How environment and self-motion combine in neural representations of space

Journal of Physiology

Volumn 594, Issue 22, 2016, Pages 6535-6546

  Evans, Talfan ^a,b,c   Bicanski, Andrej ^b,c   Bush, Daniel ^b,c   Burgess, Neil ^b,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASSOCIATION; DEPTH PERCEPTION; FIRING RATE; HEAD MOVEMENT; HIPPOCAMPUS; MOVEMENT (PHYSIOLOGY); NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SPATIAL ORIENTATION; ANIMAL; BIOLOGICAL MODEL; ENVIRONMENT; HEAD; HUMAN; MOTION; ORIENTATION; PHYSIOLOGY;

ANIMALS; ENVIRONMENT; HEAD; HUMANS; MODELS, NEUROLOGICAL; MOTION; NEURONS; ORIENTATION; SPACE PERCEPTION;

EID: 84953791669     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270666     Document Type: Article

References (99)

1. Anderson MI & Jeffery KJ (2003). Heterogeneous modulation of place cell firing by changes in context. J Neurosci 23, 8827–8835.
2. Barry C & Burgess N (2014). Neural mechanisms of self-location. Curr Biol 24, R330–R339.
3. Barry C, Ginzberg LL, O'Keefe J & Burgess N (2012). Grid cell firing patterns signal environmental novelty by expansion. Proc Natl Acad Sci USA 109, 17687–17692.
4. Barry C, Hayman R, Burgess N & Jeffery K (2007). Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10, 682–684.
5. Barry C, Lever C, Hayman R, Hartley T, Burton S, O'Keefe J, Jeffery K & Burgess N (2006). The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci 17, 71–97.
6. Bassett JP & Taube JS (2001). Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21, 5740–5751.
7. Bassett JP, Tullman ML & Taube JS (2007). Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. J Neurosci 27, 7564–7577.
8. Blair HT, Cho J & Sharp PE (1998). Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron 21, 1387–1397.
9. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI & Moser M-B (2010). Grid cells in pre- and parasubiculum. Nat Neurosci 13, 987–994.
10. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI & Moser M-B (2013). Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16, 309–317.
11. Bostock E, Muller RU & Kubie JL (1991). Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193–205.
12. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K & Hasselmo ME (2011). Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595–599.
13. Brun VH, Leutgeb S, Wu H-Q, Schwarcz R, Witter MP, Moser EI & Moser M-B (2008). Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57, 290–302.
14. Brun VH, Otnæss MK, Molden S, Steffenach H-A, Witter MP, Moser M-B & Moser EI (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243–2246.
15. Burgess N, Barry C & O'Keefe J (2007). An oscillatory interference model of grid cell firing. Hippocampus 17, 801–812.
16. Burgess N, Becker S, King JA & O'Keefe J (2001). Memory for events and their spatial context: models and experiments. Philos Trans R Soc Lond B Biol Sci 356, 1493–1503.
17. Bush D, Barry C, Manson D & Burgess N (2015). Using grid cells for navigation. Neuron 87, 507–520.
18. Bush D & Burgess N (2014). A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J Neurosci 34, 5065–5079.
19. Byrne P, Becker S & Burgess N (2007). Remembering the past and imagining the future: A neural model of spatial memory and imagery. Psychol Rev 114, 340–375.
20. Carpenter F, Manson D, Jeffery K, Burgess N & Barry C (2015). Grid cells form a global representation of connected environments. Curr Biol 25, 1–7.
21. Chen G, King JA, Burgess N & O'Keefe J (2013). How vision and movement combine in the hippocampal place code. Proc Natl Acad Sci USA 110, 378–383.
22. Chen LL, Lin L-H, Green EJ, Barnes CA & McNaughton BL (1994). Head-direction cells in the rat posterior cortex. Exp Brain Res 101, 8–23.
23. Clark BJ, Harris MJ & Taube JS (2012). Control of anterodorsal thalamic head direction cells by environmental boundaries: Comparison with conflicting distal landmarks. Hippocampus 22, 172–187.
24. Dudchenko PA & Zinyuk LE (2005). The formation of cognitive maps of adjacent environments: evidence from the head direction cell system. Behav Neurosci 119, 1511–1523.
25. Deshmukh SS & Knierim JJ (2011). Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front Behav Neurosci 5, 69.
26. Etienne AS & Jeffery KJ (2004). Path integration in mammals. Hippocampus 14, 180–192.
27. Etienne AS, Maurer R & Séguinot V (1996). Path integration in mammals and its interaction with visual landmarks. J Exp Biol 199, 201–209.
28. Fiete IR, Burak Y & Brookings T (2008). What grid cells convey about rat location. J Neurosci 28, 6858–6871.
