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The Journal of Neuroscience, November 1, 2002, 22(21):9541-9548
Neural Correlates of Successful Encoding Identified Using Functional Magnetic Resonance Imaging
Paul J. Reber1, 3, Robert M. Siwiec1, Darren R. Gitleman2, 3, Todd B. Parrish2, 3, M.-Marsel Mesulam3, and Ken A. Paller1, 3 Departments of 1 Psychology and 2 Radiology and the 3 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University, Evanston, Illinois 60201
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Neural activity that occurs during the creation of a new memory trace can be observed using functional magnetic resonance imaging (fMRI). Event-related designs have been used to demonstrate that activity in prefrontal and medial temporal lobe areas is associated with successful memory storage. Here we contrasted activity associated with encoding success and encoding effort. Participants viewed a series of 150 words but attempted to remember only half of them. Encoding effort was manipulated using a cue in the form of a letter (R or F) presented after each word to instruct participants either to remember or to forget that word. Increased activity in left inferior prefrontal cortex was observed when words were followed by the cue to remember. In contrast, increased left medial temporal lobe activity was observed for words that were successfully recalled later. These results show that fMRI correlates of the intention to encode a word are different from fMRI correlates of whether that encoding is successful. Prefrontal activation was strongly associated with intentional verbal encoding, whereas left medial temporal activation was crucial for the encoding that actually led to successful memory on the subsequent test.
Key words: episodic memory; medial temporal lobe; prefrontal cortex; event-related fMRI; subsequent memory; encoding effort
INTRODUCTION
Neuropsychological evidence indicates that memory for recently experienced episodes depends critically on a number of interconnected brain regions, including the medial temporal lobe (MTL) and prefrontal cortex (Squire and Knowlton, 2000
; Squire and Schacter, 2002
Neural events responsible for the formation of episodic memories have been investigated previously (for review, see Paller and Wagner, 2002
In the present study, we monitored neural activity associated with encoding and analyzed the influence of two factors. The first was whether later recognition was successful. The second was the extent to which the participant intended to memorize the stimulus information. Intention to remember was manipulated with a procedure known as directed forgetting (DF). Typical DF procedures entail cues to participants to remember some items and forget others. DF instructions at encoding can have a robust influence on subsequent memorability (Bjork, 1989
Participants viewed words and faces and were instructed to remember or forget individual items on the basis of a cue presented 1 sec after each stimulus. The 1 sec delay gave participants adequate time to perceive, identify, and attend to each study item before knowing whether to remember or forget. For analysis, trials were sorted on the basis of the instruction (remember/forget) as well as on the subsequent memory outcome, assessed with a post-scan recognition test. We thus contrasted encoding intention and encoding success.
MATERIALS AND METHODS
Participants. Twelve right-handed volunteers (9 women, 3 men) between the ages of 18 and 25 years (mean = 20) were recruited from the Northwestern University community and screened for compatibility with MRI scanning. Data from six other participants were eliminated after testing because of errors in stimulus presentation. All participants were native speakers of English. Each participant was in good health and free from neurological and psychiatric problems. All participants gave informed consent, and the study was approved by the Institutional Review Board of Northwestern University.
Stimulus materials. Word stimuli were selected from the MRC Psycholinguistic Database (http://www.psy.uwa.edu.au/MRCDataBase/uwa_mrc.htm). Words ranged in frequency from 30 to 40 occurrences per million (Kucera and Francis, 1967
Procedure. On each trial, a word or a face was shown for 1000 msec, followed by either a cue to remember (a green "R") or a cue to forget (a red "F") for 1500 msec and then by a 500 msec intertrial interval during which a fixation cross was shown. Participants were instructed to watch all stimuli but to remember only stimuli followed by the remember cue. To ensure that a minimum level of attention was paid to each stimulus, we required participants to respond on each trial by indicating with a button press whether they had seen a face or word. A short demonstration was used to familiarize participants with the stimuli and cues. They were then situated in the MR scanner, as described below, and the study phase was administered in five scanning runs. Each run included 30 words and 30 faces, half with a remember cue and half with a forget cue. To enable the separation of individual hemodynamic responses by deconvolution, an additional 30 trials in each run consisted of only the fixation stimulus for 3 sec. Randomized trial orders were selected to maximize the separation of both cue and stimulus effects.
