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The cognitive map in humans: spatial navigation and beyond

Nature Neuroscience volume 20, pages 1504–1513 (2017)Cite this article

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Abstract

The 'cognitive map' hypothesis proposes that brain builds a unified representation of the spatial environment to support memory and guide future action. Forty years of electrophysiological research in rodents suggest that cognitive maps are neurally instantiated by place, grid, border and head direction cells in the hippocampal formation and related structures. Here we review recent work that suggests a similar functional organization in the human brain and yields insights into how cognitive maps are used during spatial navigation. Specifically, these studies indicate that (i) the human hippocampus and entorhinal cortex support map-like spatial codes, (ii) posterior brain regions such as parahippocampal and retrosplenial cortices provide critical inputs that allow cognitive maps to be anchored to fixed environmental landmarks, and (iii) hippocampal and entorhinal spatial codes are used in conjunction with frontal lobe mechanisms to plan routes during navigation. We also discuss how these three basic elements of cognitive map based navigation—spatial coding, landmark anchoring and route planning—might be applied to nonspatial domains to provide the building blocks for many core elements of human thought.

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Figure 1: Neuroimaging studies reveal a network of brain regions involved in spatial navigation.
Figure 2: Map- and grid-like coding of navigable space in humans.
Figure 3: Anchoring the cognitive map to the world.
Figure 4: Hippocampus codes metrics of the environment along a journey.
Figure 5: Frontal areas involved in planning during navigation.

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References

  1. Tolman, E.C. Cognitive maps in rats and men. Psychol. Rev. 55, 189–208 (1948).

    Article  CAS  PubMed  Google Scholar 

  2. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).

    Article  CAS  PubMed  Google Scholar 

  3. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).

  4. Eichenbaum, H. & Cohen, N.J. Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83, 764–770 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Buzsáki, G. et al. Viewpoints on the hippocampus. Nat. Neurosci. 20, 1633–1641 (2017).

    Google Scholar 

  6. Grieves, R.M. & Jeffery, K.J. The representation of space in the brain. Behav. Processes 135, 113–131 (2017).

    Article  PubMed  Google Scholar 

  7. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. & Moser, M.-B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663–678 (2006).

    Article  CAS  PubMed  Google Scholar 

  8. Taube, J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207 (2007).

    Article  CAS  PubMed  Google Scholar 

  9. Byrne, P., Becker, S. & Burgess, N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sarel, A., Finkelstein, A., Las, L. & Ulanovsky, N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355, 176–180 (2017).

    Article  CAS  PubMed  Google Scholar 

  11. Clark, R.E. & Squire, L.R. Similarity in form and function of the hippocampus in rodents, monkeys, and humans. Proc. Natl. Acad. Sci. USA 110 (Suppl. 2), 10365–10370 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Aguirre, G.K., Detre, J.A., Alsop, D.C. & D'Esposito, M. The parahippocampus subserves topographical learning in man. Cereb. Cortex 6, 823–829 (1996).

    Article  CAS  PubMed  Google Scholar 

  13. Ghaem, O. et al. Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8, 739–744 (1997).

    Article  CAS  PubMed  Google Scholar 

  14. Maguire, E.A. et al. Knowing where and getting there: a human navigation network. Science 280, 921–924 (1998).

    Article  CAS  PubMed  Google Scholar 

  15. Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).