29. Fuhs MC & Touretzky (2006). A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26, 4266–4276.
30. Goodale MA & Milner AD (1992). Separate visual pathways for perception and action. Trends Neurosci 15, 20–25.
31. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ & Taube JS (1998). Cue control and head direction cells. Behav Neurosci 112, 749–761.
32. 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, 8027–8040.
33. Guanella A, Kiper D & Verschure P (2007). A model of grid cells based on a twisted torus topology. Int J Neural Syst 17, 231–240.
34. Hafting T, Fyhn M, Molden S, Moser M-B & Moser EI (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806.
35. Hafting T, Fyhn M, Bonnevie T, Moser MB & Moser EI (2008). Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248–1252.
36. Hardcastle K, Ganguli S & Giocomo LM (2015). Environmental boundaries as an error correction mechanism for grid cells. Neuron 86, 1–13.
37. 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, 369–379.
38. Jeffery KJ (1998). Learning of landmark stability and instability by hippocampal place cells. Neuropharmacology 37, 677–687.
39. Knierim JJ, Kudrimoti HS & McNaughton BL (1995). Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15, 1648–1659.
40. Knight R, Piette CE, Page H, Walters D, Marozzi E, Nardini M, Stringer S & Jeffery KJ (2013). Weighted cue integration in the rodent head direction system. Philos Trans R Soc Lond B Biol Sci 369, 20120512.
41. Koenig J, Linder AN, Leutgeb JK & Leutgeb S (2011). The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592–595.
42. Kropff E, Carmichael JE, Moser MB & Moser EI (2015). Speed cells in the medial entorhinal cortex. Nature 523, 419–424.
43. Krupic J, Bauza M, Burton S, Barry C & O'Keefe J (2015). Grid cell symmetry is shaped by environmental geometry. Nature 518, 232–235.
44. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI & Moser M-B (2010). Development of the spatial representation system in the rat. Science 328, 1576–1580.
45. 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, 9771–9777.
46. Lever C, Wills T, Cacucci F, Burgess N & O'Keefe J (2002). Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90–94.
47. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP & Wang YT (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021–1024.
48. Lu L, Leutgeb JK, Tsao A, Henriksen EJ, Leutgeb S, Barnes CA, Witter MP, Moser M-B & Moser EI (2013). Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16, 1085–1093.
49. 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, 663–678.
50. Mishkin M & Ungerlieder LG (1982). Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav Brain Res 6, 57–77.
51. Mittelstaedt M-L & Mittelstaedt H (1980). Homing by path integration in a mammal. Naturwissenschaften 67, 566–567.
52. Mizumori SJ & Williams JD (1993). Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13, 4015–4028.
53. Muessig L, Hauser J, Wills TJ & Cacucci F (2015). A developmental switch in place cell accuracy coincides with grid cell maturation. Neuron 86, 1167–1173.
54. Muir GM, Brown JE, Carey JP, Hirvonen TP, Della Santina CC, Minor LB & Taube JS (2009). Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chin-chilla. J Neurosci 29, 14521–14533.
55. Muller RU & Kubie JL (1987). The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7, 1951–1968.
56. Muller VM & Best PJ (1980). Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex. Brain Res 194, 311–323.
57. Nardini M, Jones P, Bedford R & Braddick O (2008). Development of cue integration in human navigation. Curr Biol 18, 689–693.
58. O'Keefe J & Burgess N (1996). Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428.
59. O'Keefe J & Burgess N (2005). Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853–866.
60. O'Keefe J, Burgess N, Donnett JG, Jeffery KJ & Maguire EA (1998). Place cells, navigational accuracy, and the human hippocampus. Philos Trans R Soc Lond B Biol Sci 353, 1333–1340.
61. O'Keefe J & Conway DH (1978). Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res 31, 573–590.
62. 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, 171–175.
63. O'Keefe J & Recce ML (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330.
64. Pastoll H, Solanka L, van Rossum MC & Nolan MF (2013). Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron 77, 141–154.
65. Peyrache A, Lacroix MM, Petersen PC & Buzsáki G (2015). Internally organized mechanisms of the head direction sense. Nat Neurosci 18, 569–575.