A recognition memory test was administered ~20 min after the completion of the study task, outside of the scanner. Participants were told that the test contained words and faces that were either novel or from the study phase ("old"). For each test item shown on a computer screen, participants were instructed to use two keys to indicate whether the stimulus was novel or old. Participants were instructed to make these responses regardless of whether the stimulus had been followed by a remember or forget cue and to respond as quickly and accurately as possible.
Imaging methods. A Siemens Vision 1.5-T magnet and head coil were used. The subject's head was comfortably secured using padding and a vacuum-immobilizer device. Stimuli were projected onto a rear-projection screen and viewed through a mirror. Whole brain T2*-weighted gradient-recalled echoplanar images were collected during the study task [24 6 mm slices; repetition time (TR) = 2000 msec; echo time (TE) = 40 msec; flip angle = 85°; field of view (FOV) = 24 cm]. Slices were oriented along the line connecting the anterior and posterior commissure (AC/PC line; slightly oblique from transverse) with a resolution of 3.75 × 3.75 × 6 mm. In each run, 154 whole-brain volumes were collected (4 initial volumes to reach steady state, 135 volumes during the study phase, and an additional 15 volumes at the end of the scan to collect the residual hemodynamic responses of the final trials). For anatomical localization, 3DFLASH T1-weighted images (TR = 15 msec; TE = 5.6 msec; flip angle = 20°, 160 1 mm axial slices; FOV = 240 mm; 256 × 256 matrix) were acquired after the study phase.
Image analysis. Images were coregistered through time using a three-dimensional registration algorithm (Cox, 1996
RESULTS
Recognition memory performance on the post-scanning test demonstrated the expected directed forgetting effects for words, as shown in Figure 1. Participants endorsed more words that had been given with the cue to remember (R-words) than words given with the cue to forget (F-words) (t(11) = 4.53; p < 0.001). In addition, participants exhibited successful memory for both R- words and F-words by endorsing these at a higher rate than novel words (t(11) > 6.48; p < 0.001). For face stimuli, participants exhibited successful memory for the faces seen during scanning (t(11) > 4.56; p < 0.001) but did not exhibit a directed forgetting effect, because the endorsement rates for R-faces and F-faces were not reliably different (t(11) = 1.49; p > 0.10).
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Figure 1. Recognition performance for word and face stimuli that had been studied while fMRI data were collected. Three types of items were included on the recognition test: stimuli that had been cued to be remembered (R), stimuli that had been cued to be forgotten (F), and novel stimuli (N). Endorsing the items as old is the correct response for the R and F stimuli and reflects the false alarm rate for the N stimuli. Error bars indicate the SEM.
Words
The robust effect of the remember/forget cue on encoding words was reflected in a network of brain regions that exhibited increased activity for R-words compared with F-words (Fig. 2, Table 1). Regions that exhibited increased activity during remember trials included a sizeable portion of LIPFC. This region includes both the anterior-ventral and posterior-dorsal areas observed in many previous verbal encoding studies (Wagner et al., 1998
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Figure 2. A, Brain areas in which increased activity was observed during word stimuli cued to be remembered (R-words) compared with word stimuli cued to be forgotten (F-words). Regions showing a reliable increase in activity across the group are shown in color overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between R words and F words was consistently greater than zero across the group of participants (t(11) > 3.5 in a cluster >500 mm3 in volume). Color intensity (red/orange/yellow) indicates the magnitude of the average signal change between the two conditions. The level of the images within the standard atlas is noted. B, Time course of observed activity in the left inferior prefrontal cortical region indicated within the green circle on A for remember and forget trials. The time course shown reflects averaged estimates of activity for each time point across all voxels in the region for all participants (with slight temporal smoothing for display purposes).
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Table 1. Regions that exhibited greater activity for remember trials than forget trials for word stimuli Responses on the subsequent recognition test were used to sort study trials into those subsequently remembered (i.e., participants correctly responded "old") and those subsequently forgotten (i.e., participants incorrectly responded "new"). Activity thus associated with successful encoding was contrasted regardless of the remember/forget cue. Brain regions that exhibited increased activity for subsequently remembered words (Fig. 3, Table 2) included left parahippocampal cortex and posterior hippocampus, LIPFC, right superior parietal cortex, and right cerebellum.
