Vasoactive Intestinal Polypeptide-Expressing Interneurons in the Hippocampus Support Goal-Oriented Spatial Learning
Open accessAbstract
Diverse computations in the neocortex are aided by specialized GABAergic interneurons (INs), which selectively target other INs. However, much less is known about how these canonical disinhibitory circuit motifs contribute to network operations supporting spatial navigation and learning in the hippocampus. Using chronic two-photon calcium imaging in mice performing random foraging or goal-oriented learning tasks, we found that vasoactive intestinal polypeptide-expressing (VIP+), disinhibitory INs in hippocampal area CA1 form functional subpopulations defined by their modulation by behavioral states and task demands. Optogenetic manipulations of VIP+ INs and computational modeling further showed that VIP+ disinhibition is necessary for goal-directed learning and related reorganization of hippocampal pyramidal cell population dynamics. Our results demonstrate that disinhibitory circuits in the hippocampus play an active role in supporting spatial learning. VIDEO ABSTRACT.
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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 [41]
The Results section, “Optogenetic manipulation of VIP INs alters learning performance and place cell enrichment” (page unavailable), reports enrichment of place cells near the reward after learning in control mice. The Methods describe tactile cues on the belt, but do not show that place fields over-represented those cues. They use uniform sampling as a comparison for the reward-enrichment analysis, not as a reported finding that place fields uniformly tiled the belt. (LLM, conf=0.84)
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Scikit-learn: Machine Learning in Python
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Müller, A., Nothman, J., Louppe, G., et al. (2012) · arXiv · doi:10.48550/arxiv.1201.0490 · Cited by 71,016 · see citing works
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · 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
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
The NEURON Simulation Environment
Hines, M. L., & Carnevale, N. T. (1997) · Neural Computation · doi:10.1162/neco.1997.9.6.1179 · Cited by 2,630 · see citing works
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · 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
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353 · see citing works
Cortical interneurons that specialize in disinhibitory control
Pi, H.-J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12676 · Cited by 1,136 · see citing works
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
Imaging large-scale neural activity with cellular resolution in awake, mobile mice
Dombeck, D. A., Khabbaz, A. N., Collman, F., Adelman, T. L., & Tank, D. W. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.003 · Cited by 1,099 · see citing works
A Cortical Circuit for Gain Control by Behavioral State
Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., Huang, Z. J., & Stryker, M. P. (2014) · Cell · doi:10.1016/j.cell.2014.01.050 · Cited by 937 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · 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
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 869 · see citing works
A disinhibitory microcircuit for associative fear learning in the auditory cortex
Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., & Lüthi, A. (2011) · Nature · doi:10.1038/nature10674 · Cited by 840 · see citing works
Locus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827 · see citing works
Long-range and local circuits for top-down modulation of visual cortex processing
Zhang, S., Xu, M., Kamigaki, T., Hoang Do, J. P., Chang, W.-C., Jenvay, S., Miyamichi, K., Luo, L., & Dan, Y. (2014) · Science · doi:10.1126/science.1254126 · Cited by 804 · see citing works
The 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
A disinhibitory circuit mediates motor integration in the somatosensory cortex
Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G., & Rudy, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3544 · Cited by 758 · see citing works
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G. (2012) · Nature Neuroscience · doi:10.1038/nn.3077 · Cited by 728 · see citing works
Self-citationBehavioral time scale synaptic plasticity underlies CA1 place fields
