Homogeneous inhibition is optimal for the phase precession of place cells in the CA1 field

Baker, J. L., & Olds, J. L. (2007). Theta phase precession emerges from a hybrid computational model of a ca3 place cell. Cognitive neurodynamics, 1(3), 237–248. https://doi.org/10.1007/s11571-007-9018-9

Article  PubMed  PubMed Central  Google Scholar 

Behnel, S., Bradshaw, R., Citro, C., Dalcin, L., Seljebotn, D. S., & Smith, K. (2011). Cython: The best of both worlds. Computing in science and engineering, 13(2), 31–39. https://doi.org/10.1109/MCSE.2010.118

Article  Google Scholar 

Bezaire, M. J., & Soltesz, I. (2013). Quantitative assessment of ca1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. Hippocampus, 23(9), 751–785. https://doi.org/10.1002/hipo.22141

Article  PubMed  PubMed Central  Google Scholar 

Burgess, N., & O’Keefe, J. (2011). Models of place and grid cell firing and theta rhythmicity. Current Opinion in Neurobiology, 21(5), 734–744. https://doi.org/10.1016/j.conb.2011.07.002

Article  CAS  PubMed  PubMed Central  Google Scholar 

Buzsáki, G., & Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neuroscience, 16(2), 130–138. https://doi.org/10.1038/nn.3304

Article  CAS  PubMed  PubMed Central  Google Scholar 

Castro, L., & Aguiar, P. (2012). Phase precession through acceleration of local theta rhythm: a biophysical model for the interaction between place cells and local inhibitory neurons. Journal of Computational Neuroscience, 33(1), 141–150. https://doi.org/10.1007/s10827-011-0378-0

Article  PubMed  Google Scholar 

Chance, F. S. (2012). Hippocampal phase precession from dual input components. The Journal of Neuroscience, 32(47), 16693–703. https://doi.org/10.1523/JNEUROSCI.2786-12.2012

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cutsuridis, V., & Hasselmo, M. (2012). Gabaergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations. Hippocampus, 22(7), 1597–1621. https://doi.org/10.1002/hipo.21002

Article  CAS  PubMed  Google Scholar 

Dudok, B., Szoboszlay, M., Paul, A., Klein, P. M., Liao, Z., Hwaun, E., Szabo, G. G., Geiller, T., Vancura, B., Wang, B.-S., et al. (2021). Recruitment and inhibitory action of hippocampal axo-axonic cells during behavior. Neuron, 109(23), 3838–38508. https://doi.org/10.1016/j.neuron.2021.09.033

Article  CAS  PubMed  PubMed Central  Google Scholar 

Eichenbaum, H. (2014). Time cells in the hippocampus: a new dimension for mapping memories. Nature Reviews. Neuroscience, 15(11), 732–744. https://doi.org/10.1038/nrn3827

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ferguson, K. A., & Campbell, S. A. (2009). A two compartment model of a ca1 pyramidal neuron. Canadian Applied Mathematics Quarterly, 17(2), 293–307.

Google Scholar 

Fernandez-Lamo, I., Gomez-Dominguez, D., Sanchez-Aguilera, A., Oliva, A., Morales, A.V., Valero, M., Cid, E., Berenyi, A., & Menendez dela Prida, L. (2019). Proximodistal organization of the ca2 hippocampal area. Cell Reports, 26(7), 1734–17466. https://doi.org/10.1016/j.celrep.2019.01.060

Fernández-Ruiz, A., Oliva, A., Nagy, G. A., Maurer, A. P., Berényi, A., & Buzsáki, G. (2017). Entorhinal-ca3 dual-input control of spike timing in the hippocampus by theta-gamma coupling. Neuron, 93(5), 1213–12265. https://doi.org/10.1016/j.neuron.2017.02.017

Article  CAS  PubMed  PubMed Central  Google Scholar 

Geiller, T., Sadeh, S., Rolotti, S. V., Blockus, H., Vancura, B., Negrean, A., Murray, A. J., Rózsa, B., Polleux, F., Clopath, C., & Losonczy, A. (2022). Local circuit amplification of spatial selectivity in the hippocampus. Nature, 601(7891), 105–109. https://doi.org/10.1038/s41586-021-04169-9

Article  CAS  PubMed  Google Scholar 

Geiller, T., Vancura, B., Terada, S., Troullinou, E., Chavlis, S., Tsagkatakis, G., Tsakalides, P., ócsai, K., Poirazi, P., Rózsa, B. J., et al. (2020). Large-scale 3d two-photon imaging of molecularly identified ca1 interneuron dynamics in behaving mice. Neuron, 108(5), 968–9839. https://doi.org/10.1016/j.neuron.2020.09.013

Geisler, C., Robbe, D., Zugaro, M., Sirota, A., & Buzsáki, G. (2007). Hippocampal place cell assemblies are speed-controlled oscillators. Proceedings of the National Academy of Sciences of the United States of America, 104(19), 8149–8154. https://doi.org/10.1073/pnas.0610121104

Article  CAS  PubMed  PubMed Central  Google Scholar 

Grienberger, C., Milstein, A. D., Bittner, K. C., Romani, S., & Magee, J. C. (2017). Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in ca1 place cells. Nature Neuroscience, 20(3), 417–426. https://doi.org/10.1038/nn.4486

Article  CAS  PubMed  Google Scholar 

Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.-B., & Moser, E. I. (2008). Hippocampus-independent phase precession in entorhinal grid cells. Nature, 453(7199), 1248–1252. https://doi.org/10.1038/nature06957

Article  CAS  PubMed  Google Scholar 

Harris, C. R., Millman, K. J., van der Walt, S. J., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N. J., et al. (2020). Array programming with numpy. Nature, 585(7825), 357–362. https://doi.org/10.1038/s41586-020-2649-2

