Representation of spatial information in the CA1 field
- Authors: Mysin I.E.1, Vasilev A.O.1, Dubrovin S.V.2, Skorokhod S.N.3
-
Affiliations:
- Institute of Theoretical and Experimental Biophysics oof the Russian Academy of Sciences
- Ufa University of Science and Technology
- Peter the Great St. Petersburg Polytechnic University University
- Issue: Vol 74, No 5 (2024)
- Pages: 517-537
- Section: ОБЗОРЫ И ТЕОРЕТИЧЕСКИЕ СТАТЬИ
- URL: https://cardiosomatics.orscience.ru/0044-4677/article/view/652069
- DOI: https://doi.org/10.31857/S0044467724050019
- ID: 652069
Cite item
Abstract
Information in the brain is encoded by large populations of neurons – neural ensembles. The place cells in the hippocampal CA1 field have become an experimental model for the study of neural ensembles of the brain due to the convenience of research. This review is devoted to the latest studies of place cells in the CA1 field. We consider the principles of encoding space by place cells, mechanisms for controlling the activity of place cells, anatomical and physiological features of place cells in different parts of the CA1 field. Key points: 1. There are rate and phase coding; 2. Dense local connections between pyramidal neurons can provide information processing; 3. Interneurons are involved in the formation of both the rate and phase code of place cells; 4. Pyramidal neurons are anatomically and functionally divided into deep and superficial; 5. Along the dorsoventral axis, the spatial and non-spatial component of information is generalized. The CA1 field has extensive capabilities for signal processing and can implement a computationally complex operation in the cognitive processes of the brain.
Full Text

About the authors
I. E. Mysin
Institute of Theoretical and Experimental Biophysics oof the Russian Academy of Sciences
Author for correspondence.
Email: imysin@mail.ru
Laboratory of the Systemic Organization of Neurons
Russian Federation, PushchinoA. O. Vasilev
Institute of Theoretical and Experimental Biophysics oof the Russian Academy of Sciences
Email: imysin@mail.ru
Laboratory of the Systemic Organization of Neurons
Russian Federation, PushchinoS. V. Dubrovin
Ufa University of Science and Technology
Email: imysin@mail.ru
Russian Federation, Ufa
S. N. Skorokhod
Peter the Great St. Petersburg Polytechnic University University
Email: imysin@mail.ru
Russian Federation, St. Petersburg
References
- Казанович Я.Б., Мысин И.Е. Как животные ориентируются в пространстве? Клетки места и клетки решетки. Математическая биология и биоинформатика. 2015. 10(1): 88–115.
- Мысин И.Е. Механизмы типпокампального тета-ритма. Журн. высш. нервн. деят. им. И.П. Павлова. 2020. 70 (3): 291–-313.
- Alexander A.S., Carstensen L.C., Hinman J.R., Raudies F., Chapman G.W., Hasselmo M.E. Egocentric boundary vector tuning of the retrosplenial cortex. Sci. Adv. 2020. 6 (8).
- Arriaga M., Han E.B. Structured inhibitory activity dynamics in new virtual environments. eLife / ed. Scharfman H., Colgin L.L., Fenton A.A. eLife. 2019. 8.
- Attili S.M., Moradi K., Wheeler D.W., Ascoli G.A. Quantification of neuron types in the rodent hippocampal formation by data mining and numerical optimization. Eur. J. Neurosci. 2022. 55 (7): 1724–1741.
- Barrientos S.A., Tiznado V. Hippocampal CA1 Subregion as a Context Decoder. J. Neurosci. 2016. 36(25): 6602–6604.
- Belluscio M.A., Mizuseki K., Schmidt R., Kempter R., Buzsáki G. Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus. J. Neurosci. 2012. 32 (2): 423–435.
- Berndt M., Trusel M., Roberts T.F., Pfeiffer B.E., Volk L.J. Bidirectional synaptic changes in deep and superficial hippocampal neurons following in vivo activity. Neuron. 2023. 111 (19): 2984-2994.e4.
