Human hippocampal CA1 involvement during allocentric encoding of spatial information

Journal of Neuroscience

Volumn 29, Issue 34, 2009, Pages 10512-10519

  Suthana, Nanthia A ^a   Ekstrom, Arne D ^a   Moshirvaziri, Saba ^a   Knowlton, Barbara ^b   Bookheimer, Susan Y ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NORMAL HUMAN; PRIORITY JOURNAL; TEMPORAL LOBE;

ADULT; BRAIN MAPPING; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; SPACE PERCEPTION; SPATIAL BEHAVIOR; USER-COMPUTER INTERFACE; YOUNG ADULT;

EID: 69449092267     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0621-09.2009     Document Type: Article

References (58)

1. Aguirre GK, Detre JA, Alsop DC, D'EspositoM (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823-829.
2. Ainge JA, Tamosiunaite M, Woergoetter F, Dudchenko PA (2007) Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. J Neurosci 27:9769-9779.
3. Amaral DG, Insausti R (1990) The hippocampal formation. In: The human nervous system (Paxinos G, ed), pp 711-755. San Diego: Academic.
4. Bakker A, Kirwan CB, Miller M, Stark CE (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-1642.
5. Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008) Impaired spatial representation in CA1 after lesion of direct input form entorhinal cortex. Neuron 57:290-302.
6. Colombo M, Fernandez T, Nakamura K, Gross CG (1998) Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. J Neurophysiol 80:1002-1005.
7. Duvernoy HM (1998) The human hippocampus: functional anatomy, vascularization, and serial sections with MRI. Berlin: Springer.
8. 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.
9. Ekstrom AD, Bazih AJ, Suthana NA, Al-Hakim R, Ogura K, Zeineh M, Burggren AC, Bookheimer SY (2009) Advances in high-resolution imaging and computational unfolding of the human hippocampus. Neuroimage 47:42-49.
10. Eldridge LL, Engel SA, Zeineh MM, Bookheimer SY, Knowlton BJ (2005) A dissociation of encoding and retrieval processes in the human hippocampus. J Neurosci 25:3280-3286.
11. Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181-192.
12. Fernández G, Weyerts H, Schrader-Bölsche M, Tendolkar I, Smid HG, Tempelmann C, Hinrichs H, Scheich H, Elger CE, Mangun GR, Heinze HJ (1998) Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study. J Neurosci 18:1841-1847.
13. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169-178.
14. Gabrieli JD, Brewer JB, Desmond JE, GloverGH(1997) Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276:264-266.
15. Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP (2008) The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information. Behav Neurosci 122:16-26.
16. 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.
17. Hassabis D, Chu C, Rees G, Weiskopf N, Molyneux PD, Maguire EA (2009) Decoding neuronal ensembles in the human hippocampus. Curr Biol 19:546-554.
18. Howard IP (1982) Human visual orientation. Chichester, UK: Wiley.
19. 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.
20. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825-841.
21. King JA, Burgess N, Hartley T, Vargha-Khadem F, O'Keefe J (2002) The human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12:811-820.
22. Knowlton BJ, Fanselow MS (1998) Hippocampus, consolidation, and online memory. Curr Opin Neurobiol 8:293-296.
23. Köhler S, Crane J, Milner B (2002) Networks of domain-specific and general regions involved in episodic memory for spatial location and object identity. Hippocampus 12:718-723.
24. Kumaran D, Maguire EA (2005) The human hippocampus: cognitive maps or relational memory? J Neurosci 25:7254-7259.
25. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456-459.
26. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI (2005) Pregressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48:345-358.
27. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
28. Levy WB (1989) A computational approach to the hippocampal function. In: Computational models of learning in simple neural systems (Hawkins RD, Gower GH, eds), pp 243-305. Orlando, FL: Academic.
29. Maguire EA, Woollett K, Spiers HJ (2006) London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 12:1091-1101.
30. Malkova L, Mishkin M (2003) One-trial memory for object-place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey. J Neurosci 23:1956-1965.
31. McNamara TP, Shelton AL (2003) Cognitive maps and the hippocampus. Trends Cogn Sci 7:333-335.
32. Mellet E, Briscogne S, Tzourio-Mazoyer N, Ghaëm O, Petit L, Zago L, Etard O, Berthoz A, Mazoyer B, Denis M (2000) Neural correlates of topo graphic mental exploration: the impact of route versus survey perspective learning. Neuroimage 12:588-600.
33. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
34. Muller RU, Kubie JL, Ranck JB Jr (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
35. Nadel L, MacDonald L (1980) Hippocampus: cognitive map or working memory? Behav Neural Biol 29:405-409.
36. 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.
37. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map, pp 190- 230. Oxford: Clarendon.
38. 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.
39. Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M (2004) I have often walked down this street before: fMRI studies of hippocampus and other structures during mental navigation of an old environment. Hippocampus 14:826-835.
40. Shelton AL, Gabrieli JD (2002) Neural correlates of encoding space from route and survey perspectives. J Neurosci 22:2711-2717.
41. Shrager Y, Bayley PJ, Bontempi B, Hopkins RO, Squire LR (2007) Spatial memory and the human hippocampus. Proc Natl Acad Sci U S A 104:2961-2966.
42. Smith SM (2002) Fast robust automated brain extraction.HumBrain Mapp 17:143-155.
43. Sommer T, Rose M, Gläscher J, Wolbers T, Büchel C (2005) Dissociable contributions within the medial temporal lobe to encoding of objectlocation associations. Learn Mem 12:343-351.
44. Spiers HJ, Burgess N, Maguire EA, Baxendale SA, Hartley T, Thompson PJ, O'Keefe J (2001) Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 124:2476-2489.
45. Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279-306.
46. Stark CE, Squire LR (2001) When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci U S A 98: 12760-12766.
47. Teo PC, Sapiro G, Wandell BA (1997) Creating connected representations of cortical gray matter for functional MRI visualization. IEEE Trans Med Imaging 16:852-863.
48. Thompson PM, Woods RP, Mega MS, Toga AW (2000) Mathematical/ computational challenges in creating deformable and probabilistic atlases of the human brain. Hum Brain Mapp 9:81-92.
49. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55: 189-208.
50. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578-598.
51. Wills TJ, Lever C, Cacucci F, Burgess N, O'Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308:873-876.
52. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
53. Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000) Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci 911:1-24.
54. Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14:1370-1386.
55. Zeineh MM, Engel SA, Bookheimer SY (2000) Application of cortical unfolding techniques to functional MRI of the human hippocampal region. Neuroimage 11:668-683.
56. Zeineh MM, Engel SA, Thompson PM, Bookheimer SY (2001) Unfolding the human hippocampus with high resolution structural and functional MRI. Anat Rec 265:111-120.
57. 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.
58. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal lobe region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.