1932

Abstract

In mammals, the activity of neurons in the entorhinal-hippocampal network is modulated by the animal's position and its movement through space. At multiple stages of this distributed circuit, distinct populations of neurons can represent a rich repertoire of navigation-related variables like the animal's location, the speed and direction of its movements, or the presence of borders and objects. Working together, spatially tuned neurons give rise to an internal representation of space, a cognitive map that supports an animal's ability to navigate the world and to encode and consolidate memories from experience. The mechanisms by which, during development, the brain acquires the ability to create an internal representation of space are just beginning to be elucidated. In this review, we examine recent work that has begun to investigate the ontogeny of circuitry, firing patterns, and computations underpinning the representation of space in the mammalian brain.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-090922-010618
2023-07-10
2024-04-14
Loading full text...

Full text loading...

/deliver/fulltext/neuro/46/1/annurev-neuro-090922-010618.html?itemId=/content/journals/10.1146/annurev-neuro-090922-010618&mimeType=html&fmt=ahah

Literature Cited

  1. Ackman JB, Burbridge TJ, Crair MC. 2012. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 490:219–25
    [Google Scholar]
  2. Altman J, Bayer SA. 1990. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. Comp. Neurol. 301:325–42
    [Google Scholar]
  3. Andersen P. 2007. The Hippocampus Book Oxford, UK: Oxford Univ. Press
  4. Asumbisa K, Peyrache A, Trenholm S. 2022. Flexible cue anchoring strategies enable stable head direction coding in both sighted and blind animals. Nat. Commun. 13:5483
    [Google Scholar]
  5. Banino A, Barry C, Uria B, Blundell C, Lillicrap T et al. 2018. Vector-based navigation using grid-like representations in artificial agents. Nature 557:429–33
    [Google Scholar]
  6. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10:682–84
    [Google Scholar]
  7. Bassett JP, Wills TJ, Cacucci F. 2018. Self-organized attractor dynamics in the developing head direction circuit. Curr. Biol. 28:609–15.e3
    [Google Scholar]
  8. Bayer SA. 1980. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J. Comp. Neurol. 190:87–114
    [Google Scholar]
  9. Behrens TEJ, Muller TH, Whittington JCR, Mark S, Baram AB et al. 2018. What is a cognitive map? Organizing knowledge for flexible behavior. Neuron 100:490–509
    [Google Scholar]
  10. Berkes P, Orban G, Lengyel M, Fiser J. 2011. Spontaneous cortical activity reveals hallmarks of an optimal internal model of the environment. Science 331:83–87
    [Google Scholar]
  11. Bjerknes TL, Dagslott NC, Moser EI, Moser MB. 2018. Path integration in place cells of developing rats. PNAS 115:E1637–46
    [Google Scholar]
  12. Bjerknes TL, Langston RF, Kruge IU, Moser EI, Moser MB. 2015. Coherence among head direction cells before eye opening in rat pups. Curr. Biol. 25:103–8
    [Google Scholar]
  13. Bjerknes TL, Moser EI, Moser MB. 2014. Representation of geometric borders in the developing rat. Neuron 82:71–78
    [Google Scholar]
  14. 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]
  15. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5:e1000291
    [Google Scholar]
  16. Buzsaki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16:130–38
    [Google Scholar]
  17. Campbell MG, Ocko SA, Mallory CS, Low IIC, Ganguli S, Giocomo LM. 2018. Principles governing the integration of landmark and self-motion cues in entorhinal cortical codes for navigation. Nat. Neurosci. 21:1096–106
    [Google Scholar]
  18. Cavalieri D, Angelova A, Islah A, Lopez C, Bocchio M et al. 2021. CA1 pyramidal cell diversity is rooted in the time of neurogenesis. eLife 10:e69270
    [Google Scholar]
  19. Chaudhuri R, Gercek B, Pandey B, Peyrache A, Fiete I. 2019. The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep. Nat. Neurosci. 22:1512–20
