Implicit and Explicit Memory in Amnesia - APA PsycNET

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Neuropsychology 1995, Vol. 9, No. 3, 281-290

Implicit and Explicit Memory in Amnesia: An Analysis of Data-Driven and Conceptually Driven Processes Laird S. Cermak, Mieke Verfaellie, and Kenneth A. Chase Boston University School of Medicine and Department of Veterans Affairs Medical Center, Boston The extent to which data-driven and conceptually driven processing determines amnesic patients' differential performance on implicit and explicit tasks was investigated. In 2 data-driven tasks, words that looked visually similar to target words were used as cues for a graphemic production task (implicit) and a graphemic cued-recall task (explicit). In 2 conceptually driven tasks, words semantically related to the target words were used as cues for both a production task and a cued-recall task. The nature of the task instructions consistently determined amnesic patient performance, regardless of the nature of the processing required. Thus, the distinction between implicit and explicit tasks captured the performance of amnesic patients better than did the distinction between data-driven and conceptually driven processes.

differentially benefit from different types of processing at study. Although different investigators have forwarded processing distinctions that vary in their specifics, they all share the belief that implicit task performance can be explained without recourse to the existence of a separate memory system. In the present study, we focus on the process distinction between data-driven and conceptually driven processing that has been advanced by Roediger and his colleagues (Blaxton, 1989; Roediger, Srinivas, & Weldon, 1989; Roediger, Weldon, & Challis, 1989), and we examine the usefulness of this framework for the understanding of the memory performance of amnesic patients. According to Roediger's (1990) view, task dissociations in normal individuals occur because explicit and implicit tasks differ in their reliance on data-driven versus conceptually driven processes. Because explicit tests such as recall and recognition rely heavily on conceptually driven processes, performance by normal participants is better under study conditions that emphasize conceptual rather than perceptual analysis. Conversely, implicit tests such as perceptual identification (Jacoby & Dallas, 1981) and stem completion (Graf, Squire, & Mandler, 1984) rely heavily on data-driven processes; thus, performance is better under data-driven than under conceptually driven study conditions. Central to Roediger's view (1990) is the notion that there is no necessary correlation between the implicit or explicit nature of a memory task and the requirement for data-driven or conceptually driven processing. Instead, these processing dimensions are thought to be orthogonal to the implicit-explicit memory distinction emphasized by systems theories. Thus, even though traditional implicit memory tests depend primarily on perceptual processing and traditional explicit memory tests depend primarily on conceptual processing, it is also logically possible to develop explicit tests that are largely data driven and implicit tests that are largely conceptually driven. In several studies, Roediger and his colleagues (Blaxton, 1989; Weldon & Roediger, 1987) did precisely this and demonstrated that study manipulations emphasizing conceptual processing benefited performance on both explicit and implicit conceptual tasks and that study manipulations emphasizing

Two theoretical perspectives currently exist to account for the well-documented dissociations in performance on implicit and explicit tasks of memory. These accounts can be referred to respectively as memory systems theories and memory processing theories. Based primarily on studies of patients with amnesia, systems theorists have postulated the existence of multiple memory systems in the brain, each felt to be neuroanatomically and functionally distinct (Cohen & Squire, 1980; Schacter, 1990,1992; Squire, 1987; Tulving & Schacter, 1990). Although various systems theories differ in their characterization of the precise nature of the memory system that mediates implicit memory, they can be treated together for present purposes because they share the assumption that performance on implicit tasks is mediated by a memory system that does not depend on the integrity of limbic-diencephalic brain structures. The performance of amnesic patients on implicit tasks is thought to be intact because it relies on a neural system not affected by their specific brain damage. Theories about memory processing, in contrast, have been advanced mainly to account for dissociations between implicit and explicit measures of memory in normal individuals (Graf & Ryan, 1990; Jacoby, 1983; Roediger, 1990). These theories are based on the notion that performance on any memory test depends on the degree of overlap that exists between study and test processing (Morris, Bransford, & Franks, 1977). Generally, it is assumed that implicit and explicit memory tests differ in the nature of their processing requirements and hence Laird S. Cermak, Mieke Verfaellie, and Kenneth A. Chase, Memory Disorders Research Center, Boston University School of Medicine, and Veterans Affairs Medical Center, Boston, Massachusetts. This research was supported by National Institute of Neurological Disease and Stroke Grant NS 26985 and National Institute of Alcohol and Alcohol Abuse Grant AA 00187. We thank Teresa Blaxton for sharing stimulus materials and Margaret Keane, William Milberg, and Daniel Schacter for input on study design and helpful comments. Correspondence concerning this article should be addressed to Laird S. Cermak, Memory Disorders Research Center (151-A), Veterans Affairs Medical Center, 150 South Huntington Avenue, Boston, Massachusetts 02130. Electronic mail may be sent via Internet to [email protected].

