The role of recollection and familiarity in the functional differentiation of the medial temporal lobes

Hippocampus

Volumn 20, Issue 11, 2010, Pages 1291-1314

  Montaldi, Daniela ^a   Mayes, Andrew R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Dual process theory; Familiarity; Hippocampus; Medial temporal lobe; Perirhinal cortex; Recognition; Recollection

Indexed keywords

ARTICLE; ASSOCIATIVE MEMORY; BRAIN CORTEX; BRAIN FUNCTION; CONVERGENCE RECOLLECTION AND FAMILIARITY THEORY; CYTOARCHITECTURE; DECLARATIVE MEMORY; DENTATE GYRUS; ENTORHINAL CORTEX; EPISODIC MEMORY; FAMILIARITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPAL FIMBRIA; HUMAN; MEDIAL TEMPORAL LOBE; MEMORY; PRIORITY JOURNAL; RECALL; RECOGNITION; RECOLLECTION; SEMANTIC MEMORY; SUBICULUM; TEMPORAL LOBE; THEORY;

ANIMALS; HUMANS; MAGNETIC RESONANCE IMAGING; MENTAL RECALL; MODELS, PSYCHOLOGICAL; RECOGNITION (PSYCHOLOGY); TEMPORAL LOBE;

EID: 77958165866     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20853     Document Type: Article

References (109)