    [Google Scholar]
  20. Chen G, King JA, Burgess N, O'Keefe J. 2013. How vision and movement combine in the hippocampal place code. PNAS 110:378–83
    [Google Scholar]
  21. Chen G, Manson D, Cacucci F, Wills TJ. 2016. Absence of visual input results in the disruption of grid cell firing in the mouse. Curr. Biol. 26:2335–42
    [Google Scholar]
  22. Colgin LL. 2016. Rhythms of the hippocampal network. Nat. Rev. Neurosci. 17:239–49
    [Google Scholar]
  23. Colgin LL, Moser EI, Moser MB. 2008. Understanding memory through hippocampal remapping. Trends Neurosci. 31:469–77
    [Google Scholar]
  24. Cossart R, Khazipov R. 2022. How development sculpts hippocampal circuits and function. Physiol. Rev. 102:343–78
    [Google Scholar]
  25. Cremer J, Honda T, Tang Y, Wong-Ng J, Vergassola M, Hwa T 2019. Chemotaxis as a navigation strategy to boost range expansion. Nature 575:658–63
    [Google Scholar]
  26. Curthoys IS. 1982. Postnatal developmental changes in the response of rat primary horizontal semicircular canal neurons to sinusoidal angular accelerations. Exp. Brain Res. 47:295–300
    [Google Scholar]
  27. Danglot L, Triller A, Marty S 2006. The development of hippocampal interneurons in rodents. Hippocampus 16:1032–60
    [Google Scholar]
  28. Deguchi Y, Donato F, Galimberti I, Cabuy E, Caroni P. 2011. Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat. Neurosci. 14:495–504
    [Google Scholar]
  29. Donato F. 2017. Assembling the brain from deep within. Science 358:456–57
    [Google Scholar]
  30. Donato F, Alberini CM, Amso D, Dragoi G, Dranovsky A, Newcombe NS. 2021. The ontogeny of hippocampus-dependent memories. J. Neurosci. 41:920–26
    [Google Scholar]
  31. Donato F, Jacobsen RI, Moser MB, Moser EI. 2017. Stellate cells drive maturation of the entorhinal-hippocampal circuit. Science 355:eaai8178
    [Google Scholar]
  32. Drieu C, Zugaro M. 2019. Hippocampal sequences during exploration: mechanisms and functions. Front. Cell Neurosci. 13:232
    [Google Scholar]
  33. Druckmann S, Feng L, Lee B, Yook C, Zhao T et al. 2014. Structured synaptic connectivity between hippocampal regions. Neuron 81:629–40
    [Google Scholar]
  34. Dudchenko PA, Wallace D. 2018. Neuroethology of spatial cognition. Curr. Biol. 28:R988–92
    [Google Scholar]
  35. Etienne AS, Jeffery KJ. 2004. Path integration in mammals. Hippocampus 14:180–92
    [Google Scholar]
  36. Farooq U, Dragoi G. 2019. Emergence of preconfigured plastic time-compressed sequences in early postnatal development. Science 363:168–73
    [Google Scholar]
  37. Foster DJ, Wilson MA. 2006. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–83
    [Google Scholar]
  38. Fuhs MC, Touretzky DS. 2006. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26:4266–76
    [Google Scholar]
  39. Fyhn M, Hafting T, Treves A, Moser MB, Moser EI. 2007. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446:190–94
    [Google Scholar]
  40. Gardner RJ, Hermansen E, Pachitariu M, Burak Y, Baas NA et al. 2022. Toroidal topology of population activity in grid cells. Nature 602:123–28
    [Google Scholar]
  41. Gardner RJ, Lu L, Wernle T, Moser MB, Moser EI. 2019. Correlation structure of grid cells is preserved during sleep. Nat. Neurosci. 22:598–608
    [Google Scholar]
  42. Ge X, Zhang K, Gribizis A, Hamodi AS, Sabino AM, Crair MC. 2021. Retinal waves prime visual motion detection by simulating future optic flow. Science 373:abd0830
    [Google Scholar]
  43. Gil M, Ancau M, Schlesiger MI, Neitz A, Allen K et al. 2018. Impaired path integration in mice with disrupted grid cell firing. Nat. Neurosci. 21:81–91
    [Google Scholar]
  44. Gillespie AK, Astudillo Maya DA, Denovellis EL, Liu DF, Kastner DB et al. 2021. Hippocampal replay reflects specific past experiences rather than a plan for subsequent choice. Neuron 109:3149–63.e6
    [Google Scholar]
  45. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. 2009. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12:1222–23
