Medial temporal lobe contributions to short-term memory for faces

Journal of Experimental Psychology: General

Volumn 142, Issue 4, 2013, Pages 1309-1322

  Race, Elizabeth ^a   LaRocque, Karen F ^a   Keane, Margaret M ^b   Verfaellie, Mieke ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

Amnesia; Episodic memory; Hippocampus; Working memory

Indexed keywords

ARTICLE; BRAIN MAPPING; FACE; FEMALE; HUMAN; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; SHORT TERM MEMORY; TEMPORAL LOBE;

BRAIN MAPPING; FACE; FEMALE; HUMANS; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; TEMPORAL LOBE;

EID: 84887883437     PISSN: 00963445     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0033612     Document Type: Article

References (91)

1. Aggleton, J. P., Shaw, C., & Gaffan, E. A. (1992) The performance of postencephalitic amnesic subjects on two behavioural tests of memory: Concurrent discrimination learning and delayed matching-to-sample. Cortex, 28, 359-372. doi:10.1016/S0010-9452(13)80146-3
2. Atkinson, R. C., & Shiffrin, R. M. (1968). Human memory: A proposed system and its control processes. In K. W. Spence & J. T. Spence (Eds.), The psychology of learning and motivation (Vol. 2, pp. 89-195). doi: 10.1016/S0079-7421(08)60422-3
3. Awh, E., Jonides, J., Smith, E. E., Schumacher, E. H., Koeppe, R. A., & Katz, S. (1996) Dissociation of storage and rehearsal in verbal working memory: Evidence from positron emission tomography. Psychological Science, 7, 25-31. doi:10.1111/j.1467-9280.1996.tb00662.x
4. Axmacher, N., Mormann, F., Fernandez, G., Cohen, M. X., Elger, C. E., & Fell, J. (2007) Sustained neural activity patterns during working memory in the human medial temporal lobe. The Journal of Neuroscience, 27, 7807-7816. doi:10.1523/JNEUROSCI.0962-07.2007
5. Baddeley, A., Allen, R., & Vargha-Khadem, F. (2010). Is the hippocampus necessary for visual and verbal binding in working memory? Neuropsychologia, 48, 1089-1095. doi:10.1016/j.neuropsychologia.2009.12.009
6. Baddeley, A. D., & Warrington, E. K. (1970) Amnesia and the distinction between long-and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, 176-189. doi:10.1016/S0022-5371(70)80048-2
7. Barense, M. D., Henson, R. N., Lee, A. C., & Graham, K. S. (2010) Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint. Hippocampus, 20, 389-401. doi:10.1002/hipo.20641
8. Barrouillet, P., & Camos, V. (2012) As time goes by: Temporal constraints in working memory. Current Directions in Psychological Science, 21, 413-419. doi:10.1177/0963721412459513
9. Bergmann, H. C., Rijpkema, M., Fernandez, G., & Kessels, R. P. (2012) Distinct neural correlates of associative working memory and long-term memory encoding in the medial temporal lobe. NeuroImage, 63, 989-997. doi:10.1016/j.neuroimage.2012.03.047
10. Buffalo, E. A., Reber, P. J., & Squire, L. R. (1998). The human perirhinal cortex and recognition memory. Hippocampus, 8, 330-339. doi:10.1002/(SICI)1098-1063(1998)8:4<330::AID-HIPO3>3.0.CO;2-L
11. Cashdollar, N., Malecki, U., Rugg-Gunn, F. J., Duncan, J. S., Lavie, N., & Duzel, E. (2009) Hippocampus-dependent and -independent thetanetworks of active maintenance. Proceedings of the National Academy of Sciences, USA, 106, 20493-20498. doi:10.1073/pnas.0904823106
12. Cave, C. B., & Squire, L. R. (1992) Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus, 2, 151-163. doi:10.1002/hipo.450020207
13. Cohen, N. J., & Eichenbaum, H. E. (1993). Memory, amnesia, and the hippocampal system. Cambridge, MA: MIT Press.
14. Cohen, N. J., Ryan, J., Hunt, C., Romine, L., Wszalek, T., & Nash, C. (1999) Hippocampal system and declarative (relational) memory: Summarizing the data from functional neuroimaging studies. Hippocampus, 9, 83-98. doi:10.1002/(SICI)1098-1063(1999)9:1<83::AID-HIPO9>3.0.CO;2-7
15. Cowan, N. (1988) Evolving conceptions of memory storage, selective attention, and their mutual constraints within the human informationprocessing system. Psychological Bulletin, 104, 163-191. doi:10.1037/0033-2909.104.2.163