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Figure 3. A, Brain areas in which increased activity was observed during word stimuli that were subsequently remembered on the recognition test compared with word stimuli that were not. Regions showing a reliable increase in activity across the group are shown in color overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between remembered and forgotten was consistently greater than zero across the group of participants (t(11) > 3.5 in a cluster >500 mm3 in volume). Color intensity (red/orange/yellow) indicates the magnitude of the average signal change between the two conditions. The level of the images within the standard atlas is noted. B, Time course of observed activity in the left posterior hippocampus and parahippocampal cortex region indicated with the blue circle on A for successful and unsuccessful memory trials. The time course shown reflects averaged estimates of activity for each time point across all voxels in the region for all participants (with slight temporal smoothing for display purposes).
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Table 2. Regions that exhibited greater activity for subsequently remembered words than for subsequently forgotten words The previous two contrasts reinforce the roles of both prefrontal cortex and left medial temporal lobe in episodic encoding. In addition, because the cue associated with each word was not completely predictive of subsequent memory (i.e., some R-words were forgotten and some F-words were remembered), it was possible to compare the effect of the cue and subsequent memory performance separately. In this analysis, each word was classified by both the subsequent memory outcome [successful (SM); unsuccessful (UM)] and the cue [remember (R); forget (F)]. The four possible conditions were thus SM-R, SM-F, UM-R, and UM-F. There were an average of 41.2 SM-R trials for each participant (range, 19-55), an average of 24.6 SM-F trials (range, 9-43), an average of 31.2 UM-R trials (range, 17-55), and an average of 47.9 UM-F trials (range, 25-66).
The critical comparison is between R-words that were not successfully remembered (UM-R) and F-words that were successfully remembered despite the cue to forget them (SM-F). To identify areas in which activity was more associated with the remember/forget cue than with subsequent memory, differential activity associated with UM-R and SM-F trials was compared within the network of brain areas already associated with the remember cue. [Note that this comparison is effectively the difference between the cue effect and the subsequent memory effect. The effect of the cue = (SM-R + UM-R)
(SM-F + UM-F) and the subsequent memory effect = (SM-R + SM-F)
A similar analysis examined regions that exhibited increased activity for encoding success rather than encoding cue. In other words, activations for SM-F trials versus UM-R trials indicated which areas were reliably associated with successful encoding as opposed to the attempt to encode. Two such subregions were identified: left parahippocampal cortex, x =
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Figure 4. Comparison of encoding effort and success in the left inferior prefrontal cortex and medial temporal lobe. A, The LIPFC region in which encoding effort was more predictive of activity than encoding success (for words). B, Time courses of observed activity for the four trial types: successfully remembered R-words (SM-R), unsuccessfully remembered R-words (UM-R), successfully remembered F-words (SM-F), and unsuccessfully remembered F-words (UM-F). Of particular note is the fact that this area exhibits a strong response to R-words, even when this effort does not produce successful memory (UM-R > SM-F). C, The left MTL region in which encoding success was more predictive of activity than encoding effort (for words). D, Time courses of observed activity in the MTL region for the four trial types. In this region, successful encoding is associated with an increase in activity, even after the forget cue, whereas an unsuccessful encoding attempt is not associated with increased activity (SM-F > UM-R).
