Partially segregated neural networks for spatial and contextual memory in virtual navigation

Hippocampus

Volumn 18, Issue 5, 2008, Pages 503-518

  Rauchs, Géraldine ^a   Orban, Pierre ^a,b   Balteau, Evelyne ^a   Schmidt, Christina ^a   Degueldre, Christian ^a   Luxen, André ^a   Maquet, Pierre ^a   Peigneux, Philippe ^a,c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Ecologically valid environment; fMRI; Hippocampus; Parahippocampal cortex

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN REGION; COGNITION; DATA ANALYSIS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PERFORMANCE; PRIORITY JOURNAL; SPATIAL MEMORY; SUBICULUM; VIRTUAL REALITY; VOLUNTEER;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NERVE NET; SPATIAL BEHAVIOR; USER-COMPUTER INTERFACE;

EID: 43449126834     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20411     Document Type: Article

References (54)

1. Aguirre GK, Detre JA, Alsop DC, D'Esposito M. 1996. The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823-829.
2. Aminoff E, Gronau N, Bar M. 2007. The parahippocampal cortex mediates spatial and nonspatial associations. Cereb Cortex 17:1493-1503.
3. Berthoz A. 2001. [Neural basis of spatial orientation and memory of routes: Topokinetic memory or topokinesthesic memory]. Rev Neurol (Paris) 157:779-789.
4. Bohbot V, 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. Bohbot VD, Iaria G, Petrides M. 2004. Hippocampal function and spatial memory: Evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18:418-425.
6. Burgess N, Maguire EA, Spiers HJ, O'Keefe J. 2001. A temporoparietal and prefrontal network for retrieving the spatial context of life-like events. Neuroimage 14:439-453.
7. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
8. Cabeza R, Nyberg L. 2000. Imaging cognition. II. An empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1-47.
9. Cavanna AE, Trimble MR. 2006. The precuneus: A review of its functional anatomy and behavioural correlates. Brain 129:564-583.
10. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr Opin Neurobiol 16:693-700.
11. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I. 2003. Cellular networks underlying human spatial navigation. Nature 425:184-188.
12. Epstein R, Kanwisher N. 1998. A cortical representation of the local visual environment. Nature 392:598-601.
13. Epstein RA, Higgins JS. 2007. Differential parahippocampal and retrosplenial involvement in three types of visual scene recognition. Cereb Cortex 17:1680-1693.
14. Fan J, Snodgrass JG, Bilder RM. 2003. Functional magnetic resonance imaging of source versus item memory. NeuroReport 14:2275-2281.
15. Fellows LK. 2004. The cognitive neuroscience of human decision making: A review and conceptual framework. Behav Cogn Neurosci Rev 3:159-172.
16. Frick KM, Stearns NA, Pan JY, Berger-Sweeney J. 2003. Effects of environmental enrichment on spatial memory and neurochemistry in middle-aged mice. Learn Mem 10:187-198.
17. Fristen KJ, Glaser DE, Henson RN, Kiebel S, Phillips C, Ashburner J. 2002. Classical and Bayesian inference in neuroimaging: Applications. Neuroimage 16:484-512.
18. Fristen KJ, Penny W. 2003. Posterior probability maps and SPMs. Neuroimage 19:1240-1249.
19. Fristen KJ, Penny W, Glaser DE. 2005. Conjunction revisited. Neuroimage 25:661-667.
20. Gold JJ, Smith CN, Bayley PJ, Shrager Y, Brewer JB, Stark CE, Hopkins RO, Squire LR. 2006. Item memory, source memory, and the medial temporal lobe: Concordant findings from fMRI and memory-impaired patients, Proc Natl Acad Sci USA 103:9351-9356.
21. Grefkes C, Fink GR. 2005. The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3-17.
22. Gron G, Wunderlich AP, Spitzer M, Tomczak R, Riepe MW. 2000. Brain activation during human navigation: Gender-different neural networks as substrate of performance. Nat Neurosci 3:404-408.
23. Hartley T, Maguire EA, Spiers HJ, Burgess N. 2003. The well-worn route and the path less travelled: Distinct neural bases of route following and wayfinding in humans. Neuron 37:877-888.
24. 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.
25. Janzen G, van Turennout M. 2004. Selective neural representation of objects relevant for navigation. Nat Neurosci 7:673-677.