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data-driven processing benefited performance on both datadriven tasks. Thus, they showed that in normal individuals dissociations exist between tasks that tap different types of processing rather than between tasks that presumably tap different underlying memory systems. Initially advanced to account for findings in normal individuals, the distinction between data-driven and conceptually driven processing has also been offered as an explanation for the task dissociations observed in patients with amnesia. Blaxton (1992) has suggested that amnesic patients may perform poorly on all conceptually driven memory tasks regardless of explicit-implicit status but will perform normally on all tasks with data-driven processing requirements. In support of this view, she found that patients with left temporal lobe epilepsy performed normally on a graphemic cued-recall task, an explicit task thought to require data-driven processing, and below normal on a task of general knowledge that was felt to be a conceptually driven implicit task. Thus, the data-driven versus conceptually driven processing requirement, rather than the implicit or explicit nature of the task, predicted patients' performance. These findings are of considerable importance because they suggest that the performance of amnesic patients may be understood better by a processing framework of memory rather than by a memory systems account. Although the attempt to explain amnesics' performance in terms of underlying processing dimensions is highly appealing, the evidence advanced by Blaxton (1992) is not entirely convincing for several reasons. First, Blaxton used patients with temporal lobe epilepsy as participants, and their memory disorders were clearly less severe than those typically observed in amnesic patients. Second, in the development of implicit and explicit memory tasks with data-driven versus conceptually driven processing demands, Blaxton relied on four totally different paradigms. This approach could be criticized because it confounds task difficulty with the manipulations of interest. A more accepted method of manipulating the implicit versus explicit status of memory tasks is by changing task instructions but otherwise keeping stimuli and task conditions constant. Studies using this approach to examine amnesics' performance on conceptual tasks (Graf, Shimamura, & Squire, 1985; Shimamura & Squire, 1984) have shown that amnesic patients can demonstrate intact conceptually mediated implicit performance, a finding that is contrary to Blaxton's (1992) proposal. The other prediction of her hypothesis—that amnesic patients might demonstrate intact data-driven performance across both implicit and explicit paradigms—has so far not been tested using matched versions of the same task. In the present study, we examined the validity of the processing account advanced by Roediger (1990) for explaining memory performance in amnesia by comparing amnesics' performance on matched implicit and explicit versions of both a data-driven and a conceptually driven task. Blaxton's (1992) graphemic cued-recall task was used as the explicit data-driven task. The implicit data-driven task we used was a graphemic production task with cues similar to those in the explicit task without references to the study episode. The two conceptually driven tasks consisted of a semantic cued-recall and a semantic production task. Thus, by varying the instructional set, we

created four different tasks: an implicit task with either graphemic or semantic cues and an explicit task with either graphemic or semantic cues. In addition, during the study phase of each task, participants were required to either simply read each stimulus word or to generate a word in response to a highly associated cue. These manipulations were intended to emphasize data-driven and conceptually driven processing, respectively. In line with previous studies (Blaxton, 1989; Weldon & Roediger, 1987), we expected in normal participants better performance on graphemic tasks following read than following generate instructions and better performance on semantic tasks following generate than following read instructions. With regard to the amnesic patients' performance, we hypothesized that if amnesic patient performance depends solely on the nature of the processing required, then they should perform normally on both graphemic tasks (production and recall) and should be impaired on both semantic tasks irrespective of the task instructions. Alternatively, if amnesic patients' performance depends exclusively on the implicit or explicit nature of the task, then they should perform normally on both implicit tasks and be impaired on both explicit tasks, irrespective of the underlying processing demands.

