Homogeneous inhibition is optimal for the phase precession of place cells in the CA1 field. (English) Zbl 1533.92016
Summary: Place cells are hippocampal neurons encoding the position of an animal in space. Studies of place cells are essential to understanding the processing of information by neural networks of the brain. An important characteristic of place cell spike trains is phase precession. When an animal is running through the place field, the discharges of the place cells shift from the ascending phase of the theta rhythm through the minimum to the descending phase. The role of excitatory inputs to pyramidal neurons along the Schaffer collaterals and the perforant pathway in phase precession is described, but the role of local interneurons is poorly understood. Our goal is estimating of the contribution of field CA1 interneurons to the phase precession of place cells using mathematical methods. The CA1 field is chosen because it provides the largest set of experimental data required to build and verify the model. Our simulations discover optimal parameters of the excitatory and inhibitory inputs to the pyramidal neuron so that it generates a spike train with the effect of phase precession. The uniform inhibition of pyramidal neurons best explains the effect of phase precession. Among interneurons, axo-axonal neurons make the greatest contribution to the inhibition of pyramidal cells.
MSC:
| 92B20 | Neural networks for/in biological studies, artificial life and related topics |
References:
| [1] | Baker, JL; Olds, JL, Theta phase precession emerges from a hybrid computational model of a ca3 place cell, Cognitive neurodynamics, 1, 3, 237-248 (2007) · doi:10.1007/s11571-007-9018-9 |
| [2] | Behnel, S.; Bradshaw, R.; Citro, C.; Dalcin, L.; Seljebotn, DS; Smith, K., Cython: The best of both worlds, Computing in science and engineering, 13, 2, 31-39 (2011) · doi:10.1109/MCSE.2010.118 |
| [3] | Bezaire, MJ; Soltesz, I., Quantitative assessment of ca1 local circuits: knowledge base for interneuron-pyramidal cell connectivity, Hippocampus, 23, 9, 751-785 (2013) · doi:10.1002/hipo.22141 |
| [4] | Burgess, N.; O’Keefe, J., Models of place and grid cell firing and theta rhythmicity, Current Opinion in Neurobiology, 21, 5, 734-744 (2011) · doi:10.1016/j.conb.2011.07.002 |
| [5] | Buzsáki, G.; Moser, EI, Memory, navigation and theta rhythm in the hippocampal-entorhinal system, Nature Neuroscience, 16, 2, 130-138 (2013) · doi:10.1038/nn.3304 |
| [6] | Castro, L.; Aguiar, P., 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 (2012) · Zbl 1446.92115 · doi:10.1007/s10827-011-0378-0 |
| [7] | Chance, FS, Hippocampal phase precession from dual input components, The Journal of Neuroscience, 32, 47, 16693-703 (2012) · doi:10.1523/JNEUROSCI.2786-12.2012 |
| [8] | Cutsuridis, V.; Hasselmo, M., Gabaergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations, Hippocampus, 22, 7, 1597-1621 (2012) · doi:10.1002/hipo.21002 |
| [9] | Dudok, B.; Szoboszlay, M.; Paul, A.; Klein, PM; Liao, Z.; Hwaun, E.; Szabo, GG; Geiller, T.; Vancura, B.; Wang, B-S, Recruitment and inhibitory action of hippocampal axo-axonic cells during behavior, Neuron, 109, 23, 3838-38508 (2021) · doi:10.1016/j.neuron.2021.09.033 |
| [10] | Eichenbaum, H., Time cells in the hippocampus: a new dimension for mapping memories, Nature Reviews. Neuroscience, 15, 11, 732-744 (2014) · doi:10.1038/nrn3827 |
| [11] | Ferguson, KA; Campbell, SA, A two compartment model of a ca1 pyramidal neuron, Canadian Applied Mathematics Quarterly, 17, 2, 293-307 (2009) · Zbl 1209.92010 |