    Article  CAS  PubMed  Google Scholar 

  16. Spiers, H.J. & Maguire, E.A. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31, 1826–1840 (2006).

    Article  PubMed  Google Scholar 

  17. Spiers, H.J. & Gilbert, S.J. Solving the detour problem in navigation: a model of prefrontal and hippocampal interactions. Front. Hum. Neurosci. 9, 125 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hartley, T., Maguire, E.A., Spiers, H.J. & Burgess, N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37, 877–888 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. Iaria, G., Petrides, M., Dagher, A., Pike, B. & Bohbot, V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J. Neurosci. 23, 5945–5952 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Marchette, S.A., Bakker, A. & Shelton, A.L. Cognitive mappers to creatures of habit: differential engagement of place and response learning mechanisms predicts human navigational behavior. J. Neurosci. 31, 15264–15268 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Suthana, N.A., Ekstrom, A.D., Moshirvaziri, S., Knowlton, B. & Bookheimer, S.Y. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J. Neurosci. 29, 10512–10519 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Woollett, K. & Maguire, E.A. Acquiring “the Knowledge” of London's layout drives structural brain changes. Curr. Biol. 21, 2109–2114 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schinazi, V.R., Nardi, D., Newcombe, N.S., Shipley, T.F. & Epstein, R.A. Hippocampal size predicts rapid learning of a cognitive map in humans. Hippocampus 23, 515–528 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Hartley, T. & Harlow, R. An association between human hippocampal volume and topographical memory in healthy young adults. Front. Hum. Neurosci. 6, 338 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Morgan, L.K., Macevoy, S.P., Aguirre, G.K. & Epstein, R.A. Distances between real-world locations are represented in the human hippocampus. J. Neurosci. 31, 1238–1245 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hassabis, D. et al. Decoding neuronal ensembles in the human hippocampus. Curr. Biol. 19, 546–554 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Deuker, L., Bellmund, J.L., Navarro Schröder, T. & Doeller, C.F. An event map of memory space in the hippocampus. Elife 5, e16534 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Nielson, D.M., Smith, T.A., Sreekumar, V., Dennis, S. & Sederberg, P.B. Human hippocampus represents space and time during retrieval of real-world memories. Proc. Natl. Acad. Sci. USA 112, 11078–11083 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Doeller, C.F., Barry, C. & Burgess, N. Evidence for grid cells in a human memory network. Nature 463, 657–661 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Horner, A.J., Bisby, J.A., Zotow, E., Bush, D. & Burgess, N. Grid-like processing of imagined navigation. Curr. Biol. 26, 842–847 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ekstrom, A.D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184–188 (2003).

    Article  CAS  PubMed  Google Scholar 

  32. Jacobs, J. et al. Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16, 1188–1190 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Miller, J.F., Fried, I., Suthana, N. & Jacobs, J. Repeating spatial activations in human entorhinal cortex. Curr. Biol. 25, 1080–1085 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Jeffery, K.J., Anderson, M.I., Hayman, R. & Chakraborty, S. A proposed architecture for the neural representation of spatial context. Neurosci. Biobehav. Rev. 28, 201–218 (2004).

    Article  PubMed  Google Scholar 

  35. Colgin, L.L., Moser, E.I. & Moser, M.-B. Understanding memory through hippocampal remapping. Trends Neurosci. 31, 469–477 (2008).

    Article  CAS  PubMed  Google Scholar 

  36. Lever, C., Wills, T., Cacucci, F., Burgess, N. & O'Keefe, J. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90–94 (2002).

    Article  CAS  PubMed  Google Scholar 

  37. Wills, T.J., Lever, C., Cacucci, F., Burgess, N. & O'Keefe, J. Attractor dynamics in the hippocampal representation of the local environment. Science 308, 873–876 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Steemers, B. et al. Hippocampal attractor dynamics predict memory-based decision making. Curr. Biol. 26, 1750–1757 (2016).

    Article  CAS  PubMed  Google Scholar 

  39. Yassa, M.A. & Stark, C.E. Pattern separation in the hippocampus. Trends Neurosci. 34, 515–525 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kyle, C.T., Stokes, J.D., Lieberman, J.S., Hassan, A.S. & Ekstrom, A.D. Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms. Elife 4, e10499 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Chanales, A.J.H., Oza, A., Favila, S.E. & Kuhl, B.A. Overlap among spatial memories triggers repulsion of hippocampal representations. Curr. Biol. 27, 2307–2317.e5 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. McKenzie, S. et al. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83, 202–215 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Teng, E. & Squire, L.R. Memory for places learned long ago is intact after hippocampal damage. Nature 400, 675–677 (1999).

    Article  CAS  PubMed  Google Scholar 

  44. Maguire, E.A., Nannery, R. & Spiers, H.J. Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 129, 2894–2907 (2006).

    Article  PubMed  Google Scholar 

  45. Kolarik, B.S. et al. Impairments in precision, rather than spatial strategy, characterize performance on the virtual Morris water maze: a case study. Neuropsychologia 80, 90–101 (2016).

    Article  PubMed  Google Scholar 

  46. Wolbers, T. & Büchel, C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J. Neurosci. 25, 3333–3340 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rosenbaum, R.S., Ziegler, M., Winocur, G., Grady, C.L. & Moscovitch, M. “I have often walked down this street before”: fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus 14, 826–835 (2004).

