When encoding yields remembering: Insights from event-related neuroimaging

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1387, 1999, Pages 1307-1324

  Wagner, Anthony D ^a,b   Koutstaal, Wilma ^a   Schacter, Daniel L ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Episodic encoding; Episodic memory; Event related potentials; FMRI; PET; Subsequent memory effect

Indexed keywords

EID: 0033614972     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0481     Document Type: Article

References (101)

1. Alkire, M. T., Haier, R. J., Fallon, J. H. & Cahill, L. 1998 Hippocampal, but not amygdala, activity at encoding correlates with long-term, free recall of non-emotional information. Proc. Natl Acad. Sci. USA 95, 14 506 14 510.
2. Awh, E. & Jonides, J. 1998 Spatial working memory and spatial selective attention. In The attentive brain (ed. R. Parasuraman), pp. 353-380. Cambridge, MA: MIT Press.
3. Awh, E., Jonides, J., Smith, E., Schumacher, E., Koeppe, R. & Katz, S. 1996 Dissociation of storage and rehearsal in verbal working memory: evidence from positron emission tomography. Psychol. Sci. 7, 25-31.
4. Besson, M. & Kutas, M. 1993 The many facets of repetition: a cued-recall and event-related potential analysis of repeating words in same versus different sentence contexts. J. Exp. Psychol. Learn. Mem. Cogn. 19, 1115-1133.
5. Brewer, J. B., Zhao, A., Desmund, J. E., Glover, G. H. & Gabrieli, J. D. E. 1998 Making memories: brain activity that predicts how well visual experience will be remembered. Science 281, 1185-1187.
6. Buckner, R. L. 1996 Beyond HERA: contributions of specific prefrontal brain areas to long-term memory retrieval. Psychonomic Bull. Rev. 3, 149-158.
7. Buckner, R. L. & Koutstaal, W. 1998 Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. Proc. Natl Acad. Sci. USA 95, 891-898.
8. Buckner, R. L., Bandettini, P., O'Craven, K., Savoy, R., Petersen, S. E., Raichle, M. E. & Rosen, B. R. 1996 Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proc. Natl Acad. Sci. USA 93, 14 878-14 883.
9. Chapman, R. M., McCrary, J. W. & Chapman, J. A. 1978 Short-term memory: the 'storage' component of human brain responses predicts recall. Science 202, 1211-1214.
10. Craik, F. I. M. & Lockhart, R. S. 1972 Levels of processing: a framework for memory research. J. Verb. Learn. Verb. Behav. 11, 671-684.
11. Craik, F. I. M. & Tulving, E. 1975 Depth of processing and the retention of words in episodic memory. J. Exp. Psychol. 104, 268-294.
12. Dale, A. M. & Buckner, R. L. 1997 Selective averaging of rapidly presented individual trials using fMRI. Hum. Brain Mapp. 5, 329-340.
13. Demb, J. B., Desmond, J. E., Wagner, A. D., Vaidya, C. J., Glover, G. H. & Gabrieli, J. D. E. 1995 Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity. J. Neurosci. 15, 5870-5878.
14. D'Esposito, M., Aguirre, G., Zarahn, E., Ballard, D., Shin, R. & Lease, J. 1998 Functional MRI studies of spatial and nonspatial working memory. Cog. Brain Res. 7, 1-13.
15. Dolan, R. J. & Fletcher, P. C. 1997 Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature 388, 582-585.
16. Donchin, E. 1981 Surprise? ... Surprise! Psychophysiology 18, 493-513.
17. Einstein, G. O. & Hunt, R. R. 1980 Levels of processing and organization: additive effects of individual-item and relational processing. J. Exp. Psychol. Hum. Learn. Mem. 6, 588-598.
18. Elger, C. E., Grunwald, T., Lehnertz, K., Kutas, M., Helmstaedter, C., Brockhaus, A., Van Roost, D. & Heinze, H. J. 1997 Human temporal lobe potentials in verbal learning and memory processes, Neuropsychologia 35, 657-667.