Bittner, K. C., Milstein, A. D., Grienberger, C., Romani, S., & Magee, J. C. (2017) · Science · doi:10.1126/science.aan3846 · Cited by 707 · 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
Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons
Bittner, K. C., Grienberger, C., Vaidya, S. P., Milstein, A. D., Macklin, J. J., Suh, J., Tonegawa, S., & Magee, J. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4062 · Cited by 540 · 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
Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03397.1996 · Cited by 512 · see citing works
Projections from neocortex mediate top-down control of memory retrieval
Rajasethupathy, P., Sankaran, S., Marshel, J. H., Kim, C. K., Ferenczi, E., Lee, S. Y., Berndt, A., Ramakrishnan, C., Jaffe, A., Lo, M., et al. (2015) · Nature · doi:10.1038/nature15389 · Cited by 509 · see citing works
Dendritic Inhibition in the Hippocampus Supports Fear Learning
Lovett-Barron, M., Kaifosh, P., Kheirbek, M. A., Danielson, N., Zaremba, J. D., Reardon, T. R., Turi, G. F., Hen, R., Zemelman, B. V., & Losonczy, A. (2014) · Science · doi:10.1126/science.1247485 · Cited by 509 · see citing works
Self-citationDopaminergic neurons promote hippocampal reactivation and spatial memory persistence
McNamara, C. G., Tejero-Cantero, Á., Trouche, S., Campo-Urriza, N., & Dupret, D. (2014) · Nature Neuroscience · doi:10.1038/nn.3843 · Cited by 486 · see citing works
From grid cells to place cells: A mathematical model
Solstad, T., Moser, E. I., & Einevoll, G. T. (2006) · Hippocampus · doi:10.1002/hipo.20244 · Cited by 477 · see citing works
Klausberger, T., Marton, L. F., O'Neill, J., Huck, J. H. J., Dalezios, Y., Fuentealba, P., Suen, W. Y., Papp, E., Kaneko, T., Watanabe, M., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3269-05.2005 · Cited by 469 · see citing works
Arithmetic of Subthreshold Synaptic Summation in a Model CA1 Pyramidal Cell
Poirazi, P., Brannon, T., & Mel, B. W. (2003) · Neuron · doi:10.1016/s0896-6273(03)00148-x · Cited by 441 · see citing works
Self-citationDisinhibition, a Circuit Mechanism for Associative Learning and Memory
Letzkus, J. J., Wolff, S. B. E., & Lüthi, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.024 · Cited by 401 · see citing works
Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback
Hangya, B., Ranade, S. P., Lorenc, M., & Kepecs, A. (2015) · Cell · doi:10.1016/j.cell.2015.07.057 · Cited by 399 · see citing works
A Dedicated Population for Reward Coding in the Hippocampus
Gauthier, J. L., & Tank, D. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.008 · Cited by 394 · see citing works
Bezaire, M. J., & Soltesz, I. (2013) · Hippocampus · doi:10.1002/hipo.22141 · Cited by 373 · see citing works
Global Representations of Goal-Directed Behavior in Distinct Cell Types of Mouse Neocortex
Allen, W. E., Kauvar, I., Chen, M. Z., Richman, E. B., Yang, S., Chan, K. Y., Gradinaru, V., Deverman, B. E., Luo, L., & Deisseroth, K. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.017 · Cited by 369 · see citing works
Parallel processing by cortical inhibition enables context-dependent behavior
Kuchibhotla, K. V., Gill, J. V., Lindsay, G. W., Papadoyannis, E. S., Field, R. E., Sten, T. H., Miller, K. D., & Froemke, R. C. (2016) · Nature Neuroscience · doi:10.1038/nn.4436 · Cited by 350 · see citing works
Fuhrmann, F., Justus, D., Sosulina, L., Kaneko, H., Beutel, T., Friedrichs, D., Schoch, S., Schwarz, M. K., Fuhrmann, M., & Remy, S. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.001 · Cited by 347 · see citing works
Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior
Pinto, L., & Dan, Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.021 · Cited by 323 · see citing works
Rabies Virus CVS-N2c ΔG Strain Enhances Retrograde Synaptic Transfer and Neuronal Viability
Reardon, T. R., Murray, A., Turi, G. F., Wirblich, C., Croce, K. R., Schnell, M. J., Jessell, T. M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.004 · Cited by 311 · see citing works
Self-citationAcsády, L., Görcs, T. J., & Freund, T. F. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00609-5 · Cited by 310 · see citing works
Nathanson, J. L., Yanagawa, Y., Obata, K., & Callaway, E. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.032 · 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-citationBehavior-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
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
Opening Holes in the Blanket of Inhibition: Localized Lateral Disinhibition by VIP Interneurons
