Mechanism of Graded Persistent Cellular Activity of Entorhinal Cortex Layer V Neurons
Open accessAbstract
Working memory is an emergent property of neuronal networks, but its cellular basis remains elusive. Recent data show that principal neurons of the entorhinal cortex display persistent firing at graded firing rates that can be shifted up or down in response to brief excitatory or inhibitory stimuli. Here, we present a model of a potential mechanism for graded firing. Our multicompartmental model provides stable plateau firing generated by a nonspecific calcium-sensitive cationic (CAN) current. Sustained firing is insensitive to small variations in Ca2+ concentration in a neutral zone. However, both high and low Ca2+ levels alter firing rates. Specifically, increases in persistent firing rate are triggered only during high levels of calcium, while decreases in rate occur in the presence of low levels of calcium. The model is consistent with detailed experimental observations and provides a mechanism for maintenance of memory-related activity in individual neurons.
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ACh enhances persistent spiking or plateau potentials within cortical structures, as demonstrated in brain slice preparations of the entorhinal cortex, prefrontal cortex, postsubiculum and perirhinal cortex.
“ACh enhances persistent spiking or plateau potentials within cortical structures, as demonstrated in brain slice preparations of the entorhinal cortex (Klink and Alonso, 1997; Egorov et al., 2002; Fransen et al., 2006; Tahvildari et al., 2007), prefrontal cortex (Haj-Dahmane and Andrade, 1996, 1997, 1998), postsubiculum (Yoshida and Hasselmo, 2009) and perirhinal cortex (Leung et al., 2006).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Fransen et al., 2006
Persistent spiking appears to result from muscarinic receptor activation of a calcium-sensitive non-specific cation current I(CAN).
“Persistent spiking appears to result from muscarinic receptor activation of a calcium-sensitive non-specific cation current I(CAN) (Egorov et al., 2002; Shalinsky et al., 2002; Fransen et al., 2006).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Fransen et al., 2006
Cites
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
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
Storage of 7 +/- 2 short-term memories in oscillatory subcycles
Lisman, J. E., & Idiart, M. A. P. (1995) · Science · doi:10.1126/science.7878473 · Cited by 1,471 · see citing works
Compte, A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.9.910 · Cited by 1,143 · see citing works
Amit, D. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.237 · Cited by 1,061 · see citing works
Segev, I., & Bradford, A. (1988) · Cited by 911 · see citing works
Neuronal correlates of parametric working memory in the prefrontal cortex
Romo, R., Brody, C. D., Hernández, A., & Lemus, L. (1999) · Nature · doi:10.1038/20939 · Cited by 822 · see citing works
Graded persistent activity in entorhinal cortex neurons
Egorov, A. V., Hamam, B. N., Fransén, E., Hasselmo, M. E., & Alonso, A. A. (2002) · Nature · doi:10.1038/nature01171 · Cited by 769 · see citing works
Self-citationThe Book of GENESIS: Exploring Realistic Neural Models with the GEneral NEural SImulation System
Bower, J. M., & Beeman, D. (1994) · Medical Entomology and Zoology · Cited by 750 · see citing works
Cyclopiazonic Acid is a Specific Inhibitor of the Ca2+-ATPase of Sarcoplasmic Reticulum
Seidler, N. W., Jóna, I., Vegh, M., & Martonosi, A. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84646-x · Cited by 746 · see citing works
Trajectory Encoding in the Hippocampus and Entorhinal Cortex
Frank, L. M., Brown, E. N., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00018-0 · Cited by 731 · see citing works
Traub, R. D., Wong, R. K. S., Miles, R., & Michelson, H. B. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.2.635 · Cited by 715 · see citing works
A model of the electrophysiological properties of thalamocortical relay neurons
McCormick, D. A., & Huguenard, J. R. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.4.1384 · Cited by 648 · see citing works
The CaM kinase II hypothesis for the storage of synaptic memory.
