Parvalbumin interneurons provide grid cell–driven recurrent inhibition in the medial entorhinal cortex
Abstract
Grid cells in the medial entorhinal cortex (MEC) generate metric spatial representations. Recent attractor-network models suggest an essential role for GABAergic interneurons in the emergence of the grid-cell firing pattern through recurrent inhibition dependent on grid-cell phase. To test this hypothesis, we studied identified parvalbumin-expressing (PV(+)) interneurons that are the most likely candidate for providing this recurrent inhibition onto grid cells. Using optogenetics and tetrode recordings in mice, we found that PV(+) interneurons exhibited high firing rates, low spatial sparsity and no spatial periodicity. PV(+) interneurons inhibited all functionally defined cell types in the MEC and were in turn recruited preferentially by grid cells. To our surprise, we found that individual PV(+) interneurons received input from grid cells with various phases, which most likely accounts for the broadly tuned spatial firing activity of PV(+) interneurons. Our data argue against the notion that PV(+) interneurons provide phase-dependent recurrent inhibition and challenge recent attractor-network models of grid cells.
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Spike downsampling was implemented by randomly removing spikes during immobility periods from behaviorally-modulated units to match the median firing rate of non-modulated units.
“Spike downsampling was implemented by randomly removing spikes during immobility periods from behaviorally-modulated units to match the median firing rate of non-modulated units (Supplementary Figs. 6b and 3g)135,136.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [135]
Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · 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
Generalized lacZ expression with the ROSA26 Cre reporter strain
Soriano, P. (1999) · Nature Genetics · doi:10.1038/5007 · Cited by 5,237 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Channelrhodopsin-2, a directly light-gated cation-selective membrane channel
Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P. R., Ollig, D., Hegemann, P., & Bamberg, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1936192100 · Cited by 2,672 · see citing works
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex
McCormick, D. A., Connors, B. W., Lighthall, J. W., & Prince, D. A. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.4.782 · Cited by 1,935 · see citing works
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809 · see citing works
Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M.-B., & Moser, E. I. (2006) · Science · doi:10.1126/science.1125572 · Cited by 1,485 · see citing works
Representation of Geometric Borders in the Entorhinal Cortex
Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B., & Moser, E. I. (2008) · Science · doi:10.1126/science.1166466 · Cited by 1,213 · see citing works
Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm
Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., & Buzsáki, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.014 · Cited by 1,015 · see citing works
Accurate Path Integration in Continuous Attractor Network Models of Grid Cells
Burak, Y., & Fiete, I. R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000291 · Cited by 779 · 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
The entorhinal grid map is discretized
Stensola, H., Stensola, T., Solstad, T., Frøland, K., Moser, M., & Moser, E. I. (2012) · Nature · doi:10.1038/nature11649 · Cited by 702 · see citing works
An oscillatory interference model of grid cell firing
Burgess, N., Barry, C., & O'Keefe, J. M. (2007) · Hippocampus · doi:10.1002/hipo.20327 · Cited by 688 · see citing works
A Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex
Fuhs, M. C., & Touretzky, D. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4353-05.2006 · Cited by 628 · see citing works
Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli
Atallah, B. V., Bruns, W., Carandini, M., & Scanziani, M. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.013 · Cited by 612 · see citing works
Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus
Csicsvari, J., Hirase, H., Czurko, A., & Buzsáki, G. (1998) · Neuron · doi:10.1016/s0896-6273(00)80525-5 · Cited by 606 · see citing works
Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., Rozov, A., Whittington, M. A., Traub, R. D., Rawlins, J. N. P., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.031 · Cited by 532 · see citing works
Self-citationGrid cells in pre- and parasubiculum
Boccara, C. N., Sargolini, F., Thoresen, V. H., Solstad, T., Witter, M. P., Moser, E. I., & Moser, M. (2010) · Nature Neuroscience · doi:10.1038/nn.2602 · Cited by 518 · see citing works
What Does the Anatomical Organization of the Entorhinal Cortex Tell Us?