Karnani, M. M., Jackson, J., Ayzenshtat, I., Hamzehei Sichani, A., Manoocheri, K., Kim, S., & Yuste, R. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3646-15.2016 · Cited by 236 · see citing works
Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”
Fishell, G., & Rudy, B. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113717 · Cited by 233 · 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
SIMA: Python software for analysis of dynamic fluorescence imaging data
Kaifosh, P., Zaremba, J. D., Danielson, N., & Losonczy, A. (2014) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2014.00080 · Cited by 225 · see citing works
Self-citationIncreased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation
Sheffield, M. E. J., Adoff, M. D., & Dombeck, D. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.029 · Cited by 214 · see citing works
Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior
Kamigaki, T., & Dan, Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4554 · Cited by 208 · see citing works
Somogyi, J., Baude, A., Omori, Y., Shimizu, H., Mestikawy, S. E., Fukaya, M., Shigemoto, R., Watanabe, M., & Somogyi, P. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03091.x · Cited by 207 · see citing works
In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons
Jia, H., Rochefort, N. L., Chen, X., & Konnerth, A. (2010) · Nature Protocols · doi:10.1038/nprot.2010.169 · Cited by 199 · see citing works
Bezaire, M. J., Raikov, I., Burk, K., Vyas, D., & Soltesz, I. (2016) · eLife · doi:10.7554/elife.18566 · Cited by 198 · see citing works
A cortical disinhibitory circuit for enhancing adult plasticity
Fu, Y., Kaneko, M., Tang, Y., Álvarez-Buylla, A., & Stryker, M. P. (2015) · eLife · doi:10.7554/elife.05558 · Cited by 196 · see citing works
Acsády, L., Arabadzisz, D., & Freund, T. F. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00610-9 · Cited by 187 · see citing works
Encoding and retrieval in a model of the hippocampal CA1 microcircuit
Vassilis Cutsuridis, A., Cobb, S., & Graham, B. P. (2009) · Hippocampus · doi:10.1002/hipo.20661 · Cited by 176 · see citing works
Grienberger, C., Milstein, A. D., Bittner, K. C., Romani, S., & Magee, J. C. (2017) · Nature Neuroscience · doi:10.1038/nn.4486 · Cited by 165 · 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 158 · 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
Cell-type-specific modulation of neocortical activity by basal forebrain input
Alitto, H. J., & Dan, Y. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00079 · Cited by 156 · see citing works
Tyan, L., Chamberland, S., Magnin, E., Camiré, O., Francavilla, R., David, L. S., Deisseroth, K., & Topolnik, L. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3813-13.2014 · Cited by 140 · see citing works
Inhibitory control of hippocampal inhibitory neurons
Chamberland, S., & Topolnik, L. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00165 · Cited by 134 · see citing works
Encoding and Retrieval in the CA3 Region of the Hippocampus: A Model of Theta-Phase Separation
Kunec, S., Hasselmo, M. E., & Kopell, N. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00731.2004 · Cited by 131 · 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
Self-citationDávid, C., Schleicher, A., Zuschratter, W., & Staiger, J. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05496.x · Cited by 120 · see citing works
Marshall, L., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., & Buzsáki, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-j0001.2002 · Cited by 119 · see citing works
Spatial selectivity and theta phase precession in CA1 interneurons
Ego‐Stengel, V., & Wilson, M. A. (2006) · Hippocampus · doi:10.1002/hipo.20253 · Cited by 112 · see citing works
Cea-del Rio, C. A., Lawrence, J. J., Tricoire, L., Erdelyi, F., Szabo, G., & McBain, C. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5040-09.2010 · Cited by 99 · see citing works
Abnormal wiring of CCK+ basket cells disrupts spatial information coding
del Pino, I., Brotons‐Mas, J. R., Marques–Smith, A., Marighetto, A., Frick, A., Marín, Ó., & Rico, B. (2017) · Nature Neuroscience · doi:10.1038/nn.4544 · Cited by 96 · see citing works
Dedicated Hippocampal Inhibitory Networks for Locomotion and Immobility
Arriaga, M., & Han, E. B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1076-17.2017 · Cited by 95 · see citing works
FISSA: A neuropil decontamination toolbox for calcium imaging signals
Keemink, S., Lowe, S., Pakan, J. M. P., Dylda, E., van Rossum, M. C. W., & Rochefort, N. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-21640-2 · Cited by 88 · see citing works