Lisman, J. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90014-0 · Cited by 526 · see citing works
Methods in neuronal modeling: From synapses to networks
Rolls, E. T. (1990) · Biological Psychology · doi:10.1016/0301-0511(90)90081-7 · Cited by 400 · see citing works
Stability of the memory of eye position in a recurrent network of conductance-based model neurons
Seung, H. S., Lee, D. D., Reis, B. Y., & Tank, D. W. (2000) · Neuron · doi:10.1016/s0896-6273(00)81155-1 · Cited by 339 · see citing works
Methods in neuronal modeling: From synapses to networks
Koch, C., & Segev, I. (1989) · Medical Entomology and Zoology · Cited by 338 · see citing works
Camperi, M., & Wang, X. (1998) · Journal of Computational Neuroscience · doi:10.1023/a:1008837311948 · Cited by 323 · see citing works
Persistent neural activity: prevalence and mechanisms
Major, G., & Tank, D. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.10.017 · Cited by 320 · see citing works
Model for a robust neural integrator
Koulakov, A. A., Raghavachari, S., Kepecs, Á., & Lisman, J. E. (2002) · Nature Neuroscience · doi:10.1038/nn893 · Cited by 308 · see citing works
Brody, C. D., Romo, R., & Kepecs, A. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00050-3 · Cited by 284 · see citing works
Howard, M. W., Fotedar, M. S., Datey, A. V., & Hasselmo, M. E. (2005) · Psychological Review · doi:10.1037/0033-295x.112.1.75 · Cited by 283 · cited 1× · see citing works
“Howard et al. (2005) showed that integration of head direction input enables the system to obtain high precision in a spatial location estimate and could contribute to trajectory encoding by EC cells (Frank et al., 2000).”
MethodSelf-citationLisman, J. E., & Goldring, M. A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5320 · Cited by 257 · see citing works
Efficient computation of branched nerve equations
Hines, M. L. (1984) · International Journal of Bio-Medical Computing · doi:10.1016/0020-7101(84)90008-4 · Cited by 255 · see citing works
Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior
Heckman, C. J., Lee, R. H., & Brownstone, R. M. (2003) · Trends in Neurosciences · doi:10.1016/j.tins.2003.10.002 · Cited by 245 · see citing works
Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli
Stern, C. E., Sherman, S. J., Kirchhoff, B. A., & Hasselmo, M. E. (2001) · Hippocampus · doi:10.1002/hipo.1048 · Cited by 244 · see citing works
Self-citationMultiple channels and calcium dynamics
Yamada, W. M., Koch, C., & Adams, P. R. (1989) · Cited by 242 · see citing works
Georges‐François, P. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.3.197 · Cited by 226 · see citing works
Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land
Lisman, J. E. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0285f.x · Cited by 223 · see citing works
Self-Organizing Neural Integrator Predicts Interval Times through Climbing Activity
Durstewitz, D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05342.2003 · Cited by 194 · see citing works
Cho, K., Aggleton, J. P., Brown, M. W., & Bashir, Z. I. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0459f.x · Cited by 174 · see citing works
A proposed neural network for the integrator of the oculomotor system
Cannon, S., Robinson, D. A., & Shamma, S. (1983) · Biological cybernetics · doi:10.1007/bf00320393 · Cited by 173 · see citing works
Persistent Neural Activity in Head Direction Cells
Taube, J. S. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg102 · Cited by 167 · see citing works
Ionic Mechanisms of Muscarinic Depolarization in Entorhinal Cortex Layer II Neurons
Klink, R., & Alonso, Á. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.4.1829 · Cited by 164 · see citing works
Temporal integration by calcium dynamics in a model neuron
Loewenstein, Y., & Sompolinsky, H. (2003) · Nature Neuroscience · doi:10.1038/nn1109 · Cited by 148 · see citing works
A recurrent network model of somatosensory parametric working memory in the prefrontal cortex
Miller, P. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg101 · Cited by 144 · see citing works
Fransén, E., Alonso, A. A., & Hasselmo, M. E. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01081.2002 · Cited by 137 · see citing works
Self-citationSchon, K., Atri, A., Hasselmo, M. E., Tricarico, M. D., LoPresti, M. L., & Stern, C. E. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1982-05.2005 · Cited by 132 · see citing works
