1932

Abstract

The world has a complex, three-dimensional (3-D) spatial structure, but until recently the neural representation of space was studied primarily in planar horizontal environments. Here we review the emerging literature on allocentric spatial representations in 3-D and discuss the relations between 3-D spatial perception and the underlying neural codes. We suggest that the statistics of movements through space determine the topology and the dimensionality of the neural representation, across species and different behavioral modes. We argue that hippocampal place-cell maps are metric in all three dimensions, and might be composed of 2-D and 3-D fragments that are stitched together into a global 3-D metric representation via the 3-D head-direction cells. Finally, we propose that the hippocampal formation might implement a neural analogue of a Kalman filter, a standard engineering algorithm used for 3-D navigation.

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2016-07-08
2024-06-24
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Literature Cited

  1. Alme CB, Miao C, Jezek K, Treves A, Moser EI, Moser M-B. 2014. Place cells in the hippocampus: eleven maps for eleven rooms. PNAS 111:18428–35 [Google Scholar]
  2. Bjerknes TL, Langston RF, Kruge IU, Moser EI, Moser M-B. 2015. Coherence among head direction cells before eye opening in rat pups. Curr. Biol. 25:103–8 [Google Scholar]
  3. Blohm G, Keith GP, Crawford JD. 2009. Decoding the cortical transformations for visually guided reaching in 3D space. Cereb. Cortex 19:1372–93 [Google Scholar]
  4. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D. et al. 2013. Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16:309–17 [Google Scholar]
  5. Bousquet O, Balakrishnan K, Honavar V. 1998. Is the hippocampus a Kalman filter?. Proc. Pac. Symp. Biocomput. 1998:657–68 [Google Scholar]
  6. Brandt T, Huber M, Schramm H, Kugler G, Dieterich M, Glasauer S. 2015. “Taller and shorter”: Human 3-D spatial memory distorts familiar multilevel buildings. PLOS ONE 10:e0141257 [Google Scholar]
  7. Breveglieri R, Hadjidimitrakis K, Bosco A, Sabatini SP, Galletti C, Fattori P. 2012. Eye position encoding in three-dimensional space: integration of version and vergence signals in the medial posterior parietal cortex. J. Neurosci. 32:159–69 [Google Scholar]
  8. Brown W, Bäcker A. 2006. Optimal neuronal tuning for finite stimulus spaces. Neural Comput. 18:1511–26 [Google Scholar]
  9. Brun VH, Leutgeb S, Wu H-Q, Schwarcz R, Witter MP. et al. 2008. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57:290–302 [Google Scholar]
  10. Bueti D, Walsh V. 2009. The parietal cortex and the representation of time, space, number and other magnitudes. Philos. Trans. R. Soc. B 364:1831–40 [Google Scholar]
  11. Buneo CA, Jarvis MR, Batista AP, Andersen RA. 2002. Direct visuomotor transformations for reaching. Nature 416:632–36 [Google Scholar]
  12. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5:e1000291 [Google Scholar]
  13. Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS. 2003. Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23:9719–31 [Google Scholar]
  14. Calton JL, Taube JS. 2005. Degradation of head direction cell activity during inverted locomotion. J. Neurosci. 25:2420–28 [Google Scholar]
  15. Carpenter F, Manson D, Jeffery K, Burgess N, Barry C. 2015. Grid cells form a global representation of connected environments. Curr. Biol. 25:1176–82 [Google Scholar]
  16. Channon AJ, Crompton RH, Günther MM, D'Août K, Vereecke EE. 2010. The biomechanics of leaping in gibbons. Am. J. Phys. Anthropol. 143:403–16 [Google Scholar]
  17. Chen X, DeAngelis GC, Angelaki DE. 2013. Diverse spatial reference frames of vestibular signals in parietal cortex. Neuron 80:1310–21 [Google Scholar]
  18. Chen Z, Kloosterman F, Brown EN, Wilson MA. 2012. Uncovering spatial topology represented by rat hippocampal population neuronal codes. J. Comput. Neurosci. 33:227–55 [Google Scholar]