| [12] | 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. doi:10.1016/j.celrep.2019.01.060 |
| [13] | Fernández-Ruiz, A.; Oliva, A.; Nagy, GA; Maurer, AP; Berényi, A.; Buzsáki, G., Entorhinal-ca3 dual-input control of spike timing in the hippocampus by theta-gamma coupling, Neuron, 93, 5, 1213-12265 (2017) · doi:10.1016/j.neuron.2017.02.017 |
| [14] | Geiller, T.; Sadeh, S.; Rolotti, SV; Blockus, H.; Vancura, B.; Negrean, A.; Murray, AJ; Rózsa, B.; Polleux, F.; Clopath, C.; Losonczy, A., Local circuit amplification of spatial selectivity in the hippocampus, Nature, 601, 7891, 105-109 (2022) · doi:10.1038/s41586-021-04169-9 |
| [15] | 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. doi:10.1016/j.neuron.2020.09.013 |
| [16] | Geisler, C.; Robbe, D.; Zugaro, M.; Sirota, A.; Buzsáki, G., 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 (2007) · doi:10.1073/pnas.0610121104 |
| [17] | Grienberger, C.; Milstein, AD; Bittner, KC; Romani, S.; Magee, JC, Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in ca1 place cells, Nature Neuroscience, 20, 3, 417-426 (2017) · doi:10.1038/nn.4486 |
| [18] | Hafting, T.; Fyhn, M.; Bonnevie, T.; Moser, M-B; Moser, EI, Hippocampus-independent phase precession in entorhinal grid cells, Nature, 453, 7199, 1248-1252 (2008) · doi:10.1038/nature06957 |
| [19] | Harris, CR; Millman, KJ; van der Walt, SJ; Gommers, R.; Virtanen, P.; Cournapeau, D.; Wieser, E.; Taylor, J.; Berg, S.; Smith, NJ, Array programming with numpy, Nature, 585, 7825, 357-362 (2020) · doi:10.1038/s41586-020-2649-2 |
| [20] | Harris, KD; Henze, DA; Hirase, H.; Leinekugel, X.; Dragoi, G.; Czurkó, A.; Buzsáki, G., Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells, Nature, 417, 6890, 738-741 (2002) · doi:10.1038/nature00808 |
| [21] | Hunter, JD, Matplotlib: A 2d graphics environment, Computing in science and engineering, 9, 3, 90-95 (2007) · doi:10.1109/MCSE.2007.55 |
| [22] | Jeffery, KJ, Place cells, grid cells, attractors, and remapping, Neural plasticity, 2011, 182602 (2011) · doi:10.1155/2011/182602 |
| [23] | Kamondi, A.; Acsády, L.; Wang, XJ; Buzsáki, G., Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials, Hippocampus, 8, 3, 244-261 (1998) · doi:10.1002/(SICI)1098-1063(1998)8:3<244::AID-HIPO7>3.0.CO;2-J |
| [24] | Kempter, R.; Leibold, C.; Buzsáki, G.; Diba, K.; Schmidt, R., Quantifying circular-linear associations: hippocampal phase precession, Journal of Neuroscience Methods, 207, 1, 113-124 (2012) · doi:10.1016/j.jneumeth.2012.03.007 |
| [25] | Klausberger, T.; Magill, PJ; Márton, LF; Roberts, JDB; Cobden, PM; Buzsáki, G.; Somogyi, P., Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo, Nature, 421, 6925, 844-848 (2003) · doi:10.1038/nature01374 |
| [26] | Lam, S. K., Pitrou, A., & Seibert, S. (2015). Numba: A LLVM-based Python JIT compiler, pp. 1-6. ACM Press. doi:10.1145/2833157.2833162 |
| [27] | Lasztóczi, B.; Klausberger, T., Hippocampal place cells couple to three different gamma oscillations during place field traversal, Neuron, 91, 1, 34-40 (2016) · doi:10.1016/j.neuron.2016.05.036 |
| [28] | Lee, A., Circular data, Wiley Interdisciplinary Reviews: Computational Statistics, 2, 4, 477-486 (2010) · doi:10.1002/wics.98 |
| [29] | Losonczy, A.; Zemelman, BV; Vaziri, A.; Magee, JC, Network mechanisms of theta related neuronal activity in hippocampal ca1 pyramidal neurons, Nature Neuroscience, 13, 8, 967-972 (2010) · doi:10.1038/nn.2597 |
| [30] | Magee, JC, Dendritic mechanisms of phase precession in hippocampal ca1 pyramidal neurons, Journal of Neurophysiology, 86, 1, 528-532 (2001) · doi:10.1152/jn.2001.86.1.528 |