16. Cowan, N. (1999). An embedded-processes model of working memory. In A. Miyake & P. Shah (Eds.), Models of working memory: Mechanisms of active maintenance and executive control (pp. 62-101). doi:10.1017/CBO9781139174909.006
17. Crawford, J. R., & Howell, D. C. (1998) Comparing an individual's test score against norms derived from small samples. Clinical Neuropsychologist, 12, 482-486. doi:10.1076/clin.12.4.482.7241
18. Curby, K. M., & Gauthier, I. (2007) A visual short-term memory advantage for faces. Psychonomic Bulletin & Review, 14, 620-628. doi: 10.3758/BF03196811
19. Desmond, J. E., Gabrieli, J. D., Wagner, A. D., Ginier, B. L., & Glover, G. H. (1997). Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. The Journal of Neuroscience, 17, 9675-9685.
20. Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2007) Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends in Cognitive Sciences, 11, 379-386. doi:10.1016/j.tics .2007.08.001
21. Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2010) Medial temporal lobe activity during source retrieval reflects information type, not memory strength. Journal of Cognitive Neuroscience, 22, 1808-1818. doi: 10.1162/jocn.2009.21335
22. Eichenbaum, H., Schoenbaum, G., Young, B., & Bunsey, M. (1996) Functional organization of the hippocampal memory system. Proceedings of the National Academy of Sciences, USA, 93, 13500-13507. doi:10.1073/pnas.93.24.13500
23. Ezzyat, Y., & Olson, I. R. (2008) The medial temporal lobe and visual working memory: Comparisons across tasks, delays, and visual similarity. Cognitive, Affective, & Behavioral Neuroscience, 8, 32-40. doi:10.3758/CABN.8.1.32
24. Finke, C., Braun, M., Ostendorf, F., Lehmann, T. N., Hoffmann, K. T., Kopp, U., & Ploner, C. J. (2008) The human hippocampal formation mediates short-term memory of colour-location associations. Neuropsychologia, 46, 614-623. doi:10.1016/j.neuropsychologia.2007.10.004
25. Ford, J. H., Verfaellie, M., & Giovanello, K. S. (2010) Neural correlates of familiarity-based associative retrieval. Neuropsychologia, 48, 3019-3025. doi:10.1016/j.neuropsychologia.2010.06.010
26. Georghiades, A. S., Belhumeur, P. N., & Kriegman, D. J. (2001) From few to many: Illumination cone models for face recognition under variable lighting and pose. IEEE Transactions on Pattern Analysis and Machine Intelligence, 23, 643-660. doi:10.1109/34.927464
27. Giovanello, K. S., Keane, M. M., & Verfaellie, M. (2006) The contribution of familiarity to associative memory in amnesia. Neuropsychologia, 44, 1859-1865. doi:10.1016/j.neuropsychologia.2006.03.004
28. Giovanello, K. S., Verfaellie, M., & Keane, M. M. (2003) Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cognitive, Affective, & Behavioral Neuroscience, 3, 186-194. doi:10.3758/CABN.3.3.186
29. Graham, K. S., Barense, M. D., & Lee, A. C. (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. doi:10.1016/j.neuropsychologia.2010.01.001
30. Hannula, D. E., & Ranganath, C. (2008) Medial temporal lobe activity predicts successful relational memory binding. The Journal of Neuroscience, 28, 116-124. doi:10.1523/JNEUROSCI.3086-07.2008
31. Hannula, D. E., Tranel, D., & Cohen, N. J. (2006) The long and the short of it: Relational memory impairments in amnesia, even at short lags. The Journal of Neuroscience, 26, 8352-8359. doi:10.1523/JNEUROSCI.5222-05.2006
32. Hartley, T., Bird, C. M., Chan, D., Cipolotti, L., Husain, M., Vargha-Khadem, F., & Burgess, N. (2007) The hippocampus is required for short-term topographical memory in humans. Hippocampus, 17, 34-48. doi:10.1002/hipo.20240
33. Haskins, A. L., Yonelinas, A. P., Quamme, J. R., & Ranganath, C. (2008) Perirhinal cortex supports encoding and familiarity-based recognition of novel associations. Neuron, 59, 554-560. doi:10.1016/j.neuron.2008.07.035
34. Holdstock, J. S., Gutnikov, S. A., Gaffan, D., & Mayes, A. R. (2000) Perceptual and mnemonic matching-to-sample in humans: Contributions of the hippocampus, perirhinal and other medial temporal lobe cortices. Cortex, 36, 301-322. doi:10.1016/S0010-9452(08)70843-8
