Cognitive maps were originally proposed as internal representations of spatial environments that enable flexible navigation and adaptive behaviour beyond rigid stimulus-response associations. Since Tolman’s seminal formulation, the concept has expanded dramatically to encompass temporal sequences, conceptual knowledge, social hierarchies, and abstract relational structures. This expansion has generated substantial theoretical and empirical progress, yet it has also produced considerable conceptual ambiguity: what, precisely, qualifies a representation as a cognitive map rather than a simpler associative, schematic, or statistical structure? In this critical narrative review we examine the historical evolution of the cognitive-map construct, its proposed neural substrates (with particular emphasis on the hippocampal-entorhinal system), and the methodological approaches used to identify cognitive maps and to reconstruct their structure from behavioural, computational, and neural data. Here, ‘construction’ refers to the researcher’s methodological reconstruction of putative map-like structure from empirical data, as distinct from the organism’s own process of learning such a representation (the latter is addressed separately in Chapter 5). These approaches target relational structure, metric or topological organisation, generalisation, flexible inference, and navigation through representational space, and are contrasted with alternative frameworks that emphasise memory, prediction, or hierarchical coding. Behavioural paradigms, computational models, multivariate neuroimaging analyses, and high-resolution anatomical approaches are compared with respect to their ability to operationalise map-like representations. Building on this synthesis, we propose a framework that distinguishes the content of a map from the computational and neural mechanisms that encode it, and we discuss how multimodal integration of functional, structural, and microstructural data may refine future investigations. The review concludes by outlining principles for the empirical identification of cognitive maps and by highlighting unresolved tensions between spatial origins and domain-general claims.
References
[1]
Tolman, E.C. (1948) Cognitive Maps in Rats and Men. PsychologicalReview, 55, 189-208. https://doi.org/10.1037/h0061626
[2]
O’Keefe, J. and Dostrovsky, J. (1971) The Hippocampus as a Spatial Map. Preliminary Evidence from Unit Activity in the Freely-Moving Rat. BrainResearch, 34, 171-175. https://doi.org/10.1016/0006-8993(71)90358-1
[3]
O’Keefe, J. and Nadel, L. (1978) The Hippocampus as a Cognitive Map. Clarendon Press. https://books.google.pt/books/about/The_Hippocampus_as_a_Cognitive_Map.html?id=trR-AAAAIAAJ&redir_esc=y
[4]
Hafting, T., Fyhn, M., Molden, S., Moser, M. and Moser, E.I. (2005) Microstructure of a Spatial Map in the Entorhinal Cortex. Nature, 436, 801-806. https://doi.org/10.1038/nature03721
[5]
Moser, E.I., Kropff, E. and Moser, M. (2008) Place Cells, Grid Cells, and the Brain’s Spatial Representation System. AnnualReviewofNeuroscience, 31, 69-89. https://doi.org/10.1146/annurev.neuro.31.061307.090723
[6]
Constantinescu, A.O., O’Reilly, J.X. and Behrens, T.E.J. (2016) Organizing Conceptual Knowledge in Humans with a Gridlike Code. Science, 352, 1464-1468. https://doi.org/10.1126/science.aaf0941
[7]
Garvert, M.M., Dolan, R.J. and Behrens, T.E.J. (2017) A Map of Abstract Relational Knowledge in the Human Hippocampal-Entorhinal Cortex. eLife, 6, e17086.
[8]
Behrens, T.E.J., Muller, T.H., Whittington, J.C.R., Mark, S., Baram, A.B., Stachenfeld, K.L., et al. (2018) What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior. Neuron, 100, 490-509. https://doi.org/10.1016/j.neuron.2018.10.002
[9]
Bellmund, J.L.S., G?rdenfors, P., Moser, E.I. and Doeller, C.F. (2018) Navigating Cognition: Spatial Codes for Human Thinking. Science, 362, eaat6766. https://doi.org/10.1126/science.aat6766
[10]
Eichenbaum, H. (2017) The Role of the Hippocampus in Navigation Is Memory. Journal of Neurophysiology, 117, 1785-1796. https://doi.org/10.1152/jn.00005.2017
[11]
Ekstrom, A.D. and Ranganath, C. (2018) Space, Time, and Episodic Memory: The Hippocampus Is All over the Cognitive Map. Hippocampus, 28, 680-687. https://doi.org/10.1002/hipo.22750
[12]
Schiller, D., Eichenbaum, H., Buffalo, E.A., Davachi, L., Foster, D.J., Leutgeb, S., et al. (2015) Memory and Space: Towards an Understanding of the Cognitive Map. The Journal of Neuroscience, 35, 13904-13911. https://doi.org/10.1523/jneurosci.2618-15.2015
[13]
Greenhalgh, T., Thorne, S. and Malterud, K. (2018) Time to Challenge the Spurious Hierarchy of Systematic over Narrative Reviews? European Journal of Clinical Investigation, 48, e12931. https://doi.org/10.1111/eci.12931
[14]
K?hler, W. (1925) The Mentality of Apes. E. Winter, Trans., Harcourt, Brace.