19. Fabiani, M. & Donchin, E. 1995 Encoding processes and memory organization: a model of the Von Restoff effect. J. Exp. Psychol. Learn. Mem. Cogn. 21, 224-240.
20. Fabiani, M., Karis, D. & Donchin, E. 1985 Effects of strategy manipulation on P300 amplitude in a Von Rostorff paradigm. Psychophysiology 22, 588-589.
21. Fabiani, M., Karis, D. & Donchin, E. 1986 P300 and recall in an incidental memory paradigm. Psychophysiology 23, 298-308.
22. Fabiani, M., Karis, D. & Donchin, E. 1990 Effects of mnemonic strategy manipulation in a Von Restorff paradigm. Electroencephalogr. Clin. Neurophysiol. 75, 22-35.
23. Fernandez, G. (and 10 others) 1998 Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance study. J. Neurosci. 18, 1841-1847.
24. Fernandez, G., Brewer, J. B., Zhao, Z., Glover, G. H. & Gabrieli, J. D. E. 1999 The magnitude of sustained entorhinal activity during intentional memorizing of words predicts subsequent cued recall performance: an event-related functional MRI study. Hippocampus 9, 35-44.
25. Fiez, J., Raichle, M., Balota, D., Tallal, P. & Petersen, S. 1996 PET activation of posterior temporal regions during auditory word presentation and verb generation. Cereb. Cortex 6, 1-10.
26. Fletcher, P. C., Frith, C. D., Grasby, P. M., Shallice, T., Frackowiak, R. S. J. & Dolan, R. J. 1995 Brain systems for encoding and retrieval of auditory verbal memory: an in vivo study in humans. Brain 118, 401-446.
27. Fox, A. M., Michie, P. T. & Coltheart, M. 1990 ERP effects of temporal and spatial recall with verbal and visual stimuli. In Psychophysiological brain research (ed. C. H. M. Brunia, A. W. Gaillard & A. Kok), pp. 236-239. Tilburg, Germany: Tilburg University Press.
28. Friedman, D. 1990a Cognitive event-related potential components during continuous recognition memory for pictures. Psychophysiology 27, 136-148.
29. Friedman, D. 1990b ERPs during continuous recognition memory for words. Biol. Psychol. 30, 61-87.
30. Friedman, D. 1992 Event-related potential investigations of cognitive development and aging. Ann. NY Acad. Sci. 658, 33-64.
31. Friedman, D. & Sutton, S. 1987 Event-related potentials during continuous recognition memory. In Current trends in event-related potential research, EEG Suppl. 40 (ed. R. Johnson, Jr, J. W. Rohrbaugh & R. Parasuraman), pp. 316-321. Amsterdam: Elsevier.
32. Friedman, D., Ritter, W. & Snodgrass, J. G. 1996 ERPs during study as a function of subsequent direct and indirect memory testing in young and old adults. Cog. Brain Res. 4, 1-13.
33. Gabrieli, J. D. E. 1998 Cognitive neuroscience of human memory. A. Rev. Psychol. 49, 87-115.
34. Gabrieli, J. D. E., Brewer, J. B., Desmond, J. E. & Glover, G. H. 1997 Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276, 264-266.
35. Gardiner, J. M. & Java, R. I. 1993 Recognizing and remembering. In Theories of memory (ed. A. F. Collins, S. E. Gathercole, M. A. Conway & P. E. Morris), pp. 163-188. Hove, UK: Erlbaum Associates.
36. Halgren, E. & Smith, M. E. 1987 Cognitive evoked potentials as modulatory processes in human memory formation and retrieval. Hum. Neurobiol. 6, 129-139.
37. Halgren, E., Lewine, J. D., Marinkovic, K., Buckner, R. L., Paulson, K. M., Chauvel, P., Rosen, B. R. & Dale, A. M. 1998 Anatomically-constrained distributed cortical activation patterns from MEG during word-processing: validation using fMRI and intracranial EEG. NeuroImage 4, S175.