1. Adlam AR, Malloy M, Mishkin M, Vargha-Khadem F. 2009. Dissociation between recognition and recall in developmental amnesia. Neuropsychologia 47: 2207-2210.
2. Aggleton JP, Brown MW. 1999. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22: 425-444.
3. Aggleton JP, Brown MW. 2005. Contrasting hippocampal and perirhinal cortex function using immediate early gene imaging. Quart J Exp Psychol B 58: 218-223.
4. Aggleton JP, Vann SD, Denby C, Dix S, Mayes AR, Roberts N, Yonelinas AP. 2005. Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology. Neuropsychologia 43: 1810-1823.
5. Albasser MM, Poirier GL, Aggleton JP. 2010. Qualitatively different modes of perirhinal-hippocampal engagement when rats explore novel vs familiar objects as revealed by c-Fos imaging. Eur J Neurosci 31: 134-147.
6. Amin E, Pearce JM, Brown MW, Aggleton JP. 2006. Novel temporal configurations of stimuli produce discrete changes in immediate-early gene expression in the rat hippocampus. Eur J Neurosci 24: 2611-2621.
7. Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J, editors. 2007. The Hippocampus Book. Oxford: Oxford University Press.
8. Bachevalier J, Nemanic S. 2008. Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus 18: 64-80.
9. Baddeley A, Emslie H, Nimmo-Smith I. 1994. The Doors and People Test: A Test of Visual and Verbal Recall and Recognition. Bury St Edmonds, UK: Thames Valley Test Company.
10. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319: 1640-1642.
11. Bastin C, Van der Linden M, Charnallet A, Denby C, Montaldi D, Roberts N, Mayes AR. 2004. Dissociation between recall and recognition memory performance in an amnesic patient following carbon monoxide poisoning. Neurocase 10: 330-344.
12. Bastin C, Van der Linden M, Schnakers C, Montaldi D, Mayes AR. 2010. The contribution of familiarity to within- and between-domain associative recognition memory: Use of a modified remember/know procedure. Eur J Cogn Psychol 22: 922-943.
13. Bird CM, Burgess N. 2008. The hippocampus supports recognition memory for familiar words but not unfamiliar faces. Curr Biol 18: 1932-1936.
14. 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.
15. Bowles B, Crupi C, Mirsattari SM, Pigott SE, Parrent AG, Pruessner JC, Yonelinas AP, Kohler S. 2007. Impaired familiarity with preserved recollection after anterior temporal-lobe resection that spares the hippocampus. Proc Natl Acad Sci 104: 16382-16387.
16. Brown MW, Aggleton JP. 2001. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51-61.
17. Buffalo EA, Ramus SJ, Squire LR, Zola SM. 2000. Perception and recognition memory in monkeys following lesions of area TE, perirhinal cortex. Learn Mem 7: 375-382.
18. Cassaday HJ, Rawlins JNP. 1997. The hippocampus, objects, and their contexts. Behav Neurosci 111: 1228-1244.
19. Clelland CD, Choi M, Romberg C, Clemenson GD, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ. 2009. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325: 210-213.
20. Cohn M, Moscovitch M, Lahat A, McAndrews MP. 2009. Recollection versus strength as the primary determinant of hippocampal engagement at retrieval. Proc Natl Acad Sci 106: 22451-22455.
21. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr Opin Neurobiol 16: 693-700.
22. 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 100: 2157-2162.
23. Davies RR, Graham KS, Xuereb JH, Williams GB, Hodges JR. 2004. The human perirhinal cortex and semantic memory. Eur J Neurosci 20: 2441-2446.
24. Dewhurst SA, Holmes SJ, Brandt KR, Dean GM. 2006. Measuring the speed of the conscious components of recognition memory: Remembering is faster than knowing. Consciousness Cogn 15: 147-162.
25. 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.
26. Diana RA, Yonelinas AP, Ranganath C. 2010. Medial temporal lobe activity during source retrieval reflects information type, not memory strength. J Cogn Neurosci 22: 1808-1818.
27. Duzel E, Vargha-Khadem F, Heinze HJ, Mishkin M. 2001. Brain activity evidence for recognition without recollection early hippocampal damage. Proc Natl Acad Sci 98: 8101-8106.
28. Easton A, Zinkivskay A, Eacott MJ. 2009. Recollection is impaired, but familiarity remains intact in rats with lesions of the fornix. Hippocampus 19: 837-843.
29. Eichenbaum H, Cohen NJ. 2001. From Conditioning to Conscious Recollection: Memory Systems of the Brain. New York: Oxford University Press.
30. Fanselow MS. 2010. From contextual fear to a dynamic view of memory systems. Trends Cogn Sci 14: 7-15.
31. Fernandez G, Tendolkar I. 2006. The rhinal cortex: 'Gatekeeper' of the declarative memory system. Trends Cogn Sci 10: 358-362.
32. Gilbert PE, Kesner RP, Lee I. 2001. Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1. Hippocampus 11: 626-636.
33. Graham KS, Barense MD, Lee ACH. 2010. Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia 48: 831-853.
34. Griffiths S, Scott H, Glover C, Bienemann A, Ghorbel MT, Uney J, Brown MW, Warburton EC, Bashir ZI. 2009. Expression of long-term depression underlies visual recognition memory. Neuron 58: 186-194.
35. Hannula DE, Ryan JD, Tranel D, Cohen NJ. 2007. Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia. J Cogn Neurosci 19: 1690-1705.
36. Harlow IM, MacKenzie G, Donaldson DI. Familiarity for associations? A test of domain dichotomy theory. J Exp Psychol: Learn Mem Cogn (in press).
37. Holdstock JS, Mayes AR, Roberts N, Cezayirli E, Isaac CL, O'Reilly RC, Norman KA. 2002. Under what conditions is recognition spared relative to recall following selective hippocampal lesions in humans? Hippocampus 12: 341-351.