[15]
Tolman, E.C. (1932) Purposive Behavior in Animals and Men. Century Company. https://books.google.pt/books?id=jdIxUArYUpgC&redir_esc=y
[16]
Tolman, E.C. and Honzik, C.H. (1930) Introduction and Removal of Reward, and Maze Performance in Rats. University of California Publications in Psychology, 4, 257-275. https://books.google.pt/books/about/Introduction_and_Removal_of_Reward_and_M.html?id=4L4bzwEACAAJ&redir_esc=y
[17]
Tolman, E.C., Ritchie, B.F. and Kalish, D. (1946) Studies in Spatial Learning. I. Orientation and the Short-Cut. Journal of Experimental Psychology, 36, 13-24. https://doi.org/10.1037/h0053944
[18]
Taube, J., Muller, R. and Ranck, J. (1990) Head-Direction Cells Recorded from the Postsubiculum in Freely Moving Rats. I. Description and Quantitative Analysis. The Journal of Neuroscience, 10, 420-435. https://doi.org/10.1523/jneurosci.10-02-00420.1990
[19]
Solstad, T., Boccara, C.N., Kropff, E., Moser, M. and Moser, E.I. (2008) Representation of Geometric Borders in the Entorhinal Cortex. Science, 322, 1865-1868. https://doi.org/10.1126/science.1166466
[20]
Lever, C., Burton, S., Jeewajee, A., O’Keefe, J. and Burgess, N. (2009) Boundary Vector Cells in the Subiculum of the Hippocampal Formation. The Journal of Neuroscience, 29, 9771-9777. https://doi.org/10.1523/jneurosci.1319-09.2009
[21]
Kropff, E., Carmichael, J.E., Moser, M. and Moser, E.I. (2015) Speed Cells in the Medial Entorhinal Cortex. Nature, 523, 419-424. https://doi.org/10.1038/nature14622
[22]
McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. and Moser, M. (2006) Path Integration and the Neural Basis of the ‘Cognitive Map’. Nature Reviews Neuroscience, 7, 663-678. https://doi.org/10.1038/nrn1932
[23]
Burgess, N., Barry, C. and O’Keefe, J. (2007) An Oscillatory Interference Model of Grid Cell Firing. Hippocampus, 17, 801-812. https://doi.org/10.1002/hipo.20327
[24]
Bush, D., Barry, C., Manson, D. and Burgess, N. (2015) Using Grid Cells for Navigation. Neuron, 87, 507-520. https://doi.org/10.1016/j.neuron.2015.07.006
[25]
Kjelstrup, K.B., Solstad, T., Brun, V.H., Hafting, T., Leutgeb, S., Witter, M.P., et al. (2008) Finite Scale of Spatial Representation in the Hippocampus. Science, 321, 140-143. https://doi.org/10.1126/science.1157086
[26]
Strange, B.A., Witter, M.P., Lein, E.S. and Moser, E.I. (2014) Functional Organization of the Hippocampal Longitudinal Axis. Nature Reviews Neuroscience, 15, 655-669. https://doi.org/10.1038/nrn3785
[27]
Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M. and Tanila, H. (1999) The Hippocampus, Memory, and Place Cells: Is It Spatial Memory or a Memory Space? Neuron, 23, 209-226. https://doi.org/10.1016/s0896-6273(00)80773-4
[28]
Cohen, N. J. and Eichenbaum, H. (1993) Memory, Amnesia, and the Hippocampal System. MIT Press. https://books.google.pt/books?id=0nAfZGLlQh4C&redir_esc=y
[29]
Manns, J.R., Howard, M.W. and Eichenbaum, H. (2007) Gradual Changes in Hippocampal Activity Support Remembering the Order of Events. Neuron, 56, 530-540. https://doi.org/10.1016/j.neuron.2007.08.017
[30]
Tavares, R.M., Mendelsohn, A., Grossman, Y., Williams, C.H., Shapiro, M., Trope, Y., et al. (2015) A Map for Social Navigation in the Human Brain. Neuron, 87, 231-243. https://doi.org/10.1016/j.neuron.2015.06.011
[31]
Aronov, D., Nevers, R. and Tank, D.W. (2017) Mapping of a Non-Spatial Dimension by the Hippocampal-Entorhinal Circuit. Nature, 543, 719-722. https://doi.org/10.1038/nature21692
[32]
Whittington, J.C.R., Muller, T.H., Mark, S., Chen, G., Barry, C., Burgess, N., et al. (2020) The Tolman-Eichenbaum Machine: Unifying Space and Relational Memory through Generalization in the Hippocampal Formation. Cell, 183, 1249-1263.e23. https://doi.org/10.1016/j.cell.2020.10.024
[33]
Bottini, R. and Doeller, C.F. (2020) Knowledge across Reference Frames: Cognitive Maps and Image Spaces. Trends in Cognitive Sciences, 24, 606-619. https://doi.org/10.1016/j.tics.2020.05.008