38. Haxby, J., Ungerleider, L., Horwitz, B., Maisog, J., Rappapori, S. & Grady, C. 1996 Face encoding and recognition in the human brain. Proc. Natl Acad. Sci. USA 93, 922-927.
39. Heinze, II. J. (and 11 others) 1994 Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature 372, 543-546.
40. Hunt, R. R. & Einstein, G. O. 1981 Relational and item-specific information in memory. J. Verb. Learn. Verb. Behav. 20, 497-514.
41. Johnson, M. K., Hashtroudi, S. & Lindsay, D. S. 1993 Source monitoring. Psychol. Bull. 114, 3-28.
42. Johnson, R., Pfefferbaum, A. & Kopell, B. S. 1985 P300 and long-term memory: latency predicts recognition performance. Psychophysiology 22, 497-507.
43. Josephs, O., Turner, R, & Friston, K. 1997 Event-related fMRI. Hum. Brain Mapp. 5, 243-248.
44. Kapur, S., Craik, F. I. M., Tulving, E., Wilson, A. A., Houle, S. & Brown, G. M. 1994 Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proc. Natl Acad. Sci. USA 91, 2008-2011.
45. Kapur, S., Tulving, E., Cabeza, R., McIntosh, R., Houle, S. & Craik, F. 1996 Neural correlates of intentional learning of verbal materials: a PET study in humans. Cog. Brain Res. 4, 243-249.
46. Karis, D., Bashore, T., Fabiani, M. & Donchin, E. 1982 P300 and memory. Psychophysioloy 19, 328.
47. Karis, D., Fabiani, M. & Donchin, E. 1984 'P300' and memory: individual differences in the Von Restorff effect. Cog. Psychol. 16, 177-216.
48. Kelley, W. M. (and 10 others) 1998 Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20, 927-936.
49. Klein, D., Milner, B., Zatorre, R. J., Meyer, M. & Evans, A. C. 1995 The neural substrates underlying word generation: a bilingual functional-imaging study. Proc. Natl Acad. Sci. USA 92, 2899-2903.
50. Konishi, S., Yoneyama, R., Itagaki, H., Uchida, I., Nakajima, K., Kato, H., Okajima, K., Koizumi, H. & Miyashita, Y. 1996 Transient brain activity used in magnetic resonance imaging to detect functional areas. NeoroReport 8, 19-23.
51. Kutas, M. 1988 Review of event-related potential studies of memory. In Perspectives in memory research (ed. M. S. Gazzaniga), pp. 182-217. Cambridge, MA: MIT Press.
52. Lepage, M., Habib, R. & Tulving, E. 1998 Hippocampal PDT activations of memory encoding and retrieval: the HIPER model. Hippocampus 8, 313-322.
53. Liu, A. K., Bellivean, J. W. & Dale, A. M. 1998 Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. Proc. Natl Acad. Sci. USA 95, 8945-8950.
54. McCarthy, G., Blamire, A., Rothman, D., Gruetter, R. & Shulman, R. 1993 Echo-planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc. Natl Acad. Sci. USA 90, 4952-4956.
55. Mandler, G. 1980 Rocognizing: the judgment of previous occurrence. Psychol. Rev. 87, 252-271.
56. Mangun, G. R., Buonocore, M. H., Girelli, M. & Jha, A. P. 1998 ERF and fMRI measures of visual spatial selective attention. Hum. Brain Mapp. 6, 383-389.
57. Martin, A., Wiggs, C. L. & Weisberg. J. 1997 Modulation of human medial temporal lobe activity by form, meaning, and experience, Hippocampus 7, 587-593.
58. Menon, R. S., Luknowsky, D. C. & Gati, J. S. 1998 Mental chronometry using latency-resolved functional MRI. Proc. Natl Acad. Sci. USA 95, 10 902-10 907.
59. Morris, C. D., Bransford, J. D. & Franks, J. J. 1977 Levels of processing versus transfer appropriate processing. J. Verb. Learn. Verb. Behav. 16, 519-533.
