Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms

eLife

Volumn 4, Issue NOVEMBER2015, 2015, Pages

  Kyle, Colin T ^a   Stokes, Jared D ^a   Lieberman, Jennifer S ^a   Hassan, Abdul S ^a   Ekstrom, Arne D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERROR; HIPPOCAMPUS; HUMAN; INFORMATION RETRIEVAL; MEMORY; BRAIN MAPPING; DEPTH PERCEPTION; FEMALE; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

BRAIN MAPPING; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; SPACE PERCEPTION;

EID: 84952899838     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10499     Document Type: Article

References (59)

1. Anderson M. 2003. Rethinking interference theory: executive control and the mechanisms of forgetting. Journal of Memory and Language 49:415-445. doi: 10.1016/j.jml.2003.08.006
2. Anderson MC. 2004. Neural systems underlying the suppression of unwanted memories. Science 303:232-235. doi: 10.1126/science.1089504
3. Aron AR, Robbins TW, Poldrack RA. 2014. Inhibition and the right inferior frontal cortex: one decade on. Trends in Cognitive Sciences 18:177-185. doi: 10.1016/j.tics.2013.12.003
4. Avants B, Epstein C, Grossman M, Gee J. 2008. Symmetric diffeomorphic image registration with cross- correlation: evaluating automated labeling of elderly and neurodegenerative brain. Medical Image Analysis 12: 26-41. doi: 10.1016/j.media.2007.06.004
5. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-1642. doi: 10.1126/science.1152882
6. Bell AJ, Sejnowski TJ. 1995. An information-maximization approach to blind separation and blind deconvolution. Neural Computation 7:1129-1159. doi: 10.1162/neco.1995.7.6.1129
7. Brown TI, Hasselmo ME, Stern CE. 2014. A high-resolution study of hippocampal and medial temporal lobe correlates of spatial context and prospective overlapping route memory. Hippocampus 24:819-839. doi: 10. 1002/hipo.22273
8. Buzsáki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neuroscience 16:130-138. doi: 10.1038/nn.3304
9. Chadwick MJ, Hassabis D, Weiskopf N, Maguire EA. 2010. Decoding individual episodic memory traces in the human hippocampus. Current Biology 20:544-547. doi: 10.1016/j.cub.2010.01.053
10. Colgin LL, Moser EI, Moser M-B. 2008. Understanding memory through hippocampal remapping. Trends in Neurosciences 31:469-477. doi: 10.1016/j.tins.2008.06.008
11. Copara MS, Hassan AS, Kyle CT, Libby LA, Ranganath C, Ekstrom AD. 2014. Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context. Journal of Neuroscience 34:6834-6842. doi: 10.1523/JNEUROSCI.5341-13.2014
12. Davis T, LaRocque KF, Mumford JA, Norman KA, Wagner AD, Poldrack RA. 2014. What do differences between multi-voxel and univariate analysis mean? how subject-, voxel-, and trial-level variance impact fMRI analysis. NeuroImage 97:271-283. doi: 10.1016/j.neuroimage.2014.04.037
13. Detre G. 2006. The multi-voxel pattern analysis (mVPA) toolbox. in poster presented at the annual meeting of the organization for human brain mapping (florence, italy). Available at http://www.csbmb.princeton.edu/mvpa.
14. Duncan K, Ketz N, Inati SJ, Davachi L. 2012. Evidence for area CA1 as a match/mismatch detector: a high- resolution fMRI study of the human hippocampus. Hippocampus 22:389-398. doi: 10.1002/hipo.20933
15. 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. doi: 10.1016/j.neuroimage.2009.03.017
16. 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. doi: 10.1038/nature01964
17. Etzel JA, Zacks JM, Braver TS. 2013. Searchlight analysis: promise, pitfalls, and potential. NeuroImage 78:261-269. doi: 10.1016/j.neuroimage.2013.03.041
18. Friston KJ, Frith CD, Frackowiak RSJ, Turner R. 1995. Characterizing dynamic brain responses with fMRI: a multivariate approach. NeuroImage 2:166-172. doi: 10.1006/nimg.1995.1019
19. Goldman-Rakic PS, Selemon LD, Schwartz ML. 1984. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12: 719-743. doi: 10.1016/0306-4522(84)90166-0
20. Guterstam A, Björnsdotter M, Gentile G, Ehrsson HH. 2015. Posterior cingulate cortex integrates the senses of self-location and body ownership. Current Biology 25:1416-1425. doi: 10.1016/j.cub.2015.03.059
21. Guzowski JF, Knierim JJ, Moser EI. 2004. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 44: 581-584. doi: 10.1016/j.neuron.2004.11.003
22. Hassabis D, Chu C, Rees G, Weiskopf N, Molyneux PD, Maguire EA. 2009. Decoding neuronal ensembles in the human hippocampus. Current Biology 19:546-554. p. . doi: 10.1016/j.cub.2009.02.033
23. Hill AJ. 1978. First occurrence of hippocampal spatial firing in a new environment. Experimental Neurology 62: 282-297. doi: 10.1016/0014-4886(78)90058-4
24. Hunsaker MR, Kesner RP. 2013. The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neuroscience & Biobehavioral Reviews 37:36-58. doi: 10.1016/j.neubiorev.2012.09.014
25. Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei X-X, Suthana N, Sperling MR, Sharan AD, Fried I, Kahana MJ. 2013. Direct recordings of grid-like neuronal activity in human spatial navigation. Nature Neuroscience 16:1188-1190. doi: 10.1038/nn.3466
26. Jeffery KJ, Gilbert A, Burton S, Strudwick A. 2003. Preserved performance in a hippocampal-dependent spatial task despite complete place cell remapping. Hippocampus 13:175-189. doi: 10.1002/hipo.10047