[34]
Stachenfeld, K.L., Botvinick, M.M. and Gershman, S.J. (2017) The Hippocampus as a Predictive Map. Nature Neuroscience, 20, 1643-1653. https://doi.org/10.1038/nn.4650
[35]
Barron, H.C., Auksztulewicz, R. and Friston, K. (2020) Prediction and Memory: A Predictive Coding Account. Progress in Neurobiology, 192, Article 101821. https://doi.org/10.1016/j.pneurobio.2020.101821
[36]
McNamee, D.C., Stachenfeld, K.L., Botvinick, M.M. and Gershman, S.J. (2021) Flexible Modulation of Sequence Generation in the Entorhinal-Hippocampal System. Nature Neuroscience, 24, 851-862. https://doi.org/10.1038/s41593-021-00831-7
[37]
Tse, D., Langston, R.F., Kakeyama, M., Bethus, I., Spooner, P.A., Wood, E.R., et al. (2007) Schemas and Memory Consolidation. Science, 316, 76-82. https://doi.org/10.1126/science.1135935
[38]
van Kesteren, M.T.R., Ruiter, D.J., Fernández, G. and Henson, R.N. (2012) How Schema and Novelty Augment Memory Formation. Trends in Neurosciences, 35, 211-219. https://doi.org/10.1016/j.tins.2012.02.001
[39]
Muller, R. and Kubie, J. (1987) The Effects of Changes in the Environment on the Spatial Firing of Hippocampal Complex-Spike Cells. The Journal of Neuroscience, 7, 1951-1968. https://doi.org/10.1523/jneurosci.07-07-01951.1987
[40]
Leutgeb, S., Leutgeb, J.K., Barnes, C.A., Moser, E.I., McNaughton, B.L. and Moser, M. (2005) Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles. Science, 309, 619-623. https://doi.org/10.1126/science.1114037
[41]
Colgin, L.L., Moser, E.I. and Moser, M. (2008) Understanding Memory through Hippocampal Remapping. Trends in Neurosciences, 31, 469-477. https://doi.org/10.1016/j.tins.2008.06.008
[42]
Brun, V.H., Solstad, T., Kjelstrup, K.B., Fyhn, M., Witter, M.P., Moser, E.I., et al. (2008) Progressive Increase in Grid Scale from Dorsal to Ventral Medial Entorhinal Cortex. Hippocampus, 18, 1200-1212. https://doi.org/10.1002/hipo.20504
[43]
Stensola, H., Stensola, T., Solstad, T., Fr?land, K., Moser, M. and Moser, E.I. (2012) The Entorhinal Grid Map Is Discretized. Nature, 492, 72-78. https://doi.org/10.1038/nature11649
[44]
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B.L., Witter, M.P., Moser, M., et al. (2006) Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex. Science, 312, 758-762. https://doi.org/10.1126/science.1125572
[45]
Stemmler, M., Mathis, A. and Herz, A.V.M. (2015) Connecting Multiple Spatial Scales to Decode the Population Activity of Grid Cells. Science Advances, 1, e1500816. https://doi.org/10.1126/science.1500816
[46]
Banino, A., Barry, C., Uria, B., Blundell, C., Lillicrap, T., Mirowski, P., et al. (2018) Vector-Based Navigation Using Grid-Like Representations in Artificial Agents. Nature, 557, 429-433. https://doi.org/10.1038/s41586-018-0102-6
Jacobs, J., Weidemann, C.T., Miller, J.F., Solway, A., Burke, J.F., Wei, X., et al. (2013) Direct Recordings of Grid-Like Neuronal Activity in Human Spatial Navigation. Nature Neuroscience, 16, 1188-1190. https://doi.org/10.1038/nn.3466
[49]
Miller, J.F., Neufang, M., Solway, A., Brandt, A., Trippel, M., Mader, I., et al. (2013) Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories. Science, 342, 1111-1114. https://doi.org/10.1126/science.1244056
[50]
Qasim, S.E., Miller, J., Inman, C.S., Gross, R.E., Willie, J.T., Lega, B., et al. (2019) Memory Retrieval Modulates Spatial Tuning of Single Neurons in the Human Entorhinal Cortex. Nature Neuroscience, 22, 2078-2086. https://doi.org/10.1038/s41593-019-0523-z
[51]
Hartley, T., Maguire, E.A., Spiers, H.J. and Burgess, N. (2003) The Well-Worn Route and the Path Less Traveled: Distinct Neural Bases of Route Following and Wayfinding in Humans. Neuron, 37, 877-888. https://doi.org/10.1016/s0896-6273(03)00095-3
[52]