60. Munte, T. F., Heinze, II. J., Scbolz, M. & Kunkel, H. 1988 Effects of a cholinergic nootropic (WEB 1881 FU) on event-related potentials recorded in incidental and intentional memory tasks. Neuropsychobiohgy 19, 158-168.
61. Musen, G. & Triesman, A. 1990 Implicit and explicit memory for visual patterns. J. Exp. Pychol. Learn. Mem. Cogn. 16, 127-137.
62. Neville, H. J., Kutas, M., Chesney, G. & Schmidt, A. L. 1986 Event-related brain potentials during initial encoding and recognition memory of congruous and incongruous words. J. Mem. Lang. 25, 75-92.
63. Nyberg, L. 1998 Mapping episodic memory. Behav. Brain Res. 90, 107-114.
64. Nyberg, L., Cabeza, R. & Tulving, E. 1996 PET studies of encoding and retrieval: the HERA model. Psychonomic Bull. Rev. 3, 135-148.
65. Paller, K. A. 1990 Recall and stem-completion priming have different electrophysiological correlates and are modified differentially by directed forgetting. J. Exp. Psychol. Learn. Mem. Cogn. 16, 1021-1032.
66. Paller, K. A. & Kutas, M. 1992 Brain potentials during memory retrieval provide neurophysiological support for the distinction between conscious recollection and priming, J. Cog. Neorosci. 4, 375-391.
67. Paller, K. A., Kutas, M. & Mayes, A. R. 1987a Neural correlates of encoding in an incidental learning paradigm. Electroencephalogr. Clin. Neurophysiol. 67, 360-371.
68. Paller, K. A., Kutas, M., Shimamura, A. P. & Squire, L. R. 1987b Brain responses to concrete and abstract words reflect processes that correlate with later performance on a test of stem-completion priming. In Current trends in event-related potential research, EEG Suppl. 40 (ed. R. Johnson Jr. J. W. Rohrbaugh & R. Parasuraman), pp. 360-365. Amsterdam: Elsevier.
69. Paller, K. A., McCarthy, G. & Wood, C. C. 1988 ERPs predictive of subsequent recall and recognition performance. Biol. Psychol. 26, 269-276.
70. Paulesu, E., Frith, C. D. & Frackowiak, R. S. J. 1993 The neural correlates of the verbal component of working memory. Nature 362, 342-345.
71. Petersen, S. E., Fox, P. T., Posner, M. I., Mintum, M. & Raichle, M. E. 1988 Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 331, 585-589.
72. Ruediger III, H. L. & McDermott, K. B. 1993 Implicit memory in normal human subjects. In Handbook of neuropsychology, vol. 8 (ed. H. Spinnler & F. Boller), pp. 63-131. Amsterdam: Elsevier.
73. Rombouts, S., Machielsen, W., Witter, M., Barkhof, F, Lindeboom, J. & Seheltens, P. 1997 Visual association encoding activates the medial temporal lobe: a functional magnetic resonance imaging study. Hippocampus 7, 594-601.
74. Rosen, B. R., Buckner, R. L, & Dale, A. M. 1998 Event-related functional MRI: past, present, and future. Proc. Natl Acad. Sci. USA 95, 773-780.
75. Rugg, M. D. 1990 The recall of repeated and unrepeated words: an ERP analysis. In Psychophysiological brain research (ed. C. H. M. Brunia, A. W. Gaillard & A. Kok), pp. 248-251. Tilburg, Germany: Tilburg University Press.
76. Rugg, M. D. 1995a Event-related potential studies of human memory. In The cognitive neurosciences (ed. M. S. Gazzaniga), pp. 789-801. Cambridge, MA: MIT Press.
77. Rugg, M. D. 1995b ERP studies of memory. In Electrophysiology of mind (ed. M. D. Rugg & M. G. H. Coles), pp. 130-170. Oxford University Press.