Self-citationKoene, R. A., Anatoli Gorchetchnikov, A., Cannon, R. C., & Hasselmo, M. E. (2003) · Neural Networks · doi:10.1016/s0893-6080(03)00106-0 · Cited by 87 · see citing works
Self-citationA model of cortical associative memory based on a horizontal network of connected columns
Fransén, E. A., & Lansner, A. (1998) · Network Computation in Neural Systems · doi:10.1088/0954-898x_9_2_006 · Cited by 82 · see citing works
Self-citationA role for prefrontal calcium-sensitive protein phosphatase and kinase activities in working memory
Runyan, J. D., Moore, A. N., & Dash, P. K. (2005) · Learning & Memory · doi:10.1101/lm.89405 · Cited by 68 · see citing works
Shalinsky, M. H., Magistretti, J., Ma, L., & Alonso, A. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1197 · Cited by 65 · see citing works
Self-citationGloveli, T., Egorov, A. V., Schmitz, D., Heinemann, U., & Müller, W. S. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00785.x · Cited by 59 · see citing works
Self-citationFuhs, M. C., VanRhoads, S. R., Casale, A. E., McNaughton, B., & Touretzky, D. S. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00132.2005 · Cited by 53 · see citing works
Connors, B. W. (2002) · Nature · doi:10.1038/420133a · Cited by 50 · see citing works
Low spiking rates in a population of mutually exciting pyramidal cells
Fransén, E., & Lansner, A. (1995) · Network Computation in Neural Systems · doi:10.1088/0954-898x_6_2_008 · Cited by 48 · see citing works
Self-citationInoue, R., Waniishi, Y., Yamada, K., & Ito, Y. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.2339 · Cited by 42 · see citing works
Persistent activity and memory in the entorhinal cortex
Frank, L. M., & Brown, E. N. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00176-0 · Cited by 33 · see citing works
On the nature of visual-oculomotor connections.
Robinson, D. A. (1972) · PubMed · Cited by 31 · see citing works
Teramae, J.-N., & Fukai, T. (2005) · Journal of Computational Neuroscience · doi:10.1007/s10827-005-5474-6 · Cited by 29 · see citing works
Regulation of cGMP-dependent current in On bipolar cells by calcium/calmodulin-dependent kinase
Walters, R. J., Kramer, R., & Nawy, S. (1998) · Visual Neuroscience · doi:10.1017/s0952523898152057 · Cited by 24 · see citing works
Presubicular Input to the Dendrites of Layer‐V Entorhinal Neurons in the Rat
van Haeften, T., Wouterlood, F. G., & Witter, M. P. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06748.x · Cited by 22 · see citing works
Low spiking rates in a population of mutually exciting pyramidal cells
Fransen, E. J., & Lansner, A. (1995) · Network Computation in Neural Systems · doi:10.1088/0954-898x/6/2/008 · Cited by 11 · see citing works
Integrating over time with dendritic wave-fronts
Wang, S. S. ‐., & Major, G. (2003) · Nature Neuroscience · doi:10.1038/nn0903-906 · Cited by 5 · see citing works
Model for an enzymatic reaction-diffusion system realizing storage of graded information
Okamoto, H., & Ichikawa, K. (1994) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.50.1704 · Cited by 3 · see citing works
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Mongillo, G., Barak, O., & Tsodyks, M. (2008) · Science · doi:10.1126/science.1150769 · Cited by 1,253 · see citing works
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Knudsen, E. I. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094256 · Cited by 1,020 · see citing works
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Herz, A. V. M., Gollisch, T., Machens, C. K., & Jaeger, D. (2006) · Science · doi:10.1126/science.1127240 · Cited by 450 · see citing works
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Giocomo, L. M., Zilli, E. A., Fransén, E., & Hasselmo, M. E. (2007) · Science · doi:10.1126/science.1139207 · Cited by 377 · see citing works
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Inagaki, H. K., Fontolan, L., Romani, S., & Svoboda, K. (2019) · Nature · doi:10.1038/s41586-019-0919-7 · Cited by 334 · see citing works
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Self-citationGilmartin, M. R., & Helmstetter, F. J. (2010) · Learning & Memory · doi:10.1101/lm.1597410 · Cited by 196 · see citing works
Beyond working memory: the role of persistent activity in decision making
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Neural underpinnings of the evidence accumulator