    [Google Scholar]
  46. Gomez-Di Cesare CM, Smith KL, Rice FL, Swann JW. 1997. Axonal remodeling during postnatal maturation of CA3 hippocampal pyramidal neurons. J. Comp. Neurol. 384:165–80
    [Google Scholar]
  47. Gonzalo Cogno S, Obenhaus HA, Jacobsen RI, Donato F, Moser M-B, Moser EI 2022. Minute-scale oscillatory sequences in medial entorhinal cortex. bioRxiv 2022.05.02.490273. https://doi.org/10.1101/2022.05.02.490273
    [Crossref]
  48. Gothard KM, Skaggs WE, McNaughton BL. 1996. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16:8027–40
    [Google Scholar]
  49. Gregory EH, Pfaff DW. 1971. Development of olfactory-guided behavior in infant rats. Physiol. Behav. 6:573–76
    [Google Scholar]
  50. Gretenkord S, Kostka JK, Hartung H, Watznauer K, Fleck D et al. 2019. Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice. PLOS Biol. 17:e2006994
    [Google Scholar]
  51. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6
    [Google Scholar]
  52. Hahnloser RH. 2003. Emergence of neural integration in the head-direction system by visual supervision. Neuroscience 120:877–91
    [Google Scholar]
  53. Hardcastle K, Ganguli S, Giocomo LM. 2015. Environmental boundaries as an error correction mechanism for grid cells. Neuron 86:827–39
    [Google Scholar]
  54. Hardcastle K, Maheswaranathan N, Ganguli S, Giocomo LM. 2017. A multiplexed, heterogeneous, and adaptive code for navigation in medial entorhinal cortex. Neuron 94:375–87.e7
    [Google Scholar]
  55. Hartley T, Burgess N, Lever C, Cacucci F, O'Keefe J. 2000. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10:369–79
    [Google Scholar]
  56. Hensch TK. 2005. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6:877–88
    [Google Scholar]
  57. Heys JG, Dombeck DA. 2018. Evidence for a subcircuit in medial entorhinal cortex representing elapsed time during immobility. Nat. Neurosci. 21:1574–82
    [Google Scholar]
  58. Hoydal OA, Skytoen ER, Andersson SO, Moser MB, Moser EI. 2019. Object-vector coding in the medial entorhinal cortex. Nature 568:400–4
    [Google Scholar]
  59. Huszár R, Zhang Y, Blockus H, Buzsaki G. 2022. Preconfigured dynamics in the hippocampus are guided by embryonic birthdate and rate of neurogenesis. Nat. Neurosci. 25:1201–12
    [Google Scholar]
  60. Karlsson KA, Mohns EJ, di Prisco GV, Blumberg MS. 2006. On the co-occurrence of startles and hippocampal sharp waves in newborn rats. Hippocampus 16:959–65
    [Google Scholar]
  61. Knierim JJ, Zhang K. 2012. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35:267–85
    [Google Scholar]
  62. 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]
  63. Kostka JK, Gretenkord S, Spehr M, Hanganu-Opatz IL. 2020. Bursting mitral cells time the oscillatory coupling between olfactory bulb and entorhinal networks in neonatal mice. J. Physiol. 598:5753–69
    [Google Scholar]
  64. Kropff E, Carmichael JE, Moser MB, Moser EI. 2015. Speed cells in the medial entorhinal cortex. Nature 523:419–24
    [Google Scholar]
  65. Kruge I, Waaga T, Wernle T, Moser EI, Moser M-B. 2014. Grid cells require experience with local boundaries during development Paper presented at the Annual Meeting of the Society for Neuroscience Washington, DC: Novemb. 15
  66. Landers M, Zeigler HP. 2006. Development of rodent whisking: trigeminal input and central pattern generation. Somatosens. Mot. Res. 23:1–10
    [Google Scholar]
  67. 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]
  68. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G. 2002. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049–52
    [Google Scholar]
  69. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–66
    [Google Scholar]
  70. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. 2005. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619–23
    [Google Scholar]
  71. 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]
  72. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. 2011. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71:737–49