Doeller, C.F., King, J.A. and Burgess, N. (2008) Parallel Striatal and Hippocampal Systems for Landmarks and Boundaries in Spatial Memory. Proceedings of the National Academy of Sciences, 105, 5915-5920. https://doi.org/10.1073/pnas.0801489105
[53]
Howard, L.R., Javadi, A.H., Yu, Y., Mill, R.D., Morrison, L.C., Knight, R., et al. (2014) The Hippocampus and Entorhinal Cortex Encode the Path and Euclidean Distances to Goals during Navigation. Current Biology, 24, 1331-1340. https://doi.org/10.1016/j.cub.2014.05.001
[54]
Doeller, C.F., Barry, C. and Burgess, N. (2010) Evidence for Grid Cells in a Human Memory Network. Nature, 463, 657-661. https://doi.org/10.1038/nature08704
[55]
Nau, M., Navarro Schr?der, T., Bellmund, J.L.S. and Doeller, C.F. (2018) Hexadirectional Coding of Visual Space in Human Entorhinal Cortex. Nature Neuroscience, 21, 188-190. https://doi.org/10.1038/s41593-017-0050-8
[56]
Stangl, M., Achtzehn, J., Huber, K., Dietrich, C., Tempelmann, C. and Wolbers, T. (2018) Compromised Grid-Cell-Like Representations in Old Age as a Key Mechanism to Explain Age-Related Navigational Deficits. Current Biology, 28, 1108-1115.e6. https://doi.org/10.1016/j.cub.2018.02.038
[57]
Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O’Keefe, J., et al. (2006) The Boundary Vector Cell Model of Place Cell Firing and Spatial Memory. Reviews in the Neurosciences, 17, 71-97. https://doi.org/10.1515/revneuro.2006.17.1-2.71
[58]
Johnson, A. and Redish, A.D. (2007) Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point. The Journal of Neuroscience, 27, 12176-12189. https://doi.org/10.1523/jneurosci.3761-07.2007
[59]
Pfeiffer, B.E. and Foster, D.J. (2013) Hippocampal Place-Cell Sequences Depict Future Paths to Remembered Goals. Nature, 497, 74-79. https://doi.org/10.1038/nature12112
[60]
ólafsdóttir, H.F., Bush, D. and Barry, C. (2018) The Role of Hippocampal Replay in Memory and Planning. Current Biology, 28, R37-R50. https://doi.org/10.1016/j.cub.2017.10.073
[61]
Recanatesi, S., Farrell, M., Lajoie, G., Deneve, S., Rigotti, M. and Shea-Brown, E. (2021) Predictive Learning as a Network Mechanism for Extracting Low-Dimensional Latent Space Representations. Nature Communications, 12, Article No. 1417. https://doi.org/10.1038/s41467-021-21696-1
[62]
Yassa, M.A. and Stark, C.E.L. (2011) Pattern Separation in the Hippocampus. Trends in Neurosciences, 34, 515-525. https://doi.org/10.1016/j.tins.2011.06.006
[63]
MacDonald, C.J., Lepage, K.Q., Eden, U.T. and Eichenbaum, H. (2011) Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events. Neuron, 71, 737-749. https://doi.org/10.1016/j.neuron.2011.07.012
[64]
Kraus, B.J., Robinson, R.J., White, J.A., Eichenbaum, H. and Hasselmo, M.E. (2013) Hippocampal “Time Cells”: Time versus Path Integration. Neuron, 78, 1090-1101. https://doi.org/10.1016/j.neuron.2013.04.015
[65]
Eichenbaum, H. (2014) Time Cells in the Hippocampus: A New Dimension for Mapping Memories. Nature Reviews Neuroscience, 15, 732-744. https://doi.org/10.1038/nrn3827
[66]
Umbach, G., Kantak, P., Jacobs, J., Kahana, M., Pfeiffer, B.E., Sperling, M., et al. (2020) Time Cells in the Human Hippocampus and Entorhinal Cortex Support Episodic Memory. Proceedings of the National Academy of Sciences, 117, 28463-28474. https://doi.org/10.1073/pnas.2013250117
[67]
Nieh, E.H., Schottdorf, M., Freeman, N.W., Low, R.J., Lewallen, S., Koay, S.A., et al. (2021) Geometry of Abstract Learned Knowledge in the Hippocampus. Nature, 595, 80-84. https://doi.org/10.1038/s41586-021-03652-7
[68]
Park, S.A., Miller, D.S., Nili, H., Ranganath, C. and Boorman, E.D. (2020) Map Making: Constructing, Combining, and Inferring on Abstract Cognitive Maps. Neuron, 107, 1226-1238.e8. https://doi.org/10.1016/j.neuron.2020.06.030
[69]
Solomon, E.A., Lega, B.C., Sperling, M.R. and Kahana, M.J. (2019) Hippocampal Theta Codes for Distances in Semantic and Temporal Spaces. Proceedings of the National Academy of Sciences, 116, 24343-24352. https://doi.org/10.1073/pnas.1906729116