    Article  PubMed  Google Scholar 

  48. Epstein, R.A., Parker, W.E. & Feiler, A.M. Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J. Neurosci. 27, 6141–6149 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Patai, E.Z. et al. Long-term consolidation switches goal proximity coding from hippocampus to retrosplenial cortex. Preprint at bioRxiv https://doi.org/10.1101/167882 (2017).

  50. Epstein, R.A. & Vass, L.K. Neural systems for landmark-based wayfinding in humans. Phil. Trans. R. Soc. Lond. B 369, 20120533 (2013).

    Article  Google Scholar 

  51. Etienne, A.S. & Jeffery, K.J. Path integration in mammals. Hippocampus 14, 180–192 (2004).

    Article  PubMed  Google Scholar 

  52. Gallistel, C.R. The Organization of Learning (MIT Press, 1990).

  53. Wolbers, T., Wiener, J.M., Mallot, H.A. & Büchel, C. Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. J. Neurosci. 27, 9408–9416 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sherrill, K.R. et al. Hippocampus and retrosplenial cortex combine path integration signals for successful navigation. J. Neurosci. 33, 19304–19313 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sholl, M.J. Cognitive maps as orienting schemata. J. Exp. Psychol. Learn. Mem. Cogn. 13, 615–628 (1987).

    Article  CAS  PubMed  Google Scholar 

  56. Knierim, J.J. & Hamilton, D.A. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol. Rev. 91, 1245–1279 (2011).

    Article  PubMed  Google Scholar 

  57. Yoder, R.M., Clark, B.J. & Taube, J.S. Origins of landmark encoding in the brain. Trends Neurosci. 34, 561–571 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Shelton, A.L. & McNamara, T.P. Systems of spatial reference in human memory. Cognit. Psychol. 43, 274–310 (2001).

    Article  CAS  PubMed  Google Scholar 

  59. Krupic, J., Bauza, M., Burton, S., Barry, C. & O'Keefe, J. Grid cell symmetry is shaped by environmental geometry. Nature 518, 232–235 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Stensola, T., Stensola, H., Moser, M.-B. & Moser, E.I. Shearing-induced asymmetry in entorhinal grid cells. Nature 518, 207–212 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Cheng, K., Huttenlocher, J. & Newcombe, N.S. 25 years of research on the use of geometry in spatial reorientation: a current theoretical perspective. Psychon. Bull. Rev. 20, 1033–1054 (2013).

    Article  PubMed  Google Scholar 

  62. Cheng, K. A purely geometric module in the rat's spatial representation. Cognition 23, 149–178 (1986).

    Article  CAS  PubMed  Google Scholar 

  63. Keinath, A.T., Julian, J.B., Epstein, R.A. & Muzzio, I.A. Environmental geometry aligns the hippocampal map during spatial reorientation. Curr. Biol. 27, 309–317 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Knight, R., Hayman, R., Lin Ginzberg, L. & Jeffery, K. Geometric cues influence head direction cells only weakly in nondisoriented rats. J. Neurosci. 31, 15681–15692 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Biegler, R. & Morris, R.G. Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361, 631–633 (1993).

    Article  CAS  PubMed  Google Scholar 

  66. Auger, S.D., Zeidman, P. & Maguire, E.A. A central role for the retrosplenial cortex in de novo environmental learning. Elife 4, e09031 (2015).

    Article  PubMed Central  Google Scholar 

  67. Knierim, J.J., Kudrimoti, H.S. & McNaughton, B.L. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 1648–1659 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Bicanski, A. & Burgess, N. Environmental anchoring of head direction in a computational model of retrosplenial cortex. J. Neurosci. 36, 11601–11618 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996).

    Article  CAS  PubMed  Google Scholar 

  70. Barry, C., Hayman, R., Burgess, N. & Jeffery, K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682–684 (2007).

    Article  CAS  PubMed  Google Scholar 

  71. Bird, C.M., Capponi, C., King, J.A., Doeller, C.F. & Burgess, N. Establishing the boundaries: the hippocampal contribution to imagining scenes. J. Neurosci. 30, 11688–11695 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Doeller, C.F., King, J.A. & Burgess, N. Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc. Natl. Acad. Sci. USA 105, 5915–5920 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hartley, T., Trinkler, I. & Burgess, N. Geometric determinants of human spatial memory. Cognition 94, 39–75 (2004).

    Article  PubMed  Google Scholar 

  74. Hamilton, D.A., Akers, K.G., Weisend, M.P. & Sutherland, R.J. How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector. J. Exp. Psychol. Anim. Behav. Process. 33, 100–114 (2007).