    [Google Scholar]
  73. Martini FJ, Guillamon-Vivancos T, Moreno-Juan V, Valdeolmillos M, Lopez-Bendito G. 2021. Spontaneous activity in developing thalamic and cortical sensory networks. Neuron 109:2519–34
    [Google Scholar]
  74. Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S et al. 2010. A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J. Comp. Neurol. 518:4479–90
    [Google Scholar]
  75. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. 2006. Path integration and the neural basis of the ‘cognitive map. ’. Nat. Rev. Neurosci. 7:663–78
    [Google Scholar]
  76. Meister M, Wong RO, Baylor DA, Shatz CJ. 1991. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939–43
    [Google Scholar]
  77. Miao C, Cao Q, Ito HT, Yamahachi H, Witter MP et al. 2015. Hippocampal remapping after partial inactivation of the medial entorhinal cortex. Neuron 88:590–603
    [Google Scholar]
  78. Mittelstaedt M-L, Mittelstaedt H. 1980. Homing by path integration in a mammal. Naturwissenschaften 67:566–67
    [Google Scholar]
  79. Mohns EJ, Blumberg MS. 2008. Synchronous bursts of neuronal activity in the developing hippocampus: modulation by active sleep and association with emerging gamma and theta rhythms. J. Neurosci. 28:10134–44
    [Google Scholar]
  80. Monaco JD, Abbott LF. 2011. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J. Neurosci. 31:9414–25
    [Google Scholar]
  81. Muessig L, Hauser J, Wills TJ, Cacucci F. 2015. A developmental switch in place cell accuracy coincides with grid cell maturation. Neuron 86:1167–73
    [Google Scholar]
  82. Muessig L, Hauser J, Wills TJ, Cacucci F. 2016. Place cell networks in pre-weanling rats show associative memory properties from the onset of exploratory behavior. Cereb. Cortex 26:3627–36
    [Google Scholar]
  83. Muessig L, Lasek M, Varsavsky I, Cacucci F, Wills TJ. 2019. Coordinated emergence of hippocampal replay and theta sequences during post-natal development. Curr. Biol. 29:834–40.e4
    [Google Scholar]
  84. Muller RU, Kubie JL. 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7:1951–68
    [Google Scholar]
  85. Newcombe NS. 2019. Navigation and the developing brain. J. Exp. Biol. 222:Suppl. 1jeb186460
    [Google Scholar]
  86. 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]
  87. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map New York: Clarendon Press
  88. O'Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–30
    [Google Scholar]
  89. Olafsdottir HF, Bush D, Barry C. 2018. The role of hippocampal replay in memory and planning. Curr. Biol. 28:R37–50
    [Google Scholar]
  90. Palmer L, Lynch G. 2010. A Kantian view of space. Science 328:1487–88
    [Google Scholar]
  91. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G. 2008. Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–27
    [Google Scholar]
  92. Peyrache A, Lacroix MM, Petersen PC, Buzsaki G. 2015. Internally organized mechanisms of the head direction sense. Nat. Neurosci. 18:569–75
    [Google Scholar]
  93. Pfeiffer BE, Foster DJ. 2013. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:74–79
    [Google Scholar]
  94. Poulter S, Hartley T, Lever C. 2018. The neurobiology of mammalian navigation. Curr. Biol. 28:R1023–42
    [Google Scholar]
  95. Rochefort NL, Garaschuk O, Milos RI, Narushima M, Marandi N et al. 2009. Sparsification of neuronal activity in the visual cortex at eye-opening. PNAS 106:15049–54
    [Google Scholar]
  96. 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]
  97. Scott RC, Richard GR, Holmes GL, Lenck-Santini PP. 2011. Maturational dynamics of hippocampal place cells in immature rats. Hippocampus 21:347–53
    [Google Scholar]
  98. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL. 1995. A model of the neural basis of the rat's sense of direction. Adv. Neural Inf. Process. Syst. 7:173–80
    [Google Scholar]
  99. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149–72
    [Google Scholar]
  100. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322:1865–68