Experiment 1 General Method Participants Two groups of adults participated in this experiment. The first group consisted of 13 amnesic patients, 10 men and 3 women. Six patients had a diagnosis of alcoholic Korsakoff syndrome. All had histories of chronic alcoholism, were unable to recall day-to-day events, and had extensive retrograde amnesia. The other 7 in the amnesia group had various etiologies, and 2 suffered from anoxia secondary to cardiac arrest. Neuroimaging studies revealed enlarged ventricles and diffuse cortical atrophy in one of these patients, but no structural changes were observed in the other. A 3rd patient underwent removal of a left hematoma secondary to a head injury and subsequently became amnesic following an episode of status epilepticus. His MRI scan revealed extensive Joss of tissue in the left temporal lobe, including all of the anterior hippocampus, amygdala, and anterior efferent pathways. Two patients had suffered from encephalitis; neuroimaging studies revealed extensive bilateral damage to the medial and anterolateral regions of the temporal lobes in both patients. Another patient became amnesic following a bilateral medial thalamic infarction, which was confirmed by CT imaging. Still another patient developed amnesia following rupture of an anterior communicating artery aneurysm. All patients in this group lived at home and, like the Korsakoff patients, they displayed a severe memory disorder. The mean age of the entire amnesic group was 53 years (SD = 14.8), with an average of 13 years of education (SD = 3.8). The average Wechsler Adult Intelligence Scale—Revised Verbal IQ (WAIS-R VIQ) score for this group was 100 (SD = 15.5). The attention score on the Wechsler Memory Scale—Revised (WMS-R) was 101 (SD = 12.3). The General Memory score was 74 (SD = 14.8), and the Delayed Memory score was 57 (SD = 9.0). The control group consisted of 13 participants living in private homes, 6 of whom had diagnoses of chronic alcoholism. These alcoholic patients were matched in terms of age and education with the Korsakoff patients, and all had abstained from alcohol for at least 1 month prior to participation in this experiment. The remaining 7

IMPLICIT AND EXPLICIT MEMORY IN AMNESIA controls were individuals without a history of alcoholism, and they were matched with the other amnesic patients. None evidenced any signs of neurological or psychiatric illness. The mean age for the entire group was 53 years (SD = 14.8), with an average education of 14 years (SD = 2.0), and a mean WAIS-R VIQ score of 105 (SD = 13.5).

Tasks Each participant completed a matched graphemic cued-recall and graphemic production task (Experiment 1A) and a matched semantic cued-recall and semantic production task (Experiment IB). The graphemic tasks were always administered first and at least 1 week elapsed between participation in Experiments 1A and IB. This ordering was motivated by our experience that amnesic patients do not retain paradigm-specific mnemonic skills from week to week, whereas controls often do. Because we were particularly interested in the level of graphemic cued recall of both participant groups, we wanted to be certain that retention of task requirements from the preceding condition did not favor any particular group. Because it was more likely that semantic skills would benefit graphemic recall rather than the reverse, we consistently presented the graphemic condition first for all participants. For all tasks, the study phase involved presentation of a set of words to be read and a set of words to be generated on the basis of an associative cue and first letter of the target word (e.g., needle in response to pin; n—). The test phase differed as a function of the specific task and instruction condition. During the graphemic tasks, participants were asked to think of words that were visually similar to cue words presented on the computer screen (e.g., pepper in response to peeper). In the graphemic cued-recall task, participants were told to use these cues to come up with words that had been read or generated during the study phase. In the graphemic production task, they were told to respond with the first physically similar word that came to mind. During the semantic tasks, participants were asked to produce words that were semantically related to cue words presented on the computer screen (e.g., needle in response to syringe). These semantic cues were always different from those that had been used to generate targets during the study task. In the cued-recall task, these semantically related cues were to be used to recall words that had been read or generated during the study phase, whereas in the production task, participants were told to respond with the first semantically related word that came to mind.