78. Rugg, M. D. 1998 Memories are made of this. Science 281, 1151-1152.
79. Sanquist, T. F., Rohrbaugh, J. W., Syndulko, K. & Lindsley, D. B. 1980 Electrophysiological signs of levels of processing: perceptual analysis and recognition memory. Psychophysiology 17, 568-576.
80. Schaden, D. L. 1987 Implicit memory: history and current status. J. Exp. Psychol. Learn. Mem. Cogn. 13, 501-518.
81. Schacter, D. L. 1996 Searching for memory: the brain, the mind, and the past. New York: Basic Books.
82. Schacter, D. L. & Tulving, E. 1982 Memory, amnesia, and the episodic/semantic distinction. In The expression of knowledge (ed. R. L. Isaacson & N. L. Spear), pp. 33-61. New York: Plenum Press.
83. Schacter, D. L. & Wagner, A. D. 1999 Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9, 7-24.
84. Schacter, D. L., Bowers, J. & Booker, J. 1989 Intention, awareness, and implicit memory: the retrieval intentionality criterion. In Implicit memory: theoretical issues (ed. S. Lewandowsky, J. C. Dunn & K. Kirsner), pp. 47-69. Hillsdale, NJ: Erlbaum.
85. Schacter, D. L., Chiu, C. Y. P. & Ochsner, K. N. 1993 Implicit memory: a selective review. A. Rev. Neurosci. 16, 159-182.
86. Schmidt, S. R. 1985 Encoding and retrieval processes in the memory for conceptually distinctive events. J. Exp. Psychol. Learn. Mem. Cogn. 11, 565-578.
87. Shallire,T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S. J. & Dolan, R. J. 1994 Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 368, 633-635.
88. Smith, M. E. 1993 Neurophysiological manifestations of re-collective experience during recognition memory judgments. J. Cog. Neorosci. 5, 1-13.
89. Squire, L. R. 1992 Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195-231.
90. Stern, C. E., Corkin, S., Gonzalez, R. G., Guimaraes, A. R., Baker, J. R., Jennings, P. J., Carr, C. A., Sugiura, R. M., Vedantham, V. & Rosen, B. R. 1996 The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc. Natl Acad. Sci. USA 93, 8660-8665.
91. Tulving, E. 1983 Elements of episodic memory. Oxford: Clarendon Press.
92. Tulving, E. 1985 Memory and consciousness. Can. Psychol. 26, 1-12.
93. Tulving, E. & Thompson, D. M. 1973 Encoding specificity and retrieval processes in episodic memory. Psychol. Rev. 80, 352-373.
94. Tulving, E., Kapur, S., Craik, F. I. M., Moscovitch, M. & Houle, S. 1994 Hemispheric, encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc. Natl Acad. Sci. USA 91, 2016-2020.
95. Tulving, E., Markowitsch, H., Craik, F., Habib, R. & Houle, S. 1996 Novelty and familiarity activations in PET studies of memory encoding and retrieval. Cereb. Cortex 6, 71-79.
96. Van Petten, C. & Senkfor, A. J. 1996 Memory for words and novel visual patterns: repetition, recognition, and encoding effects in the event-related brain potential. Psychophysiology 33, 491-506.
97. Wagner, A. D. 1999 Working memory contributions to human learning and remembering. Neuron 22, 19-22.
98. Wagner, A. D., Poldrack, R. A., Eldridge, L., Desmond, J. E., Glover, G. H. & Gabrieli, J. D. E. 1998a Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. NeuroReport 9, 3711-3717.
99. Wagner, A. D., Schacten D. L., Rotte, M., Koutstaal, W., Maril, A., Dale, A. M., Rosen, B. R. & Buckner, R. L. 1998b Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188-1191.
100. Weyerts, H., Tendolkar, I., Smid, H. G. O. M. & Heinze, H.-J. 1997 ERPs to encoding and recognition in two different inter-item association tasks. NeoroReport 8, 1583-1588.
101. Zarahn, E., Aguirre, G. & D'Esposito, M. 1997 A trial-based experimental design for fMRI. NeuroImage 6, 122-138.