To further verify that the analysis comparing the SM-F and UM-R trials effectively captures differential activity for the regions examined, an ROI analysis was done by combining the data for all voxels within each region that exhibited increased activity for the remember cue and then comparing the peak activity for the UM-R and SM-F trial types estimated from the resulting time series. This analysis showed that the anterior cingulate and superior frontal gyrus regions each exhibited consistently higher activity for the UM-R trials (t(11) > 3.25; p < 0.01). The region-wide effect in the LIPFC was only marginal (t(11) = 1.83; p < 0.10), reflecting the fact that the region exhibiting increased UM-R activity was only a portion of the entire ROI. It is worth noting that this analysis is strongly affected by a single outlying participant who performed much worse than the rest of the group on the memory post-test (remembering 25% of the R-words, compared with the group average of 57%), suggesting that this participant may have failed to use an effective encoding strategy. Adjusting the analysis to weight functional activity by memory performance or holding aside this outlier finds the effect to be reliable across the rest of the group (t(11) = 2.21, p < 0.05 and t(10) = 2.59, p < 0.05, respectively). Another possible reason for the weaker ROI-wide response in the LIPFC is that the large LIPFC area that exhibited greater activity for "remember" than "forget" trials may include multiple sub-areas (Kirchhoff et al., 2000
A similar analysis was performed for the combined voxels within each ROI that exhibited increased activity for successful memory. Reliably increased activity was observed for the SM-F trials compared with UM-R trials in both the left parahippocampal region and the right superior parietal region (t(11) = 3.48, p < 0.01 and t(11) = 2.51, p < 0.03, respectively).
Faces
Because participants did not exhibit a robust directed forgetting effect for faces, it is not surprising that few brain areas showed differential activity for faces associated with the remember cue (R-faces) versus the forget cue (F-faces). Regions with greater activity for R-faces and F-faces are shown in Figure 5; coordinates are listed in Table 3. For R-faces, increased activity was observed in left posterior occipital cortex, left fusiform gyrus, and right inferior occipitotemporal cortex. In addition, two areas exhibited greater activity for F-faces: right parietal cortex and right middle frontal gyrus. It is unclear whether these areas reflect activity associated with an attempt to forget or some other cognitive activity that occurs after the forget cue (e.g., rehearsal of other previously presented stimuli, vigilance for the next stimulus).
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Figure 5. Brain areas in which increased activity was observed during face stimuli cued to be remembered (R-faces) compared with face stimuli cued to be forgotten (F-faces). Regions showing a reliable increase in activity across the group are shown in color overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between R-faces and F-faces was consistently different from zero across the group of participants (t(11) > 3.5 in a cluster >500 mm3 in volume). Warm colors (red/orange/yellow) indicate areas in which increased activity was observed for R-faces. Cool colors (blue/cyan) indicate areas in which increased activity was observed during F-face trials. The level of the images within the standard atlas is noted.
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Table 3. Regions that exhibited different levels of activity for remember and forget trials for face stimuli No brain areas showed greater encoding activity for successfully remembered faces compared with forgotten faces. This absence of subsequent memory effects is likely attributable to the low recognition accuracy for faces. Given the high false alarm rate (30% of the novel faces were incorrectly endorsed as old) relative to the hit rate (40% of the old faces were correctly endorsed as old), a large proportion of faces considered to be subsequently remembered may reflect guessing rather than a veridical memory.
Brain areas in which activity differed for word and face trials are listed in Table 4. Areas where words evoked consistent activity included the LIPFC (Broca's area) and left superior temporal gyrus (Wernicke's area). Face stimuli evoked more activity in the right amygdala and parahippocampal gyrus.
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Table 4. Regions that exhibited differential activity for face and word stimuli
DISCUSSION
Encoding words
The conjoint analysis of subsequent memory effects and directed forgetting effects yielded evidence that left inferior prefrontal cortex and the medial temporal lobe play different roles in verbal encoding. Based on the directed forgetting procedure, increased encoding effort on remember trials was associated with increased activity in LIPFC. Furthermore, comparisons between successful and unsuccessful encoding based on subsequent recognition revealed what have been termed declarative memory (DM) effects (Paller and Wagner, 2002
Although effort and success were correlated, high effort did not always lead to success and low effort did not always lead to forgetting. Therefore, it was possible to separate these factors by comparing trials when recognition was unsuccessful despite a remember cue (UM-R trials) and trials when successful recognition followed a forget cue (SM-F trials). The anterior, ventral portion of LIPFC exhibited greater activity for UM-R trials, indicating that activity in this brain area was more closely associated with the effort to encode a new memory than with successful creation of a new memory. In contrast, left MTL exhibited greater activity for SM-F trials, indicating that activity in that area was more closely linked with the creation of a memory that could be retrieved subsequently than with the intention to create a memory.