[70]
Dordek, Y., Soudry, D., Meir, R. and Derdikman, D. (2016) Extracting Grid Cell Characteristics from Place Cell Inputs Using Non-Negative Principal Component Analysis. eLife, 5, e10094. https://doi.org/10.7554/elife.10094
[71]
Sorscher, B., Mel, G.C., Ocko, S.A., Giocomo, L.M. and Ganguli, S. (2023) A Unified Theory for the Computational and Mechanistic Origins of Grid Cells. Neuron, 111, 121-137.e13. https://doi.org/10.1016/j.neuron.2022.10.003
[72]
Kriegeskorte, N., Mur, M. and Bandettini, P. (2008) Representational Similarity Analysis-Connecting the Branches of Systems Neuroscience. Frontiers in Systems Neuroscience, 2, Article ID: 4. https://doi.org/10.3389/neuro.06.004.2008
[73]
Nastase, S.A., Connolly, A.C., Oosterhof, N.N., Halchenko, Y.O., Guntupalli, J.S., Visconti di Oleggio Castello, M., et al. (2017) Attention Selectively Reshapes the Geometry of Distributed Semantic Representation. Cerebral Cortex, 27, 4277-4291. https://doi.org/10.1093/cercor/bhx138
[74]
Epstein, R.A., Patai, E.Z., Julian, J.B. and Spiers, H.J. (2017) The Cognitive Map in Humans: Spatial Navigation and Beyond. Nature Neuroscience, 20, 1504-1513. https://doi.org/10.1038/nn.4656
[75]
Vann, S.D., Aggleton, J.P. and Maguire, E.A. (2009) What Does the Retrosplenial Cortex Do? Nature Reviews Neuroscience, 10, 792-802. https://doi.org/10.1038/nrn2733
[76]
Julian, J.B., Keinath, A.T., Marchette, S.A. and Epstein, R.A. (2018) The Neurocognitive Basis of Spatial Reorientation. Current Biology, 28, R1059-R1073. https://doi.org/10.1016/j.cub.2018.04.057
[77]
Taube, J.S. (2007) The Head Direction Signal: Origins and Sensory-Motor Integration. Annual Review of Neuroscience, 30, 181-207. https://doi.org/10.1146/annurev.neuro.29.051605.112854
[78]
Schuck, N.W., Cai, M.B., Wilson, R.C. and Niv, Y. (2016) Human Orbitofrontal Cortex Represents a Cognitive Map of State Space. Neuron, 91, 1402-1412. https://doi.org/10.1016/j.neuron.2016.08.019
[79]
Wilson, R.C., Takahashi, Y.K., Schoenbaum, G. and Niv, Y. (2014) Orbitofrontal Cortex as a Cognitive Map of Task Space. Neuron, 81, 267-279. https://doi.org/10.1016/j.neuron.2013.11.005
[80]
Baram, A.B., Muller, T.H., Nili, H., Garvert, M.M. and Behrens, T.E.J. (2021) Entorhinal and Ventromedial Prefrontal Cortices Abstract and Generalize the Structure of Reinforcement Learning Problems. Neuron, 109, 713-723.e7. https://doi.org/10.1016/j.neuron.2020.11.024
[81]
Ranganath, C. and Ritchey, M. (2012) Two Cortical Systems for Memory-Guided Behaviour. Nature Reviews Neuroscience, 13, 713-726. https://doi.org/10.1038/nrn3338
[82]
Ritchey, M., Libby, L.A. and Ranganath, C. (2015) Cortico-Hippocampal Systems Involved in Memory and Cognition: The PMAT Framework. In: Progress in Brain Research, Elsevier, 45-64. https://doi.org/10.1016/bs.pbr.2015.04.001
[83]
Stangl, M., Shine, J. and Wolbers, T. (2017) The Gridcat: A Toolbox for Automated Analysis of Human Grid Cell Codes in fMRI. Frontiers in Neuroinformatics, 11, Article No. 47. https://doi.org/10.3389/fninf.2017.00047
[84]
Hales, J.B., Schlesiger, M.I., Leutgeb, J.K., Squire, L.R., Leutgeb, S. and Clark, R.E. (2014) Medial Entorhinal Cortex Lesions Only Partially Disrupt Hippocampal Place Cells and Hippocampus-Dependent Place Memory. Cell Reports, 9, 893-901. https://doi.org/10.1016/j.celrep.2014.10.009
[85]
Gil, M., Ancau, M., Schlesiger, M.I., Neitz, A., Allen, K., De Marco, R.J., et al. (2018) Impaired Path Integration in Mice with Disrupted Grid Cell Firing. Nature Neuroscience, 21, 81-91. https://doi.org/10.1038/s41593-017-0039-3
[86]
Robinson, N.T.M., Descamps, L.A.L., Russell, L.E., Buchholz, M.O., Bicknell, B.A., Antonov, G.K., et al. (2020) Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior. Cell, 183, 1586-1599.e10. https://doi.org/10.1016/j.cell.2020.09.061
[87]