Canto, C. B., Wouterlood, F. G., & Witter, M. P. (2008) · Neural Plasticity · doi:10.1155/2008/381243 · Cited by 418 · see citing works
Recurrent inhibitory circuitry as a mechanism for grid formation
Couey, J. J., Witoelar, A., Zhang, S., Zheng, K., Ye, J., Dunn, B. A., Czajkowski, R., Moser, M., Moser, E. I., Roudi, Y., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3310 · Cited by 413 · see citing works
Grid cells require excitatory drive from the hippocampus
Bonnevie, T., Dunn, B. A., Fyhn, M., Hafting, T., Derdikman, D., Kubie, J. L., Roudi, Y., Moser, E. I., & Moser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3311 · Cited by 341 · see citing works
Miyamichi, K., Shlomai, Y., Shu, M., Weissbourd, B., Luo, L., & Mizrahi, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.027 · Cited by 310 · see citing works
Membrane potential dynamics of grid cells
Domnisoru, C., Kinkhabwala, A. A., & Tank, D. W. (2013) · Nature · doi:10.1038/nature11973 · Cited by 309 · see citing works
Meyer, A. H., Katona, I., Blatow, M., Rozov, A. V., & Monyer, H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07055.2002 · Cited by 286 · see citing works
Self-citationFeedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields
Pastoll, H., Solanka, L., van Rossum, M. C. W., & Nolan, M. F. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.032 · Cited by 278 · see citing works
Cellular mechanisms of spatial navigation in the medial entorhinal cortex
Schmidt‐Hieber, C., & Häusser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3340 · Cited by 273 · see citing works
The emergence of grid cells: Intelligent design or just adaptation?
Kropff, E., & Treves, A. (2008) · Hippocampus · doi:10.1002/hipo.20520 · Cited by 254 · see citing works
Computational Models of Grid Cells
Giocomo, L. M., Moser, M., & Moser, E. I. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.023 · Cited by 231 · 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
Klugmann, M., Symes, C. W., Leichtlein, C. B., Klaussner, B. K., Dunning, J., Fong, D. M., Young, D., & During, M. J. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.10.002 · Cited by 196 · see citing works
Parvalbumin-Expressing Interneurons Linearly Control Olfactory Bulb Output
Kato, H., Gillet, S. N., Peters, A. J., Isaacson, J. S., & Komiyama, T. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.036 · Cited by 182 · see citing works
Jones, R. S. G., & Buhl, E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90341-h · Cited by 174 · see citing works
Transgenic mice for conditional gene manipulation in astroglial cells
Ślęzak, M., Göritz, C., Niemiec, A., Frisén, J., Chambon, P., METZGER, D., & Pfrieger, F. W. (2007) · Glia · doi:10.1002/glia.20570 · Cited by 171 · see citing works
Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro
Dhillon, A., & Jones, R. S. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00225-6 · Cited by 171 · see citing works
Maurer, A. P., Cowen, S. L., Burke, S. N., Barnes, C. A., & McNaughton, B. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2882-06.2006 · Cited by 129 · see citing works
Wouterlood, F. G., H�rtig, W., Br�ckner, G., & Witter, M. P. (1995) · Journal of Neurocytology · doi:10.1007/bf01181556 · Cited by 125 · 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
Zilli, E. A., & Hasselmo, M. E. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0547-10.2010 · Cited by 107 · see citing works
Allen, K. L., Fuchs, E. C., Jaschonek, H., Bannerman, D. M., & Monyer, H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6512-10.2011 · Cited by 88 · see citing works