Experiment 1A: Graphemic Tasks Method Materials and design. Sixty-four words, randomly selected from a list of 128 words used by Blaxton (1992), formed the stimuli in this experiment; the remaining 64 words were retained for later use in Experiment IB. Words ranged in frequency from 1 to 152 per million with a mean of 18 per million (Francis & Kucera, 1982). The graphemic cue word assigned to each word was taken from Blaxton's (1992) materials and consisted of a word that was graphemically but not semantically similar to the target word (e.g., cattle as a cue for castle). Stimuli were divided into four lists of 16 items that were matched for frequency. Two of the lists were used as target items during the study phase of the cued-recall and production tasks, respectively, whereas the remaining two lists were used as filler items during the test phase. The inclusion of filler items allowed calculation of baseline scores for both the recall and production tasks. Target and filler items were randomly intermixed during the test phase. The assignment of lists to task (cued recall or production) and condition (target or filler) was counterbalanced across participants.

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Within a study list, items were further subdivided into items to be read and items to be generated. On read trials, participants simply read target words aloud (e.g., pepper). On generate trials, participants generated target words on the basis of a semantic associate that was followed by a single letter (e.g., salt; p—). Read and generate trials were blocked, with the assignment of words to conditions and order of conditions counterbalanced across participants. Procedure. Participants completed both a graphemic cued-recall and a graphemic production task during the same session, with the order of tasks counterbalanced across participants. At least 20 min elapsed between completion of the first task and the beginning of the second task. During the study phase of each task, participants read words or provided associates to words that were presented on a computer screen. For items to be read, a 2-s presentation of a series of 4 Xs was followed immediately by presentation of the target word for 5 s. For items to be generated, a cue word was presented in the middle of the screen for 2 s and was then replaced with a single letter, which remained on the screen for 5 s. Participants were instructed to read the cue word silently and to provide an associate that began with the letter shown on the screen. At the beginning of the study phase, participants were given three practice trials in the generate condition to ensure their understanding of the task instructions. Read and generate instructions were then given during the study phase as appropriate. If during the generate condition, a participant gave an incorrect response or was unable to provide a response within the allotted time, the experimenter provided the correct solution. Participants performed the test phase immediately following the study phase. During the cued-recall task, they were asked to recall the words they had read or generated during the study phase. Each word was to be recalled in the presence of a graphemic cue presented on the screen. These words were presented one at a time, and the participants were asked to use these cues as potential reminders of words on the study list. If the graphemic cue did not remind them of a studied word, they were simply asked to indicate so and the next trial was initiated. During the production task, participants were asked to provide the first word that came to mind whenever they looked similar to the cue words presented on the screen. In both tasks, the graphemic cues remained on the screen until participants responded or 30 s had elapsed. Thirty-two trials, 16 with graphemic cues for previously studied items, and 16 with graphemic cues for filler items, were presented in each of the tests.

Results For each participant, we computed the mean proportion of items correctly provided at test as a function of task (cued recall or production) and study (read, generated, or nonstudied) condition. These data were initially analyzed in two ways: conditionalized on correct generation at study and unconditionalized so that all data were included. The pattern of results was identical in the two analyses. However, because both amnesic patients and controls performed quite poorly at generating target words on the basis of the associative cues provided at study across both the cued-recall and production task; amnesics mean = .51; controls mean = .54; F(l, 24) < 1; we report the analyses of the conditionalized results. Table 1 presents the proportion of correct responses in the cued-recall and the production tasks for previously studied and nonstudied words. Accuracy scores in the nonstudied condition represent baseline response rates; scores in the read and generate condition were priming scores and were obtained by subtracting the baseline response rate from the proportion of read and

