Human neural systems underlying rigid and flexible forms of allocentric spatial representation

Human Brain Mapping

Volumn 34, Issue 5, 2013, Pages 1070-1087

  Zhang, Hui ^a   Ekstrom, Arne ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hippocampus; Parahippocampus; Partial learning paradigm; Posterior superior parietal cortex; Retrosplenial; Spatial memory; Spatial navigation

Indexed keywords

ANGULAR GYRUS; ARTICLE; BOLD SIGNAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; LATENT PERIOD; LEARNING; MALE; MEMORY; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; NERVOUS SYSTEM; NORMAL HUMAN; OCCIPITAL GYRUS; PARAHIPPOCAMPAL GYRUS; PARIETAL CORTEX; POSTERIOR CINGULATE; POSTERIOR PARIETAL CORTEX; PRECUNEUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESPONSE TIME; RETROSPLENIAL CORTEX; SUPERIOR PARIETAL LOBULE; SUPERIOR TEMPORAL GYRUS; TEMPORAL LOBE;

BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MENTAL RECALL; NEURAL PATHWAYS; ORIENTATION; OXYGEN; PHOTIC STIMULATION; REACTION TIME; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 84875878818     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21494     Document Type: Article

References (84)

1. Aguirre GK, Detre JA, Alsop DC, D'Esposito M ( 1996): The parahippocampus subserves topographical learning in man. Cereb Cortex 6: 823-829.
2. Baumann O, Chan E, Mattingley JB ( 2010): Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans. Neuroimage 49: 2816-2825.
3. Bohbot VD, Corkin S ( 2007): Posterior parahippocampal place learning in H.M. Hippocampus 17: 863-872.
4. Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M, Nadel L ( 1998): Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 36: 1217-1238.
5. Brown TI, Ross RS, Keller JB, Hasselmo ME, Stern CE ( 2010): Which way was I going? Contextual retrieval supports the disambiguation of well learned overlapping navigational routes. J Neurosci 30: 7414-7422.
6. Burgess N, Maguire EA, O'Keefe J ( 2002): The human hippocampus and spatial and episodic memory. Neuron 35: 625-641.
7. Cansino S, Maquet P, Dolan RJ, Rugg MD ( 2002): Brain activity underlying encoding and retrieval of source memory. Cereb Cortex 12: 1048-1056.
8. Cohen NJ, Eichenbaum H ( 1991): The theory that wouldn't die: A critical look at the spatial mapping theory of hippocampal function. Hippocampus 1: 265-268.
9. Committeri G, Galati G, Paradis AL, Pizzamiglio L, Berthoz A, LeBihan D ( 2004): 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.
10. Daselaar SM, Fleck MS, Cabeza R ( 2006): Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. J Neurophysiol 96: 1902-1911.
11. Davachi L, Mitchell JP, Wagner AD ( 2003): Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci USA 100: 2157-2162.
12. Diana RA, Yonelinas AP, Ranganath C ( 2009): Medial temporal lobe activity during source retrieval reflects information type, not memory strength. J Cogn Neurosci 22: 1808-1822.
13. Eichenbaum H, Cohen NJ ( 2001): From Conditioning to Conscious Recollection: Memory Systems of the Brain. New York: Oxford University Press.
14. Eichenbaum H, Otto T, Cohen NJ ( 1992): The hippocampus-What does it do? Behav Neural Biol 57: 2-36.
15. Ekstrom A, Suthana N, Millett D, Fried I, Bookheimer S ( 2009): Correlation Between BOLD fMRI and theta-band local field potentials in the human hippocampal area. J Neurophysiol 101: 2668-2678.
16. Ekstrom AD, Bookheimer SY ( 2007): Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain. Learn Mem 14: 645-654.
17. Epstein R, Kanwisher N ( 1998): A cortical representation of the local visual environment. Nature 392: 598-601.
18. Epstein R, Graham KS, Downing PE ( 2003): Viewpoint-specific scene representations in human parahippocampal cortex. Neuron 37: 865-876.
19. Epstein RA ( 2008): Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12: 388-396.
20. Epstein RA, Higgins JS ( 2007): Differential parahippocampal and retrosplenial involvement in three types of visual scene recognition. Cereb Cortex 17: 1680-1693.
21. Epstein RA, Parker WE, Feiler AM ( 2007): Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27: 6141-6149.
22. Evans GW, Pezdek K ( 1980): Cognitive mapping: knowledge of real-world distance and location information. J Exp Psychol Hum Learn 6: 13-24.
23. Fitts PM ( 1954): The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47: 381-391.
24. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC ( 1995): Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magn Reson Med 33: 636-647.
25. Friston KJ, Frith CD, Frackowiak RS, Turner R ( 1995): Characterizing dynamic brain responses with fMRI: A multivariate approach. Neuroimage 2: 166-172.