35. Hole, G. J. (1994) Configural factors in the perception of unfamiliar faces. Perception, 23, 65-74. doi:10.1068/p230065
36. Iidaka, T., Harada, T., Eifuku, S., Nakata, R., & Sadato, N. (2012) Distinct human face representations in the perirhinal cortex and fusiform gyrus. Brain Research, 1452, 119-129. doi:10.1016/j.brainres.2012.02.072
37. Jeneson, A., Mauldin, K. N., Hopkins, R. O., & Squire, L. R. (2011) The role of the hippocampus in retaining relational information across short delays: The importance of memory load. Learning & Memory, 18, 301-305. doi:10.1101/lm.2010711
38. Jeneson, A., Mauldin, K. N., & Squire, L. R. (2010). Intact working memory for relational information after medial temporal lobe damage. The Journal of Neuroscience, 30, 13624-13629. doi:10.1523/JNEUROSCI.2895-10.2010
39. Jeneson, A., & Squire, L. R. (2012) Working memory, long-term memory, and medial temporal lobe function. Learning & Memory, 19, 15-25. doi:10.1101/lm.024018.111
40. Jeneson, A., Wixted, J. T., Hopkins, R. O., & Squire, L. R. (2012) Visual working memory capacity and the medial temporal lobe. The Journal of Neuroscience, 32, 3584-3589. doi:10.1523/JNEUROSCI.6444-11.2012
41. Jonides, J., Lewis, R. L., Nee, D. E., Lustig, C. A., Berman, M. G., & Moore, K. S. (2008) The mind and brain of short-term memory. Annual Review of Psychology, 59, 193-224. doi:10.1146/annurev.psych.59.103006.093615
42. Jonides, J., Schumacher, E. H., Smith, E. E., Koeppe, R. A., Awh, E., Reuter-Lorenz, P. A., . . . Willis, C. R. (1998). The role of parietal cortex in verbal working memory. The Journal of Neuroscience, 18, 5026-5034.
43. Kan, I. P., Giovanello, K. S., Schnyer, D. M., Makris, N., & Verfaellie, M. (2007) Role of the medial temporal lobes in relational memory: Neuropsychological evidence from a cued recognition paradigm. Neuropsychologia, 45, 2589-2597. doi:10.1016/j.neuropsychologia.2007.03.006
44. Konkel, A., & Cohen, N. J. (2009) Relational memory and the hippocampus: Representations and methods. Frontiers in Neuroscience, 3, 166-174. doi:10.3389/neuro.01.023.2009
45. Lee, A. C., Scahill, V. L., & Graham, K. S. (2008) Activating the medial temporal lobe during oddity judgment for faces and scenes. Cerebral Cortex, 18, 683-696. doi:10.1093/cercor/bhm104
46. Logie, R. H., Zucco, G. M., & Baddeley, A. D. (1990) Interference with visual short-term memory. Acta Psychologica, 75, 55-74. doi:10.1016/0001-6918(90)90066-O
47. Luck, D., Danion, J. M., Marrer, C., Pham, B. T., Gounot, D., & Foucher, J. (2010) The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory. Brain and Cognition, 72, 255-263. doi:10.1016/j.bandc.2009.09.009
48. Maurer, D., Grand, R. L., & Mondloch, C. J. (2002) The many faces of configural processing. Trends in Cognitive Sciences, 6, 255-260. doi: 10.1016/S1364-6613(02)01903-4
49. Mayes, A., Montaldi, D., & Migo, E. (2007) Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11, 126-135. doi:10.1016/j.tics.2006.12.003
50. Mitchell, K. J., Johnson, M. K., Raye, C. L., & D'Esposito, M. (2000) fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Cognitive Brain Research, 10, 197-206. doi: 10.1016/S0926-6410(00)00029-X
51. Nee, D. E., & Jonides, J. (2011) Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory. NeuroImage, 54, 1540-1548. doi:10.1016/j .neuroimage.2010.09.002
52. Nichols, E. A., Kao, Y. C., Verfaellie, M., & Gabrieli, J. D. (2006) Working memory and long-term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus, 16, 604-616. doi:10.1002/hipo.20190
53. Norman, K. A., & O'Reilly, R. C. (2003) Modeling hippocampal and neocortical contributions to recognition memory: A complementarylearning-systems approach. Psychological Review, 110, 611-646. doi: 10.1037/0033-295X.110.4.611
54. Olsen, R. K., Moses, S. N., Riggs, L., & Ryan, J. D. (2012). The hippocampus supports multiple cognitive processes through relational binding and comparison. Frontiers in Human Neuroscience, 6, 146. doi: 10.3389/fnhum.2012.00146