Morris, R.G.M. (1981) Spatial Localization Does Not Require the Presence of Local Cues. Learning and Motivation, 12, 239-260. https://doi.org/10.1016/0023-9690(81)90020-5
[88]
Morris, R.G.M., Garrud, P., Rawlins, J.N.P. and O’Keefe, J. (1982) Place Navigation Impaired in Rats with Hippocampal Lesions. Nature, 297, 681-683. https://doi.org/10.1038/297681a0
[89]
Packard, M.G. and McGaugh, J.L. (1996) Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning. Neurobiology of Learning and Memory, 65, 65-72. https://doi.org/10.1006/nlme.1996.0007
[90]
Alvernhe, A., Save, E. and Poucet, B. (2011) Local Remapping of Place Cell Firing in the Tolman Detour Task. European Journal of Neuroscience, 33, 1696-1705. https://doi.org/10.1111/j.1460-9568.2011.07653.x
[91]
Spiers, H.J. and Maguire, E.A. (2006) Thoughts, Behaviour, and Brain Dynamics during Navigation in the Real World. NeuroImage, 31, 1826-1840. https://doi.org/10.1016/j.neuroimage.2006.01.037
[92]
Coutrot, A., Silva, R., Manley, E., de Cothi, W., Sami, S., Bohbot, V.D., et al. (2018) Global Determinants of Navigation Ability. Current Biology, 28, 2861-2866.e4. https://doi.org/10.1016/j.cub.2018.06.009
[93]
Dusek, J.A. and Eichenbaum, H. (1997) The Hippocampus and Memory for Orderly Stimulus Relations. Proceedings of the National Academy of Sciences, 94, 7109-7114. https://doi.org/10.1073/pnas.94.13.7109
[94]
Heckers, S., Zalesak, M., Weiss, A.P., Ditman, T. and Titone, D. (2004) Hippocampal Activation during Transitive Inference in Humans. Hippocampus, 14, 153-162. https://doi.org/10.1002/hipo.10189
[95]
Theves, S., Fernandez, G. and Doeller, C.F. (2019) The Hippocampus Encodes Distances in Multidimensional Feature Space. Current Biology, 29, 1226-1231.e3. https://doi.org/10.1016/j.cub.2019.02.035
[96]
Foo, P., Warren, W.H., Duchon, A. and Tarr, M.J. (2005) Do Humans Integrate Routes into a Cognitive Map? Map-versus Landmark-Based Navigation of Novel Shortcuts. Journal of Experimental Psychology: Learning, Memory, and Cognition, 31, 195-215. https://doi.org/10.1037/0278-7393.31.2.195
[97]
Burak, Y. and Fiete, I.R. (2009) Accurate Path Integration in Continuous Attractor Network Models of Grid Cells. PLOS Computational Biology, 5, e1000291. https://doi.org/10.1371/journal.pcbi.1000291
[98]
Couey, J.J., Witoelar, A., Zhang, S., Zheng, K., Ye, J., Dunn, B., et al. (2013) Recurrent Inhibitory Circuitry as a Mechanism for Grid Formation. Nature Neuroscience, 16, 318-324. https://doi.org/10.1038/nn.3310
[99]
Bush, D. and Burgess, N. (2014) A Hybrid Oscillatory Interference/Continuous Attractor Network Model of Grid Cell Firing. The Journal of Neuroscience, 34, 5065-5079. https://doi.org/10.1523/jneurosci.4017-13.2014
[100]
Dayan, P. (1993) Improving Generalization for Temporal Difference Learning: The Successor Representation. NeuralComputation, 5, 613-624. https://doi.org/10.1162/neco.1993.5.4.613
[101]
Momennejad, I., Russek, E.M., Cheong, J.H., Botvinick, M.M., Daw, N.D. and Gershman, S.J. (2017) The Successor Representation in Human Reinforcement Learning. NatureHumanBehaviour, 1, 680-692. https://doi.org/10.1038/s41562-017-0180-8
[102]
Benna, M.K. and Fusi, S. (2021) Place Cells May Simply Be Memory Cells: Memory Compression Leads to Spatial Tuning and History Dependence. ProceedingsoftheNationalAcademyofSciences, 118, e2018422118. https://doi.org/10.1073/pnas.2018422118
[103]
Bicanski, A. and Burgess, N. (2018) A Neural-Level Model of Spatial Memory and Imagery. eLife, 7, e33752.
[104]
de Cothi, W., Nyberg, N., Griesbauer, E., Ghanamé, C., Zisch, F., Lefort, J.M., et al. (2022) Predictive Maps in Rats and Humans for Spatial Navigation. CurrentBiology, 32, 3676-3689.e5. https://doi.org/10.1016/j.cub.2022.06.090
[105]
Deuker, L., Bellmund, J.L.S., Navarro Schr?der, T. and Doeller, C.F. (2016) An Event Map of Memory Space in the Hippocampus. eLife, 5, e16534.
