Dynamic changes in the medial temporal lobe during incidental learning of object-location associations

Cerebral Cortex

Volumn 22, Issue 4, 2012, Pages 828-837

  Manelis, Anna ^a,b   Reder, Lynne M ^a,b   Hanson, Stephen José ^c  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

associative memory encoding; fMRI; medial temporal lobe; multivoxel pattern classification; object location associations

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; ASSOCIATIVE MEMORY; BRAIN MAPPING; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MEMORY CONSOLIDATION; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; PRIORITY JOURNAL; SPATIAL MEMORY; SPATIAL ORIENTATION; TEMPORAL LOBE;

EID: 84859064821     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr151     Document Type: Article

References (75)

1. Achim AM, Lepage M. 2005. Neural correlates of memory for items and for associations: an event-related functional magnetic resonance imaging study. J Cogn Neurosc. 17:652-667.
2. Aminoff E, Gronau N, Bar M. 2007. The parahippocampal cortex mediates spatial and nonspatial associations. Cereb Cortex. 17:1493-1503.
3. Anderson JR. 1982. Acquisition of cognitive skill. Psychol Rev. 89:369-406.
4. Bast T. 2007. Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior. Rev Neurosci. 18:253-281.
5. Baxendale SA, Thompson PJ, Paesschen WV. 1998. A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia. 36:591-602.
6. Blaizot X, Mansilla F, Insausti AM, Constans JM, Salinas-Alamán A, Pró-Sistiaga P, Mohedano-Moriano A, Insausti R. 2010. The human parahippocampal region: I. temporal pole cytoarchitectonic and MRI correlation. Cereb Cortex. 20:2198-2212.
7. Bohbot VD, Allen JJ, Nadel L. 2000. Memory deficits characterized by patterns of lesions to the hippocampus and parahippocampal cortex. Ann N Y Acad Sci. 911:355-368.
8. Brown MW, Aggleton JP. 2001. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci. 2:51-61.
9. Buffalo EA, Bellgowan PSF, Martin A. 2006. Distinct roles for medial temporal lobe structures in memory for objects and their locations. Learn Mem. 13:638-643.
10. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron. 35:625-641.
11. Chase WG, Simon HA. 1973. Perception in chess. Cogn Psychol. 4:55-81.
12. Danckert SL, Gati JS, Menon RS, Köhler S. 2007. Perirhinal and hippocampal contributions to visual recognition memory can be distinguished from those of occipito-temporal structures based on conscious awareness of prior occurrence. Hippocampus. 17:1081-1092.
13. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr Opin Neurobiol. 16:693-700.
14. Diana RA, Yonelinas AP, Ranganath C. 2007. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn Sci. 11:379-386.
15. Diana RA, Yonelinas AP, Ranganath C. 2008. High-resolution multi-voxel pattern analysis of category selectivity in the medial temporal lobes. Hippocampus. 18:536-541.
16. Duff MC, Hengst J, Tranel D, Cohen NJ. 2006. Development of shared information in communication despite hippocampal amnesia. Nat Neurosci. 9:140-146.
17. Eichenbaum H. 2004. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron. 44:109-120.
18. Eichenbaum H, Yonelinas AP, Ranganath C. 2007. The medial temporal lobe and recognition memory. Annu Rev Neurosci. 30:123-152.
19. Epstein R, Kanwisher N. 1998. A cortical representation of the local visual environment. Nature. 392:598-601.
20. Gallagher M, Holland PC. 1994. The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA. 91:11771-11776.
21. Glosser G, Salvucci AE, Chiaravalloti ND. 2003. Naming and recognizing famous faces in temporal lobe epilepsy. Neurology. 61:81-86.
22. Gobet F, Lane PC, Croker S, Cheng PCH, Jones G, Oliver I, Pine JM. 2001. Chunking mechanisms in human learning. Trends Cogn Sci. 5:236-243.