- Bezaire M.J., Soltesz I. Quantitative assessment of CA1 local circuits: Knowledge base for interneuron-pyramidal cell connectivity. Hippocampus. 2013. 23 (9): 751–785.
- Bi G., Poo M. Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type. J. Neurosci. 1998. 18 (24): 10464–10472.
- Both M., Bähner F., von Bohlen und Halbach O., Draguhn A. Propagation of specific network patterns through the mouse hippocampus. Hippocampus. 2008. 18 (9): 899–908.
- Brandon M.P., Bogaard A.R., Libby C.P., Connerney M.A., Gupta K., Hasselmo M.E. Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning. Science. 2011. 332 (6029): 595–599.
- Brun V.H., Solstad T., Kjelstrup K.B., Fyhn M., Witter M.P., Moser E.I., Moser M.B. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus. 2008. 18 (12): 1200–1212.
- Buckner R.L., Carroll D.C. Self-projection and the brain. Trends Cogn. Sci. 2007. 11 (2): 49–57.
- Burak Y. Spatial coding and attractor dynamics of grid cells in the entorhinal cortex. Curr. Opin. Neurobiol. 2014. 25: 169–175.
- Burgess N., O’Keefe J. Models of place and grid cell firing and theta rhythmicity. Curr. Opin. Neurobiol. 2011. 21 (5): 734–744.
- Buzsáki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986. 398 (2): 242–252.
- Buzsáki G. Theta Oscillations in the Hippocampus. Neuron. 2002. 33 (3): 325–340.
- Buzsáki G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning: hippocampal sharp wave-ripple. Hippocampus. 2015. 25 (10): 1073–1188.
- Buzsáki G., Moser E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 2013. 16 (2): 130–138.
- Buzsáki G., Wang X.J. Mechanisms of Gamma Oscillations. Annu. Rev. Neurosci. 2012. 35 (1): 203–225.
- Carr M.F., Karlsson M.P., Frank L.M. Transient Slow Gamma Synchrony Underlies Hippocampal Memory Replay. Neuron. 2012. 75 (4): 700–713.
- Cenquizca L.A., Swanson L.W. Spatial Organization of Direct Hippocampal Field CA1 Axonal Projections To the Rest of the Cerebral Cortex. Brain Res. Rev. 2007. 56 (1): 1–26.
- Chen L., Lin X., Ye Q., Nenadic Z., Holmes T.C., Nitz D.A., Xu X. Anatomical organization of temporally correlated neural calcium activity in the hippocampal CA1 region. iScience. 2023. 26 (5): 106703.
- Colgin L.L. Mechanisms and Functions of Theta Rhythms. Annu. Rev. Neurosci. 2013. 36 (1): 295–312.
- Colgin L.L. Theta–gamma coupling in the entorhinal–hippocampal system. Curr. Opin. Neurobiol. 2015. 31: 45–50.
- Colgin L.L. Rhythms of the hippocampal network. Nat. Rev. Neurosci. 2016. 17(4): 239–249.
- Contreras M., Pelc T., Llofriu M., Weitzenfeld A., Fellous J.M. The ventral hippocampus is involved in multi-goal obstacle-rich spatial navigation. Hippocampus. 2018. 28 (12): 853–866.
- Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat. Neuron. 2003. 37(2): 311–322.
- Cutsuridis V., Hasselmo M. GABAergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations. Hippocampus. 2012. 22 (7): 1597–1621.
- Diehl G.W., Hon O.J., Leutgeb S., Leutgeb J.K. Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes. Neuron. 2017. 94 (1): 83–92.e6.
- Dombeck D.A., Harvey C.D., Tian L., Looger L.L., Tank D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 2010. 13 (11): 1433–1440.