26. Konishi S, Wheeler ME, Donaldson DI, Buckner RL. 2000. Neural correlates of episodic retrieval success. Neuroimage 12:276-286.
27. 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 309:619-623.
28. Lundstrom BN, Petersson KM, Andersson J, Johansson M, Fransson P, Ingvar M. 2003. Isolating the retrieval of imagined pictures during episodic memory: Activation of the left precuneus and the left prefrontal cortex. Neuroimage 20:1934-1943.
29. Lundstrom BN, Ingvar M, Petersson KM. 2005. The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage 27:824-834.
30. 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.
31. 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.
32. Meunier M, Bachevalier J, Mishkin M, Murray EA. 1993. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13:5418-5432.
33. Nyberg L. 2005. Any novelty in hippocampal formation and memory? Curr Opin Neurol 18:424-428.
34. Ojemann GA, Schoenfield-McNeill J, Corina DP. 2002. Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory. Nat Neurosci 5:64-71.
35. Orban P, Rauchs G, Balteau E, Degueldre C, Luxen A, Maquet P, Peigneux P. 2006. Sleep after spatial learning promotes covert reorganization of brain activity. Proc Natl Acad Sci USA 103:7124-7129.
36. Packard MG, Knowlton BJ. 2002. Learning and memory functions of the Basal Ganglia. Annu Rev Neurosci 25:563-593.
37. Pazzaglia F, De Beni R. 2001. Strategies of processing spatial information in survey and landmark-centred individuals. European Journal of Cognitive Psychology 13:493-508.
38. Penny W, Holmes A. 2003. Random-effect analysis. In: Frackowiak RJS, Friston KJ, Frith C, Dolan R, Price CJ, Zeki S, Ashburner J, editors. Human Brain Function, 2nd ed. London: Academic Press, pp 843-850.
39. Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Philipps C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P. 2004. Are spatial memories strengthened in the human hippocampus during slow-wave sleep? Neuron 44:535-545.
40. Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S, Maquet P. 2006. Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 4:e100.
41. Ranganath C, Knight RT. 2003. Prefrontal cortex and episodic memory: Integrating findings from neuropsychology and functional brain imaging. In: Parker A, editor. The cognitive neuroscience of memory encoding and retrieval. Philadelphia: Psychology Press. pp 83-99.
42. Rauchs G, Blaizot X, Giffard C, Baron JC, Insausti R, Chavoix C. 2006. Imaging visual recognition memory network by PET in the baboon: Perirhinal cortex heterogeneity and plasticity after perirhinal lesion. J Cereb Blood Flow Metab 26:301-309.
43. 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.
44. Rosenzweig MR, Bennett EL. 1996. Psychobiology of plasticity: Effects of training and experience on brain and behavior. Behav Brain Res 78:57-65.
45. Shallice T. 1982. Specific impairments of planning. Philos Trans R Soc London Ser B 298:199-209.
46. Spiers HJ, Maguire EA. 2006a. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31:1826-1840.
47. Spiers HJ, Maguire EA. 2006b. Spontaneous mentalizing during an interactive real world task: An fMRI study. Neuropsychologia 44:1674-1682.
48. Talairach J, Tournoux P. 1988. Co-planar stereotaxic atlas of the human brain: Three-dimensional proportional system. Stuttgart, Germany: Georg Thieme. 122 p.
49. Tendolkar I, Arnold J, Petersson KM, Weis S, Brockhaus-Dumke A, van Eijndhoven P, Buitelaar J, Fernandez G. 2007. Probing the neural correlates of associative memory function: A parametrically analyzed event-related functional MRI study. Brain Res 1142:159-168.
50. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289.
51. Voermans NC, Petersson KM, Daudey L, Weber B, Van Spaendonck KP, Kremer HP, Fernandez G. 2004. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 43:427-435.
52. Wagner AD, Shannon BJ, Kahn I, Buckner RL. 2005. Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9:445-453.
53. Wolbers T, Weiller C, Buchel C. 2004. Neural foundations of emerging route knowledge in complex spatial environments. Brain Res Cogn Brain Res 21:401-411.
54. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. 1996. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58-73.