    Article  PubMed  Google Scholar 

  75. Epstein, R.A. Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn. Sci. 12, 388–396 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Nasr, S. et al. Scene-selective cortical regions in human and nonhuman primates. J. Neurosci. 31, 13771–13785 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Troiani, V., Stigliani, A., Smith, M.E. & Epstein, R.A. Multiple object properties drive scene-selective regions. Cereb. Cortex 24, 883–897 (2014).

    Article  PubMed  Google Scholar 

  78. Janzen, G. & van Turennout, M. Selective neural representation of objects relevant for navigation. Nat. Neurosci. 7, 673–677 (2004).

    Article  CAS  PubMed  Google Scholar 

  79. Kornblith, S., Cheng, X., Ohayon, S. & Tsao, D.Y. A network for scene processing in the macaque temporal lobe. Neuron 79, 766–781 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Auger, S.D., Mullally, S.L. & Maguire, E.A. Retrosplenial cortex codes for permanent landmarks. PLoS One 7, e43620 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Committeri, G. et al. Reference frames for spatial cognition: different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. J. Cogn. Neurosci. 16, 1517–1535 (2004).

    Article  PubMed  Google Scholar 

  82. Sulpizio, V., Committeri, G., Lambrey, S., Berthoz, A. & Galati, G. Selective role of lingual/parahippocampal gyrus and retrosplenial complex in spatial memory across viewpoint changes relative to the environmental reference frame. Behav. Brain Res. 242, 62–75 (2013).

    Article  PubMed  Google Scholar 

  83. Vass, L.K. & Epstein, R.A. Common neural representations for visually guided reorientation and spatial imagery. Cereb. Cortex 27, 1457–1471 (2017).

    PubMed  Google Scholar 

  84. Marchette, S.A., Vass, L.K., Ryan, J. & Epstein, R.A. Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat. Neurosci. 17, 1598–1606 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Shine, J.P., Valdés-Herrera, J.P., Hegarty, M. & Wolbers, T. The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36, 6371–6381 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Baumann, O. & Mattingley, J.B. Medial parietal cortex encodes perceived heading direction in humans. J. Neurosci. 30, 12897–12901 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Vass, L.K. & Epstein, R.A. Abstract representations of location and facing direction in the human brain. J. Neurosci. 33, 6133–6142 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Meilinger, T. The network of reference frames theory: a synthesis of graphs and cognitive maps. in Spatial Cognition VI. Learning, Reasoning, and Talking about Space (eds. Freksa, C. et al.) 344–360 (Springer, 2008).

  89. Marchette, S.A., Ryan, J. & Epstein, R.A. Schematic representations of local environmental space guide goal-directed navigation. Cognition 158, 68–80 (2017).

    Article  PubMed  Google Scholar 

  90. Chen, L.L., Lin, L.-H., Green, E.J., Barnes, C.A. & McNaughton, B.L. Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101, 8–23 (1994).

    Article  CAS  PubMed  Google Scholar 

  91. Cho, J. & Sharp, P.E. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115, 3–25 (2001).

    Article  CAS  PubMed  Google Scholar 

  92. Alexander, A.S. & Nitz, D.A. Retrosplenial cortex maps the conjunction of internal and external spaces. Nat. Neurosci. 18, 1143–1151 (2015).

    Article  CAS  PubMed  Google Scholar 

  93. Sato, N., Sakata, H., Tanaka, Y.L. & Taira, M. Navigation-associated medial parietal neurons in monkeys. Proc. Natl. Acad. Sci. USA 103, 17001–17006 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Jacob, P.-Y. et al. An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex. Nat. Neurosci. 20, 173–175 (2017).