  19. Childs SB, Buchler ER. 1981. Perception of simulated stars by Eptesicus fuscus (Vespertilionidae): a potential navigational mechanism. Anim. Behav. 29:1028–35 [Google Scholar]
  20. Clark BJ, Taube JS. 2011. Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex. Hippocampus 21:767–82 [Google Scholar]
  21. Cohen RG, Rosenbaum DA. 2004. Where grasps are made reveals how grasps are planned: generation and recall of motor plans. Exp. Brain Res. 157:486–95 [Google Scholar]
  22. Cowen SL, Nitz DA. 2014. Repeating firing fields of CA1 neurons shift forward in response to increasing angular velocity. J. Neurosci. 34:232–41 [Google Scholar]
  23. Curto C, Itskov V. 2008. Cell groups reveal structure of stimulus space. PLOS Comput. Biol. 4:e1000205 [Google Scholar]
  24. Dabaghian Y, Brandt VL, Frank LM. 2014. Reconceiving the hippocampal map as a topological template. eLife 3:e03476 [Google Scholar]
  25. Dan Y, Poo M-M. 2004. Spike timing-dependent plasticity of neural circuits. Neuron 44:23–30 [Google Scholar]
  26. Davis VA, Holbrook RI, Schumacher S, Guilford T, de Perera TB. 2014. Three-dimensional spatial cognition in a benthic fish, Corydoras aeneus. Behav. Process. 109:151–56 [Google Scholar]
  27. Denève S, Duhamel J-R, Pouget A. 2007. Optimal sensorimotor integration in recurrent cortical networks: a neural implementation of Kalman filters. J. Neurosci. 27:5744–56 [Google Scholar]
  28. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T. et al. 2009. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12:1325–32 [Google Scholar]
  29. Domnisoru C, Kinkhabwala AA, Tank DW. 2013. Membrane potential dynamics of grid cells. Nature 495:199–204 [Google Scholar]
  30. Dunbar DC, Macpherson JM, Simmons RW, Zarcades A. 2008. Stabilization and mobility of the head, neck and trunk in horses during overground locomotion: comparisons with humans and other primates. J. Exp. Biol. 211:3889–907 [Google Scholar]
  31. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N. 2015. Three-dimensional head-direction coding in the bat brain. Nature 517:159–64 [Google Scholar]
  32. Foley JM. 1980. Binocular distance perception. Psychol. Rev. 87:411–34 [Google Scholar]
  33. Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N. 2015. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat. Rev. Neurosci. 16:94–108 [Google Scholar]
  34. Golob EJ, Taube JS. 1999. Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration. J. Neurosci. 19:7198–211 [Google Scholar]
  35. Grobéty M-C, Schenk F. 1992. Spatial learning in a three-dimensional maze. Anim. Behav. 43:1011–20 [Google Scholar]
  36. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6 [Google Scholar]
  37. Hales JB, Schlesiger MI, Leutgeb JK, Squire LR, Leutgeb S, Clark RE. 2014. Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. Cell Rep. 9:893–901 [Google Scholar]
  38. Hayman RMA, Casali G, Wilson JJ, Jeffery KJ. 2015. Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding. Front. Psychol. 6:925 [Google Scholar]
  39. Hayman RMA, Verriotis MA, Jovalekic A, Fenton AA, Jeffery KJ. 2011. Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat. Neurosci. 14:1182–88 [Google Scholar]
  40. Hedrick K, Zhang K. 2013. Megamap: Continuous attractor model for place cells representing large environments. Program No. 578.01. Presented at Soc. Neurosci. Annu. Meet., Nov. 12, San Diego [Google Scholar]
  41. Honda Y, Ishizuka N. 2004. Organization of connectivity of the rat presubiculum: I. Efferent projections to the medial entorhinal cortex. J. Comp. Neurol. 473:463–84 [Google Scholar]
  42. Horiuchi TK, Moss CF. 2015. Grid cells in 3-D: reconciling data and models. Hippocampus 25:1489–1500 [Google Scholar]
  43. Iriarte-Díaz J, Swartz SM. 2008. Kinematics of slow turn maneuvering in the fruit bat Cynopterus brachyotis. J. Exp. Biol. 211:3478–89 [Google Scholar]
  44. Jacob P-Y, Poucet B, Liberge M, Save E, Sargolini F. 2014. Vestibular control of entorhinal cortex activity in spatial navigation. Front. Integr. Neurosci. 8:38 [Google Scholar]