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Rubin, J. E., Hayes, J. A., Mendenhall, J., & Negro, C. A. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808776106 · Cited by 163 · see citing works
The what, where and how of delay activity
Sreenivasan, K. K., & D’Esposito, M. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0176-7 · Cited by 156 · see citing works
A model of episodic memory: Mental time travel along encoded trajectories using grid cells
Hasselmo, M. E. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.07.005 · Cited by 157 · see citing works
Self-citationSUZUKI, W. A., & Naya, Y. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014207 · Cited by 157 · see citing works
Canto, C. B., & Witter, M. P. (2011) · Hippocampus · doi:10.1002/hipo.20997 · Cited by 141 · see citing works
Spatial gradients and multidimensional dynamics in a neural integrator circuit
Miri, A., Daie, K., Arrenberg, A. B., Baier, H., Aksay, E., & Tank, D. W. (2011) · Nature Neuroscience · doi:10.1038/nn.2888 · Cited by 138 · see citing works
A Scale-Invariant Internal Representation of Time
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Persistent Activity in Neural Networks with Dynamic Synapses
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Functional dissection of circuitry in a neural integrator
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Neural dynamics and circuit mechanisms of decision-making
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Intrinsic neuronal dynamics predict distinct functional roles during working memory
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DC-shifts in amplitude in-field generated by an oscillatory interference model of grid cell firing
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Self-citationHahn, T. T. G., McFarland, J. M., Berberich, S., Sakmann, B. J., & Mehta, M. R. (2012) · Nature Neuroscience · doi:10.1038/nn.3236 · Cited by 117 · see citing works
Tahvildari, B., Fransén, E. A., Alonso, A. A., & Hasselmo, M. E. (2007) · Hippocampus · doi:10.1002/hipo.20270 · Cited by 113 · see citing works
Self-citationEstrogens directly potentiate neuronal L-type Ca 2+ channels
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Ensembles of human MTL neurons “jump back in time” in response to a repeated stimulus
Howard, M. W., Viskontas, I. V., Shankar, K. H., & Fried, I. (2012) · Hippocampus · doi:10.1002/hipo.22018 · Cited by 92 · see citing works
Yoshida, M., & Hasselmo, M. E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5154-08.2009 · Cited by 94 · see citing works
Self-citationmGluR‐dependent persistent firing in entorhinal cortex layer III neurons
Yoshida, M., Fransén, E. A., & Hasselmo, M. E. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06409.x · Cited by 93 · see citing works
Self-citationComputational significance of transient dynamics in cortical networks
Durstewitz, D., & Deco, G. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05976.x · Cited by 90 · see citing works
Thuault, S., Malleret, G., Constantinople, C. M., Nicholls, R. E., Chen, I., Zhu, J., Panteleyev, A. A., Vronskaya, S., Nolan, M. F., Bruno, R. M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2427-12.2013 · Cited by 91 · see citing works
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MacNeil, D., & Eliasmith, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022885 · Cited by 84 · see citing works
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Goldman, M. S., Compte, A., & Wang, X.-J. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01434-0 · Cited by 77 · see citing works
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Salaj, D., Subramoney, A., Kraišniković, C., Bellec, G., Legenstein, R. A., & Maass, W. (2021) · eLife · doi:10.7554/elife.65459 · Cited by 80 · see citing works
Ca2+ entry into neurons is facilitated by cooperative gating of clustered CaV1.3 channels
Moreno, C. M., Dixon, R. E., Tajada, S., Yuan, C., Opitz-Araya, X., Binder, M. D., & Santana, L. F. (2016) · eLife · doi:10.7554/elife.15744 · Cited by 80 · see citing works
Dynamics of Memory Representations in Networks with Novelty-Facilitated Synaptic Plasticity
Blumenfeld, B., Preminger, S., Sagi, D., & Tsodyks, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.016 · Cited by 79 · see citing works
