Building memories: Remembering and forgetting of verbal experiences as predicted by brain activity

Science

Volumn 281, Issue 5380, 1998, Pages 1188-1191

  Wagner, Anthony D ^a,b   Schacter, Daniel L ^b   Rotte, Michael ^a,b,d   Koutstaal, Wilma ^b   Maril, Anat ^b   Dale, Anders M ^a   Rosen, Bruce R ^a   Buckner, Randy L ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY   (United States)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; EVENT RELATED POTENTIAL; EXPERIENCE; HUMAN; HUMAN EXPERIMENT; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; TEMPORAL CORTEX; VERBAL MEMORY;

EID: 0032555511     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.281.5380.1188     Document Type: Article

References (43)

1. F. I. M. Craik and R. S. Lockhart, J. Verbal Learn. Verbal Behav. 11, 671 (1972).
2. S. E. Petersen, P. T. Fox, M. I. Posner, M. Mintun, M. E. Raichle, Nature 331, 585 (1988); S. Kapur et al., Proc. Natl. Acad. Sci. U.S.A. 91, 2008 (1994); J. D. E. Gabrieli et al., Psychol. Sci. 7, 278 (1996). For reviews, see L. Nyberg, R. Cabeza, E. Tulving, Psychonomic Bull. Rev. 3, 135 (1996); R. L. Buckner and W. Koutstaal, Proc. Natl. Acad. Sci. U.S.A. 95, 891 (1998).
3. S. E. Petersen, P. T. Fox, M. I. Posner, M. Mintun, M. E. Raichle, Nature 331, 585 (1988); S. Kapur et al., Proc. Natl. Acad. Sci. U.S.A. 91, 2008 (1994); J. D. E. Gabrieli et al., Psychol. Sci. 7, 278 (1996). For reviews, see L. Nyberg, R. Cabeza, E. Tulving, Psychonomic Bull. Rev. 3, 135 (1996); R. L. Buckner and W. Koutstaal, Proc. Natl. Acad. Sci. U.S.A. 95, 891 (1998).
4. S. E. Petersen, P. T. Fox, M. I. Posner, M. Mintun, M. E. Raichle, Nature 331, 585 (1988); S. Kapur et al., Proc. Natl. Acad. Sci. U.S.A. 91, 2008 (1994); J. D. E. Gabrieli et al., Psychol. Sci. 7, 278 (1996). For reviews, see L. Nyberg, R. Cabeza, E. Tulving, Psychonomic Bull. Rev. 3, 135 (1996); R. L. Buckner and W. Koutstaal, Proc. Natl. Acad. Sci. U.S.A. 95, 891 (1998).
5. S. E. Petersen, P. T. Fox, M. I. Posner, M. Mintun, M. E. Raichle, Nature 331, 585 (1988); S. Kapur et al., Proc. Natl. Acad. Sci. U.S.A. 91, 2008 (1994); J. D. E. Gabrieli et al., Psychol. Sci. 7, 278 (1996). For reviews, see L. Nyberg, R. Cabeza, E. Tulving, Psychonomic Bull. Rev. 3, 135 (1996); R. L. Buckner and W. Koutstaal, Proc. Natl. Acad. Sci. U.S.A. 95, 891 (1998).
6. S. E. Petersen, P. T. Fox, M. I. Posner, M. Mintun, M. E. Raichle, Nature 331, 585 (1988); S. Kapur et al., Proc. Natl. Acad. Sci. U.S.A. 91, 2008 (1994); J. D. E. Gabrieli et al., Psychol. Sci. 7, 278 (1996). For reviews, see L. Nyberg, R. Cabeza, E. Tulving, Psychonomic Bull. Rev. 3, 135 (1996); R. L. Buckner and W. Koutstaal, Proc. Natl. Acad. Sci. U.S.A. 95, 891 (1998).