Discrete Place Fields of Hippocampal Formation Interneurons
Wilent, W. B., & Nitz, D. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01200.2006 · Cited by 78 · see citing works
Scheyltjens, I., Laramée, M., den Haute, C. V., Gijsbers, R., Debyser, Z., Baekelandt, V., Vreysen, S., & Arckens, L. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23819 · Cited by 56 · see citing works
Activity-dependent plasticity of hippocampal place maps
Schoenenberger, P., O’Neill, J., & Csicsvari, J. L. (2016) · Nature Communications · doi:10.1038/ncomms11824 · Cited by 52 · 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
Modulatory effects of inhibition on persistent activity in a cortical microcircuit model
Konstantoudaki, X., Papoutsi, A., Chalkiadaki, K., Poirazi, P., & Sidiropoulou, K. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00007 · Cited by 34 · see citing works
Self-citationCoordination of dendritic inhibition through local disinhibitory circuits
Francavilla, R., Luo, X., Magnin, E., Tyan, L., & Topolnik, L. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00005 · Cited by 29 · see citing works
Single-Trial Properties of Place Cells in Control and CA1 NMDA Receptor Subunit 1-KO Mice
Cabral, H., Fouquet, C., Rondi‐Reig, L., Pennartz, C. M. A., & Battaglia, F. P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5320-13.2014 · Cited by 24 · see citing works
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Poirazi, P., & Papoutsi, A. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0301-7 · Cited by 303 · see citing works
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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
Kaufman, A. M., Geiller, T., & Losonczy, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.029 · Cited by 193 · see citing works
Self-citationBreakdown of spatial coding and interneuron synchronization in epileptic mice
Shuman, T., Aharoni, D. B., Cai, D. J., Lee, C. R., Chavlis, S., Page-Harley, L., Vetere, L. M., Feng, Y., Yang, C. Y., Mollinedo-Gajate, I., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0559-0 · Cited by 192 · see citing works
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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
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Humeau, Y., & Choquet, D. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0480-6 · Cited by 154 · see citing works
Geiller, T., Vancura, B., Terada, S., Troullinou, E., Chavlis, S., Tsagkatakis, G., Tsakalides, P., Ócsai, K., Poirazi, P., Rózsa, B. J., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.013 · Cited by 159 · see citing works
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Dudok, B., Klein, P., Hwaun, E., Lee, B. R., Yao, Z., Fong, O., Bowler, J. C., Terada, S., Sparks, F. T., Szabo, G. G., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.003 · Cited by 161 · see citing works
Self-citationSosa, M., & Giocomo, L. M. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00479-z · Cited by 142 · see citing works
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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
Hippocampal GABAergic interneurons and memory
Tzilivaki, A., Tukker, J. J., Maier, N., Poirazi, P., Sammons, R. P., & Schmitz, D. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.016 · Cited by 145 · see citing works
Self-citationTop-down control of hippocampal signal-to-noise by prefrontal long-range inhibition
Malik, R., Li, Y., Schamiloglu, S., & Sohal, V. S. (2022) · Cell · doi:10.1016/j.cell.2022.04.001 · Cited by 138 · see citing works
Compartment-specific tuning of dendritic feature selectivity by intracellular Ca 2+ release
O’Hare, J. K., Gonzalez, K. C., Herrlinger, S. A., Hirabayashi, Y., Hewitt, V. L., Blockus, H., Szoboszlay, M., Rolotti, S. V., Geiller, T., Negrean, A., et al. (2022) · Science · doi:10.1126/science.abm1670 · Cited by 124 · see citing works
Self-citationHippocampal 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
Dynamics of a disinhibitory prefrontal microcircuit in controlling social competition
Zhang, C., Zhu, H. L., Ni, Z., Xin, Q., Zhou, T., Wu, R., Gao, G., Gao, Z., Ma, H., Li, H., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.034 · Cited by 123 · see citing works
Self-citationLocal 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
Self-citationNeural 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