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Table 1 Corrected Cued Recall Scores and Priming Scores in the Read (R) and Generate (G) Conditions and Proportion of Nonstudied (NS) Target Words Controls

Experiment IB: Semantic Tasks Method

Amnesia patients

Task

R

G

NS

R

G

NS

Cued recall Production

.38 .17

.42 .13

.02 .20

.08 .15

.17 .12

.08 .13

Note. Experiment 1A findings only.

generated items provided as correct responses. Because in some conditions, accuracy scores were quite disparate in the amnesic and control groups, a concern existed regarding the homogeneity of variance across participant groups. To ensure that the use of analyses of variance was appropriate, we compared for all analyses in this experiment, as well as in subsequent experiments the variance across participant groups. In all instances, Fmax was nonsignificant, indicating that the assumption of homogeneity of variance was met. Cued recall. Table 1 indicates that baseline response rates were marginally higher for amnesic patients than for controls, t(24) = 1.95, p < .10, suggesting that the amnesic patients may have used a more liberal response strategy. Notwithstanding this response bias, analysis of the cued-recall data adjusted for differences in baseline guessing rate revealed a significant main effect of group, F(\, 24) = 13.2, MSB = .075, p < .01, indicating that amnesic patients performed significantly worse than did controls. The effect of encoding manipulation was not significant, F(l, 24) - 1.09, MSB = .055, nor was the Group x Encoding interaction, F( 1,24) < 1. Production. As can be seen in Table 1, baseline response rates were somewhat higher in the controls than in the amnesic patients, but this difference was not reliable, < .05, and generate conditions, t(l2) = 2.11,p < .05. For amnesic patients, in contrast, the same comparisons revealed significant priming in the generate condition, t (12) = 2.20, p < .05, but not in the read condition, ((12) = 1.25, ns. In a second analysis, the magnitude of the priming scores was compared across participant groups and encoding conditions. Results of the ANO VA revealed no effect of group, F( 1,24) < 1, no effect of encoding, F(l, 24) = 1.43, MSE = .036, and no Group x Encoding interaction, F(l, 24) = 2.26, MSE = .036. Therefore, it appears that priming was equivalent across groups in both the read and the generate condition. Finally, an ANOVA on the combined results of the cuedrecall and production tasks revealed several significant effects involving task. In addition to a main effect of task, F(l, 24) = 13.70, MSE = .047, p < .01, the Group x Task, F(l, 24) = 18.41, MSE = .047, p < .01, and Group x Task x Encoding interaction, F(l, 24) = 8.12, MSE = .051,p < .01, were both significant. These effects reflected the fact that amnesic patients were impaired in the cued-recall but not in the production task and that controls, but not amnesic patients, showed an improvement in cued-recall performance associated with the generate condition.

Discussion The results of the present experiment are only partially consistent with those obtained in patients with mild memory disorders secondary to temporal lobe epilepsy (Blaxton, 1992). Like those patients, our amnesic patients demonstrated intact performance on an implicit graphemic task, but unlike patients with milder memory deficits their performance on a graphemic cued-recall task was significantly impaired. On the semantic production task, amnesic patients differed from controls in that they did not show significant priming (above baseline) in the read condition. However, more importantly, their performance in the generate condition was entirely normal, suggesting that amnesic patients can obtain normal benefits from