- Dudok B., Szoboszlay M., Paul A., Klein P.M., Liao Z., Hwaun E., Szabo G.G., Geiller T., Vancura B., Wang B.S., McKenzie S., Homidan J., Klaver L.M.F., English D.F., Huang Z.J., Buzsáki G., Losonczy A., Soltesz I. Recruitment and inhibitory action of hippocampal axo-axonic cells during behavior. Neuron. 2021. 109 (23): 3838–3850.
- Duvelle É., Grieves R.M., Hok V., Poucet B., Arleo A., Jeffery K.J., Save E. Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task. J. Neurosci. 2019. 39 (13): 2522–2541.
- Ego‐Stengel V., Wilson M.A. Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus. 2007. 17 (2): 161–174.
- Eichenbaum H. Time cells in the hippocampus: a new dimension for mapping memories. Nat. Rev. Neurosci. 2014. 15 (11): 732–744.
- English D.F., McKenzie S., Evans T., Kim K., Yoon E., Buzsáki G. Pyramidal cell-interneuron circuit architecture and dynamics in hippocampal networks. Neuron. 2017. 96 (2): 505-520.
- Euston D.R., Tatsuno M., McNaughton B.L. Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep. Science. 2007. 318 (5853): 1147–1150.
- Fanselow M.S., Dong H.W. Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?. Neuron. 2010. 65 (1): 7–19.
- Fernández-Ruiz A., Oliva A., Nagy G.A., Maurer A.P., Berényi A., Buzsáki G. Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling. Neuron. 2017. 93 (5): 1213–1226.e5.
- Forro T., Valenti O., Lasztoczi B., Klausberger T. Temporal Organization of GABAergic Interneurons in the Intermediate CA1 Hippocampus During Network Oscillations. Cereb. Cortex. 2015. 25 (5): 1228–1240.
- Frank L.M., Stanley G.B., Brown E.N. Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments. J. Neurosci. 2004. 24 (35): 7681–7689.
- Geiller T., Fattahi M., Choi J.S., Royer S. Place cells are more strongly tied to landmarks in deep than in superficial CA1. Nat. Commun. 2017. 8: 14531.
- Geiller T., Royer S., Choi J.S. Segregated Cell Populations Enable Distinct Parallel Encoding within the Radial Axis of the CA1 Pyramidal Layer. Exp. Neurobiol. 2017. 26 (1): 1–10.
- Geiller T., Sadeh S., Rolotti S.V., Blockus H., Vancura B., Negrean A., Murray A.J., Rózsa B., Polleux F., Clopath C., Losonczy A. Local circuit amplification of spatial selectivity in the hippocampus. Nature. 2022. 601 (7891): 105–109.
- Geiller T., Vancura B., Terada S., Troullinou E., Chavlis S., Tsagkatakis G., Tsakalides P., Ócsai K., Poirazi P., Rózsa B.J., Losonczy A. Large-Scale 3D Two-Photon Imaging of Molecularly Identified CA1 Interneuron Dynamics in Behaving Mice. Neuron. 2020. 108 (5): 968–983.e9.
- Girardeau G., Benchenane K., Wiener S.I., Buzsáki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009. 12 (10): 1222–1223.
- Grienberger C., Milstein A.D., Bittner K.C., Romani S., Magee J.C. Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells. Nat. Neurosci. 2017. 20 (33): 417–426.
- Guan H., Middleton S.J., Inoue T., McHugh T.J. Lateralization of CA1 assemblies in the absence of CA3 input. Nat. Commun. 2021. 12 (1): 6114.
- Guardamagna M., Stella F., Battaglia F.P. Heterogeneity of network and coding states in mouse CA1 place cells. Cell Rep. 2023. 42(2).
- Hangya B., Li Y., Muller R.U., Czurkó A. Complementary spatial firing in place cell–interneuron pairs. J. Physiol. 2010. 588(Pt 21): 4165–4175.
- Harris K.D., Csicsvari J., Hirase H., Dragoi G., Buzsáki G. Organization of cell assemblies in the hippocampus. Nature. 2003. 424 (6948): 552–556.
- Harvey C.D., Collman F., Dombeck D.A., Tank D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature. 2009. 461 (7266): 941–946.