Self-citationGoff, K. M., & Goldberg, E. M. (2019) · eLife · doi:10.7554/elife.46846 · Cited by 93 · see citing works
Cortical disinhibitory circuits: cell types, connectivity and function
Kullander, K., & Topolnik, L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.04.009 · Cited by 83 · see citing works
Naskar, S., Qi, J., Pereira, F., Gerfen, C. R., & Lee, S. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108774 · Cited by 72 · see citing works
Guet-McCreight, A., Skinner, F. K., & Topolnik, L. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00032 · Cited by 64 · 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
Synaptogenic activity of the axon guidance molecule Robo2 underlies hippocampal circuit function
Blockus, H., Rolotti, S. V., Szoboszlay, M., Pezé-Heidsieck, E., Ming, T., Schroeder, A., Apóstolo, N., Vennekens, K. M., Katsamba, P. S., Bahna, F. A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109828 · Cited by 62 · see citing works
Self-citationRipple-selective GABAergic projection cells in the hippocampus
Szabo, G. G., Farrell, J. S., Dudok, B., Hou, W., Ortiz, A. L., Varga, C., Moolchand, P., Gülsever, C. İ., Gschwind, T., Dimidschstein, J., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.002 · Cited by 61 · see citing works
Solés-Tarrés, I., Cabezas-Llobet, N., Vaudry, D., & Xifró, X. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00221 · Cited by 55 · see citing works
Reliability of an interneuron response depends on an integrated sensory state
Dobosiewicz, M., Liu, Q., & Bargmann, C. I. (2019) · eLife · doi:10.7554/elife.50566 · Cited by 51 · see citing works
Cortex-wide response mode of VIP-expressing inhibitory neurons by reward and punishment
Szadai, Z., Pi, H.-J., Chevy, Q., Ócsai, K., Albeanu, D. F., Chiovini, B., Szalay, G., Katona, G., Kepecs, Á., & Rózsa, B. J. (2022) · eLife · doi:10.7554/elife.78815 · Cited by 45 · 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
Luo, X. M., Guet-McCreight, A., Villette, V., Francavilla, R., Marino, B., Chamberland, S., Skinner, F. K., & Topolnik, L. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz334 · Cited by 50 · 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
Generation of Sharp Wave-Ripple Events by Disinhibition
Evangelista, R., Cano, G., Cooper, C., Schmitz, D., Maier, N., & Kempter, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2174-19.2020 · Cited by 46 · 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
Leroy, F., de Solis, C. A., Boyle, L. M., Bock, T., Lofaro, O. M., Buss, E. W., Asok, A., Kandel, E. R., & Siegelbaum, S. A. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01124-y · Cited by 48 · see citing works
Anxiety-related activity of ventral hippocampal interneurons
Forro, T., Volitaki, E., Malagon‐Vina, H., Klausberger, T., Nevian, T., & Ciocchi, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102368 · Cited by 46 · see citing works
Bilash, O. M., Chavlis, S., Johnson, C. D., Poirazi, P., & Basu, J. (2023) · Cell Reports · doi:10.1016/j.celrep.2022.111962 · Cited by 50 · see citing works
Self-citationReorganization 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
Self-citationA hippocampal circuit mechanism to balance memory reactivation during sleep
Karaba, L. A., Robinson, H. L., Harvey, R. E., Chen, W., Fernández‐Ruiz, A., & Oliva, A. (2024) · Science · doi:10.1126/science.ado5708 · Cited by 43 · see citing works
Mechanisms of memory-supporting neuronal dynamics in hippocampal area CA3
Li, Y., Briguglio, J. J., Romani, S., & Magee, J. C. (2024) · Cell · doi:10.1016/j.cell.2024.09.041 · Cited by 54 · see citing works
Inhibitory top-down projections from zona incerta mediate neocortical memory
Schroeder, A., Pardi, M. B., Keijser, J., Dalmay, T., Groisman, A. I., Schuman, E. M., Sprekeler, H., & Letzkus, J. J. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.010 · Cited by 40 · see citing works
Cunha‐Reis, D., & Caulino‐Rocha, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00153 · Cited by 40 · see citing works
Distinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors
Li, K., Koukoutselos, K., Sakaguchi, M., & Ciocchi, S. (2024) · Nature Communications · doi:10.1038/s41467-024-52466-4 · Cited by 41 · 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
Albrecht, A., Redavide, E., Regev-Tsur, S., Stork, O., & Richter‐Levin, G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.002 · Cited by 38 · see citing works
Ramos-Prats, A., Paradiso, E., Castaldi, F., Sadeghi, M., Mir, M. Y., Hörtnagl, H., Göbel, G., & Ferraguti, F. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110893 · Cited by 37 · see citing works