38. Holdstock JS, Parslow DM, Morris RG, Fleminger S, Abrahams S, Denby C, Montaldi D, Mayes AR. 2008. Two case studies illustrating how relatively selective hippocampal lesions in humans can have quite different effects on memory. Hippocampus 18: 679-691.
39. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey. II. Cortical afferents. J Comp Neurol 264: 356-395.
40. Jeneson A, Kirwan CB, Hopkins RO, Wixted JT, Squire LR. 2010. Recognition memory and the hippocampus: A test of the hippocampal contribution to recollection and familiarity. Learn Mem 17: 63-70.
41. Jenkins TA, Amin E, Pearce JM, Brown MW, Aggleton JP. 2004. Novel spatial arrangements of familiar visual stimuli promote activity in the rats' hippocampal formation but not the parahippocampal cortices: A c-Fos expression study. Neuroscience 124: 43-52.
42. Jenkins TA, Amin E, Brown MW, Aggleton JP. 2006. Changes in immediate early gene expression in the rat brain after unilateral lesions of the hippocampus. Neuroscience 137: 747-759.
43. Johnson JD, McDuff SGR, Rugg MD, Norman KA. 2009. Recollection, familiarity and cortical reinstatement: A multivoxel pattern analysis. Neuron 63: 697-708.
44. Kemp A, Manahan-Vaughan D. 2007. Hippocampal long-term depression: Master or minion in hippocampal declarative memory processing? Trends Neurosci 30: 111-118.
45. Kesner RP, Lee I, Gilbert P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15: 333-351.
46. Kirwan CB, Wixted JT, Squire LR. 2010a. Activity in the medial temporal lobe predicts memory strength, whereas activity in the prefrontal cortex predicts recollection. J Neurosci 28: 10541-10548.
47. Kirwan CB, Wixted JT, Squire LR. 2010b. A demonstration that the hippocampus supports both recollection and familiarity. Proc Natl Acad Sci 107: 344-348.
48. Kohler S, Danckert S, Gati JS, Menon RS. 2005. Novelty responses to relational and non-relational information in the hippocampus and the parahippocampal region: A comparison based on event-related fMRI. Hippocampus 15: 763-774.
49. Lavenex P, Amaral DG. 2000. Hippocampal-neocortical interactivity: A hierarchy of associativity. Hippocampus 10: 420-430.
50. McHugh TJ, Jones MW, Quinn JJ, Balthazar 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: 94-97.
51. Macken WJ. 2002. Environmental context and recognition: The role of recollection and familiarity. J Exp Psychol: Learn Mem Cogn 28: 153-161.
52. Maguire EA, Frith CD, Rudge P, Cipolotti L. 2001. The effect of adult-acquired hippocampal damage on memory retrieval: An fMRI study. Neuroimage 27: 146-152.
53. Maguire EA, Vargha-Khadem F, Mishkin M. 2005. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124: 1156-1170.
54. Manns JR, Squire LR. 1999. Impaired recognition memory on the Doors and People test after damage limited to the hippocampal region. Hippocampus 9: 495-499.
55. Manns JR, Squire LR. 2001. Perceptual learning, awareness, and the hippocampus. Hippocampus 11: 776-782.
56. Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR. 2003. Recognition memory and the human hippocampus. Neuron 37: 171-180.
57. Mayes A, Montaldi D, Migo E. 2007. Associative memory and the medial temporal lobes. Trends Cogn Sci 11: 126-135.
58. Mayes AR, Holdstock JS, Isaac CL, Hunkin NM, Roberts N. 2002. Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 12: 325-340.
59. Mayes AR, Isaac CL, Holdstock JS, Cariga P, Gummer A, Roberts N. 2003. Long-term amnesia: A review and illustrative case study. Cortex 39: 567-603.
60. Mayes AR, Holdstock JS, Isaac CL, Montaldi D, Grigor J, Gummer A, Cariga P, Downes JJ, Tsivilis D, Gaffan D, Norman KA 2004. Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition. Hippocampus 14: 763-784.
61. Mickes L, Wais PE, Wixted JT. 2009. Recollection is a continuous process: Implications for dual-process theories of recognition memory. Psychol Sci 20: 509-515.
62. Migo E, Montaldi D, Norman KA, Quamme J, Mayes AR. 2009. The contribution of familiarity to recognition memory is a function of test format when using similar foils. Quart J Exp Psychol 62: 1198-1215.
63. Montaldi D, Mayes AR, Barnes A, Pirie H, Hadley DM, Patterson J, Wyper D. 1998. Associative encoding of pictures activates the medial temporal lobes. Hum Brain Mapp 6: 85-104.
64. Montaldi D, Spencer TJ, Roberts N, Mayes AR. 2006. The neural system that mediates familiarity memory. Hippocampus 16: 504-520.
65. Mountcastle VB. 1997. The columnar organization of the neocortex. Brain 120: 701-722.
66. Murray EA, Wise SP. 2004. What, if anything, is the medial temporal lobe, and how can the amygdala be part of it if there is no such thing? Neurobiol Learn Mem 82: 178-198.
67. Norman G, Eacott MJ. 2005. Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav Neurosci 119: 557-566.
68. Norman KA, O'Reilly RC. 2003. Modeling hippocampal and neocortical contributions to recognition memory: A complementary learning systems approach. Psychol Rev 110: 611-646.
69. Parkinson J, Aggleton JP. 1994. The failure of context shifts to alter the recognition of faces: Implications for contextual deficits in amnesia. Cortex 30: 351-354.
70. Parks CM, Yonelinas AP. 2007. Moving beyond pure signal-detection models: Comment on Wixted (2007). Psychol Rev 114: 188-201.
71. Parks CM, Yonelinas AP. 2009. Evidence for a memory threshold in second choice recognition memory responses. Proc Natl Acad Sci 106: 11515-11519.
72. Perfect T, Mayes AR, Downes JJ, Van Eijk R. 1996. Does context discriminate recollection from familiarity in recognition memory? Quart J Exp Psychol A 49: 797-813.