Self-citationZariwala, H. A., Madisen, L., Ahrens, K. F., Bernard, A., Lein, E. S., Jones, A. R., & Zeng, H. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2010.00162 · Cited by 56 · see citing works
Coexistence of parvalbumin and GABA in nonpyramidal neurons of the rat entorhinal cortex
Miettinen, M., Koivisto, E., Riekkinen, P. J., & Miettinen, R. A. (1996) · Brain Research · doi:10.1016/0006-8993(95)01203-6 · Cited by 55 · see citing works
Chandelier cells in the hippocampal formation of the rat: The entorhinal area and subicular complex
Soriano, E., Martı́nez, A., Fariñas, I., & Frotscher, M. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903370110 · Cited by 38 · see citing works
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Perineuronal nets stabilize the grid cell network
Christensen, A. C., Lensjø, K. K., Lepperød, M. E., Dragly, S.-A., Sutterud, H., Blackstad, J. S., Fyhn, M., & Hafting, T. (2021) · Nature Communications · doi:10.1038/s41467-020-20241-w · Cited by 1,865 · see citing works
Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · see citing works
Optogenetics: 10 years of microbial opsins in neuroscience
Deisseroth, K. A. (2015) · Nature Neuroscience · doi:10.1038/nn.4091 · Cited by 1,286 · 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
Speed cells in the medial entorhinal cortex
Kropff, E., Carmichael, J. E., Moser, M.-B., & Moser, E. I. (2015) · Nature · doi:10.1038/nature14622 · Cited by 668 · see citing works
Open Ephys: an open-source, plugin-based platform for multichannel electrophysiology
Siegle, J. H., Cuevas-López, A., Patel, Y., Abramov, K., Ohayon, S., & Voigts, J. (2017) · Journal of Neural Engineering · doi:10.1088/1741-2552/aa5eea · Cited by 530 · see citing works
Grid cells and cortical representation
Moser, E. I., Roudi, Y., Witter, M. P., Kentros, C., Bonhoeffer, T., & Moser, M.-B. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3766 · Cited by 335 · see citing works
Witter, M. P., Doan, T. P., Jacobsen, B., Nilssen, E. S., & Ohara, S. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00046 · Cited by 352 · see citing works
Inhibitory Plasticity: Balance, Control, and Codependence
Hennequin, G., Agnes, E. J., & Vogels, T. P. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031005 · Cited by 234 · see citing works
Tasks for inhibitory interneurons in intact brain circuits
Roux, L., & Buzsáki, G. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.011 · Cited by 218 · see citing works
Rowland, D. C., Roudi, Y., Moser, M., & Moser, E. I. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013824 · Cited by 219 · see citing works
Nilssen, E. S., Doan, T. P., Nigro, M. J., Ohara, S., & Witter, M. P. (2019) · Hippocampus · doi:10.1002/hipo.23145 · Cited by 178 · see citing works
Local and Distant Input Controlling Excitation in Layer II of the Medial Entorhinal Cortex
Fuchs, E. C., Neitz, A., Pinna, R., Melzer, S., Caputi, A., & Monyer, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.029 · Cited by 179 · see citing works
Self-citationMultiple Running Speed Signals in Medial Entorhinal Cortex
Hinman, J. R., Brandon, M. P., Climer, J. R., Chapman, G. W., & Hasselmo, M. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.027 · Cited by 156 · see citing works
Leitner, F. C., Melzer, S., Lütcke, H., Pinna, R., Seeburg, P. H., Helmchen, F., & Monyer, H. (2016) · Nature Neuroscience · doi:10.1038/nn.4303 · Cited by 158 · see citing works
Self-citationYekhlef, L., Breschi, G. L., Lagostena, L., Russo, G., & Taverna, S. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00841.2014 · Cited by 152 · see citing works