Functional specialization of hippocampal somatostatin-expressing interneurons
Chamberland, S., Grant, G., Machold, R. P., Nebet, E. R., Tian, G., Stich, J. L., Hanani, M., Kullander, K., & Tsien, R. W. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2306382121 · Cited by 38 · see citing works
A local circuit-basis for spatial navigation and memory processes in hippocampal area CA1
Geiller, T. C., Priestley, J. B., & Losonczy, A. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102701 · Cited by 34 · see citing works
Self-citationGoff, K. M., Liebergall, S. R., Jiang, E., Somarowthu, A., & Goldberg, E. M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112628 · Cited by 38 · see citing works
A Role for Vasoactive Intestinal Peptide Interneurons in Neurodevelopmental Disorders
Goff, K. M., & Goldberg, E. M. (2021) · Developmental Neuroscience · doi:10.1159/000515264 · Cited by 34 · see citing works
Tamboli, S., Singh, S. P., Topolnik, D., Barkat, M. E. A., Radhakrishnan, R., Guet-McCreight, A., & Topolnik, L. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114115 · Cited by 33 · see citing works
The impact of Hodgkin–Huxley models on dendritic research
Petousakis, K., Apostolopoulou, A. A., & Poirazi, P. (2022) · The Journal of Physiology · doi:10.1113/jp282756 · Cited by 36 · see citing works
Self-citationHernández‐Frausto, M., Bilash, O. M., Masurkar, A. V., & Basu, J. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1223891 · Cited by 33 · see citing works
Durá-Bernal, S., Griffith, E. Y., Barczak, A., O’Connell, M. N., McGinnis, T., Moreira, J. V. S., Schroeder, C. E., Lytton, W. W., Lakatos, P., & Neymotin, S. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113378 · Cited by 35 · see citing works
Stimulus novelty uncovers coding diversity in survey of visual cortexPreprint
Garrett, M., Groblewski, P. A., Piet, A. T., Ollerenshaw, D. R., Najafi, F., Yavorska, I., Amster, A., Bennett, C., Buice, M. A., Caldejon, S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.14.528085 · Cited by 29 · see citing works
Inhibitory circuits in fear memory and fear-related disorders
Singh, S. P., & Topolnik, L. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1122314 · Cited by 29 · see citing works
Cartographers of the Cognitive Map: Locus Coeruleus Is Part of the Guild
Király, B., & Hangya, B. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.020 · Cited by 26 · see citing works
Cell-type-specific responses to associative learning in the primary motor cortex
Lee, C., Harkin, E. F., Yin, X., Naud, R., & Chen, S. X. (2022) · eLife · doi:10.7554/elife.72549 · Cited by 23 · see citing works
Zemla, R., Moore, J. J., Hopkins, M. D., & Basu, J. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111700 · Cited by 28 · see citing works
Tuncdemir, S. N., Grosmark, A., Chung, H., Luna, V. M., Lacefield, C., Losonczy, A., & Hen, R. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.016 · Cited by 26 · see citing works
Self-citationThe Engram’s Dark Horse: How Interneurons Regulate State-Dependent Memory Processing and Plasticity
Raven, F., & Aton, S. J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.750541 · Cited by 27 · see citing works
Offline memory replay in recurrent neuronal networks emerges from constraints on online dynamics
Milstein, A. D., Tran, S., Ng, G. Y., & Soltész, I. (2022) · The Journal of Physiology · doi:10.1113/jp283216 · Cited by 22 · see citing works
Brief synaptic inhibition persistently interrupts firing of fast-spiking interneurons
Chamberland, S., Nebet, E. R., Valero, M., Hanani, M., Egger, R., Larsen, S. B., Eyring, K. W., Buzsáki, G., & Tsien, R. W. (2023) · Neuron · doi:10.1016/j.neuron.2023.01.017 · Cited by 24 · see citing works
Rahmatullah, N., Schmitt, L., Stefano, L. A. D., Post, S., Robledo, J., Chaudhari, G., Pedapati, E. V., Erickson, C. A., Portera‐Cailliau, C., & Goel, A. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0571-23.2023 · Cited by 22 · see citing works
Neural circuit dynamics of drug-context associative learning in the mouse hippocampus
Sun, Y., & Giocomo, L. M. (2022) · Nature Communications · doi:10.1038/s41467-022-34114-x · Cited by 19 · see citing works
Bidirectional synaptic plasticity rapidly modifies hippocampal representationsPreprint
Milstein, A. D., Li, Y., Bittner, K. C., Grienberger, C., Soltész, I., Magee, J. C., & Romani, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.04.934182 · Cited by 20 · see citing works