[106]
Naselaris, T., Kay, K.N., Nishimoto, S. and Gallant, J.L. (2011) Encoding and Decoding in fMRI. NeuroImage, 56, 400-410. https://doi.org/10.1016/j.neuroimage.2010.07.073
[107]
Nielson, D.M., Smith, T.A., Sreekumar, V., Dennis, S. and Sederberg, P.B. (2015) Human Hippocampus Represents Space and Time during Retrieval of Real-World Memories. ProceedingsoftheNationalAcademyofSciences, 112, 11078-11083. https://doi.org/10.1073/pnas.1507104112
[108]
Gardner, R.J., Hermansen, E., Pachitariu, M., Burak, Y., Baas, N.A., Dunn, B.A., et al. (2022) Toroidal Topology of Population Activity in Grid Cells. Nature, 602, 123-128. https://doi.org/10.1038/s41586-021-04268-7
[109]
Liu, Y., Dolan, R.J., Kurth-Nelson, Z. and Behrens, T.E.J. (2019) Human Replay Spontaneously Reorganizes Experience. Cell, 178, 640-652.e14. https://doi.org/10.1016/j.cell.2019.06.012
[110]
Viganò, S. and Piazza, M. (2020) Distance and Direction Codes Underlie Navigation of a Novel Semantic Space in the Human Brain. TheJournalofNeuroscience, 40, 2727-2736. https://doi.org/10.1523/jneurosci.1849-19.2020
[111]
Schapiro, A.C., Rogers, T.T., Cordova, N.I., Turk-Browne, N.B. and Botvinick, M.M. (2013) Neural Representations of Events Arise from Temporal Community Structure. NatureNeuroscience, 16, 486-492. https://doi.org/10.1038/nn.3331
[112]
Mark, S., Moran, R., Parr, T., Kennerley, S.W. and Behrens, T.E.J. (2020) Transferring Structural Knowledge across Cognitive Maps in Humans and Models. NatureCommunications, 11, Article No. 4783. https://doi.org/10.1038/s41467-020-18254-6
[113]
Baldassano, C., Chen, J., Zadbood, A., Pillow, J.W., Hasson, U. and Norman, K.A. (2017) Discovering Event Structure in Continuous Narrative Perception and Memory. Neuron, 95, 709-721.e5. https://doi.org/10.1016/j.neuron.2017.06.041
[114]
Kumaran, D. and McClelland, J.L. (2012) Generalization through the Recurrent Interaction of Episodic Memories: A Model of the Hippocampal System. PsychologicalReview, 119, 573-616. https://doi.org/10.1037/a0028681
[115]
Bao, X., Gjorgieva, E., Shanahan, L.K., Howard, J.D., Kahnt, T. and Gottfried, J.A. (2019) Grid-Like Neural Representations Support Olfactory Navigation of a Two-Dimensional Odor Space. Neuron, 102, 1066-1075.e5. https://doi.org/10.1016/j.neuron.2019.03.034
[116]
Amunts, K., Lepage, C., Borgeat, L., Mohlberg, H., Dickscheid, T., Rousseau, M., et al. (2013) Bigbrain: An Ultrahigh-Resolution 3D Human Brain Model. Science, 340, 1472-1475. https://doi.org/10.1126/science.1235381
[117]
Wisse, L.E.M., Daugherty, A.M., Olsen, R.K., Berron, D., Carr, V.A., Stark, C.E.L., et al. (2016) A Harmonized Segmentation Protocol for Hippocampal and Parahippocampal Subregions: Why Do We Need One and What Are the Key Goals? Hippocampus, 27, 3-11. https://doi.org/10.1002/hipo.22671
[118]
Yushkevich, P.A., Amaral, R.S.C., Augustinack, J.C., Bender, A.R., Bernstein, J.D., Boccardi, M., et al. (2015) Quantitative Comparison of 21 Protocols for Labeling Hippocampal Subfields and Parahippocampal Subregions in in Vivo MRI: Towards a Harmonized Segmentation Protocol. NeuroImage, 111, 526-541. https://doi.org/10.1016/j.neuroimage.2015.01.004
[119]
Maass, A., Berron, D., Libby, L.A., Ranganath, C. and Düzel, E. (2015) Functional Subregions of the Human Entorhinal Cortex. eLife, 4, e06426.
[120]
Huber, L., Handwerker, D.A., Jangraw, D.C., Chen, G., Hall, A., Stüber, C., et al. (2017) High-Resolution CBV-fMRI Allows Mapping of Laminar Activity and Connectivity of Cortical Input and Output in Human M1. Neuron, 96, 1253-1263.e7. https://doi.org/10.1016/j.neuron.2017.11.005
[121]
Finn, E.S., Huber, L., Jangraw, D.C., Molfese, P.J. and Bandettini, P.A. (2019) Layer-Dependent Activity in Human Prefrontal Cortex during Working Memory. NatureNeuroscience, 22, 1687-1695. https://doi.org/10.1038/s41593-019-0487-z
[122]
Maller, J.J., Welton, T., Middione, M., Callaghan, F.M., Rosenfeld, J.V. and Grieve, S.M. (2019) Revealing the Hippocampal Connectome through Super-Resolution 1150-Direction Diffusion MRI. ScientificReports, 9, Article No. 2418. https://doi.org/10.1038/s41598-018-37905-9
[123]
Dalton, M.A., D’Souza, A., Lv, J. and Calamante, F. (2022) New Insights into Anatomical Connectivity along the Anterior-Posterior Axis of the Human Hippocampus Using in Vivo Quantitative Fibre Tracking and High-Resolution Diffusion MRI. eLife, 11, e76143.