  45. Jeffery KJ, Anand RL, Anderson MI. 2005. A role for terrain slope in orienting hippocampal place fields. Exp. Brain Res. 169:218–25 [Google Scholar]
  46. Jeffery KJ, Jovalekic A, Verriotis M, Hayman R. 2013. Navigating in a three-dimensional world. Behav. Brain Sci. 36:523–87 [Google Scholar]
  47. Jeffery KJ, Wilson JJ, Casali G, Hayman RM. 2015. Neural encoding of large-scale three-dimensional space—properties and constraints. Front. Psychol. 6:927 [Google Scholar]
  48. Jovalekic A, Hayman R, Becares N, Reid H, Thomas G. et al. 2011. Horizontal biases in rats' use of three-dimensional space. Behav. Brain Res. 222:279–88 [Google Scholar]
  49. Kaplan ED, Hegarty C. 2005. Understanding GPS: Principles and Applications Boston: Artech House, 2nd ed.. [Google Scholar]
  50. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S. et al. 2008. Finite scale of spatial representation in the hippocampus. Science 321:140–43 [Google Scholar]
  51. Klatzky RL, Giudice NA. 2013. The planar mosaic fails to account for spatially directed action. Behav. Brain Sci. 36:554–55 [Google Scholar]
  52. Kleven H, Gatome W, Las L, Ulanovsky N, Witter MP. 2014. Organization of entorhinal-hippocampal projections in the Egyptian fruit bat FENS-3642, Poster No. F045. Presented at FENS Forum Neurosci., July 6, Milan [Google Scholar]
  53. Knierim JJ, Hamilton DA. 2011. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol. Rev. 91:1245–79 [Google Scholar]
  54. Knierim JJ, McNaughton BL. 2001. Hippocampal place-cell firing during movement in three-dimensional space. J. Neurophysiol. 85:105–16 [Google Scholar]
  55. Knierim JJ, McNaughton BL, Poe GR. 2000. Three-dimensional spatial selectivity of hippocampal neurons during space flight. Nat. Neurosci. 3:209–10 [Google Scholar]
  56. Knierim JJ, Rao G. 2003. Distal landmarks and hippocampal place cells: effects of relative translation versus rotation. Hippocampus 13:604–17 [Google Scholar]
  57. Ko H, Cossell L, Baragli C, Antolik J, Clopath C. et al. 2013. The emergence of functional microcircuits in visual cortex. Nature 496:96–100 [Google Scholar]
  58. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. 2011. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332:592–95 [Google Scholar]
  59. Kress D, Egelhaaf M. 2012. Head and body stabilization in blowflies walking on differently structured substrates. J. Exp. Biol. 215:1523–32 [Google Scholar]
  60. Kropff E, Carmichael JE, Moser M-B, Moser EI. 2015. Speed cells in the medial entorhinal cortex. Nature 523:419–424 [Google Scholar]
  61. Kruge IU, Wernle T, Moser EI, Moser M-B. 2013. Grid cells of animals raised in spherical environments Program No. 769.14. Presented at Soc. Neurosci. Annu. Meet., Nov. 13, San Diego [Google Scholar]
  62. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL. et al. 2010. Development of the spatial representation system in the rat. Science 328:1576–80 [Google Scholar]
  63. Laurens J, Meng H, Angelaki DE. 2013. Neural representation of orientation relative to gravity in the macaque cerebellum. Neuron 80:1508–18 [Google Scholar]
  64. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N. 2009. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29:9771–77 [Google Scholar]
  65. Ludvig N, Tang HM, Gohil BC, Botero JM. 2004. Detecting location-specific neuronal firing rate increases in the hippocampus of freely-moving monkeys. Brain Res. 1014:97–109 [Google Scholar]
  66. Mathis A, Stemmler MB, Herz AVM. 2015. Probable nature of higher-dimensional symmetries underlying mammalian grid-cell activity patterns. eLife 4:e05979 [Google Scholar]
  67. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B. 2006. Path integration and the neural basis of the ‘cognitive map.’. Nat. Rev. Neurosci. 7:663–78 [Google Scholar]
  68. Mohamed AH, Schwarz KP. 1999. Adaptive Kalman filtering for INS/GPS. J. Geodesy 73:193–203 [Google Scholar]
  69. Montello DR, Pick HL. 1993. Integrating knowledge of vertically aligned large-scale spaces. Environ. Behav. 25:457–84 [Google Scholar]