- Hasselmo M.E., Brandon M.P. A Model Combining Oscillations and Attractor Dynamics for Generation of Grid Cell Firing. Front. Neural Circuits. 2012. 6.
- Hernández-Pérez J.J., Cooper K.W., Newman E.L. Medial entorhinal cortex activates in a traveling wave in the rat. eLife. 2020. 9: e52289.
- Heys J.G., Rangarajan K.V., Dombeck D.A. The Functional Micro-organization of Grid Cells Revealed by Cellular-Resolution Imaging. Neuron. 2014. 84(5): 1079–1090.
- Hinman J.R., Chapman G.W., Hasselmo M.E. Neuronal representation of environmental boundaries in egocentric coordinates. Nat. Commun. 2019. 10: 2772.
- Huxter J., Burgess N., O’Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature. 2003. 425(69606960): 828–832.
- Ibbotson M., Jung Y.J. Origins of Functional Organization in the Visual Cortex. Front. Syst. Neurosci. 2020. 14: 10.
- Issa J.B., Radvansky B.A., Xuan F., Dombeck D.A. Lateral entorhinal cortex subpopulations represent experiential epochs surrounding reward. Nat. Neurosci. 2024. 27(3): 536–546.
- Jarzebowski P., Hay Y.A., Grewe B.F., Paulsen O. Different encoding of reward location in dorsal and intermediate hippocampus. Curr. Biol. 2022. 32(4): 834-841.e5.
- Jeffery K.J. Place cells, grid cells, attractors, and remapping. Neural Plast. 2011. 2011: 182602.
- Jin S.W., Lee I. Differential encoding of place value between the dorsal and intermediate hippocampus. Curr. Biol. 2021. 31(14): 3053–3072.e5.
- Jones B.F., Witter M.P. Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus. 2007. 17(10): 957–976.
- Kamondi A., Acsády L., Wang X.J., Buzsáki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity-dependent phase-precession of action potentials. Hippocampus. 1998. 8(3): 244–261.
- Kazanovich Y., Mysin I.E. How Animals Find Their Way in Space. Experiments and Modeling. Math. Biol. Bioinforma. 2018. 13: 29.
- Keinath A.T., Wang M.E., Wann E.G., Yuan R.K., Dudman J.T., Muzzio I.A. Precise spatial coding is preserved along the longitudinal hippocampal axis. Hippocampus. 2014. 24(12): 1533–1548.
- Kesner R.P., Rolls E.T. A computational theory of hippocampal function, and tests of the theory: New developments. Neurosci. Biobehav. Rev. 2015. 48: 92–147.
- Kjelstrup K.B., Solstad T., Brun V.H., Hafting T., Leutgeb S., Witter M.P., Moser E.I., Moser M.B. Finite Scale of Spatial Representation in the Hippocampus. Science. 2008. 321(5885): 140–143.
- Klausberger T., Magill P.J., Márton L.F., Roberts J.D.B., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature. 2003. 421(6925): 844–848.
- Kohara K., Pignatelli M., Rivest A.J., Jung H.Y., Kitamura T., Suh J., Frank D., Kajikawa K., Mise N., Obata Y., Wickersham I.R., Tonegawa S. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat. Neurosci. 2014. 17(2): 269–279.
- Korotkova T., Fuchs E.C., Ponomarenko A., von Engelhardt J., Monyer H. NMDA Receptor Ablation on Parvalbumin-positive Interneurons Impairs Hippocampal Synchrony, Spatial Representations, and Working Memory. Neuron. 2010. 68(3): 557–569.
- Kwon O., Feng L., Druckmann S., Kim J. Schaffer Collateral Inputs to CA1 Excitatory and Inhibitory Neurons Follow Different Connectivity Rules. J. Neurosci. Off. J. Soc. Neurosci. 2018. 38 (22): 5140–5152.
- LaChance P.A., Todd T.P., Taube J.S. A Sense of Space in Postrhinal Cortex. Nat.Science. 2019. 365 (6449).