66. Pouget A & Sejnowski TJ (1997). A new view of hemineglect based on the response properties of parietal neurones. Philos Trans R Soc Lond B Biol Sci 352, 1449–1459.
67. Ranck JB Jr (1984). Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10, 176.12.
68. Salinas E & Abbott LF (1996). A model of multiplicative neural responses in parietal cortex. Proc Natl Acad Sci USA 93, 11956–11961.
69. Sargolini F (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758–762.
70. Savelli F, Yoganarasimha D & Knierim JJ (2008). Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270–1282.
71. Sharp PE, Blair HT & Brown M (1996). Neural network modeling of the hippocampal formation spatial signals and their possible role in navigation: a modular approach. Hippocampus 6, 720–734.
72. Sharp PE, Blair HT & Cho J (2001). The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24, 289–294.
73. Sharp PE & Turner-Williams S (2005). Movement-related correlates of single-cell activity in the medial mammillary nucleus of the rat during a pellet-chasing task. J Neurophysiol 94, 1920–1927.
74. Sharp PE, Turner-Williams S & Tuttle S (2006). Movement-related correlates of single cell activity in the interpeduncular nucleus and habenula of the rat during a pellet-chasing task. Behav Brain Res 166, 55–70.
75. Skaggs WE, Knierim JJ, Kudrimoti HS & McNaughton BL (1995) A mode of the neural basis of the rat's sense of direction. Adv Neural Inf Process Syst 7, 173–180.
76. Solstad T, Boccara CN, Kropff E, Moser M-B & Moser EI (2008). Representation of geometric borders in the entorhinal cortex. Science 322, 1865–1868.
77. Stackman RW & Taube JS (1997). Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17, 4349–4358.
78. Stackman RW & Taube JS (1998). Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J Neurosci 18, 9020–9037.
79. Stackman RW, Clark AS & Taube JS (2002). Hippocampal spatial representations require vestibular input. Hippocampus 12, 291–303.
80. Stensola H, Stensola T, Solstad T, Frøland K, Moser M-B & Moser EI (2012). The entorhinal grid map is discretized. Nature 492, 72–78.
81. Stensola T, Stensola H, Moser M-B & Moser EI (2015). Shearing-induced asymmetry in entorhinal grid cells. Nature 518, 207–212.
82. Taube JS (2007). The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30, 181–207.
83. Taube JS, Muller RU & Ranck JB (1990a). Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10, 436–447.
84. Taube JS, Muller RU & Ranck JB (1990b). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10, 420–435.
85. Tcheang L, Bulthoff HH & Burgess N (2011). Visual influence on path integration in darkness indicates a multimodal representation of large-scale space. Proc Natl Acad Sci USA 108, 1152–1157.
86. Tsao A, Moser M-B & Moser EI (2013). Traces of experience in the lateral entorhinal cortex. Curr Biol 23, 399–405.
87. Valerio S & Taube JS (2012). Path integration: how the head direction signal maintains and corrects spatial orientation. Nat Neurosci 15, 1445–1453.
88. Van Cauter T, Camon J, Alvernhe A, Elduayen C, Sargolini F & Save E (2013). Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb Cortex 23, 451–459.
89. Vann SD, Aggleton JP & Maguire EA (2009). What does the retrosplenial cortex do? Nat Rev Neurosci 10, 792–802.
90. Vann SD & Aggleton JP (2005). Selective dysgranular retrosplenial cortex lesions in rats disrupt allocentric performance of the radial-arm maze task. Behav Neurosci 119, 1682–1686.
91. van Strien NM, Cappaert NLM & Witter MP (2009). The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network. Nat Rev Neurosci 10, 272–282.
92. Wills TJ, Cacucci F, Burgess N & O'Keefe J (2010). Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573–1576.
93. Winter SS, Clark BJ & Taube JS (2015a). Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347, 870–874.
94. Winter SS, Mehlman ML, Clark BJ & Taube JS (2015b). Passive transport disrupts grid signals in the parahippocampal cortex. Curr Biol 25, 2493–2502.
95. Yoder RM, Clark BJ & Taube JS (2011). Origins of landmark encoding in the brain. Trends Neurosci 34, 561–571.
96. Yoder RM, Peck JR & Taube JS (2015). Visual landmark information gains control of the head direction signal at the lateral mammillary nuclei. J Neurosci 35, 1354–1367.
97. 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, 1077–1084.
98. Zhang K (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16, 2112–2126.
99. 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.