Learning, Fast and Slow: Single- and Many-Shot Learning in the Hippocampus
Liao, Z., & Losonczy, A. (2024) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102423-100258 · Cited by 21 · see citing works
Self-citationSun, D., Unnithan, R. R., & French, C. R. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.640350 · Cited by 19 · see citing works
Alterations in Intrinsic and Synaptic Properties of Hippocampal CA1 VIP Interneurons During Aging
Francavilla, R., Guet-McCreight, A., Amalyan, S., Hui, C. W., Topolnik, D., Michaud, F., Marino, B., Tremblay, M., Skinner, F. K., & Topolnik, L. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.554405 · Cited by 18 · see citing works
Relationship Between Item and Source Memory: Explanation of Connection-Strength Model
Guo, J., Shubeck, K. T., & Hu, X. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.691577 · Cited by 19 · see citing works
Dendritic Mechanisms forIn VivoNeural Computations and Behavior
Fischer, L. F., Soto-Albors, R. M., Tang, V. D., Bicknell, B. A., Grienberger, C., Francioni, V., Naud, R., Palmer, L. M., & Takahashi, N. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1132-22.2022 · Cited by 18 · see citing works
Cunha‐Reis, D., & Caulino‐Rocha, A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.691978 · Cited by 20 · see citing works
Ultrafast simulation of large-scale neocortical microcircuitry with biophysically realistic neurons
Oláh, V. J., Pedersen, N. P., & Rowan, M. J. (2022) · eLife · doi:10.7554/elife.79535 · Cited by 17 · see citing works
VIPergic neuroprotection in epileptogenesis: challenges and opportunities
Cunha‐Reis, D., Caulino‐Rocha, A., & Correia‐de‐Sá, P. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105356 · Cited by 16 · see citing works
Inhibitory and disinhibitory VIP IN-mediated circuits in neocortexPreprint
Dellal, S. S., Zurita, H., Kruglikov, I., Valero, M., Abad-Perez, P., Geron, E., Meng, J. H., Prönneke, A., Hanson, J. L., Mir, E., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.26.640383 · Cited by 23 · see citing works
Forro, T., & Klausberger, T. (2023) · Neuron · doi:10.1016/j.neuron.2023.05.007 · Cited by 17 · see citing works
Functional networks of inhibitory neurons orchestrate synchrony in the hippocampus
Bocchio, M., Vorobyev, A., Sadeh, S., Brustlein, S., Dard, R. F., Reichinnek, S., Emiliani, V., Baude, A., Claudia Clopath, A., & Cossart, R. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002837 · Cited by 16 · see citing works
Durá-Bernal, S., Griffith, E. Y., Barczak, A., O’Connell, M. N., McGinnis, T., Schroeder, C. E., Lytton, W. W., Lakatos, P., & Neymotin, S. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.03.479036 · Cited by 16 · see citing works
Speigel, I. A., & Hemmings, H. C. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.812905 · Cited by 15 · see citing works
Fear memory recall involves hippocampal somatostatin interneurons
Zichó, K., Sos, K. E., Papp, P., Barth, A. M., Misák, E., Orosz, A., Mayer, M. I., Sebestény, R. Z., & Nyíri, G. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002154 · Cited by 14 · see citing works
Troullinou, E., Tsagkatakis, G., Chavlis, S., Turi, G. F., Li, W., Losonczy, A., Tsakalides, P., & Poirazi, P. (2020) · IEEE Transactions on Emerging Topics in Computational Intelligence · doi:10.1109/tetci.2020.3028581 · Cited by 15 · see citing works
Self-citationSong, C., Kang, X., Yang, F., Du, W., Zhang, J., Liu, L., Kang, J., Jia, N., Yue, H., Fan, L., et al. (2021) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0134 · Cited by 15 · see citing works
Self-citationHighly unstable heterogeneous representations in VIP interneurons of the anterior cingulate cortex
Johnson, C., Kretsge, L. N., Yen, W., Sriram, B., O’Connor, A., Liu, R. S., Jimenez, J., Phadke, R. A., Wingfield, K. K., Yeung, C., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01485-y · Cited by 13 · see citing works
Chatzikalymniou, A. P., Gumus, M., Lunyov, A. R., Rich, S., Lefebvre, J., & Skinner, F. K. (2021) · Hippocampus · doi:10.1002/hipo.23364 · Cited by 12 · see citing works
Medial entorhinal cortex mediates learning of context-dependent interval timing behavior
Bigus, E. R., Lee, H., Bowler, J. C., Shi, J., & Heys, J. G. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01683-7 · Cited by 19 · see citing works
Katona, L., Hartwich, K., Tomioka, R., Somogyi, J., Roberts, J. D. B., Wagner, K., Joshi, A., Klausberger, T., Rockland, K. S., & Somogyi, P. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02029-2 · Cited by 13 · see citing works