| [31] | Malvache, A.; Reichinnek, S.; Villette, V.; Haimerl, C.; Cossart, R., Awake hippocampal reactivations project onto orthogonal neuronal assemblies, Science, 353, 6305, 1280-1283 (2016) · doi:10.1126/science.aaf3319 |
| [32] | Mardia, J. (1999). Directional Statistics. John Wiley and Sons, Inc. doi:10.1002/9780470316979 · Zbl 0940.62049 |
| [33] | Mardia, KV, Linear-circular correlation coefficients and rhythmometry, Biometrika, 63, 2, 403 (1976) · doi:10.2307/2335637 |
| [34] | 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. doi:10.7554/eLife.71774 |
| [35] | Marshall, L.; Henze, DA; Hirase, H.; Leinekugel, X.; Dragoi, G.; Buzsáki, G., Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge, The Journal of Neuroscience, 22, 2, 197 (2002) · doi:10.1523/JNEUROSCI.22-02-j0001.2002 |
| [36] | Masurkar, AV; Srinivas, KV; Brann, DH; Warren, R.; Lowes, DC; Siegelbaum, SA, Medial and lateral entorhinal cortex differentially excite deep versus superficial ca1 pyramidal neurons, Cell Reports, 18, 1, 148-160 (2017) · doi:10.1016/j.celrep.2016.12.012 |
| [37] | Maurer, AP; Cowen, SL; Burke, SN; Barnes, CA; McNaughton, BL, Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells, The Journal of Neuroscience, 26, 52, 13485-13492 (2006) · doi:10.1523/JNEUROSCI.2882-06.2006 |
| [38] | Mehta, MR; Lee, AK; Wilson, MA, Role of experience and oscillations in transforming a rate code into a temporal code, Nature, 417, 6890, 741-746 (2002) · doi:10.1038/nature00807 |
| [39] | 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. doi:10.12688/f1000research.3895.1 |
| [40] | Mizuseki, K.; Royer, S.; Diba, K.; Buzsáki, G., Activity dynamics and behavioral correlates of ca3 and ca1 hippocampal pyramidal neurons, Hippocampus, 22, 8, 1659-1680 (2012) · doi:10.1002/hipo.22002 |
| [41] | Mizuseki, K.; Sirota, A.; Pastalkova, E.; Buzsáki, G., Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop, Neuron, 64, 2, 267-280 (2009) · doi:10.1016/j.neuron.2009.08.037 |
| [42] | Montgomery, SM; Betancur, MI; Buzsáki, G., Behavior-dependent coordination of multiple theta dipoles in the hippocampus, The Journal of Neuroscience, 29, 5, 1381-1394 (2009) · doi:10.1523/JNEUROSCI.4339-08.2009 |
| [43] | O’Keefe, J.; Burgess, N., Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells, Hippocampus, 15, 7, 853-866 (2005) · doi:10.1002/hipo.20115 |
| [44] | O’Keefe, J.; Recce, ML, Phase relationship between hippocampal place units and the eeg theta rhythm, Hippocampus, 3, 3, 317-330 (1993) · doi:10.1002/hipo.450030307 |
| [45] | Oliva, A.; Fernández-Ruiz, A.; Buzsáki, G.; Berényi, A., Spatial coding and physiological properties of hippocampal neurons in the cornu ammonis subregions, Hippocampus, 26, 12, 1593-1607 (2016) · doi:10.1002/hipo.22659 |
| [46] | Petersen, PC; Hernandez, M.; Buzsáki, G., The buzsaki lab databank - public electrophysiological datasets from awake animals, Zenodo (2020) · doi:10.5281/zenodo.4307883 |
| [47] | Pinsky, PF; Rinzel, J., Intrinsic and network rhythmogenesis in a reduced traub model for ca3 neurons, Journal of computational neuroscience, 1, 1-2, 39-60 (1994) · doi:10.1007/BF00962717 |
| [48] | Quiroga, RQ; Reddy, L.; Kreiman, G.; Koch, C.; Fried, I., Invariant visual representation by single neurons in the human brain, Nature, 435, 7045, 1102-1107 (2005) · doi:10.1038/nature03687 |
| [49] | Royer, S.; Zemelman, BV; Losonczy, A.; Kim, J.; Chance, F.; Magee, JC; Buzsaki, G., Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition, Nature Neuroscience, 15, 5, 769-775 (2012) · doi:10.1038/nn.3077 |