Lensjø, K. K., Christensen, A. C., Tennøe, S., Fyhn, M., & Hafting, T. (2017) · eneuro · doi:10.1523/eneuro.0379-16.2017 · Cited by 133 · see citing works
Comparative density of CCK- and PV-GABA cells within the cortex and hippocampus
Whissell, P. D., Cajanding, J. D., Fogel, N., & Kim, J. C. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00124 · Cited by 118 · see citing works
Miao, C., Cao, Q., Moser, M., & Moser, E. I. (2017) · Cell · doi:10.1016/j.cell.2017.08.050 · Cited by 129 · see citing works
Neuronal ensembles: Building blocks of neural circuits
Yuste, R., Cossart, R., & Yaksi, E. (2024) · Neuron · doi:10.1016/j.neuron.2023.12.008 · Cited by 127 · see citing works
Frequency of theta rhythm is controlled by acceleration, but not speed, in running rats
Kropff, E., Carmichael, J. E., Moser, E. I., & Moser, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.017 · Cited by 125 · see citing works
Pérez‐Escobar, J. A., Kornienko, O., Latuske, P., Kohler, L., & Allen, K. L. (2016) · eLife · doi:10.7554/elife.16937 · Cited by 112 · see citing works
Self-citationUnsupervised excitation: GABAergic dysfunctions in Alzheimer’s disease
Giovannetti, E. A., & Fuhrmann, M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.11.042 · Cited by 101 · see citing works
Kanter, B. R., Lykken, C. M., Avesar, D., Weible, A. P., Dickinson, J. R., Dunn, B. A., Borgesius, N. Z., Roudi, Y., & Kentros, C. G. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.001 · Cited by 100 · see citing works
Functional properties of stellate cells in medial entorhinal cortex layer II
Rowland, D. C., Obenhaus, H. A., Skytøen, E. R., Zhang, Q., Kentros, C. G., Moser, E. I., & Moser, M. (2018) · eLife · doi:10.7554/elife.36664 · Cited by 90 · see citing works
Microcircuits for spatial coding in the medial entorhinal cortex
Tukker, J. J., Beed, P. S., Brecht, M., Kempter, R., Moser, E. I., & Schmitz, D. (2021) · Physiological Reviews · doi:10.1152/physrev.00042.2020 · Cited by 89 · see citing works
GABA—from Inhibition to Cognition: Emerging Concepts
Schmidt‐Wilcke, T., Fuchs, E., Funke, K., Vlachos, A., Müller‐Dahlhaus, F., Puts, N. A. J., Harris, R. E., & Edden, R. A. E. (2017) · The Neuroscientist · doi:10.1177/1073858417734530 · Cited by 87 · see citing works
Excitatory Microcircuits within Superficial Layers of the Medial Entorhinal Cortex
Winterer, J., Maier, N., Wozny, C., Beed, P. S., Breustedt, J., Evangelista, R., Peng, Y., D’Albis, T., Kempter, R., & Schmitz, D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.04.041 · Cited by 82 · see citing works
The hippocampus converts dynamic entorhinal inputs into stable spatial maps
Cholvin, T., Hainmueller, T., & Bartos, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.019 · Cited by 75 · see citing works
Path integration in normal aging and Alzheimer’s disease
Segen, V., Ying, J., Morgan, E., Brandon, M. P., & Wolbers, T. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.11.001 · Cited by 66 · see citing works
Continuous attractor network models of grid cell firing based on excitatory–inhibitory interactions
Shipston‐Sharman, O., Solanka, L., & Nolan, M. F. (2016) · The Journal of Physiology · doi:10.1113/jp270630 · Cited by 72 · see citing works
Interneuron control of hippocampal oscillations
Allen, K., & Monyer, H. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.016 · Cited by 64 · see citing works
Self-citationCorrelations and Functional Connections in a Population of Grid Cells
Dunn, B. A., Mørreaunet, M., & Roudi, Y. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004052 · Cited by 59 · see citing works