73. Quamme JR, Yonelinas AP, Norman KA. 2007. Effect of unitization on associative recognition in amnesia. Hippocampus 17: 192-200.
74. 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.
75. Ranganath C, Heller A, Cohen MX, Brozinsky CJ, Rissman J. 2005. Functional connectivity with the hippocampus during successful memory formation. Hippocampus 15: 997-1005.
76. Rempel-Clower NL, Zola SM, Squire LR, Amaral DG. 1996. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci 16: 5233-5255.
77. Rissman J, Gazzaley A, D'Esposito M. 2008. Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. Cereb Cortex 18: 1618-1629.
78. Rockland KS, Van Hoesen GW. 1999. Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus. Cereb Cortex 9: 232-237.
79. Shimamura AP, Wickens TD. 2009. Superadditivity memory strength for item and source recognition: The role of hierarchical relational binding in the medial temporal lobe. Psychol Rev 116: 1-19.
80. Squire L, Wixted J, Clark R. 2007. Recognition memory and the medial temporal lobe: A new perspective. Nat Rev Neurosci 8: 872-883.
81. Squire LR, Shimamura AP, Amaral D. 1989. Memory and the hippocampus. In: Byrne JH, Berry WO, editors. Neural Models of Plasticity. New York: Academic Press. pp 208-239.
82. Staresina BP, Davachi L. 2006. Differential encoding mechanisms for subsequent associative recognition and free recall. J Neurosci 26: 9162-9172.
83. Staresina BP, Davachi L. 2008. Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J Cogn Neurosci 21: 581-593.
84. Sziklas V, Petrides M. 2002. Effects of lesions to the hippocampus or the fornix on allocentric conditional associative learning in rats. Hippocampus 12: 543-550.
85. Suzuki WA. 1996. The anatomy, physiology and functions of the perirhinal cortex. Curr Opin Neurobiol 6: 179-186.
86. Suzuki WA. 2010. Untangling memory from perception in the medial temporal lobe. Trends Cogn Sci 14: 195-200.
87. Suzuki WA, Amaral DG. 1994. Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. J Comp Neurol 350: 497-533.
88. Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP. 2008. A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat Neurosci 11: 834-842.
89. Turriziani P, Fadda SL, Caltagirone C, Carlesimo GA. 2008. Recollection and familiarity in hippocampal amnesia. Neuropsychologia 42: 426-433.
90. Vago DR, Bevan A, Kesner RP. 2007. The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval. Hippocampus 17: 977-987.
91. Van Strien NM, Cappaert NLM, Witter MP. 2009. The anatomy of memory: An interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10: 272-282.
92. Vann SD, Albasser MM. 2009. Hippocampal, retrosplenial and prefrontal hypoactivity in a model of diencephalic amnesia: Evidence towards an interdependent subcortical-cortical memory network. Hippocampus 19: 1090-1102.
93. Vann SD, Tsivilis D, Denby CE, Quamme JR, Yonelinas AP, Aggleton JP, Montaldi D, Mayes AR. 2009. Impaired recollection but spared familiarity in patients with extended hippocampal system damage revealed by three convergent methods. Proc Natl Acad Sci 106: 5442-5447.
94. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M. 1997. Developmental amnesia: Effect of early hippocampal pathology on episodic and semantic memory. Science 277: 376-380.
95. Wais PE, Wixted JT, Hopkins RO, Squire LR. 2006. The hippocampus supports both the recollection and the familiarity components of recognition memory. Neuron 49: 459-466.
96. Wais PE, Mickes L, Wixted JT. 2008. Remember/know judgments probe degree of recollection. J Cogn Neurosci 20: 400-405.
97. Wais PE, Squire LR, Wixted JT. 2010. In search of recollection and familiarity signals in the hippocampus. J Cogn Neurosci 22: 109-123.
98. Wan H, Aggleton JP, Brown MW. 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19: 1142-1148.
99. Wilson MA, McNaughton BL. 2009. Dynamics of the hippocampal ensemble. Science 261: 1055-1058.
100. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ. 2004. Double dissociation between the effects of peri-post rhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Heterogeneity of function within the temporal lobe. J Neurosci 24: 5901-5908.
101. Wolk DA, Dunfee KL, Dickerson BC, Aizenstein HJ, DeKosky ST. A medial temporal lobe division of labor: Insights from memory in aging and early Alzheimer disease. Hippocampus (in press).
102. Yonelinas AP. 2002. The nature of recollection and familiarity: A review of 30 years of research. J Mem Lang 46: 441-517.
103. Yonelinas AP, Kroll NEA, Dobbins IG, Soltani M. 1999. Recognition memory for faces: When familiarity supports associative recognition judgments. Psychonom Bull Rev 6: 654-661.
104. Yonelinas AP, Kroll NEA, Quamme JR, Lazzara MM, Sauve MJ, Widaman KF, Knight RT. 2002. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5: 1236-1241.
105. Yonelinas AP, Otten LJ, Shaw KN, Rugg MD. 2005. Separating the brain regions involved in recollection and familiarity in recognition memory. J Neurosci 25: 3002-3008.
106. Yonelinas AP, Widaman K, Mungas D, Reed B, Weiner MW, Chui HC. 2007. Memory in the aging brain: Doubly dissociating the contribution of the hippocampus and the entorhinal cortex. Hippocampus 17: 1134-1140.
107. Yovel G, Paller KA. 2004. The neural basis of the butcher-on-the-bus phenomenon: When a face seems familiar but is not remembered. Neuroimage 21: 789-800.
108. Zhong YM, Rockland KS. 2004. Connections between the anterior inferotemporal cortex (area TE) and CA1 of the hippocampus in monkey. Exp Brain Res 155: 311-319.
109. Zola-Morgan S, Squire LR, Ramus SJ. 1994. Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system. Hippocampus 4: 483-495.