinc finger protein Zbtb20 in mature CA1 neurons
Ren, A., Zhang, H., Xie, Z., Ma, X., Ji, W., He, D. Z. Z., Yuan, W.-J., Ding, Y., Zhang, X. H., & Zhang, W. J. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.234187 · Cited by 28 · see citing works
Nonuniform allocation of hippocampal neurons to place fields across all hippocampal subfields
Witharana, W. K. L., Cardiff, J. W., Chawla, M. K., Xie, J., Alme, C. B., Eckert, M. J., Lapointe, V., Demchuk, A. M., Maurer, A. P., Trivedi, V., et al. (2016) · Hippocampus · doi:10.1002/hipo.22609 · Cited by 28 · see citing works
Taxonomic Separation of Hippocampal Networks: Principal Cell Populations and Adult Neurogenesis
van Dijk, R. M., Huang, S., Slomianka, L., & Amrein, I. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00022 · Cited by 27 · see citing works
Moser, E. I. (2011) · Nature Neuroscience · doi:10.1038/nn.2783 · Cited by 24 · 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
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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
The subiculum is a patchwork of discrete subregions
Cembrowski, M. S., Wang, L., Lemire, A. L., Copeland, M., DiLisio, S. F., Clements, J., & Spruston, N. (2018) · eLife · doi:10.7554/elife.37701 · Cited by 98 · see citing works
Preconfigured dynamics in the hippocampus are guided by embryonic birthdate and rate of neurogenesis
Huszár, R., Zhang, Y., Blockus, H., & Buzsáki, G. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01138-x · Cited by 104 · see citing works
Hippocampo-cortical circuits for selective memory encoding, routing, and replay
Harvey, R. E., Robinson, H. L., Liu, C., Oliva, A., & Fernandez-Ruiz, A. (2023) · Neuron · doi:10.1016/j.neuron.2023.04.015 · Cited by 101 · see citing works
Functional Access to Neuron Subclasses in Rodent and Primate Forebrain
Mehta, P., Kreeger, L., Wylie, D. C., Pattadkal, J. J., Lusignan, T., Davis, M. J., Turi, G. F., Li, W.-K., Whitmire, M. P., Chen, Y., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.011 · Cited by 67 · see citing works
Self-citationMental navigation and the neural mechanisms of insight
Aru, J., Drüke, M., Pikamäe, J., & Larkum, M. E. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2022.11.002 · Cited by 38 · see citing works
Romani, A., Antonietti, A., Bella, D., Budd, J., Giacalone, E., Kurban, K., Sáray, S., Abdellah, M., Arnaudon, A., Boci, E., et al. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002861 · Cited by 39 · see citing works
Engineering brain-derived neurotrophic factor mRNA delivery for the treatment of Alzheimer’s disease
Li, H., Cao, Y., Ye, J., Yang, Z., Chen, Q., Liu, X., Zhang, B., Qiao, J., Tang, Q., Yang, H., et al. (2023) · Chemical Engineering Journal · doi:10.1016/j.cej.2023.143152 · Cited by 32 · see citing works
Subspace communication in the hippocampal–retrosplenial axis
Gonzalez, J., Vöröslakos, M., Aykan, D., Soto, N., Nitzan, N., Swanson, R., Karadas, M., Chen, Z. S., & Buzsáki, G. (2026) · Nature · doi:10.1038/s41586-026-10481-z · Cited by 7 · see citing works
Place and behavioral modulation of hippocampal neurons during immobility
Sartorato, N., Zouridis, I. S., Narantsatsralt, U.-U., Blanco-Hernández, E., & Burgalossi, A. (2026) · Nature Communications · doi:10.1038/s41467-026-75492-w · Cited by 1 · see citing works
“CA1 pyramidal neurons show a high level of heterogeneity at the molecular, cellular, connectivity, and in-vivo properties 90 – 92 .”
- Authors
- Soltesz, I., & Losonczy, A.
- Affiliations
- Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
- Corresponding author
- Losonczy, Attila
- ORCID
- Losonczy, Attila
- Venue
- Nature Neuroscience
- Published
- 2018-03-28
- Volume
- 21
- Issue
- 4
- Pages
- 484-493
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5909691
- OpenAlex
- W2796344372
- Cited by
- 333
- References
- 152
- Citations by year
- 2026: 30 · 2025: 51 · 2024: 53 · 2023: 46 · 2022: 40 · 2021: 39 · 2020: 33 · 2019: 30 · 2018: 10 · 2017: 1
- FWCI
- 3.69
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (U19NS104590, R01NS094668)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- CA1 pyramidal neurons, parallel information processing, functional segregation, parallel circuits, spatial navigation, declarative memory
- MeSH terms
- Animals, Electronic Data Processing, Hippocampus, Humans, Neural Pathways, Pyramidal Cells
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