7. P. C. Fletcher et al., Brain 118, 401 (1995); C. L. Grady et al., Science 269, 218 (1995).
8. P. C. Fletcher et al., Brain 118, 401 (1995); C. L. Grady et al., Science 269, 218 (1995).
9. T. F. Sanquist, J. W. Rohrbaugh, K. Syndulko, D. B. Lindsley, Psychophysiology 17, 568 (1980); E. Halgren and M. E. Smith, Hum. Neurobiol. 6, 129 (1987); K. A. Paller, M. Kutas, A. R. Mayes, Electroencephalogr. Clin. Neurophysiol. 67, 360 (1987); M. Fabiani and E. Donchin, J. Exp. Psychol. Learn. Mem. Cogn. 21, 224 (1995).
10. T. F. Sanquist, J. W. Rohrbaugh, K. Syndulko, D. B. Lindsley, Psychophysiology 17, 568 (1980); E. Halgren and M. E. Smith, Hum. Neurobiol. 6, 129 (1987); K. A. Paller, M. Kutas, A. R. Mayes, Electroencephalogr. Clin. Neurophysiol. 67, 360 (1987); M. Fabiani and E. Donchin, J. Exp. Psychol. Learn. Mem. Cogn. 21, 224 (1995).
11. T. F. Sanquist, J. W. Rohrbaugh, K. Syndulko, D. B. Lindsley, Psychophysiology 17, 568 (1980); E. Halgren and M. E. Smith, Hum. Neurobiol. 6, 129 (1987); K. A. Paller, M. Kutas, A. R. Mayes, Electroencephalogr. Clin. Neurophysiol. 67, 360 (1987); M. Fabiani and E. Donchin, J. Exp. Psychol. Learn. Mem. Cogn. 21, 224 (1995).
12. T. F. Sanquist, J. W. Rohrbaugh, K. Syndulko, D. B. Lindsley, Psychophysiology 17, 568 (1980); E. Halgren and M. E. Smith, Hum. Neurobiol. 6, 129 (1987); K. A. Paller, M. Kutas, A. R. Mayes, Electroencephalogr. Clin. Neurophysiol. 67, 360 (1987); M. Fabiani and E. Donchin, J. Exp. Psychol. Learn. Mem. Cogn. 21, 224 (1995).
13. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957); L. R. Squire, Psychol. Rev. 99, 195 (1992); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993).
14. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957); L. R. Squire, Psychol. Rev. 99, 195 (1992); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993).
15. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957); L. R. Squire, Psychol. Rev. 99, 195 (1992); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993).
16. C. E. Stern et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8660 (1996); E. Tulving, H. J. Markowitsch, F. I. M. Craik, R. Habib, S. Houle, Cereb. Cortex 6, 71 (1996); J. D. E. Gabrieli, J. B. Brewer, J. E. Desmond, G. H. Glover, Science 276, 264 (1997).
17. C. E. Stern et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8660 (1996); E. Tulving, H. J. Markowitsch, F. I. M. Craik, R. Habib, S. Houle, Cereb. Cortex 6, 71 (1996); J. D. E. Gabrieli, J. B. Brewer, J. E. Desmond, G. H. Glover, Science 276, 264 (1997).
18. C. E. Stern et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8660 (1996); E. Tulving, H. J. Markowitsch, F. I. M. Craik, R. Habib, S. Houle, Cereb. Cortex 6, 71 (1996); J. D. E. Gabrieli, J. B. Brewer, J. E. Desmond, G. H. Glover, Science 276, 264 (1997).
19. A. M. Dale and R. L. Buckner, Hum. Brain Mapp. 5, 329 (1997); R. L. Buckner et al., Neuron 20, 285 (1998).
20. A. M. Dale and R. L. Buckner, Hum. Brain Mapp. 5, 329 (1997); R. L. Buckner et al., Neuron 20, 285 (1998).
21. 2*-weighted asymmetric spin-echo sequence: TR = 2 s, TE = 50 ms, 180° offset = -25 ms).