55. Olsen, R. K., Nichols, E. A., Chen, J., Hunt, J. F., Glover, G. H., Gabrieli, J. D., & Wagner, A. D. (2009) Performance-related sustained and anticipatory activity in human medial temporal lobe during delayed match-to-sample. The Journal of Neuroscience, 29, 11880-11890. doi: 10.1523/JNEUROSCI.2245-09.2009
56. Olson, I. R., Moore, K. S., Stark, M., & Chatterjee, A. (2006) Visual working memory is impaired when the medial temporal lobe is damaged. Journal of Cognitive Neuroscience, 18, 1087-1097. doi:10.1162/jocn .2006.18.7.1087
57. Olson, I. R., Page, K., Moore, K. S., Chatterjee, A., & Verfaellie, M. (2006). Working memory for conjunctions relies on the medial temporal lobe. The Journal of Neuroscience, 26, 4596-4601. doi:10.1523/JNEUROSCI.1923-05.2006
58. O'Reilly, R. C., & Rudy, J. W. (2001) Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychological Review, 108, 311-345. doi:10.1037/0033-295X.108.2.311
59. Owen, A. M., Sahakian, B. J., Semple, J., Polkey, C. E., & Robbins, T. W. (1995) Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalohippocampectomy in man. Neuropsychologia, 33, 1-24. doi:10.1016/0028-3932(94)00098-A
60. Paulesu, E., Frith, C. D., & Frackowiak, R. S. (1993, March 25). The neural correlates of the verbal component of working memory. Nature, 362, 342-345. doi:10.1038/362342a0
61. Peterson, L. R., & Peterson, M. J. (1959) Short-term retention of individual verbal items. Journal of Experimental Psychology, 58, 193-198. doi:10.1037/h0049234
62. Piekema, C., Fernandez, G., Postma, A., Hendriks, M. P., Wester, A. J., & Kessels, R. P. (2007) Spatial and non-spatial contextual working memory in patients with diencephalic or hippocampal dysfunction. Brain Research, 1172, 103-109. doi:10.1016/j.brainres.2007.07.066
63. Piekema, C., Kessels, R. P., Mars, R. B., Petersson, K. M., & Fernandez, G. (2006) The right hippocampus participates in short-term memory maintenance of object-location associations. NeuroImage, 33, 374-382. doi:10.1016/j.neuroimage.2006.06.035
64. Piekema, C., Kessels, R. P., Rijpkema, M., & Fernandez, G. (2009) The hippocampus supports encoding of between-domain associations within working memory. Learning & Memory, 16, 231-234. doi:10.1101/lm .1283109
65. Piepers, D. W., & Robbins, R. A. (2012). A review and clarification of the terms "holistic," "configural," and "relational" in the face perception literature. Frontiers in Psychology, 3, 559. doi:10.3389/fpsyg.2012.00559
66. Preston, A. R., Bornstein, A. M., Hutchinson, J. B., Gaare, M. E., Glover, G. H., & Wagner, A. D. (2010) High-resolution fMRI of contentsensitive subsequent memory responses in human medial temporal lobe. Journal of Cognitive Neuroscience, 22, 156-173. doi:10.1162/jocn.2009.21195
67. Preston, A. R., & Gabrieli, J. D. E. (2008) Dissociation between explicit memory and configural memory in the human medial temporal lobe. Cerebral Cortex, 18, 2192-2207. doi:10.1093/cercor/bhm245
68. Quamme, J. R., Yonelinas, A. P., & Norman, K. A. (2007) Effect of unitization on associative recognition in amnesia. Hippocampus, 17, 192-200. doi:10.1002/hipo.20257
69. Ranganath, C., & Blumenfeld, R. S. (2005) Doubts about double dissociations between short-and long-term memory. Trends in Cognitive Sciences, 9, 374-380. doi:10.1016/j.tics.2005.06.009
70. Ranganath, C., Cohen, M. X., & Brozinsky, C. J. (2005) Working memory maintenance contributes to long-term memory formation: Neural and behavioral evidence. Journal of Cognitive Neuroscience, 17, 994-1010. doi:10.1162/0898929054475118
71. Ranganath, C., & D'Esposito, M. (2001) Medial temporal lobe activity associated with active maintenance of novel information. Neuron, 31, 865-873. doi:10.1016/S0896-6273(01)00411-1
72. Rhodes, G. (1988) Looking at faces: First-order and second-order features as determinants of facial appearance. Perception, 17, 43-63. doi: 10.1068/p170043