23. Goh JOS, Siong SC, Park D, Gutchess A, Hebrank A, Chee MWL. 2004. Cortical areas involved in object, background, and objectbackground processing revealed with functional magnetic resonance adaptation. J Neurosci. 24:10223-10228.
24. Greicius MD, Krasnow B, Boyett-Anderson JM, Eliez S, Schatzberg AF, Reiss AL, Menon V. 2003. Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study. Hippocampus. 13:164-174.
25. Hanke M, Halchenko YO, Sederberg PB, Hanson SJ, Haxby JV, Pollmann S. 2009. PyMVPA: a python toolbox for multivariate pattern analysis of fMRI data. Neuroinformatics. 7:37-53.
26. Hanke M, Halchenko YO, Sederberg PB, Olivetti E, Fründ I, Rieger JW, Herrmann CS, Haxby JV, Hanson SJ, Pollmann S. 2009. PyMVPA: a unifying approach to the analysis of neuroscientific data. Front Neuroinformatics. 3:1-13.
27. Hanson SJ, Halchenko YO. 2008. Brain reading using full brain support vector machines for object recognition: there is no "face" identification area. Neural Comput. 20:486-503.
28. Hanson SJ, Matsuka T, Haxby JV. 2004. Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a "face" area? Neuroimage. 23:156-166.
29. Hasher L, Zacks RT. 1979. Automatic and effortful processes in memory. J Exp Psychol Gen. 108:356-388.
30. Haskins AL, Yonelinas AP, Quamme JR, Ranganath C. 2008. Perirhinal cortex supports encoding and familiarity-based recognition of novel associations. Neuron. 59:554-560.
31. 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.
32. Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P. 2001. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science. 293:2425-2430.
33. Henke K. 2010. A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci. 11:523-532.
34. Jenkinson M, Bannister P, Brady M, Smith S. 2002. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 17:825-841.
35. Jenkinson M, Smith S. 2001. A global optimisation method for robust affine registration of brain images. Med Image Anal. 5:143-156.
36. Killgore WD, Casasanto DJ, Yurgelun-Todd DA, Maldjian JA, Detre JA. 2000. Functional activation of the left amygdala and hippocampus during associative encoding. Neuroreport. 11:2259-2263.
37. Kirwan CB, Stark CEL. 2004. Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus. 14:919-930.
38. Krishnapuram B, Carin L, Figueiredo MAT, Hartemink AJ. 2005. Sparse multinomial logistic regression: fast algorithms and generalization bounds. IEEE Trans Pattern Anal Mach Intell. 27:957-968.
39. Lehn H, Steffenach H-A, van Strien NM, Veltman DJ, Witter MP, Haberg AK. 2009. A specific role of the human hippocampus in recall of temporal sequences. J Neurosci. 29:3475-3484.
40. Logan GD. 1988. Toward an instance theory of automatization. Psychol Rev. 95:492-527.
41. Manelis A, Hanson C, Hanson SJ. 2011. Implicit memory for object locations depends on reactivation of encoding-related brain regions. Hum Brain Mapp. 32:32-50.
42. Martin A. 2007. The representation of object concepts in the brain. Annu Rev Psychol. 58:25-45.
43. Miller G. 1956. The magical number seven plus or minus two: some limits on our capacity for processing information. Psychol Rev. 63:81-97.
44. Musen G. 1996. Effects of task demands on implicit memory for objectlocation associations. Can J Exp Psychol. 50:104-113.
45. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S. 2004. NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci. 5:361-372.
46. Norman KA, O'Reilly RC. 2003. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learningsystems approach. Psychol Rev. 110:611-646.
47. Nunn JA, Graydon FJ, Polkey CE, Morris RG. 1999. Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. Brain. 122(Pt 1):47-59.
48. O'Reilly RC, Rudy JW. 2001. Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol Rev. 108:311-345.
49. O'Toole AJ, Jiang F, Abdi H, Pénard N, Dunlop JP, Parent MA. 2007. Theoretical, statistical, and practical perspectives on pattern-based classification approaches to the analysis of functional neuroimaging data. J Cogn Neurosci. 19:1735-1752.