  70. Moser EI, Kropff E, Moser M-B. 2008. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31:69–89 [Google Scholar]
  71. Nitz DA. 2012. Spaces within spaces: rat parietal cortex neurons register position across three reference frames. Nat. Neurosci. 15:1365–67 [Google Scholar]
  72. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–28 [Google Scholar]
  73. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:171–75 [Google Scholar]
  74. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map Oxford, UK: Clarendon [Google Scholar]
  75. Poucet B. 1993. Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol. Rev. 100:163–82 [Google Scholar]
  76. Pozzo T, Berthoz A, Lefort L. 1990. Head stabilization during various locomotor tasks in humans. Exp. Brain Res. 82:97–106 [Google Scholar]
  77. Ranck JB. 1984. Head-direction cells in the deep cell layers of dorsal presubiculum in freely moving rats. Soc. Neurosci. Abstr. 10:599 [Google Scholar]
  78. Rosenberg A, Cowan NJ, Angelaki DE. 2013. The visual representation of 3D object orientation in parietal cortex. J. Neurosci. 33:19352–61 [Google Scholar]
  79. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP. et al. 2006. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–62 [Google Scholar]
  80. Singer AC, Karlsson MP, Nathe AR, Carr MF, Frank LM. 2010. Experience-dependent development of coordinated hippocampal spatial activity representing the similarity of related locations. J. Neurosci. 30:11586–604 [Google Scholar]
  81. Solstad T, Boccara CN, Kropff E, Moser M-B, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322:1865–68 [Google Scholar]
  82. Spiers HJ, Hayman RMA, Jovalekic A, Marozzi E, Jeffery KJ. 2015. Place field repetition and purely local remapping in a multicompartment environment. Cereb. Cortex 25:10–25 [Google Scholar]
  83. Stackman RW, Taube JS. 1998. Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J. Neurosci. 18:9020–37 [Google Scholar]
  84. Stackman RW, Tullman ML, Taube JS. 2000. Maintenance of rat head direction cell firing during locomotion in the vertical plane. J. Neurophysiol. 83:393–405 [Google Scholar]
  85. Stella F, Cerasti E, Treves A. 2013. Unveiling the metric structure of internal representations of space. Front. Neural Circuits 7:81 [Google Scholar]
  86. Stella F, Treves A. 2015. The self-organization of grid cells in 3D. eLife 4:e05913 [Google Scholar]
  87. Stensola T, Stensola H, Moser M-B, Moser EI. 2015. Shearing-induced asymmetry in entorhinal grid cells. Nature 518:207–12 [Google Scholar]
  88. Tan HM, Bassett JP, O'Keefe J, Cacucci F, Wills TJ. 2015. The development of the head direction system before eye opening in the rat. Curr. Biol. 25:479–83 [Google Scholar]
  89. Taube JS. 2007. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30:181–207 [Google Scholar]
  90. Taube JS, Muller RU, Ranck JB Jr. 1990a. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10:420–35 [Google Scholar]
  91. Taube JS, Muller RU, Ranck JB Jr. 1990b. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10:436–47 [Google Scholar]
  92. Taube JS, Stackman RW, Calton JL, Oman CM. 2004. Rat head direction cell responses in zero-gravity parabolic flight. J. Neurophysiol. 92:2887–997 [Google Scholar]
  93. Taube JS, Wang SS, Kim SY, Frohardt RJ. 2013. Updating of the spatial reference frame of head direction cells in response to locomotion in the vertical plane. J. Neurophysiol. 109:873–88 [Google Scholar]
  94. Thibault G, Pasqualotto A, Vidal M, Droulez J, Berthoz A. 2012. How does horizontal and vertical navigation influence spatial memory of multifloored environments?. Atten. Percept. Psychophys. 75:10–15 [Google Scholar]
  95. Tolman EC. 1948. Cognitive maps in rats and men. Psychol. Rev. 55:189–208 [Google Scholar]
  96. Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell'Omo G, Ulanovsky N. 2011. Large-scale navigational map in a mammal. PNAS 108:E718–24 [Google Scholar]
  97. Ulanovsky N. 2011. Neuroscience: How is three-dimensional space encoded in the brain?. Curr. Biol. 21:R886–88 [Google Scholar]