| [50] | Sanchez-Aguilera, A., Wheeler, D. W., Jurado-Parras, T., Valero, M., Nokia, M. S., Cid, E., Fernandez-Lamo, I., Sutton, N., García-Rincón, D., dela Prida, L. M., et al. (2021). An update to hippocampome.org by integrating single-cell phenotypes with circuit function in vivo. PLoS Biology, 19(5), 3001213. doi:10.1371/journal.pbio.3001213 |
| [51] | Somogyi, P.; Klausberger, T., Defined types of cortical interneurone structure space and spike timing in the hippocampus, The Journal of Physiology, 562, Pt 1, 9-26 (2005) · doi:10.1113/jphysiol.2004.078915 |
| [52] | Somogyi, P., Katona, L., Klausberger, T., Lasztóczi, B., & Viney, T. J. (2014). Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 369(1635), 20120518. doi:10.1098/rstb.2012.0518 |
| [53] | Storn, R.; Price, K., Differential evolution - asimple and efficient heuristic for global optimization over continuous spaces, Springer Science and Business Media LLC (1997) · Zbl 0888.90135 · doi:10.1023/a:1008202821328 |
| [54] | Sugar, J.; Moser, M-B, Episodic memory: Neuronal codes for what, where, and when, Hippocampus, 29, 12, 1190-1205 (2019) · doi:10.1002/hipo.23132 |
| [55] | Thurley, K.; Leibold, C.; Gundlfinger, A.; Schmitz, D.; Kempter, R., Phase precession through synaptic facilitation, Neural Computation, 20, 5, 1285-1324 (2008) · Zbl 1138.92310 · doi:10.1162/neco.2008.07-06-292 |
| [56] | Traub, RD; Wong, RK; Miles, R.; Michelson, H., A model of a ca3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances, Journal of Neurophysiology, 66, 2, 635-650 (1991) · doi:10.1152/jn.1991.66.2.635 |
| [57] | Valero, M.; Navas-Olive, A.; de la Prida, LM; Buzsáki, G., Inhibitory conductance controls place field dynamics in the hippocampus, Cell reports, 40, 8, 111232 (2022) · doi:10.1016/j.celrep.2022.111232 |
| [58] | Valero, M., Zutshi, I., Yoon, E., & Buzsáki, G. (2022). Probing subthreshold dynamics of hippocampal neurons by pulsed optogenetics. Science (New York, N.Y.), 375(6580), 570-574. doi:10.1126/science.abm1891 |
| [59] | Varga, C.; Golshani, P.; Soltesz, I., Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice, Proceedings of the National Academy of Sciences of the United States of America, 109, 40, 2726-34 (2012) · doi:10.1073/pnas.1210929109 |
| [60] | Vinogradova, OS, Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information, Hippocampus, 11, 5, 578-598 (2001) · doi:10.1002/hipo.1073 |
| [61] | Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., et al. (2020). Author correction: Scipy 1.0: fundamental algorithms for scientific computing in python. Nature Methods, 17(3), 352. doi:10.1038/s41592-020-0772-5 |
| [62] | Wallenstein, GV; Hasselmo, ME, Gabaergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect, Journal of Neurophysiology, 78, 1, 393-408 (1997) · doi:10.1152/jn.1997.78.1.393 |
| [63] | Wheeler, D. W., White, C. M., Rees, C. L., Komendantov, A. O., Hamilton, D. J., & Ascoli, G. A. (2015). Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus. eLife, 4. doi:10.7554/eLife.09960 |
| [64] | Wilson, MA; McNaughton, BL, Dynamics of the hippocampal ensemble code for space, Science, 261, 5124, 1055-1058 (1993) · doi:10.1126/science.8351520 |
| [65] | Wormington, M., Panaccione, C., Matney, K. M., & Bowen, D. K. (1999). Characterization of structures from x-ray scattering data using genetic algorithms. Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, 357(1761), 2827-2848. doi:10.1098/rsta.1999.0469 |
| [66] | Zutshi, I.; Valero, M.; Fernández-Ruiz, A.; Buzsáki, G., Extrinsic control and intrinsic computation in the hippocampal ca1 circuit, Neuron, 110, 4, 658-6735 (2022) · doi:10.1016/j.neuron.2021.11.015 |
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.