GABAergic CA1 neurons are more stable following context changes than glutamatergic cells
Schuette, P. J., Ikebara, J. M., Maesta‐Pereira, S., Torossian, A., Sethi, E., Kihara, A. H., Kao, J. C., Reis, F. M., & Adhikari, A. (2022) · Scientific Reports · doi:10.1038/s41598-022-13799-6 · Cited by 14 · see citing works
Prefrontal Disinhibition in Social Fear: A Vital Action of Somatostatin Interneurons
Wang, J., Tian, Y., Zeng, L., & Xu, H. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.611732 · Cited by 12 · see citing works
Gonkowski, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134692 · Cited by 12 · see citing works
Traktirov, D. S., Nazarov, I. R., Artemova, V., Gainetdinov, R. R., Pestereva, N. S., & Karpenko, M. N. (2023) · Biomedicines · doi:10.3390/biomedicines11112881 · Cited by 12 · see citing works
Caulino‐Rocha, A., Rodrigues, N. C., Ribeiro, J. A., & Cunha‐Reis, D. (2022) · Biology · doi:10.3390/biology11050627 · Cited by 12 · see citing works
A Generative Neighborhood-Based Deep Autoencoder for Robust Imbalanced Classification
Troullinou, E., Tsagkatakis, G., Losonczy, A., Poirazi, P., & Tsakalides, P. (2023) · IEEE Transactions on Artificial Intelligence · doi:10.1109/tai.2023.3249685 · Cited by 12 · see citing works
Self-citationTomko, M., Beňušková, Ľ., & Jedlička, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-87002-7 · Cited by 11 · see citing works
Ventral hippocampal cholecystokinin interneurons gate contextual reward memory
Nguyen, R., Sivakumaran, S., Lambe, E. K., & Kim, J. C. (2024) · iScience · doi:10.1016/j.isci.2024.108824 · Cited by 12 · see citing works
ADAR3 modulates neuronal differentiation and regulates mRNA stability and translation
Karlström, V., Sagredo, E. A., Planells, J., Welinder, C., Jungfleisch, J., Barrera-Conde, A., Engfors, L., Daniel, C., Gebauer, F., Visa, N., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae753 · Cited by 11 · see citing works
Brain-wide presynaptic networks of functionally distinct cortical neurons
Inácio, A. R. L., Lam, K. C., Zhao, Y., Pereira, F., Gerfen, C. R., & Lee, S. (2025) · Nature · doi:10.1038/s41586-025-08631-w · Cited by 11 · see citing works
Learning to predict future locations with internally generated theta sequences
Parra-Barrero, E., & Cheng, S. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011101 · Cited by 11 · see citing works
Simon, R. A., Barazanji, N., Jones, M. P., Bednarska, O., Icenhour, A., Engström, M., Hamilton, J. P., Keita, Å. V., & Walter, S. (2021) · Scientific Reports · doi:10.1038/s41598-020-80873-2 · Cited by 11 · see citing works
Michaud, F., Francavilla, R., Topolnik, D., Iloun, P., Tamboli, S., Calon, F., & Topolnik, L. (2024) · bioRxiv · doi:10.7554/elife.95412 · Cited by 6 · see citing works
- Authors
- 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., Zemelman, B. V., Poirazi, P., & Losonczy, A.
- Affiliations
- Columbia University (US)
- Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
- FORTH Institute of Molecular Biology and Biotechnology (GR)
- University of Crete (GR)
- The University of Texas at Austin (US)
- Corresponding author
- Poirazi, Panayiota
- Losonczy, Attila
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2019-03
- Volume
- 101
- Issue
- 6
- Pages
- 1150-1165.e8
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6428605
- OpenAlex
- W2913259775
- Cited by
- 218
- References
- 82
- Citations by year
- 2026: 26 · 2025: 35 · 2024: 34 · 2023: 33 · 2022: 30 · 2021: 27 · 2020: 22 · 2019: 9 · 2018: 2
- FWCI
- 12.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (1R01MH100631)
- National Institute of Neurological Disorders and Stroke (1U19NS104590, 1R01NS094668)
- Zegar Family Foundation Award
- Kavli Foundation (NYSTEM-C029157, S10 OD018464)
- NIMH (F32MH118716)
- Revson Foundation
- NINDS (U01NS094330, U01NS099720)
- ERC Starting Grant dEMORY (ERC-2012-StG-311435)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- vasoactive intestinal peptide, GABAergic interneurons, hippocampal CA1, goal-directed learning, spatial learning, spatial navigation, two-photon calcium imaging, optogenetics, computational modeling, foraging behavior, behavioral state
- MeSH terms
- Animals, Appetitive Behavior, Goals, Hippocampus, Interneurons, Neural Inhibition, Vasoactive Intestinal Peptide, Pyramidal Cells, Neocortex, Mice, CA1 Region, Hippocampal, Optogenetics, Spatial Learning
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 ›
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