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conceptual processing in a conceptually driven implicit memory task. The finding of intact conceptual transfer in a semantic implicit task stands in direct contrast to the results of the semantic cued-recall task. Here amnesic patients failed to benefit from conceptual processing and their performance in both the read and generate condition was significantly impaired. Thus, in contrast to Blaxton's patients who did not demonstrate conceptual transfer on either an implicit or explicit conceptual task, the performance of the amnesic patients critically depended on the implicit or explicit nature of the task. Taken together, these findings suggest that the distinction between data-driven and conceptually driven processing does not provide a satisfactory explanation for the amnesic patients' differential implicit and explicit task performance. In contrast to the predictions based on the processing view of Roediger (1990), amnesic patients were impaired on the graphemic cued-recall task (Experiment 1A), an explicit task thought to be data driven and they performed normally on the semantic production task (Experiment IB), an implicit task thought to be conceptually driven. These results are more consistent with a dichotomous systems view because amnesic patients performed normally on both implicit tasks and were impaired on both explicit tasks irrespective of the underlying processing demands. Before accepting these conclusions, however, several aspects of the results remain to be clarified. First, the results of the graphemic cued-recall task in the normal controls call into question the extent to which this task is data driven. In contrast to Blaxton (1992), we did not find an advantage of the read over generate condition; instead, performance was equivalent across conditions. This suggests that both data-driven and conceptually driven processes may contribute to performance on the graphemic cued-recall task. Because the stimuli and task parameters in the present graphemic cued-recall task were identical to those used by Blaxton (1992), the reasons for this inconsistency remain unclear. In the graphemic production task, priming for both groups was reliably above baseline only in the read condition, a finding consistent with the notion that priming in the graphemic production task was primarily data driven. However, the effect of encoding manipulation failed to reach significance, suggesting that perhaps the encoding manipulation was not sufficiently robust. This also might account for a related problem in the semantic production task where the controls, in contrast to Blaxton's participants, failed to demonstrate the expected advantage of a conceptually driven encoding manipulation. In the hope of enhancing the effect of these encoding manipulations, we designed a second experiment in which the encoding conditions were presented in a mixed rather than a blocked format. A second, possibly related concern that led us to modify the encoding manipulation was that during the study phase of Experiment 1 participants were able to generate only about half of the items specified on the basis of their associative cues. Because we eliminated from the analysis the items that were not correctly solved, the results in this condition were based on a much smaller and potentially nonrepresentative sample of items. We attempted to rectify this problem in Experiment 2 by providing easier generation cues. This was done by presenting

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participants with sentences that preceded the to-be-generated target word and more directly promoted the desired response. In all other respects, Experiment 2 was modeled after Experiment 1.

Experiment 2 General Method Participants Twelve of the 13 amnesic patients who had participated in Experiment 1 also participated in this experiment. Their mean age was 55 years (SD = 13.3), with an average of 13.5 years of education (SD = 3.7). The average WAIS-R VIQ score for this group was 101 (SD = 14.9). The Attention score on the WMS-R was 102 (SD = 12.4). The General Memory score was 76 (SD = 13.6), and the Delayed Memory score was 58 (SD = 9.1). At least 3 months elapsed between participation in the previous and the present experiment. The control group consisted of 13 participants, 6 of whom were chronic alcoholics matched in terms of age and education with the Korsakoff patients. The remaining 7 controls were individuals without a history of alcoholism who were matched to the other amnesic patients. None had participated in the previous experiments. The mean age for the entire control group was 51 years (SD = 13.6), with an average education of 12 years (SD = 1.9), and a mean WAIS-R VIQ score of 111 (SD = 12.9).

Tasks The participants completed a matched graphemic cued-recall and graphemic production tasks (Experiment 2A) and a matched semantic cued-recall and a semantic production task (Experiment 2B). For all tasks, the study phase involved a mixed presentation of words to be read and words to be generated as the final word of a sentence. The test phase differed as a function of the specific task and instruction condition in a manner identical to that of the corresponding tasks of Experiment 1.