Weir, K., Blanquie, O., Kilb, W., Luhmann, H. J., & Sinning, A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00460 · Cited by 64 · see citing works
A Brainstem Locomotor Circuit Drives the Activity of Speed Cells in the Medial Entorhinal Cortex
Carvalho, M. M., Tanke, N., Kropff, E., Witter, M. P., Moser, M., & Moser, E. I. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108123 · Cited by 64 · see citing works
The grid code for ordered experience
Rueckemann, J. W., Sosa, M., Giocomo, L. M., & Buffalo, E. A. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00499-9 · Cited by 64 · see citing works
Recurrent circuits within medial entorhinal cortex superficial layers support grid cell firing
Zutshi, I., Fu, M. L., Lilascharoen, V., Leutgeb, J. K., Lim, B. K., & Leutgeb, S. (2018) · Nature Communications · doi:10.1038/s41467-018-06104-5 · Cited by 57 · see citing works
Learning place cells, grid cells and invariances with excitatory and inhibitory plasticity
Weber, S. N., & Sprekeler, H. (2018) · eLife · doi:10.7554/elife.34560 · Cited by 60 · see citing works
Booth, C. A., Ridler, T., Murray, T. K., Ward, M. A., de Groot, E., Goodfellow, M., Phillips, K. G., Randall, A. D., & Brown, J. T. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2845-14.2016 · Cited by 55 · see citing works
Entorhinal fast-spiking speed cells project to the hippocampus
Ye, J., Witter, M. P., Moser, M., & Moser, E. I. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720855115 · Cited by 57 · see citing works
Peng, Y., Tomás, F. J. B., Klisch, C., Vida, I., & Geiger, J. R. P. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx049 · Cited by 51 · see citing works
Disruption of the grid cell network in a mouse model of early Alzheimer’s disease
Ying, J., Keinath, A. T., Lavoie, R., Vigneault, É., Mestikawy, S. E., & Brandon, M. P. (2022) · Nature Communications · doi:10.1038/s41467-022-28551-x · Cited by 55 · see citing works
Interspike Intervals Reveal Functionally Distinct Cell Populations in the Medial Entorhinal Cortex
Latuske, P., Toader, O., & Allen, K. L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0276-15.2015 · Cited by 50 · see citing works
Self-citationOrmond, J., & McNaughton, B. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421963112 · Cited by 52 · see citing works
Hartung, H., Brockmann, M. D., Pöschel, B., Feo, V. D., & Hanganu‐Opatz, I. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3232-15.2016 · Cited by 53 · see citing works
Multi-neuronal activity and functional connectivity in cell assemblies
Roudi, Y., Dunn, B. A., & Hertz, J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.10.011 · Cited by 52 · see citing works
Maor, I., Shalev, A., & Mizrahi, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw266 · Cited by 53 · see citing works
Deep entorhinal cortex: from circuit organization to spatial cognition and memory
Gerlei, K. Z., Brown, C. M., Sürmeli, G., & Nolan, M. F. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.08.003 · Cited by 48 · see citing works
Alexander, A. S., Robinson, J. C., Dannenberg, H., Kinsky, N. R., Levy, S. J., Mau, W., Chapman, G. W., Sullivan, D. W., & Hasselmo, M. E. (2020) · Brain and Neuroscience Advances · doi:10.1177/2398212820972871 · Cited by 43 · see citing works
Subfield-Specific Interneuron Circuits Govern the Hippocampal Response to Novelty
Hainmueller, T., Cazala, A., Huang, L.-W., & Bartos, M. (2021) · Nature Communications · doi:10.1038/s41467-024-44882-3 · Cited by 43 · see citing works
Solanka, L., van Rossum, M. C. W., & Nolan, M. F. (2015) · eLife · doi:10.7554/elife.06444 · Cited by 46 · see citing works