    [Google Scholar]
  101. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: a mathematical model. Hippocampus 16:1026–31
    [Google Scholar]
  102. Soriano E, Cobas A, Fairen A. 1986. Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Brain Res. 395:88–92
    [Google Scholar]
  103. Stemmler M, Mathis A, Herz AV. 2015. Connecting multiple spatial scales to decode the population activity of grid cells. Sci. Adv. 1:e1500816
    [Google Scholar]
  104. Super H, Soriano E. 1994. The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J. Comp. Neurol. 344:101–20
    [Google Scholar]
  105. Sürmeli G, Marcu DC, McClure C, Garden DLF, Pastoll H, Nolan MF. 2015. Molecularly defined circuitry reveals input-output segregation in deep layers of the medial entorhinal cortex. Neuron 88:1040–53
    [Google Scholar]
  106. 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]
  107. Tan HM, Wills TJ, Cacucci F. 2017. The development of spatial and memory circuits in the rat. Wiley Interdiscip. Rev. Cogn. Sci. 8:e1424
    [Google Scholar]
  108. 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]
  109. 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]
  110. Tolman EC. 1948. Cognitive maps in rats and men. Psychol. Rev. 55:189–208
    [Google Scholar]
  111. Travaglia A, Bisaz R, Sweet ES, Blitzer RD, Alberini CM. 2016. Infantile amnesia reflects a developmental critical period for hippocampal learning. Nat. Neurosci. 19:1225–33
    [Google Scholar]
  112. Trettel SG, Trimper JB, Hwaun E, Fiete IR, Colgin LL. 2019. Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors. Nat. Neurosci. 22:609–17
    [Google Scholar]
  113. Treves A, Rolls ET. 1994. Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–91
    [Google Scholar]
  114. Tsao A, Sugar J, Lu L, Wang C, Knierim JJ et al. 2018. Integrating time from experience in the lateral entorhinal cortex. Nature 561:57–62
    [Google Scholar]
  115. Valeeva G, Janackova S, Nasretdinov A, Rychkova V, Makarov R et al. 2019. Emergence of coordinated activity in the developing entorhinal-hippocampal network. Cereb. Cortex 29:906–20
    [Google Scholar]
  116. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030–34
    [Google Scholar]
  117. van Strien NM, Cappaert NL, Witter MP. 2009. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 10:272–82
    [Google Scholar]
  118. Villette V, Malvache A, Tressard T, Dupuy N, Cossart R. 2015. Internally recurring hippocampal sequences as a population template of spatiotemporal information. Neuron 88:357–66
    [Google Scholar]
  119. Waaga T, Agmon H, Normand VA, Nagelhus A, Gardner RJ et al. 2022. Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues. Neuron 110:1843–56.e6
    [Google Scholar]
  120. Wills TJ, Barry C, Cacucci F. 2012. The abrupt development of adult-like grid cell firing in the medial entorhinal cortex. Front. Neural Circuits 6:21
    [Google Scholar]
  121. 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]
  122. Wills TJ, Muessig L, Cacucci F. 2014. The development of spatial behaviour and the hippocampal neural representation of space. Philos. Trans. R. Soc. B 369:20130409
    [Google Scholar]
  123. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055–58
    [Google Scholar]
  124. Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265:676–79
    [Google Scholar]
  125. Winter SS, Clark BJ, Taube JS. 2015. Spatial navigation. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347:870–74
    [Google Scholar]
  126. Witter MP, Moser EI. 2006. Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci. 29:671–78
    [Google Scholar]
  127. 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]
  128. Zugaro MB, Arleo A, Berthoz A, Wiener SI. 2003. Rapid spatial reorientation and head direction cells. J. Neurosci. 23:3478–82
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-090922-010618
Loading
/content/journals/10.1146/annurev-neuro-090922-010618
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error