[124]
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N.J., et al. (2005) Cytoarchitectonic Mapping of the Human Amygdala, Hippocampal Region and Entorhinal Cortex: Intersubject Variability and Probability Maps. Anatomy and Embryology, 210, 343-352. https://doi.org/10.1007/s00429-005-0025-5
[125]
Palomero-Gallagher, N., Kedo, O., Mohlberg, H., Zilles, K. and Amunts, K. (2020) Multimodal Mapping and Analysis of the Cyto-and Receptorarchitecture of the Human Hippocampus. Brain Structure and Function, 225, 881-907. https://doi.org/10.1007/s00429-019-02022-4
[126]
Ding, S. and Van Hoesen, G.W. (2015) Organization and Detailed Parcellation of Human Hippocampal Head and Body Regions Based on a Combined Analysis of Cyto‐ and Chemoarchitecture. Journal of Comparative Neurology, 523, 2233-2253. https://doi.org/10.1002/cne.23786
[127]
van Strien, N.M., Cappaert, N.L.M. and Witter, M.P. (2009) The Anatomy of Memory: An Interactive Overview of the Parahippocampal-Hippocampal Network. Nature Reviews Neuroscience, 10, 272-282. https://doi.org/10.1038/nrn2614
[128]
Insausti, R., Mu?oz-López, M., Insausti, A.M. and Artacho-Pérula, E. (2017) The Human Periallocortex: Layer Pattern in Presubiculum, Parasubiculum and Entorhinal Cortex. A Review. Frontiers in Neuroanatomy, 11, Article ID: 84. https://doi.org/10.3389/fnana.2017.00084
[129]
Amunts, K., Mohlberg, H., Bludau, S. and Zilles, K. (2020) Julich-Brain: A 3D Probabilistic Atlas of the Human Brain’s Cytoarchitecture. Science, 369, 988-992. https://doi.org/10.1126/science.abb4588
[130]
Paquola, C., Benkarim, O., DeKraker, J., Larivière, S., Fr?ssle, S. et al. (2020) Convergence of Cortical Types and Functional Motifs in the Human Mesiotemporal Lobe. eLife, 9, e60673.
[131]
Chadwick, M.J., Jolly, A.E.J., Amos, D.P., Hassabis, D. and Spiers, H.J. (2015) A Goal Direction Signal in the Human Entorhinal/Subicular Region. CurrentBiology, 25, 87-92. https://doi.org/10.1016/j.cub.2014.11.001
[132]
Brown, T.I., Whiteman, A.S., Aselcioglu, I. and Stern, C.E. (2014) Structural Differences in Hippocampal and Prefrontal Gray Matter Volume Support Flexible Context-Dependent Navigation Ability. TheJournalofNeuroscience, 34, 2314-2320. https://doi.org/10.1523/jneurosci.2202-13.2014
[133]
Bonilha, L., Gleichgerrcht, E., Fridriksson, J., Rorden, C., Breedlove, J.L., Nesland, T., et al. (2015) Reproducibility of the Structural Brain Connectome Derived from Diffusion Tensor Imaging. PLOSONE, 10, e0135247. https://doi.org/10.1371/journal.pone.0135247
[134]
Paquola, C., Vos De Wael, R., Wagstyl, K., Bethlehem, R.A.I., Hong, S., Seidlitz, J., et al. (2019) Microstructural and Functional Gradients Are Increasingly Dissociated in Transmodal Cortices. PLOSBiology, 17, e3000284. https://doi.org/10.1371/journal.pbio.3000284
[135]
Vogel, J.W., La Joie, R., Grothe, M.J., Diaz-Papkovich, A., Doyle, A., Vachon-Presseau, E., et al. (2020) A Molecular Gradient along the Longitudinal Axis of the Human Hippocampus Informs Large-Scale Behavioral Systems. NatureCommunications, 11, Article No. 960. https://doi.org/10.1038/s41467-020-14518-3
[136]
Berron, D., Neumann, K., Maass, A., Schütze, H., Fliessbach, K., Kiven, V., et al. (2018) Age-Related Functional Changes in Domain-Specific Medial Temporal Lobe Pathways. NeurobiologyofAging, 65, 86-97. https://doi.org/10.1016/j.neurobiolaging.2017.12.030
[137]
Lester, A.W., Moffat, S.D., Wiener, J.M., Barnes, C.A. and Wolbers, T. (2017) The Aging Navigational System. Neuron, 95, 1019-1035. https://doi.org/10.1016/j.neuron.2017.06.037