73. Richler, J. J., Tanaka, J. W., Brown, D. D., & Gauthier, I. (2008). Why does selective attention to parts fail in face processing? Journal of Experimental Psychology: Learning, Memory, and Cognition, 34, 1356-1368. doi:10.1037/a0013080
74. Rose, N. S., Olsen, R. K., Craik, F. I., & Rosenbaum, R. S. (2012) Working memory and amnesia: The role of stimulus novelty. Neuropsychologia, 50, 11-18. doi:10.1016/j.neuropsychologia.2011.10.016
75. Ryan, J. D., & Cohen, N. J. (2004) The nature of change detection and online representations of scenes. Journal of Experimental Psychology: Human Perception and Performance, 30, 988-1015. doi:10.1037/0096-1523.30.5.988
76. Schon, K., Hasselmo, M. E., Lopresti, M. L., Tricarico, M. D., & Stern, C. E. (2004) Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: A functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. The Journal of Neuroscience, 24, 11088-11097. doi:10.1523/JNEUROSCI.3807-04.2004
77. Schon, K., Ross, R. S., Hasselmo, M. E., & Stern, C. E. (2013) Complementary roles of medial temporal lobes and mid-dorsolateral prefrontal cortex for working memory for novel and familiar trial-unique visual stimuli. European Journal of Neuroscience, 37, 668-678. doi:10.1111/ejn.12062
78. Schultz, H., Sommer, T., & Peters, J. (2012) Direct evidence for domainsensitive functional subregions in human entorhinal cortex. The Journal of Neuroscience, 32, 4716-4723. doi:10.1523/JNEUROSCI.5126-11.2012
79. Schumacher, E. H., Lauber, E., Awh, E., Jonides, J., Smith, E. E., & Koeppe, R. A. (1996) PET evidence for an amodal verbal working memory system. NeuroImage, 3, 79-88. doi:10.1006/nimg.1996.0009
80. Scoville, W. B., & Milner, B. (1957) Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery & Psychiatry, 20, 11-21. doi:10.1136/jnnp.20.1.11
81. Sergent, J. (1984) An investigation into component and configural processes underlying face perception. British Journal of Psychology, 75, 221-242. doi:10.1111/j.2044-8295.1984.tb01895.x
82. Shrager, Y., Levy, D. A., Hopkins, R. O., & Squire, L. R. (2008) Working memory and the organization of brain systems. The Journal of Neuroscience, 28, 4818-4822. doi:10.1523/JNEUROSCI.0710-08.2008
83. Sidman, M., Stoddard, L. T., & Mohr, J. P. (1968) Some additional quantitative observations of immediate memory in a patient with bilat-eral hippocampal lesions. Neuropsychologia, 6, 245-254. doi:10.1016/0028-3932(68)90023-7
84. Staresina, B. P., & Davachi, L. (2008) Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. Journal of Cognitive Neuroscience, 20, 1478-1489. doi:10.1162/jocn.2008.20104
85. Trost, S., & Gruber, O. (2012) Evidence for a double dissociation of articulatory rehearsal and non-articulatory maintenance of phonological information in human verbal working memory. Neuropsychobiology, 65, 133-140. doi:10.1159/000332335
86. Warren, D. E., Duff, M. C., Tranel, D., & Cohen, N. J. (2011) Observing degradation of visual representations over short intervals when medial temporal lobe is damaged. Journal of Cognitive Neuroscience, 23, 3862-3873. doi:10.1162/jocn_a_00089
87. Warrington, E. K., & Taylor, A. M. (1973). Immediate memory for faces: Long-or short-term memory? The Quarterly Journal of Experimental Psychology, 25, 316-322. doi:10.1080/14640747308400352
88. Wickelgren, W. A. (1968) Sparing of short-term memory in an amnesic patient: Implications for strength theory of memory. Neuropsychologia, 6, 235-244. doi:10.1016/0028-3932(68)90022-5
89. Young, A. W., Hellawell, D., & Hay, D. C. (1987) Configural information in face perception. Perception, 16, 747-759. doi:10.1068/p160747
90. Yushkevich, P. A., Piven, J., Hazlett, H. C., Smith, R. G., Ho, S., Gee, J. C., & Gerig, G. (2006) User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. NeuroImage, 31, 1116-1128. doi:10.1016/j.neuroimage.2006.01.015
91. Zhao, M., & Hayward, W. G. (2010) Holistic processing underlies gender judgments of faces. Attention, Perception, & Psychophysics, 72, 591-596. doi:10.3758/APP.72.3.591