50. Patterson K, Nestor PJ, Rogers TT. 2007. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci. 8:976-987.
51. Persson J, Nyberg L. 2000. Conjunction analysis of cortical activations common to encoding and retrieval. Microsc Res Tech. 51:39-44.
52. Peters J, Daum I, Gizewski E, Forsting M, Suchan B. 2009. Associations evoked during memory encoding recruit the context-network. Hippocampus. 19:141-151.
53. Pihlajamäki M, Tanila H, Hänninen T, Könönen M, Mikkonen M, Jalkanen V, Partanen K, Aronen HJ, Soininen H. 2003. Encoding of novel picture pairs activates the perirhinal cortex: an fMRI study. Hippocampus. 13:67-80.
54. Ploner CJ, Gaymard BM, Rivaud-Péchoux S, Baulac M, Clémenceau S, Samson S, Pierrot-Deseilligny C. 2000. Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex. 10:1211-1216.
55. Poldrack RA, Clark J, Paré-Blagoev EJ, Shohamy D, Moyano JC, Myers C, Gluck MA. 2001. Interactive memory systems in the human brain. Nature. 414:546-550.
56. Quamme JR, Yonelinas AP, Norman KA. 2007. Effect of unitization on associative recognition in amnesia. Hippocampus. 17:192-200.
57. Ramsøy TZ, Liptrot MG, Skimminge A, Lund TE, Sidaros K, Christensen MS, BaaréW, Paulson OB, Jernigan TL. 2009. Regional activation of the human medial temporal lobe during intentional encoding of objects and positions. Neuroimage. 47:1863-1872.
58. Ranganath C, Yonelinas AP, Cohen MX, Dy CJ, Tom SM, D'Esposito M. 2004. Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia. 42:2-13.
59. Robinson JL, Laird AR, Glahn DC, Lovallo WR, Fox PT. 2010. Metaanalytic connectivity modeling: delineating the functional connectivity of the human amygdala. Hum Brain Mapp. 31:173-184.
60. Rutishauser U, Mamelak AN, Schuman EM. 2006. Single-trial learning of novel stimuli by individual neurons of the human hippocampusamygdala complex. Neuron. 49:805-813.
61. Schaffera JR, Kima MJ. 2007. Number of replications required in control chart Monte Carlo simulation studies. Commun Stat Simul Comput. 36:1075-1087.
62. Schon K, Quiroz YT, Hasselmo ME, Stern CE. 2009. Greater working memory load results in greater medial temporal activity at retrieval. Cereb Cortex. 19:2561-2571.
63. Sharon T, Moscovitch M, Gilboa A. 2011. Rapid neocortical acquisition of long-term arbitrary associations independent of the hippocampus. Proc Natl Acad Sci USA. 108:1146-1151.
64. Smith ML, Milner B. 1989. Right hippocampal impairment in the recall of spatial location: encoding deficit or rapid forgetting? Neuropsychologia. 27:71-81.
65. Smith S. 2002. Fast robust automated brain extraction. Hum Brain Mapp. 17:143-155.
66. Sommer T, Rose M, Weiller C, Büchel C. 2005. Contributions of occipital, parietal and parahippocampal cortex to encoding of object-location associations. Neuropsychologia. 43:732-743.
67. Squire LR, Wixted JT, Clark RE. 2007. Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci. 8:872-883.
68. Staresina BP, Davachi L. 2006. Differential encoding mechanisms for subsequent associative recognition and free recall. J Neurosci. 26:9162-9172.
69. Staresina BP, Davachi L. 2008. Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J Cogn Neurosci. 20:1478-1489.
70. Staresina BP, Davachi L. 2010. Object unitization and associative memory formation are supported by distinct brain regions. J Neurosci. 30:9890-9897.
71. Vapnik V. 1995. The nature of statistical learning theory. New York: Springer.
72. Varma S, Simon R. 2006. Bias in error estimation when using crossvalidation for model selection. BMC Bioinformatics. 7:91.
73. Voss JL, Hauner KKY, Paller KA. 2009. Establishing a relationship between activity reduction in human perirhinal cortex and priming. Hippocampus. 19:773-778.
74. Yassa MA, Stark CEL. 2008. Multiple signals of recognition memory in the medial temporal lobe. Hippocampus. 18:945-954.
75. 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.