26. Galati G, Pelle G, Berthoz A, Committeri G ( 2010): Multiple reference frames used by the human brain for spatial perception and memory. Exp Brain Res 206: 109-120.
27. Galati G, Lobel E, Vallar G, Berthoz A, Pizzamiglio L, Le Bihan D ( 2000): The neural basis of egocentric and allocentric coding of space in humans: A functional magnetic resonance study. Exp Brain Res 133: 156-164.
28. Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, Denis M ( 1997): Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8: 739-744.
29. Goodrich-Hunsaker NJ, Hopkins RO ( 2010): Spatial memory deficits in a virtual radial arm maze in amnesic participants with hippocampal damage. Behav Neurosci 124: 405-413.
30. Goodrich-Hunsaker NJ, Livingstone SA, Skelton RW, Hopkins RO ( 2010): Spatial deficits in a virtual water maze in amnesic participants with hippocampal damage. Hippocampus 20: 481-491.
31. Hartley T, Maguire EA, Spiers HJ, Burgess N ( 2003): The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron 37: 877-888.
32. Hartley T, Bird CM, Chan D, Cipolotti L, Husain M, Vargha-Khadem F, Burgess N ( 2007): The hippocampus is required for short-term topographical memory in humans. Hippocampus 17: 34-48.
33. Hayes SM, Ryan L, Schnyer DM, Nadel L ( 2004): An fMRI study of episodic memory: Retrieval of object, spatial, and temporal information. Behav Neurosci 118: 885-896.
34. Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD ( 2003): Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. J Neurosci 23: 5945-5952.
35. Igloi K, Doeller CF, Berthoz A, Rondi-Reig L, Burgess N ( 2010): Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proc Natl Acad Sci USA 107: 14466-14471.
36. Janzen G, van Turennout M ( 2004): Selective neural representation of objects relevant for navigation. Nat Neurosci 7: 673-677.
37. Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L ( 2004): Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task. Neuroreport 15: 135-140.
38. Klatzky R ( 1998) Allocentric and egocentric spatial representations: Definitions, distinctions, and interconnections. In: Freksa C, Habel C, Wender CF, editors. Spatial cognition: An Interdisciplinary Approach to Representation and Processing of Spatial Knowledge. Berlin: Springer-Verlag. pp 1-17.
39. Konkel A, Cohen NJ ( 2009): Relational memory and the hippocampus: Representations and methods. Front Neurosci 3: 166-174.
40. Konkel A, Warren DE, Duff MC, Tranel DN, Cohen NJ ( 2008): Hippocampal amnesia impairs all manner of relational memory. Front Hum Neurosci 2: 15.
41. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI ( 2009): Circular analysis in systems neuroscience: The dangers of double dipping. Nat Neurosci 12: 535-540.
42. Lepage M, Habib R, Tulving E ( 1998): Hippocampal PET activations of memory encoding and retrieval: The HIPER model. Hippocampus 8: 313-322.
43. Levine M, Marchon I, Hanley G ( 1984): The placement and misplacement of you-are-here maps. Environ Behav 16: 139.
44. Maguire EA, Frith CD, Burgess N, Donnett JG, O'Keefe J ( 1998a) Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci 10: 61-76.
45. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O'Keefe J ( 1998b) Knowing where and getting there: a human navigation network. Science 280: 921-924.
46. McClelland JL, McNaughton BL, O'Reilly RC ( 1995): Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102: 419-457.
47. McNamara TP, Rump B, Werner S ( 2003): Egocentric and geocentric frames of reference in memory of large-scale space. Psychon Bull Rev 10: 589-595.
48. Mellet E, Briscogne S, Tzourio-Mazoyer N, Ghaem O, Petit L, Zago L, Etard O, Berthoz A, Mazoyer B, Denis M ( 2000): Neural correlates of topographic mental exploration: The impact of route versus survey perspective learning. Neuroimage 12: 588-600.
49. Moeser S ( 1988) Cognitive mapping in a complex building. Environ Behav 20: 21-48.
50. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J ( 1982): Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
51. Mugikura S, Abe N, Suzuki M, Ueno A, Higano S, Takahashi S, Fujii T ( 2010): Hippocampal activation associated with successful external source monitoring. Neuropsychologia 48: 1543-1550.
52. Neggers SF, Van der Lubbe RH, Ramsey NF, Postma A ( 2006): Interactions between ego- and allocentric neuronal representations of space. Neuroimage 31: 320-331.
53. Newman EL, Caplan JB, Kirschen MP, Korolev IO, Sekuler R, Kahana MJ ( 2007): Learning your way around town: How virtual taxicab drivers learn to use both layout and landmark information. Cognition 104: 231-253.
54. O'Keefe J, Nadel L ( 1978): The Hippocampus as a Cognitive Map. Oxford: Clarendon Press.