These two areas, LIPFC and left MTL, have been found in several previous studies to coactivate as part of a circuit associated with successful memory encoding (Wagner et al., 1998
Although our a priori hypotheses concerned the roles of the LIPFC and MTL in episodic encoding, similar patterns of activity were also observed in other areas. The anterior cingulate and medial superior frontal gyrus both exhibited patterns of activity similar to LIPFC. These findings suggest that these additional frontal areas may act in concert with LIPFC as part of a network supporting verbal encoding effort. Right parietal cortex exhibited a pattern of activity similar to that of left MTL, suggesting that this area may be acting to support successful encoding of an episode. This right parietal area was also identified by Davachi et al. (2001)
Two additional regions were identified as active during both encoding effort and success. The posterior dorsal part of the LIPFC encoding area and the right cerebellum both exhibited increased activity in response to the remember cue and when encoding was successful, without preferentially activating in either contrast. This pattern of results suggests that these two areas are active when encoding is attempted and when it is successful. However, it is unclear whether these areas are engaged in a cognitive process common to both of these conditions or whether these areas play different cognitive roles depending on context. One possibility for a common process would be linking a to-be-remembered word to semantic memory in an elaborative manner (an effortful and successful encoding strategy).
Although inferences from neuropsychology did not originally point to PFC as a necessary component of episodic encoding networks, neuroimaging results have repeatedly implicated PFC. Manipulations that increase encoding effectiveness, such as deep or elaborative encoding, consistently produce increased activity in left prefrontal cortex (Kapur et al., 1994
Encoding faces
In contrast to the effectiveness of DF cues on encoding of words, the same cues had minimal effects on encoding novel faces. Given the absence of a significant behavioral difference, it is not surprising that little differential activity was observed related to the cue. Despite this, increased activity was observed for remember trials in three posterior cortical areas. Because the cue followed the faces, this activity may reflect efforts to visualize the face after the remember cue. In right midfrontal and parietal cortex, activity increased during forget trials. This may reflect active attempts to forget or to rehearse to-be-remembered stimuli from previous trials during a forget trial. If displaced rehearsal took place, it would remove power from both DF and subsequent memory analyses.
During the subsequent recognition test, participants produced a high false alarm rate to novel faces, complicating the subsequent memory analysis for faces by calling into question the proportion of correct old responses that reflected veridical memories rather than correct guessing. The resulting decrease in power likely caused the lack of subsequent memory effects observed for faces. Because of this limitation in DM studies, future test conditions should influence response criteria to minimize the false alarm rate. It is also critical that the difference between the correct old (hit) rate and the miss rate is not too large; at maximal recognition performance, power is greatly reduced for subsequent memory analysis because of a low number of forgotten trials.
Stimulus-specific effects were found for words and faces (Table 4). Increased activity for words was found throughout areas that have classically shown greater involvement in language processing. Increased activity for faces was observed only in the right amygdala and parahippocampal gyrus. Although the fusiform gyrus was not active in the group analysis, many individual subjects exhibited increases in this area [reflecting the fusiform face area of Kanwisher et al. (1997)
Conclusion
By manipulating encoding through post-stimulus directed forgetting instructions, we identified an association between the intention to encode the episode of viewing a word and increased activity in left inferior prefrontal cortex. By examining neural activity that was predictive of subsequent success in remembering across the same trials, we identified a different association between successful verbal encoding and left medial temporal activation. We conclude that these two areas collaborate in a circuit that supports the encoding of episodic memories for verbal materials, but that these two regions play divergent roles. In the normal course of operation, the intention to encode results in increased activity in left inferior prefrontal cortex. This activity in turn can potentially modulate activity in the medial temporal lobe, where an increase in activity may reflect the storage of the multidimensional links that effectively support successful encoding.
FOOTNOTES Received Feb. 15, 2002; revised July 31, 2002; accepted Aug. 21, 2002.
This research was supported by National Institutes of Health Grants R01-MH58748 (P.J.R.) and R01-NS34639 (K.A.P.). We thank Patrick Skosnik and Sara Polis for assistance with data collection, data analysis, and manuscript preparation.
Correspondence should be addressed to Dr. Paul J. Reber, Department of Psychology, Northwestern University, 2029 Sheridan Road, Evanston, IL 60201. E-mail: preber{at}northwestern.edu.
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