Neural mechanisms of navigation involving interactions of cortical and subcortical structures
Hinman, J. R., Dannenberg, H., Alexander, A. S., & Hasselmo, M. E. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00498.2017 · Cited by 42 · see citing works
Tocker, G., Barak, O., & Derdikman, D. (2015) · Hippocampus · doi:10.1002/hipo.22481 · Cited by 41 · see citing works
Toader, O., von Heimendahl, M., Schuelert, N., Nissen, W., & Rosenbrock, H. (2019) · Schizophrenia Bulletin · doi:10.1093/schbul/sbz123 · Cited by 37 · see citing works
Cell type, sub-region, and layer-specific speed representation in the hippocampal–entorhinal circuit
Iwase, M., Kitanishi, T., & Mizuseki, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-58194-1 · Cited by 39 · see citing works
Grosser, S., Tomás, F. J. B., Beed, P. S., Schmitz, D., Booker, S. A., & Vida, I. (2021) · eNeuro · doi:10.1523/eneuro.0354-20.2020 · Cited by 35 · see citing works
Anatomical and Electrophysiological Clustering of Superficial Medial Entorhinal Cortex Interneurons
Martínez, J. J., Rahsepar, B., & White, J. A. (2017) · eNeuro · doi:10.1523/eneuro.0263-16.2017 · Cited by 32 · see citing works
Kimura, R., Saiki, A., Fujiwara‐Tsukamoto, Y., Sakai, Y., & Isomura, Y. (2016) · The Journal of Physiology · doi:10.1113/jp272794 · Cited by 32 · see citing works
Shay, C. F., Ferrante, M., Chapman, G. W., & Hasselmo, M. E. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.09.004 · Cited by 31 · see citing works
Sternfeld, M. J., Hinckley, C. A., Moore, N. J., Pankratz, M. T., Hilde, K. L., Driscoll, S. P., Hayashi, M., Amin, N. D., Bonanomi, D., Gifford, W. D., et al. (2017) · eLife · doi:10.7554/elife.21540 · Cited by 31 · see citing works
Structural modularity and grid activity in the medial entorhinal cortex
Naumann, R. K., Preston‐Ferrer, P., Brecht, M., & Burgalossi, A. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00574.2017 · Cited by 34 · see citing works
Impaired speed encoding and grid cell periodicity in a mouse model of tauopathy
Ridler, T., Witton, J., Phillips, K. G., Randall, A. D., & Brown, J. T. (2020) · eLife · doi:10.7554/elife.59045 · Cited by 25 · see citing works
Ferrante, M., Tahvildari, B., Duque, A., Hadzipasic, M., Salkoff, D. B., Zagha, E., Hasselmo, M. E., & McCormick, D. A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw143 · Cited by 29 · see citing works
Ferrante, M., Shay, C. F., Tsuno, Y., Chapman, G. W., & Hasselmo, M. E. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw058 · Cited by 31 · see citing works
He, C., Luo, F., Chen, X., Chen, F., Li, C., Ren, S., Qiao, Q., Zhang, J., de Lecea, L., Gao, D., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu322 · Cited by 27 · see citing works
Dunn, B. A., Wennberg, D., Huang, Z., & Roudi, Y. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/101899 · Cited by 26 · see citing works
Local origin of excitatory–inhibitory tuning equivalence in a cortical network
Duszkiewicz, A. J., Orhan, P., Carrasco, S. S., Brown, E. H., Owczarek, E., Vite, G. R., Wood, E. R., & Peyrache, A. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01588-5 · Cited by 27 · see citing works
Structural Correlates of CA2 and CA3 Pyramidal Cell Activity in Freely-Moving Mice
Ding, L., Chen, H., Diamantaki, M., Coletta, S., Preston‐Ferrer, P., & Burgalossi, A. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0099-20.2020 · Cited by 28 · see citing works
The Art of Grid Fields: Geometry of Neuronal Time
SHILNIKOV, A. L., & Maurer, A. P. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00012 · Cited by 24 · see citing works
Multiscale relevance and informative encoding in neuronal spike trains