    Article  CAS  PubMed  Google Scholar 

  95. Epstein, R.A. Neural systems for visual scene recognition. Scene Vision (eds. Kveraga, K. & Bar, M.) 105–134 (2014).

  96. Marchette, S.A., Vass, L.K., Ryan, J. & Epstein, R.A. Outside looking in: landmark generalization in the human navigational system. J. Neurosci. 35, 14896–14908 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Turk-Browne, N.B., Simon, M.G. & Sederberg, P.B. Scene representations in parahippocampal cortex depend on temporal context. J. Neurosci. 32, 7202–7207 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Aminoff, E.M., Kveraga, K. & Bar, M. The role of the parahippocampal cortex in cognition. Trends Cogn. Sci. 17, 379–390 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Kamps, F.S., Lall, V. & Dilks, D.D. The occipital place area represents first-person perspective motion information through scenes. Cortex 83, 17–26 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Julian, J.B., Ryan, J., Hamilton, R.H. & Epstein, R.A. The occipital place area is causally involved in representing environmental boundaries during navigation. Curr. Biol. 26, 1104–1109 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Bonner, M.F. & Epstein, R.A. Coding of navigational affordances in the human visual system. Proc. Natl. Acad. Sci. USA 114, 4793–4798 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Aguirre, G.K. & D'Esposito, M. Topographical disorientation: a synthesis and taxonomy. Brain 122, 1613–1628 (1999).

    Article  PubMed  Google Scholar 

  103. Maguire, E.A. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand. J. Psychol. 42, 225–238 (2001).

    Article  CAS  PubMed  Google Scholar 

  104. 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. 34, 5431–5446 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kubie, J.L. & Fenton, A.A. Linear look-ahead in conjunctive cells: an entorhinal mechanism for vector-based navigation. Front. Neural Circuits 6, 20 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Bush, D., Barry, C., Manson, D. & Burgess, N. Using grid cells for navigation. Neuron 87, 507–520 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Erdem, U.M. & Hasselmo, M.E. A goal-directed spatial navigation model using forward trajectory planning based on grid cells. Eur. J. Neurosci. 35, 916–931 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Pfeiffer, B.E. & Foster, D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74–79 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Wikenheiser, A.M. & Redish, A.D. Hippocampal theta sequences reflect current goals. Nat. Neurosci. 18, 289–294 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Viard, A., Doeller, C.F., Hartley, T., Bird, C.M. & Burgess, N. Anterior hippocampus and goal-directed spatial decision making. J. Neurosci. 31, 4613–4621 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Howard, L.R. et al. The hippocampus and entorhinal cortex encode the path and Euclidean distances to goals during navigation. Curr. Biol. 24, 1331–1340 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Balaguer, J., Spiers, H., Hassabis, D. & Summerfield, C. Neural mechanisms of hierarchical planning in a virtual subway network. Neuron 90, 893–903 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Spiers, H.J. & Maguire, E.A. A navigational guidance system in the human brain. Hippocampus 17, 618–626 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Chadwick, M.J., Jolly, A.E., Amos, D.P., Hassabis, D. & Spiers, H.J. A goal direction signal in the human entorhinal/subicular region. Curr. Biol. 25, 87–92 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Javadi, A.-H. et al. Hippocampal and prefrontal processing of network topology to simulate the future. Nat. Commun. 8, 14652 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Dabaghian, Y., Brandt, V.L. & Frank, L.M. Reconceiving the hippocampal map as a topological template. Elife 3, e03476 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  117. Wu, X. & Foster, D.J. Hippocampal replay captures the unique topological structure of a novel environment. J. Neurosci. 34, 6459–6469 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Kaplan, R. et al. The neural representation of prospective choice during spatial planning and decisions. PLoS Biol. 15, e1002588 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Shallice, T. Specific impairments of planning. Phil. Trans. R. Soc. Lond. B 298, 199–209 (1982).

    Article  CAS  Google Scholar 

  120. Simon, D.A. & Daw, N.D. Neural correlates of forward planning in a spatial decision task in humans. J. Neurosci. 31, 5526–5539 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Ribas-Fernandes, J.J. et al. A neural signature of hierarchical reinforcement learning. Neuron 71, 370–379 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Schiller, D. et al. Memory and space: towards an understanding of the cognitive map. J. Neurosci. 35, 13904–13911 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Wood, E.R., Dudchenko, P.A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).

    Article  CAS  PubMed  Google Scholar 

  124. MacDonald, C.J., Lepage, K.Q., Eden, U.T. & Eichenbaum, H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71, 737–749 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Aronov, D., Nevers, R. & Tank, D.W. Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit. Nature 543, 719–722 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Quiroga, R.Q., Reddy, L., Kreiman, G., Koch, C. & Fried, I. Invariant visual representation by single neurons in the human brain. Nature 435, 1102–1107 (2005).

    Article  CAS  PubMed  Google Scholar 

  127. Tavares, R.M. et al. A map for social navigation in the human brain. Neuron 87, 231–243 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Constantinescu, A.O., O'Reilly, J.X. & Behrens, T.E.J. Organizing conceptual knowledge in humans with a gridlike code. Science 352, 1464–1468 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Schapiro, A.C., Turk-Browne, N.B., Norman, K.A. & Botvinick, M.M. Statistical learning of temporal community structure in the hippocampus. Hippocampus 26, 3–8 (2016).