55. Parslow DM, Morris RG, Fleminger S, Rahman Q, Abrahams S, Recce M ( 2005): Allocentric spatial memory in humans with hippocampal lesions. Acta Psychol (Amst) 118: 123-147.
56. Parslow DM, Rose D, Brooks B, Fleminger S, Gray JA, Giampietro V, Brammer MJ, Williams S, Gasston D, Andrew C, Vythelingum GN, Loannou G, Simmons A, Morris RG ( 2004): Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology 18: 450-461.
57. Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Samson S, Pierrot-Deseilligny C ( 2000): Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10: 1211-1216.
58. Ploner CJ, Gaymard BM, Ehrle N, Rivaud-Pechoux S, Baulac M, Brandt SA, Clemenceau S, Samson S, Pierrot-Deseilligny C ( 1999): Spatial memory deficits in patients with lesions affecting the medial temporal neocortex. Ann Neurol 45: 312-319.
59. Poldrack RA, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano J, Myers C, Gluck MA ( 2001): Interactive memory systems in the human brain. Nature 414: 546-550.
60. Presson CC, DeLange N, Hazelrigg MD ( 1989): Orientation specificity in spatial memory: What makes a path different from a map of the path? J Exp Psychol Learn Mem Cogn 15: 887-897.
61. Richardson AE, Montello DR, Hegarty M ( 1999): Spatial knowledge acquisition from maps and from navigation in real and virtual environments. Mem Cognit 27: 741-750.
62. Rissman J, Gazzaley A, D'Esposito M ( 2004): Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 23: 752-763.
63. Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M ( 2004): "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.
64. Rugg MD, Johnson JD, Park H, Uncapher MR ( 2008): Encoding-retrieval overlap in human episodic memory: A functional neuroimaging perspective. Prog Brain Res 169: 339-352.
65. Shelton AL, Gabrieli JD ( 2002): Neural correlates of encoding space from route and survey perspectives. J Neurosci 22: 2711-2717.
66. Shelton AL, McNamara TP ( 2004): Orientation and perspective dependence in route and survey learning. J Exp Psychol Learn Mem Cogn 30: 158-170.
67. Shelton AL, Pippitt HA ( 2007): Fixed versus dynamic orientations in environmental learning from ground-level and aerial perspectives. Psychol Res 71: 333-346.
68. Shipman SL, Astur RS ( 2008): Factors affecting the hippocampal BOLD response during spatial memory. Behav Brain Res 187: 433-441.
69. Sholl MJ ( 1987): Cognitive maps as orienting schemata. J Exp Psychol Learn Mem Cogn 13: 615-628.
70. Siegel AW, White SH ( 1975): The development of spatial representations of large-scale environments. In Reese HW, editor. Advances in Child Development and Behavior. New York: Academic.
71. Staresina BP, Davachi L ( 2009): Mind the gap: Binding experiences across space and time in the human hippocampus. Neuron 63: 267-276.
72. Stark CE, Squire LR ( 2001) When zero is not zero: The problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci USA 98: 12760-12766.
73. Sturz BR, Brown MF, Kelly DM ( 2009): Facilitation of learning spatial relations among locations by visual cues: Implications for theoretical accounts of spatial learning. Psychon Bull Rev 16: 306-312.
74. Suthana NA, Ekstrom AD, Moshirvaziri S, Knowlton B, Bookheimer SY ( 2009): Human hippocampal CA1 involvement during allocentric encoding of spatial information. J Neurosci 29: 10512-10519.
75. Taylor HA, Tversky B ( 1992): Spatial mental models derived from survey and route descriptions. J Mem Lang 31: 261-292.
76. Thorndyke PW, Hayes-Roth B ( 1982): Differences in spatial knowledge acquired from maps and navigation. Cogn Psychol 14: 560-589.
77. Tolman EC ( 1948): Cognitive maps in rats and men. Psychol Rev 55: 189-208.
78. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RG ( 2007): Schemas and memory consolidation. Science 316: 76-82.
79. Uncapher MR, Otten LJ, Rugg MD ( 2006): Episodic encoding is more than the sum of its parts: An fMRI investigation of multifeatural contextual encoding. Neuron 52: 547-556.
80. Voss JL, Gonsalves BD, Federmeier KD, Tranel D, Cohen NJ ( 2010): Hippocampal brain-network coordination during volitional exploratory behavior enhances learning. Nat Neurosci 14: 115-120.
81. Waller D, Hodgson E ( 2006): Transient and enduring spatial representations under disorientation and self-rotation. J Exp Psychol Learn Mem Cogn 32: 867-882.
82. Wang RF, Spelke ES ( 2000): Updating egocentric representations in human navigation. Cognition 77: 215-250.
83. Wolbers T, Buchel C ( 2005): Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J Neurosci 25: 3333-3340.
84. Zeineh MM, Engel SA, Thompson PM, Bookheimer SY ( 2003): Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 299: 577-580.