Cubero, R. J., Matteo Marsili, A., & Roudi, Y. (2020) · Journal of Computational Neuroscience · doi:10.1007/s10827-020-00740-x · Cited by 24 · see citing works
Ying, J., Reboreda, A., Yoshida, M., & Brandon, M. P. (2023) · Current Biology · doi:10.1016/j.cub.2023.04.065 · Cited by 24 · see citing works
Reichel, J. M., Nissel, S., Rogel-Salazar, G., Mederer, A., Kaefer, K., Bedenk, B. T., Martens, H., Anders, R. M., Grosche, J., Michalski, D., et al. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00452 · Cited by 23 · see citing works
Distinct spatial maps and multiple object codes in the lateral entorhinal cortex
Huang, X., Schlesiger, M. I., Barriuso-Ortega, I., Leibold, C., MacLaren, D. A. A., Bieber, N., & Monyer, H. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.020 · Cited by 20 · see citing works
Self-citationGrid cells in 3-D: Reconciling data and models
Horiuchi, T. K., & Moss, C. F. (2015) · Hippocampus · doi:10.1002/hipo.22469 · Cited by 21 · see citing works
Molecular Characterization of Superficial Layers of the Presubiculum During Development
Liu, J., Kashima, T., Morikawa, S., Noguchi, A., Ikegaya, Y., & Matsumoto, N. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.662724 · Cited by 20 · see citing works
An entorhinal-like region in food-caching birds
Applegate, M. C., Gutnichenko, K. S., Mackevicius, E. L., & Aronov, D. (2023) · Current Biology · doi:10.1016/j.cub.2023.05.031 · Cited by 21 · see citing works
Kecskés, M., Henn-Mike, N., Agócs-Laboda, Á., Szőcs, S., Petykó, Z., & Varga, C. (2020) · Communications Biology · doi:10.1038/s42003-020-01496-x · Cited by 18 · see citing works
Yekhlef, L., Breschi, G. L., & Taverna, S. (2017) · Scientific Reports · doi:10.1038/srep43230 · Cited by 18 · see citing works
Experimental mismatch in neural circuits
Südhof, T. C. (2015) · Nature · doi:10.1038/nature16323 · Cited by 17 · see citing works
Modular microcircuit organization of the presubicular head-direction map
Balsamo, G., Blanco-Hernández, E., Liang, F., Naumann, R. K., Coletta, S., Burgalossi, A., & Preston‐Ferrer, P. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110684 · Cited by 17 · see citing works
Caputi, A., Liu, X., Fuchs, E. C., Liu, Y., & Monyer, H. (2022) · Neuron · doi:10.1016/j.neuron.2022.08.013 · Cited by 15 · see citing works
Self-citationShi, Y., Cui, H. F., Li, X., Chen, L., Zhang, C., Zhao, X., Li, X., Shao, Q., Sun, Q., Yan, K., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112782 · Cited by 18 · see citing works
Visual stimulus features that elicit activity in object-vector cells
Andersson, S. O., Moser, E. I., & Moser, M. (2021) · Communications Biology · doi:10.1038/s42003-021-02727-5 · Cited by 15 · see citing works
Cell Type Specific Representation of Vibro-tactile Stimuli in the Mouse Primary Somatosensory Cortex
Hayashi, A., Yoshida, T., & Ohki, K. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00109 · Cited by 14 · see citing works
Grid cells in an inhibitory network
Roudi, Y., & Moser, E. I. (2014) · Nature Neuroscience · doi:10.1038/nn.3704 · Cited by 12 · see citing works
Borkowska, M., Millar, J. K., & Price, D. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156082 · Cited by 13 · see citing works
Electrophysiological and Molecular Characterization of the Parasubiculum
Sammons, R. P., Parthier, D., Stumpf, A., & Schmitz, D. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0796-19.2019 · Cited by 12 · see citing works
Effect of boundaries on grid cell patterns
Monsalve‐Mercado, M. M., & Leibold, C. (2020) · Physical Review Research · doi:10.1103/physrevresearch.2.043137 · Cited by 12 · see citing works