Article  CAS  PubMed  PubMed Central  Google Scholar 

Harris, K. D., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., Czurkó, A., & Buzsáki, G. (2002). Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature, 417(6890), 738–741. https://doi.org/10.1038/nature00808

Article  CAS  PubMed  Google Scholar 

Hunter, J. D. (2007). Matplotlib: A 2d graphics environment. Computing in science and engineering, 9(3), 90–95. https://doi.org/10.1109/MCSE.2007.55

Article  Google Scholar 

Jeffery, K. J. (2011). Place cells, grid cells, attractors, and remapping. Neural plasticity, 2011, 182602. https://doi.org/10.1155/2011/182602

Article  PubMed  PubMed Central  Google Scholar 

Kamondi, A., Acsády, L., Wang, X. J., & Buzsáki, G. (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus, 8(3), 244–261. https://doi.org/10.1002/(SICI)1098-1063(1998)8:3<244::AID-HIPO7>3.0.CO;2-J

Article  CAS  PubMed  Google Scholar 

Kempter, R., Leibold, C., Buzsáki, G., Diba, K., & Schmidt, R. (2012). Quantifying circular-linear associations: hippocampal phase precession. Journal of Neuroscience Methods, 207(1), 113–124. https://doi.org/10.1016/j.jneumeth.2012.03.007

Article  PubMed  Google Scholar 

Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003). Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature, 421(6925), 844–848. https://doi.org/10.1038/nature01374

Article  CAS  PubMed  Google Scholar 

Lam, S. K., Pitrou, A., & Seibert, S. (2015). Numba: A LLVM-based Python JIT compiler, pp. 1–6. ACM Press. https://doi.org/10.1145/2833157.2833162

Lasztóczi, B., & Klausberger, T. (2016). Hippocampal place cells couple to three different gamma oscillations during place field traversal. Neuron, 91(1), 34–40. https://doi.org/10.1016/j.neuron.2016.05.036

Article  CAS  PubMed  Google Scholar 

Lee, A. (2010). Circular data. Wiley Interdisciplinary Reviews: Computational Statistics, 2(4), 477–486. https://doi.org/10.1002/wics.98

Article  Google Scholar 

Losonczy, A., Zemelman, B. V., Vaziri, A., & Magee, J. C. (2010). Network mechanisms of theta related neuronal activity in hippocampal ca1 pyramidal neurons. Nature Neuroscience, 13(8), 967–972. https://doi.org/10.1038/nn.2597

Article  CAS  PubMed  PubMed Central  Google Scholar 

Magee, J. C. (2001). Dendritic mechanisms of phase precession in hippocampal ca1 pyramidal neurons. Journal of Neurophysiology, 86(1), 528–532. https://doi.org/10.1152/jn.2001.86.1.528

Article  CAS  PubMed  Google Scholar 

Malvache, A., Reichinnek, S., Villette, V., Haimerl, C., & Cossart, R. (2016). Awake hippocampal reactivations project onto orthogonal neuronal assemblies. Science, 353(6305), 1280–1283. https://doi.org/10.1126/science.aaf3319

Article  CAS  PubMed  Google Scholar 

Mardia, J. (1999). Directional Statistics. John Wiley and Sons, Inc. https://doi.org/10.1002/9780470316979

Mardia, K. V. (1976). Linear-circular correlation coefficients and rhythmometry. Biometrika, 63(2), 403. https://doi.org/10.2307/2335637

Article  Google Scholar 

Markiewicz, C. J., Gorgolewski, K. J., Feingold, F., Blair, R., Halchenko, Y. O., Miller, E., Hardcastle, N., Wexler, J., Esteban, O., Goncavles, M., et al. (2021). The openneuro resource for sharing of neuroscience data. eLife, 10. https://doi.org/10.7554/eLife.71774

Marshall, L., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., & Buzsáki, G. (2002). Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge. The Journal of Neuroscience, 22(2), 197.

Article  Google Scholar 

Masurkar, A. V., Srinivas, K. V., Brann, D. H., Warren, R., Lowes, D. C., & Siegelbaum, S. A. (2017). Medial and lateral entorhinal cortex differentially excite deep versus superficial ca1 pyramidal neurons. Cell Reports, 18(1), 148–160. https://doi.org/10.1016/j.celrep.2016.12.012

Article  CAS  PubMed  Google Scholar 

Maurer, A. P., Cowen, S. L., Burke, S. N., Barnes, C. A., & McNaughton, B. L. (2006). Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. The Journal of Neuroscience, 26(52), 13485–13492. https://doi.org/10.1523/JNEUROSCI.2882-06.2006

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mehta, M. R., Lee, A. K., & Wilson, M. A. (2002). Role of experience and oscillations in transforming a rate code into a temporal code. Nature, 417(6890), 741–746. https://doi.org/10.1038/nature00807

Article  CAS  PubMed  Google Scholar 

Mizuseki, K., Diba, K., Pastalkova, E., Teeters, J., Sirota, A., & Buzsáki, G. (2014). Neurosharing: large-scale data sets (spike, lfp) recorded from the hippocampal-entorhinal system in behaving rats. [version 1; peer review: 4 approved]. F1000Research, 3, 98. https://doi.org/10.12688/f1000research.3895.1

Mizuseki, K., Royer, S., Diba, K., & Buzsáki, G. (2012). Activity dynamics and behavioral correlates of ca3 and ca1 hippocampal pyramidal neurons. Hippocampus, 22(8), 1659–1680. https://doi.org/10.1002/hipo.22002

Article  CAS  PubMed 

Comments (0)

No login
gif