22. During each of four scans, blocks were ordered: nonsemantic (40 s), fixation (24 s), semantic (40 s), fixation, nonsemantic, fixation, semantic. A brief (8 s) fixation block began each scan. During semantic and nonsemantic blocks, 20 words were visually presented: 10 abstract and 10 concrete nouns; half in uppercase and half in lowercase letters. Each word was presented for 1 s followed by 1 s of fixation between words. Subjects responded by left-handed key press. During fixation blocks, a cross-hair (" + ") was presented for the entire duration.
23. Alpha was set to P < 0.05 for all behavioral analyses. Response latencies differed across tasks [F(1, 11) = 89.97]. Memory was assessed in the scanner 20 to 40 m later, using a yes-no recognition procedure (8). Subsequent memory differed across tasks [F(1,11) = 69.50].
24. Functional runs were averaged within each subject, transformed into stereotaxic atlas space, and averaged across subjects (8). Activation maps were constructed using a nonparametric Kolmogorov-Smirnov statistic to compare (i) word processing (semantic and nonsemantic) to fixation and (ii) semantic to nonsemantic processing. Peak activations were identified by selecting local statistical activation maxima that were P < 0.001 within clusters of five contiguous significant voxels. These criteria minimize false positives, as verified using the logic of control functional runs [E. Zarahn, G. K. Aguirre, M. D'Esposito, Neuroimage 5, 179 (1997)].
25. 2*-weighted gradient echo sequence (3.0-T, 128 images, TR = 2 s, TE = 30 ms, flip angle = 90°). During each scan, 40 abstract word trials, 40 concrete word trials, and 40 fixation trials were rapidly intermixed, with each trial lasting 2 s. For fixation trials, the fixation point remained on the screen for the entire 2 s. For word trials, the word was presented for 750 ms followed by 1250 ms of fixation. Abstract, concrete, and fixation trials were pseudo-randomly intermixed with counterbalancing (each trial type followed every other trial type equally often).
26. Approximately 20 min later, subjects were administered a memory test consisting of 480 studied and 480 unstudied words. Words were presented individually with self-paced timing. Subjects responded "high confidence studied," "low confidence studied," or "new."
27. An Item Type X Response interaction [F(1,12) = 22.97] revealed that studied items were endorsed as "high confidence studied" more frequently than were unstudied items [52% and 7%, respectively; F(1,12) = 57.04], whereas studied and unstudied items were similarly endorsed as "low confidence studied" [24% and 20%; (F < 1.0)]. The low confidence response class likely reflects subject guessing and does not differentiate between encountered and novel stimuli.
28. Encoding task performance was analyzed based on whether the words were subsequently remembered with high confidence ("high confidence hits"), low confidence ("low confidence hits"), or were forgotten ("misses"). Accuracy during encoding was comparable for high confidence hits (88% correct), low confidence hits (88% correct), and misses (89% correct) (F < 1.0). Semantic decision RTs declined across trial types [F(2,24) = 9.26]: RTs were longer for high confidence hits (1000 ms) compared to low confidence hits (966 ms) [F(1,12) = 5.40], which were in turn longer compared to misses (936 ms) [F(1,12) = 3.91, P < 0.06].
29. The procedures for selective averaging and statistical map generation for rapidly intermixed trials are described elsewhere (7). Statistical activation maps were constructed based on the differences between trial types using a t-statistic (7). Fixation trial events were subtracted from the word trial events (collaps-ing across subsequent memory). Miss trial events and high confidence hit events were subtracted from each other, as were those for miss trial events and low confidence hit events. Clusters of five or more voxels exceeding a statistical threshold of P < 0.001 were considered significant foci of activation (7).
30. In addition, modest but significantly greater activation for high confidence hits relative to misses was noted in a more ventral extent of left inferior frontal gyrus [Brodmann's area (BA) 47: -34, 31, -3], left precentral gyrus (BA 6: -31, 0, 56), medial superior frontal gyrus (BA 8: -3, 28, 43), and left superior occipital gyrus (BA 19: -31, -77, 34). The superior occipital and medial superior frontal activations can be seen in Fig. 2. Two regions demonstrated less activation for high confidence hits relative to misses: precuneus (BA 31: 3, -43, 40) and left middle frontal gyrus (BA 9: -12, 31, 34). No regions demonstrated greater activation for low confidence hits relative to misses, which is in accord with the behavioral data indicating that these two trial types likely did not mnemonically differ.