- Lasztóczi B., Klausberger T. Hippocampal Place Cells Couple to Three Different Gamma Oscillations during Place Field Traversal. Neuron. 2016. 91 (1): 34–40.
- Lee S.H., Marchionni I., Bezaire M., Varga C., Danielson N., Lovett-Barron M., Losonczy A., Soltesz I. Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells. Neuron. 2014. 82 (5): 1129–1144.
- Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus. Science. 2007. 315 (5814): 961–966.
- Li Y., Xu J., Liu Y., Zhu J., Liu N., Zeng W., Huang N., Rasch M.J., Jiang H., Gu X., Li X., Luo M., Li C., Teng J., Chen J., Zeng S., Lin L., Zhang X. A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning. Nat. Neurosci. 2017. 20 (4): 559–570.
- Long L.L., Bunce J.G., Chrobak J.J. Theta variation and spatiotemporal scaling along the septotemporal axis of the hippocampus. Front. Syst. Neurosci. 2015. 9.
- Loureiro M., Lecourtier L., Engeln M., Lopez J., Cosquer B., Geiger K., Kelche C., Cassel J.C., Pereira de Vasconcelos A. The ventral hippocampus is necessary for expressing a spatial memory. Brain Struct. Funct. 2012. 217 (1): 93–106.
- Lubenov E.V., Siapas A.G. Hippocampal theta oscillations are travelling waves. Nature. 2009. 459(7246): 534–539.
- Lyttle D., Gereke B., Lin K.K., Fellous J.M. Spatial scale and place field stability in a grid-to-place cell model of the dorsoventral axis of the hippocampus. Hippocampus. 2013. 23 (8): 729–744.
- Magee J.C. Dendritic Mechanisms of Phase Precession in Hippocampal CA1 Pyramidal Neurons. J. Neurophysiol. American Physiological Society. 2001. 86(1): 528–532.
- Maingret N., Girardeau G., Todorova R., Goutierre M., Zugaro M. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat. Neurosci. 2016. 19 (77): 959–964.
- Malhotra S., Cross R.W.A., Van Der Meer M.A.A. Theta phase precession beyond the hippocampus. Rev. Neurosci. 2012. 23(1).
- Malvache A., Reichinnek S., Villette V., Haimerl C., Cossart R. Awake hippocampal reactivations project onto orthogonal neuronal assemblies. Science. 2016. 353 (6305): 1280–1283.
- Manns J.R., Zilli E.A., Ong K.C., Hasselmo M.E., Eichenbaum H. Hippocampal CA1 spiking during encoding and retrieval: Relation to theta phase. Neurobiol. Learn. Mem. 2007. 87 (1): 9–20.
- Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1971. 262 (841): 23–81.
- Masurkar A.V., Srinivas K.V., Brann D.H., Warren R., Lowes D.C., Siegelbaum S.A. Medial and Lateral Entorhinal Cortex Differentially Excite Deep versus Superficial CA1 Pyramidal Neurons. Cell Rep. 2017. 18 (1): 148–160.
- Masurkar A.V., Tian C., Warren R., Reyes I., Lowes D.C., Brann D.H., Siegelbaum S.A. Postsynaptic integrative properties of dorsal CA1 pyramidal neuron subpopulations. J. Neurophysiol. 2020. 123(3): 980–992.
- Maurer A.P., Vanrhoads S.R., Sutherland G.R., Lipa P., McNaughton B.L. Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus. 2005. 15 (7): 841–852.
- Meer M.A.A., Redish A.D. Theta Phase Precession in Rat Ventral Striatum Links Place and Reward Information. J. Neurosci. 2011. 31 (8): 2843–2854.
- Mehta M.R., Barnes C.A., McNaughton B.L. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc. Natl. Acad. Sci. U. S. A. 1997. 94 (16): 8918–8921.
- Mehta M.R., Quirk M.C., Wilson M.A. Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields. Neuron. 2000. 25 (3): 707–715.