Dunmyre, J. R., Negro, C. A. D., & Rubin, J. E. (2011) · Journal of Computational Neuroscience · doi:10.1007/s10827-010-0311-y · Cited by 77 · see citing works
Muscarinic control of graded persistent activity in lateral amygdala neurons
Egorov, A., Unsicker, K., & Halbach, O. V. B. U. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05200.x · Cited by 81 · see citing works
Self-citationKoppe, G., Toutounji, H., Kirsch, P., Lis, S., & Durstewitz, D. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007263 · Cited by 74 · see citing works
Interaction of Working Memory and Long-Term Memory in the Medial Temporal Lobe
Axmacher, N., Schmitz, D. P., Weinreich, I., Elger, C. E., & Fell, J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn045 · Cited by 73 · see citing works
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Giocomo, L. M., & Hasselmo, M. E. (2008) · Hippocampus · doi:10.1002/hipo.20501 · Cited by 72 · see citing works
Self-citationHasselmo, M. E., & Brandon, M. P. (2008) · Neural Plasticity · doi:10.1155/2008/658323 · Cited by 69 · see citing works
Self-citationFriedemann Pulvermüller, A., & Garagnani, M. (2014) · Cortex · doi:10.1016/j.cortex.2014.02.015 · Cited by 70 · see citing works
Metabotropic Induction of Persistent Activity in Layers II/III of Anterior Cingulate Cortex
Zhang, Z., & Séguéla, P. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq043 · Cited by 67 · see citing works
Lisman, J. E. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63033-7 · Cited by 67 · see citing works
Auditory trace fear conditioning requires perirhinal cortex
Kholodar-Smith, D. B., Boguszewski, P. M., & Brown, T. H. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.006 · Cited by 65 · see citing works
Greater Working Memory Load Results in Greater Medial Temporal Activity at Retrieval
Schön, K., Quiroz, Y. T., Hasselmo, M. E., & Stern, C. E. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp006 · Cited by 67 · see citing works
Self-citationHyperpolarization-activated graded persistent activity in the prefrontal cortex
Winograd, M., Alain Destexhe, A., & Sanchez-Vives, M. V. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800360105 · Cited by 62 · see citing works
Optimizing Working Memory with Heterogeneity of Recurrent Cortical Excitation
Kilpatrick, Z. P., Ermentrout, B., & Doiron, B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1641-13.2013 · Cited by 61 · see citing works
The Neuronal Replicator Hypothesis
Fernando, C., Goldstein, R. A., & Szathmáry, E. (2010) · Neural Computation · doi:10.1162/neco_a_00031 · Cited by 58 · see citing works
Rathour, R. K., & Narayanan, R. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.239418 · Cited by 61 · see citing works
Barbieri, F. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.003.2008 · Cited by 60 · see citing works
How Attention Can Create Synaptic Tags for the Learning of Working Memories in Sequential Tasks
Rombouts, J. O., Bohté, S. M., & Roelfsema, P. R. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004060 · Cited by 60 · see citing works
Effects of acetylcholine on neuronal properties in entorhinal cortex
Heys, J. G., Schultheiss, N. W., Shay, C. F., Tsuno, Y., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00032 · Cited by 56 · see citing works
Self-citationZilli, E. A., Yoshida, M., Tahvildari, B., Giocomo, L. M., & Hasselmo, M. E. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000573 · Cited by 58 · see citing works
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Tiganj, Z., Hasselmo, M. E., & Howard, M. W. (2014) · Hippocampus · doi:10.1002/hipo.22347 · Cited by 57 · see citing works
Self-citationGalloway, E. M., Woo, N. H., & Lu, B. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00015-5 · Cited by 55 · see citing works
Navaroli, V. L., Zhao, Y., Boguszewski, P. M., & Brown, T. H. (2011) · Hippocampus · doi:10.1002/hipo.20975 · Cited by 55 · see citing works
Muscarinic Receptors in Perirhinal Cortex Control Trace Conditioning
Bang, S. J., & Brown, T. H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0069-09.2009 · Cited by 55 · see citing works
Feng, H., Su, J., Fang, W., Chen, X., & He, J. (2021) · eLife · doi:10.7554/elife.69333 · Cited by 55 · see citing works
A neural microcircuit model for a scalable scale‐invariant representation of time
Liu, Y., Tiganj, Z., Hasselmo, M. E., & Howard, M. W. (2018) · Hippocampus · doi:10.1002/hipo.22994 · Cited by 52 · see citing works