27. Kentros C. 1998. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280:2121-2126. doi: 10.1126/science.280.5372.2121
28. Kohonen T. 1977. Associative Memory.
29. Kriegeskorte N, Goebel R, Bandettini P. 2006. Information-based functional brain mapping. Proceedings of the National Academy of Sciences of the United States of America 103:3863-3868. doi: 10.1073/pnas.0600244103
30. Kyle CT, Smuda DN, Hassan AS, Ekstrom AD. 2015. Roles of human hippocampal subfields in retrieval of spatial and temporal context. Behavioural Brain Research 278:549-558. doi: 10.1016/j.bbr.2014.10.034
31. Larkin MC, Lykken C, Tye LD, Wickelgren JG, Frank LM. 2014. Hippocampal output area CA1 broadcasts a generalized novelty signal during an object-place recognition task. Hippocampus 24:773-783. doi: 10.1002/ hipo.22268
32. Leutgeb JK, Leutgeb S, Moser M-B, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966. doi: 10.1126/science.1135801
33. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser M-B, Moser EI. 2005. Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48: 345-358. doi: 10.1016/j.neuron.2005.09.007
34. Leutgeb S. 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295-1298. doi: 10. 1126/science.1100265
35. Marr D. 1971. Simple memory: a theory for archicortex. Philosophical Transactions of the Royal Society B: Biological Sciences 262:23-81. doi: 10.1098/rstb.1971.0078 McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA
36. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94-99. doi: 10.1126/science.1140263
37. Miller JF, Neufang M, Solway A, Brandt A, Trippel M, Mader I, Hefft S, Merkow M, Polyn SM, Jacobs J, Kahana MJ, Schulze-Bonhage A. 2013. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories. Science 342:1111-1114. doi: 10.1126/science.1244056
38. Morgan LK, MacEvoy SP, Aguirre GK, Epstein RA. 2011. Distances between real-world locations are represented in the human hippocampus. Journal of Neuroscience 31:1238-1245. doi: 10.1523/JNEUROSCI.4667-10.2011
39. Morris RGM, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long- term potentiation by an n-methyl-d-aspartate receptor antagonist, AP5. Nature 319:774-776. doi: 10.1038/ 319774a0
40. Mourão-Miranda J, Reynaud E, McGlone F, Calvert G, Brammer M. 2006. The impact of temporal compression and space selection on SVM analysis of single-subject and multi-subject fMRI data. NeuroImage 33:1055-1065. doi: 10.1016/j.neuroimage.2006.08.016
41. Muller RU, Kubie JL. 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. The Journal of Neuroscience 7:1951-1968.
42. Mumford JA, Turner BO, Ashby FG, Poldrack RA. 2012. Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses. NeuroImage 59:2636-2643. doi: 10.1016/j.neuroimage.2011.08. 076
43. 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. p. . doi: 10.1016/j.cognition.2006.05.013
44. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. preliminary evidence from unit activity in the freely-moving rat. Brain Research 34:171-175. doi: 10.1016/0006-8993(71)90358-1
45. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. Oxford: Clarendon Press.
46. Redish AD. 1999. Beyond the Cognitive Map. Boston, MA: MIT Press.
47. Remondes M, Schuman EM. 2004. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431:699-703. doi: 10.1038/nature02965
48. Rissman J, Gazzaley A, D'Esposito M. 2004. Measuring functional connectivity during distinct stages of a cognitive task. NeuroImage 23:752-763. doi: 10.1016/j.neuroimage.2004.06.035
49. Rolls ET. 2010. Attractor networks. Wiley Interdisciplinary Reviews: Cognitive Science 1:119-134. doi: 10.1002/ wcs.1
50. Shapiro ML, Olton DS. 1994. Hippocampal function and interference. Memory Systems:87-117.
51. Skaggs WE, McNaughton BL. 1998. Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. The Journal of Neuroscience 18: 8455- 8466.
52. Spiers HJ, Burgess N, Hartley T, Vargha-Khadem F, O'Keefe J. 2001. Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching. Hippocampus 11:715-725. doi: 10.1002/ hipo.1087
53. Spiers HJ, Hayman RMA, Jovalekic A, Marozzi E, Jeffery KJ. 2015. Place field repetition and purely local remapping in a multicompartment environment. Cerebral Cortex 25:10-25. doi: 10.1093/cercor/bht198
54. Stokes J, Kyle C, Ekstrom AD. 2015. Complementary roles of human hippocampal subfields in differentiation and integration of spatial context. Journal of Cognitive Neuroscience 27:546-559. doi: 10.1162/jocn_a_00736
55. Thompson LT, Best PJ. 1990. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Research 509:299-308. doi: 10.1016/0006-8993(90)90555-P
56. Wilson M, McNaughton B. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058. doi: 10.1126/science.8351520
57. Woo C-W, Krishnan A, Wager TD. 2014. Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. NeuroImage 91:412-419. doi: 10.1016/j.neuroimage.2013.12.058
58. Yassa MA, Stark CEL. 2011. Pattern separation in the hippocampus. Trends in Neurosciences 34:515-525. doi: 10.1016/j.tins.2011.06.006
59. Zhang H, Zherdeva K, Ekstrom AD. 2014. Different "routes" to a cognitive map: dissociable forms of spatial knowledge derived from route and cartographic map learning. Memory & Cognition 42:1106-1117. doi: 10. 3758/s13421-014-0418-x