Navigating the circuitry of the brain's GPS system: Future challenges for neurophysiologists
Craig, M. T., & McBain, C. J. (2015) · Hippocampus · doi:10.1002/hipo.22456 · Cited by 12 · see citing works
Sutton, N. M., Gutiérrez-Guzmán, B. E., Dannenberg, H., & Ascoli, G. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116059 · Cited by 14 · see citing works
Berggaard, N., Seifi, M., van der Want, J. J. L., & Swinny, J. D. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00046 · Cited by 11 · see citing works
Berggaard, N., Bjerke, I. E., Paulsen, A. E. B., Hoang, L., Skogaker, N. T., Witter, M. P., & van der Want, J. J. L. (2018) · eNeuro · doi:10.1523/eneuro.0438-17.2018 · Cited by 10 · see citing works
GABAA Receptor Subunit α3 in Network Dynamics in the Medial Entorhinal Cortex
Berggaard, N., Witter, M. P., & van der Want, J. J. L. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00010 · Cited by 11 · see citing works
Nakajima, R., Laskaris, N., Rhee, J. K., Baker, B. J., & Kosmidis, E. K. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15177 · Cited by 11 · see citing works
Linking Social Cognition, Parvalbumin Interneurons, and Oxytocin in Alzheimer’s Disease: An Update
Černotová, D., Hrůzová, K., Levčík, D., Svoboda, J., & Stuchlı́k, A. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-230333 · Cited by 12 · see citing works
Ridler, T., Matthews, P. M., Phillips, K. G., Randall, A. D., & Brown, J. T. (2018) · The Journal of Physiology · doi:10.1113/jp275871 · Cited by 10 · see citing works
Computational Models of Grid Cell Firing
Bush, D., & Schmidt‐Hieber, C. (2018) · Springer series in computational neuroscience · doi:10.1007/978-3-319-99103-0_16 · Cited by 11 · see citing works
The neural circuitry supporting successful spatial navigation despite variable movement speeds
Sheeran, W. M., & Ahmed, O. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.013 · Cited by 10 · see citing works
Csordás, D. É., Fischer, C., Nagele, J., Stemmler, M., & Herz, A. V. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2569-19.2020 · Cited by 10 · see citing works
Organizing Sequential Memory in a Neuromorphic Device Using Dynamic Neural Fields
Kreiser, R., Aathmani, D., Qiao, N., Indiveri, G., & Sandamirskaya, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00717 · Cited by 10 · see citing works
- Authors
- Buetfering, C., Allen, K., & Monyer, H.
- Affiliations
- German Cancer Research Center (DE)
- Corresponding author
- Monyer, Hannah
- Venue
- Nature Neuroscience
- Published
- 2014-04-06
- Volume
- 17
- Issue
- 5
- Pages
- 710-718
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2068578235
- Cited by
- 160
- References
- 46
- Citations by year
- 2026: 8 · 2025: 4 · 2024: 17 · 2023: 11 · 2022: 9 · 2021: 16 · 2020: 12 · 2019: 6 · 2018: 17 · 2017: 20 · 2016: 15 · 2015: 17 · 2014: 8
- FWCI
- 11.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Economía y Competitividad
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- parvalbumin interneurons, medial entorhinal cortex, grid cells, recurrent inhibition, spatial tuning, head direction cells, GABAergic interneurons, spatial representation, optogenetic stimulation
- MeSH terms
- Channelrhodopsins, Red Fluorescent Protein, Action Potentials, Dependovirus, Animals, Humans, Interneurons, Lasers, Luminescent Proteins, Microinjections, Models, Neurological, Nerve Net, Neural Inhibition, Parvalbumins, Theta Rhythm, Transduction, Genetic, Statistics, Nonparametric, Entorhinal Cortex, Maze Learning, Mice
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