Self-citationImplications of synaptic biophysics for recurrent network dynamics and active memory
Durstewitz, D. (2009) · Neural Networks · doi:10.1016/j.neunet.2009.07.016 · Cited by 48 · see citing works
Tahvildari, B., Alonso, A. A., & Bourque, C. W. (2008) · Journal of Neurophysiology · doi:10.1152/jn.00911.2007 · Cited by 51 · see citing works
Self-citationGrid cell spatial tuning reduced following systemic muscarinic receptor blockade
Newman, E. L., Climer, J. R., & Hasselmo, M. E. (2014) · Hippocampus · doi:10.1002/hipo.22253 · Cited by 50 · see citing works
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Tully, P. J., Hennig, M. H., & Lansner, A. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00008 · Cited by 47 · see citing works
Cruzado, N. A., Tiganj, Z., Brincat, S. L., Miller, E. K., & Howard, M. W. (2020) · Hippocampus · doi:10.1002/hipo.23282 · Cited by 43 · see citing works
Heading‐vector navigation based on head‐direction cells and path integration
Kubie, J. L., & Fenton, A. A. (2008) · Hippocampus · doi:10.1002/hipo.20532 · Cited by 49 · see citing works
Dual functions of perirhinal cortex in fear conditioning
Kent, B. A., & Brown, T. H. (2012) · Hippocampus · doi:10.1002/hipo.22058 · Cited by 49 · 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
Hasselmo, M. E., Giocomo, L. M., Brandon, M. P., & Yoshida, M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.010 · Cited by 47 · see citing works
Self-citationNeurocomputational Models of Time Perception
Haß, J., & Durstewitz, D. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1782-2_4 · Cited by 47 · see citing works
Rahman, J., & Berger, T. K. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07736.x · Cited by 46 · see citing works
First-In-First-Out Item Replacement in a Model of Short-Term Memory Based on Persistent Spiking
Koene, R. A., & Hasselmo, M. E. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl088 · Cited by 45 · see citing works
Self-citationPersistent firing supported by an intrinsic cellular mechanism in hippocampal CA 3 pyramidal cells
Jochems, A., & Yoshida, M. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12236 · Cited by 45 · see citing works
Caruana, D. A., Sorge, R. E., Stewart, J., & Chapman, C. A. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00572.2006 · Cited by 42 · see citing works
Lei, Y.-T., Thuault, S., Launay, P., Margolskee, R. F., Kandel, E. R., & Siegelbaum, S. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00267 · Cited by 43 · see citing works
Spontaneous Bursting Activity in the Developing Entorhinal Cortex
Sheroziya, M., Halbach, O. V. B. U., Unsicker, K., & Egorov, A. V. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1333-09.2009 · Cited by 42 · see citing works
Self-citation
- Authors
- Fransén, E., Tahvildari, B., Egorov, A. V., Hasselmo, M. E., & Alonso, A. A.
- Affiliations
- KTH Royal Institute of Technology (SE)
- Montreal Neurological Institute and Hospital (CA)
- Heidelberg University (DE)
- Boston University (US)
- Corresponding author
- Fransén, Erik
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2006-03
- Volume
- 49
- Issue
- 5
- Pages
- 735-746
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2156985666
- Cited by
- 279
- References
- 54
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 11 · 2023: 5 · 2022: 5 · 2021: 16 · 2020: 13 · 2019: 8 · 2018: 14 · 2017: 7 · 2016: 10 · 2015: 10 · 2014: 18 · 2013: 19 · 2012: 16
- FWCI
- 11.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Vetenskapsrådet
- Canadian Institutes of Health Research
- National Institute of Mental Health (MH 60013, MH61492, R01MH061492)
- National Institute on Drug Abuse (DA 16454, R01DA016454)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- entorhinal cortex, layer V neurons, persistent neuronal activity, working memory, multicompartmental neuron models, calcium concentration, memory maintenance
- MeSH terms
- Action Potentials, Animals, Calcium, Dose-Response Relationship, Radiation, Electric Stimulation, Enzyme Inhibitors, Indoles, Models, Neurological, Neurons, Time Factors, Calcium Channels, Potassium Channels, Nonlinear Dynamics, Entorhinal Cortex, Thapsigargin, Calcium Signaling, Rats, In Vitro Techniques
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.
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