31. M. D'Esposito et al., Neuroimage 6, 113 (1997). A similar interpretation may be applicable to the results from the blocked-design experiment. However, greater left prefrontal activation during semantic processing has been noted even when the nonsemantic processing task has a longer duty cycle [J. B. Demb et al., J. Neurosci. 15, 5870 (1995)].
32. M. D'Esposito et al., Neuroimage 6, 113 (1997). A similar interpretation may be applicable to the results from the blocked-design experiment. However, greater left prefrontal activation during semantic processing has been noted even when the nonsemantic processing task has a longer duty cycle [J. B. Demb et al., J. Neurosci. 15, 5870 (1995)].
33. RTs were matched as follows. First, the median RT across all trial types was determined for each subject. Trials with response latencies that fell below the median RT were selected and sorted based on subsequent memory. Selection of trials in this manner resulted in matched RTs for the high confidence hit (852 ms) and mist (839 ms) trial types [F(1,12) = 2.32, P > 0.15)].
34. J. B. Brewer, Z. Zhao, J. E. Desmond, G. H. Glover, J. D. E. Gabrieli, Science 281, 1185 (1998); G. Fernandez et al., J. Neurosci. 18, 1841 (1998).
35. J. B. Brewer, Z. Zhao, J. E. Desmond, G. H. Glover, J. D. E. Gabrieli, Science 281, 1185 (1998); G. Fernandez et al., J. Neurosci. 18, 1841 (1998).
36. R. J. Dolan and P. C. Fletcher, Nature 388, 582 (1997).
37. W. A. Suzuki and D. G. Amaral, J. Comp. Neurol. 350, 497 (1994).
38. J. Jonides et al., Nature 363, 623 (1993); J. A. Fiez et al., J. Neurosci. 16, 808 (1996); R. L. Buckner, Psychonomic Bull. Rev. 3, 149 (1996); A. D. Wagner, J. E. Desmond, J. B. Demb, G. H. Glover, J. D. E. Gabrieli, J. Cogn. Neurosci. 9, 714 (1997).
39. J. Jonides et al., Nature 363, 623 (1993); J. A. Fiez et al., J. Neurosci. 16, 808 (1996); R. L. Buckner, Psychonomic Bull. Rev. 3, 149 (1996); A. D. Wagner, J. E. Desmond, J. B. Demb, G. H. Glover, J. D. E. Gabrieli, J. Cogn. Neurosci. 9, 714 (1997).
40. J. Jonides et al., Nature 363, 623 (1993); J. A. Fiez et al., J. Neurosci. 16, 808 (1996); R. L. Buckner, Psychonomic Bull. Rev. 3, 149 (1996); A. D. Wagner, J. E. Desmond, J. B. Demb, G. H. Glover, J. D. E. Gabrieli, J. Cogn. Neurosci. 9, 714 (1997).
41. J. Jonides et al., Nature 363, 623 (1993); J. A. Fiez et al., J. Neurosci. 16, 808 (1996); R. L. Buckner, Psychonomic Bull. Rev. 3, 149 (1996); A. D. Wagner, J. E. Desmond, J. B. Demb, G. H. Glover, J. D. E. Gabrieli, J. Cogn. Neurosci. 9, 714 (1997).
42. M. Moscovitch, J. Cogn. Neurosci. 4, 257 (1992).
43. Supported by grants from the National Institute on Aging (AG08441 and AG05778), the National Institute on Deafness and Other Communication Disorders (DC03245-02), the Human Frontiers Science Program, and the Deutsche Forschungsgemeinschaft (SFB426). We thank Y. and W. Jacobson and two anonymous referees for helpful comments on an earlier version of this manuscript, and C. Brenner and C. Racine for assistance with data collection.