- Middleton S.J., McHugh T.J. Silencing CA3 disrupts temporal coding in the CA1 ensemble. Nat. Neurosci. 2016. 19 (7): 945–951.
- Mizuseki K., Diba K., Pastalkova E., Buzsáki G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 2011. 14 (9): 1174–1181.
- Mizuseki K., Diba K., Pastalkova E., Teeters J., Sirota A., Buzsáki G. Neurosharing: large-scale data sets (spike, LFP) recorded from the hippocampal-entorhinal system in behaving rats. 2014. 3.
- Mizuseki K., Royer S., Diba K., Buzsáki G. Activity Dynamics and Behavioral Correlates of CA3 and CA1 Hippocampal Pyramidal Neurons. Hippocampus. 2012. 22 (8): 1659–1680.
- Mizuseki K., Sirota A., Pastalkova E., Buzsáki G. Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop. Neuron. 2009. 64 (2): 267–280.
- Moser M.B., Rowland D.C., Moser E.I. Place Cells, Grid Cells, and Memory. Cold Spring Harb. Perspect. Biol. 2015. 7(2).
- Murray A.J., Sauer J.F., Riedel G., McClure C., Ansel L., Cheyne L., Bartos M., Wisden W., Wulff P. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nat. Neurosci. 2011. 14 (3): 297–299.
- Mysin I., Shubina L. From mechanisms to functions: The role of theta and gamma coherence in the intrahippocampal circuits. Hippocampus. 2022. 32 (5): 342–358.
- Mysin I., Shubina L. Hippocampal non-theta state: The “Janus face” of information processing. Front. Neural Circuits. 2023. 17.
- Nasrallah K., Therreau L., Robert V., Huang A.J.Y., McHugh T.J., Piskorowski R.A., Chevaleyre V. Routing Hippocampal Information Flow through Parvalbumin Interneuron Plasticity in Area CA2. Cell Rep. 2019. 27 (1): 86-98.
- Navas-Olive A., Valero M., Jurado-Parras T., de Salas-Quiroga A., Averkin R.G., Gambino G., Cid E., de la Prida L.M. Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations. Nat. Commun. 2020. 11.
- Newman E.L., Climer J.R., Hasselmo M.E. Grid cell spatial tuning reduced following systemic muscarinic receptor blockade. Hippocampus. 2014. 24 (6): 643–655.
- Numan R. A Prefrontal-Hippocampal Comparator for Goal-Directed Behavior: The Intentional Self and Episodic Memory. Front. Behav. Neurosci. 2015. 9.
- O’Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993. 3 (3): 317–330.
- Oliva A., Fernández-Ruiz A., Buzsáki G., Berényi A. Spatial coding and physiological properties of hippocampal neurons in the Cornu Ammonis subregions. Hippocampus. 2016. 26 (12): 1593–1607.
- O’Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J. Anat. 2005. 207 (3): 271–282.
- Patel J., Fujisawa S., Berényi A., Royer S., Buzsáki G. Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus. Neuron. 2012. 75 (3): 410–417.
- Pavlides C., Donishi T., Ribeiro S., Mello C.V., Blanco W., Ogawa S. Hippocampal functional organization: A microstructure of the place cell network encoding space. Neurobiol. Learn. Mem. 2019. 161: 122–134.
- Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 2009. 12 (7): 919–926.
- Pfeiffer B.E. The content of hippocampal “replay”. Hippocampus. 2020. 30(1): 6–18.
- Pfeiffer B.E., Foster D.J. Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science. 2015. 349 (6244): 180–183.
- del Pino I., Brotons-Mas J.R., Marques-Smith A., Marighetto A., Frick A., Marín O., Rico B. Abnormal wiring of CCK+ basket cells disrupts spatial information coding. Nat. Neurosci. 2017. 20(66): 784–792.
- Poucet B., Thinus-Blanc C., Muller R.U. Place cells in the ventral hippocampus of rats. Neuroreport. 1994. 5(16): 2045–2048.