  98. Ulanovsky N, Finkelstein A. 2013. Hippocampal representation of multiple spatial scales during 2D versus 3D navigation in bats Program No. 863.02. Presented at Soc. Neurosci. Annu. Meet., Nov. 13, San Diego [Google Scholar]
  99. Ulanovsky N, Moss CF. 2007. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10:224–33 [Google Scholar]
  100. Ulanovsky N, Moss CF. 2011. Dynamics of hippocampal spatial representation in echolocating bats. Hippocampus 21:150–61 [Google Scholar]
  101. Urdapilleta E, Troiani F, Stella F, Treves A. 2015. Can rodents conceive hyperbolic spaces?. J. R. Soc. Interface 12:20141214 [Google Scholar]
  102. Valerio S, Clark BJ, Chan JHM, Frost CP, Harris MJ, Taube JS. 2010. Directional learning, but no spatial mapping by rats performing a navigational task in an inverted orientation. Neurobiol. Learn. Mem. 93:495–505 [Google Scholar]
  103. Valerio S, Taube JS. 2012. Path integration: how the head direction signal maintains and corrects spatial orientation. Nat. Neurosci. 15:1445–53 [Google Scholar]
  104. Viollet S, Zeil J. 2013. Feed-forward and visual feedback control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera). J. Exp. Biol. 216:1280–91 [Google Scholar]
  105. Wallace DJ, Greenberg DS, Sawinski J, Rulla S, Notaro G, Kerr JND. 2013. Rats maintain an overhead binocular field at the expense of constant fusion. Nature 498:65–69 [Google Scholar]
  106. Wallraff HG. 2005. Avian Navigation: Pigeon Homing as a Paradigm Berlin/Heidelberg, Ger: Springer-Verlag [Google Scholar]
  107. Wang RF. 2012. Theories of spatial representations and reference frames: What can configuration errors tell us?. Psychon. Bull. Rev. 19:575–87 [Google Scholar]
  108. Whitlock JR, Derdikman D. 2012. Head direction maps remain stable despite grid map fragmentation. Front. Neural Circuits 6:9 [Google Scholar]
  109. Whitlock JR, Pfuhl G, Dagslott N, Moser M-B, Moser EI. 2012. Functional split between parietal and entorhinal cortices in the rat. Neuron 73:789–802 [Google Scholar]
  110. Whitlock JR, Sutherland RJ, Witter MP, Moser M-B, Moser EI. 2008. Navigating from hippocampus to parietal cortex. PNAS 105:14755–62 [Google Scholar]
  111. Wills TJ, Cacucci F, Burgess N, O'Keefe J. 2010. Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–76 [Google Scholar]
  112. Wilson JJ, Harding E, Fortier M, James B, Donnett M. et al. 2015. Spatial learning by mice in three dimensions. Behav. Brain Res. 289:125–32 [Google Scholar]
  113. Wilson PN, Foreman N, Stanton D, Duffy H. 2004. Memory for targets in a multilevel simulated environment: evidence for vertical asymmetry in spatial memory. Mem. Cogn. 32:283–97 [Google Scholar]
  114. Winter SS, Clark BJ, Taube JS. 2015. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347:870–74 [Google Scholar]
  115. Wolpert DM, Ghahramani Z. 2000. Computational principles of movement neuroscience. Nat. Neurosci. 3:1212–17 [Google Scholar]
  116. Wolpert DM, Ghahramani Z, Jordan MI. 1995. An internal model for sensorimotor integration. Science 269:1880–82 [Google Scholar]
  117. Yartsev MM, Ulanovsky N. 2013. Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–72 [Google Scholar]
  118. Yoder RM, Clark BJ, Brown JE, Lamia MV, Valerio S. et al. 2011. Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes. J. Neurophysiol. 105:2989–3001 [Google Scholar]
  119. Yoon K, Buice MA, Barry C, Hayman R, Burgess N, Fiete IR. 2013. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 16:1077–84 [Google Scholar]
  120. Yoon K, Lewallen S, Kinkhabwala AA, Tank DW, Fiete IR. 2016. Grid cell responses in 1D environments assessed as slices through a 2D lattice. Neuron 89:1086–89 [Google Scholar]
  121. Zhang K, Sejnowski TJ. 1999. Neuronal tuning: to sharpen or broaden?. Neural Comput. 11:75–84 [Google Scholar]
  122. Zugaro MB, Berthoz A, Wiener SI. 2001. Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J. Neurosci. 21:RC154 [Google Scholar]
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