    Article  PubMed  Google Scholar 

  130. Garvert, M.M., Dolan, R.J. & Behrens, T.E. A map of abstract relational knowledge in the human hippocampal-entorhinal cortex. Elife 6, e17086 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  131. Ekstrom, A.D. & Ranganath, C. Space, time, and episodic memory: the hippocampus is all over the cognitive map. Hippocampus http://dx.doi.org/10.1002/hipo.22750 (2017).

  132. Ezzyat, Y. & Davachi, L. Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity. Neuron 81, 1179–1189 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Horner, A.J., Bisby, J.A., Wang, A., Bogus, K. & Burgess, N. The role of spatial boundaries in shaping long-term event representations. Cognition 154, 151–164 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Julian, J.B., Keinath, A.T., Muzzio, I.A. & Epstein, R.A. Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice. Proc. Natl. Acad. Sci. USA 112, 6503–6508 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Anderson, M.I. & Jeffery, K.J. Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827–8835 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Bar, M. & Aminoff, E. Cortical analysis of visual context. Neuron 38, 347–358 (2003).

    Article  CAS  PubMed  Google Scholar 

  137. Fairhall, S.L. & Caramazza, A. Brain regions that represent amodal conceptual knowledge. J. Neurosci. 33, 10552–10558 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Ranganath, C. & Ritchey, M. Two cortical systems for memory-guided behaviour. Nat. Rev. Neurosci. 13, 713–726 (2012).

    Article  CAS  PubMed  Google Scholar 

  139. Lehn, H. et al. A specific role of the human hippocampus in recall of temporal sequences. J. Neurosci. 29, 3475–3484 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Milivojevic, B., Varadinov, M., Vicente Grabovetsky, A., Collin, S.H. & Doeller, C.F. Coding of event nodes and narrative context in the hippocampus. J. Neurosci. 36, 12412–12424 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Johnson, A. & Redish, A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176–12189 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Brown, T.I. et al. Prospective representation of navigational goals in the human hippocampus. Science 352, 1323–1326 (2016).

    Article  CAS  PubMed  Google Scholar 

  143. Hassabis, D. & Maguire, E.A. Deconstructing episodic memory with construction. Trends Cogn. Sci. 11, 299–306 (2007).

    Article  PubMed  Google Scholar 

  144. Redish, A.D. Beyond the Cognitive Map: From Place Cells to Episodic Memory (MIT Press, 1999).

  145. Hasselmo, M.E. How We Remember: Brain Mechanisms of Episodic Memory (MIT Press, 2011).

  146. Miller, K.J., Botvinick, M.M. & Brody, C.D. Dorsal hippocampus contributes to model-based planning. Nat. Neurosci. 20, 1269–1276 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Buckner, R.L. The role of the hippocampus in prediction and imagination. Annu. Rev. Psychol. 61, 27–48 (2010).

    Article  PubMed  Google Scholar 

  148. Buzsáki, G. & Moser, E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130–138 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Yarkoni, T., Poldrack, R.A., Nichols, T.E., Van Essen, D.C. & Wager, T.D. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 8, 665–670 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Julian, J.B., Fedorenko, E., Webster, J. & Kanwisher, N. An algorithmic method for functionally defining regions of interest in the ventral visual pathway. Neuroimage 60, 2357–2364 (2012).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank K. Jeffery for comments on the manuscript. This work was supported by the US National Institutes of Health (EY022350 and EY027047 to R.A.E.), National Science Foundation (GRFP to J.B.J.), JSMF (to H.J.S.) and Wellcome Trust (094850/Z/10/Z to H.J.S.).

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Authors and Affiliations

  1. Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Russell A Epstein & Joshua B Julian

  2. Department of Experimental Psychology, Division of Psychology and Language Sciences, Institute of Behavioural Neuroscience, University College London, London, UK

    Eva Zita Patai & Hugo J Spiers

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  1. Russell A Epstein
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  2. Eva Zita Patai
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Correspondence to Russell A Epstein or Hugo J Spiers.

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Epstein, R., Patai, E., Julian, J. et al. The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 20, 1504–1513 (2017). https://doi.org/10.1038/nn.4656

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