- Poulter S., Hartley T., Lever C. The Neurobiology of Mammalian Navigation. Curr. Biol. 2018. 28(17): R1023–R1042.
- Quiroga R.Q., Reddy L., Kreiman G., Koch C., Fried I. Invariant visual representation by single neurons in the human brain. Nature. 2005. 435(7045): 1102–1107.
- Rolls E. The mechanisms for pattern completion and pattern separation in the hippocampus. Front. Syst. Neurosci. Frontiers. 2013. 7.
- Royer S., Sirota A., Patel J., Buzsáki G. Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus. J. Neurosci. Society for Neuroscience. 2010. 30 (5): 1777–1787.
- Royer S., Zemelman B.V., Losonczy A., Kim J., Chance F., Magee J.C., Buzsáki G. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 2012. 15(5): 769–775.
- Sanders H., Rennó-Costa C., Idiart M., Lisman J. Grid Cells and Place Cells: An Integrated View of their Navigational and Memory Function. Trends Neurosci. 2015. 38 (12): 763–775.
- Schlesiger M.I., Boublil B.L., Hales J.B., Leutgeb J.K., Leutgeb S. Hippocampal Global Remapping Can Occur without Input from the Medial Entorhinal Cortex. Cell Rep. 2018. 22 (12): 3152–3159.
- Schomburg E.W., Fernández-Ruiz A., Mizuseki K., Berényi A., Anastassiou C.A., Koch C., Buzsáki G. Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks. Neuron. 2014. 84 (2): 470–485.
- Scleidorovich P., Llofriu M., Fellous J.M., Weitzenfeld A. A computational model for spatial cognition combining dorsal and ventral hippocampal place field maps: multiscale navigation. Biol. Cybern. 2020. 114 (2): 187–207.
- Sharif F., Tayebi B., Buzsáki G., Royer S., Fernandez-Ruiz A. Subcircuits of Deep and Superficial CA1 Place Cells Support Efficient Spatial Coding across Heterogeneous Environments. Neuron. 2021. 109 (2): 363–376.
- Shpokayte M., McKissick O., Guan X., Yuan B., Rahsepar B., Fernandez F.R., Ruesch E., Grella S.L., White J.A., Liu X.S., Ramirez S. Hippocampal cells segregate positive and negative engrams. Commun. Biol. 2022. 5 (1): 1–15.
- Si B., Romani S., Tsodyks M. Continuous Attractor Network Model for Conjunctive Position-by-Velocity Tuning of Grid Cells. PLoS Comput. Biol. 2014. 10 (4).
- Sirota A., Csicsvari J., Buhl D., Buzsáki G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U. S. A. 2003. 100 (4): 2065–2069.
- Skelin I., Zhang H., Zheng J., Ma S., Mander B.A., Kim McManus O., Vadera S., Knight R.T., McNaughton B.L., Lin J.J. Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans. Proc. Natl. Acad. Sci. 2021. 118 (21): e2012075118.
- Soltesz I., Losonczy A. CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus. Nat. Neurosci. 2018. 21 (4): 484–493.
- Somogyi P., Katona L., Klausberger T., Lasztóczi B., Viney T.J. Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus. Phil Trans R Soc B. 2014. 369 (1635): 20120518.
- Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008. 9 (3): 206–221.
- Strange B.A., Witter M.P., Lein E.S., Moser E.I. Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 2014. 15 (10): 655–669.
- Sugar J., Moser M.B. Episodic memory: Neuronal codes for what, where, and when. Hippocampus. 2019. 29 (12): 1190–1205.
- Tingley D., Buzsáki G. Transformation of a Spatial Map across the Hippocampal-Lateral Septal Circuit. Neuron. 2018. 98 (6): 1229–1242.e5.
- Todorova R., Zugaro M. Hippocampal ripples as a mode of communication with cortical and subcortical areas. Hippocampus. 2020. 30 (1): 39–49.
- Tsao A., Moser M.B., Moser E.I. Traces of Experience in the Lateral Entorhinal Cortex. Curr. Biol. Elsevier. 2013. 23(5): 399–405.
- 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. Vasoactive Intestinal Polypeptide-Expressing Interneurons in the Hippocampus Support Goal-Oriented Spatial Learning. Neuron. 2019. 101 (6): 1150–1165.
- Valero M., Cid E., Averkin R.G., Aguilar J., Sanchez-Aguilera A., Viney T.J., Gomez-Dominguez D., Bellistri E., de la Prida L.M. Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples. Nat. Neurosci. 2015. 18 (9): 1281–1290.
- Valero M., de la Prida L.M. The hippocampus in depth: a sublayer-specific perspective of entorhinal-hippocampal function. Curr. Opin. Neurobiol. 2018. 52: 107–114.
- Valero M., Zutshi I., Yoon E., Buzsáki G. Probing subthreshold dynamics of hippocampal neurons by pulsed optogenetics. Science. 2022. 375 (6580): 570–574.
- Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 1969. 26 (4): 407–418.
- Vandyshev G., Mysin I. Homogeneous inhibition is optimal for the phase precession of place cells in the CA1 field. J. Comput. Neurosci. 2023. 51: 389–403.
- Vinogradova O. Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus. 2001. 11 (5): 578–598.
- Wang C., Chen X., Lee H., Deshmukh S.S., Yoganarasimha D., Savelli F., Knierim J.J. Egocentric Coding of External Items in the Lateral Entorhinal Cortex. Science. 2018. 362 (6417): 945–949.
- Wilber A.A., Clark B.J., Forster T.C., Tatsuno M., McNaughton B.L. Interaction of Egocentric and World-Centered Reference Frames in the Rat Posterior Parietal Cortex. J. Neurosci. 2014. 34 (16): 5431–5446.
- Wills T.J., Cacucci F. The development of the hippocampal neural representation of space. Curr. Opin. Neurobiol. 2014. 24: 111–119.
- Willshaw D.J., Buckingham J.T. An assessment of Marr’s theory of the hippocampus as a temporary memory store. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1990. 329(1253): 205–215.
- Wilson M., McNaughton B. Dynamics of the hippocampal ensemble code for space. Science. 1993. 261 (5124): 1055–1058.
- Witter M.P., Doan T.P., Jacobsen B., Nilssen E.S., Ohara S. Architecture of the Entorhinal Cortex A Review of Entorhinal Anatomy in Rodents with Some Comparative Notes. Front. Syst. Neurosci. 2017. 11.
- Witter M.P., Wouterlood F.G., Naber P.A., Van Haeften T. Anatomical Organization of the Parahippocampal-Hippocampal Network. Ann. N. Y. Acad. Sci. 2006. 911 (1): 1–24.
- Wu C.T., Haggerty D., Kemere C., Ji D. Hippocampal awake replay in fear memory retrieval. Nat. Neurosci. 2017. 20 (4): 571–580.
- Yang X., Wan R., Liu Z., Feng S., Yang J., Jing N., Tang K. The differentiation and integration of the hippocampal dorsoventral axis are controlled by two nuclear receptor genes. eLife. 2023. 12: RP86940.
- Young C.K., McNaughton N. Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb. Cortex N. Y. 2009. 19 (1): 24–40.
- Zhang H., Jacobs J. Traveling Theta Waves in the Human Hippocampus. J. Neurosci. 2015. 35 (36): 12477–12487.
- Zhang X., Cao Q., Gao K., Chen C., Cheng S., Li A., Zhou Y., Liu R., Hao J., Kropff E., Miao C. Multiplexed representation of others in the hippocampal CA1 subfield of female mice. Nat. Commun. 2024. 15: 3702.
- Zutshi I., Valero M., Fernández-Ruiz A., Buzsáki G. Extrinsic control and intrinsic computation in the hippocampal CA1 circuit. Neuron. 2022. 110 (4): 658–673.e5.
Supplementary files