Experiment 2A: Graphemic Tasks Method Materials and design. Stimuli for this experiment consisted of 64 words ranging in frequency from 1 to 312 per million with a mean of 34 per million (Francis & Kucera, 1982). Of these words, 52 were selected from Blaxton (1992), and 12 were selected from different sources to substitute for stimuli that were deemed too difficult to generate during the study phase. As in Experiment 1, these stimuli were divided into four lists of 16 items. Two of these lists were used as targets and fillers for the cued-recall task, and the other two were used as targets and fillers for the production task. The test lists consisted of 32 graphemic cues, 16 of which corresponded to previously read or generated targets and 16 of which corresponded to filler items. Half of the target stimuli presented during the study phase were assigned to the read condition and the other half to the generate condition. In contrast to the previous experiment, read and generate items were randomly intermixed within the study list. This was done to provide greater contrast between the two conditions during presentation. Also, for each item in the generate condition, participants were presented with a sentence and were asked to fill in the missing word on the basis of its first letter (e.g., "A seasoning often used along with salt is p—."). In all other ways, the design was identical to that in Experiment JA.

Procedure. The procedure was the same as in Experiment 1A, except that words were generated during the study phase on the basis of a sentence cue and these items were randomly intermixed with items to be read. Again, the cued-recall and production tasks were administered in random order during the same session, and the instructions were identical to those used in Experiment 1A. Because the same amnesic patients who participated in this experiment had also participated in Experiment 1, we took care to ensure that words that had appeared in a read condition for a specific patient in Experiment 1 appeared in a generate condition in the present experiment.

Results For both groups, the proportion of words correctly generated at study was considerably higher than in the previous experiment. However, controls correctly generated significantly more words than did the amnesics in both the cuedrecall and production tasks; amnesics mean = .91; controls = .97; F(l, 22) = 10.08, MSB = .006,p < .01. Consequently, as in the previous experiment, we computed for each participant the proportion of correct responses conditionalized on generation as a function of task (cued recall or production) and study condition (read, generated, or nonstudied). Table 3 presents for both tasks the mean baseline response rates and corrected cued-recall and priming scores for the read and generate conditions. These corrected scores were obtained by subtracting the baseline rate from the target rates. Cued recall. As shown in Table 3, baseline response rates were somewhat higher for amnesic patients than for controls. This difference, however, was not reliable, f(22) = 1.70, ns. An ANOVA performed on the corrected cued-recall scores revealed a significant main effect of group, F(l, 22) = 47.49, MSB = .049, p < .01, indicating that amnesic patients recalled fewer words than did controls. The effect of encoding and its interaction with group were nonsignificant (Fs < 1). Production. Baseline response rates were similar across participant groups, t(22) = .78, ns. As in the previous experiments, a comparison between studied and nonstudied response rates was made to examine the presence of significant priming in the amnesic and controls. For both groups, priming was significant in both the read; amnesic patients r(ll) = 3.02, p < .01; controls: r(ll) = 5.62, p < .01, and the generate condition; amnesic patients: t(ll) = 2.39, p < .05; controls: f ( l l ) = 2.69, p < .05. To examine the magnitude of priming across conditions, an ANOVA was performed on the priming scores. Results of this analysis revealed that neither the effect of group, F(l, 22) = 2.74, MSE = .031, encoding, F(l, 22) =

Table 3 Corrected Cued Recall Scores and Priming Scores in the Read (R) and Generate (G) Conditions and Proportion of Nonstudied (NS) Target Words Controls Task Cued recall Production

R

G

NS

R

.60 .22

.59 .17

.02 .32

.19 .13

Note. Experiment 2A findings only.

Amnesia patients G NS .13 .09

.09 .29

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IMPLICIT AND EXPLICIT MEMORY IN AMNESIA 1.03, MSE = .061, nor Group x Encoding, F(l, 22) < 1, were significant. These findings were confirmed in a combined analysis of the cued-recall and production data, which revealed a main effect of task, F(l, 22) = 34.99, MSE = .036, p < .01, as well as a significant Group x Task interaction, F(l, 22) = 20.95,MS£ = .036, p < .01. These effects reflected the fact that controls performed significantly better than the amnesics on the cuedrecall task, but the two groups did not differ in their performance on the production task.

Table 4 Corrected Cued Recall Scores and Priming Scores in the Read (R) and Generate (G) Conditions and Proportion of Nonstudied (NS) Target Words Task

R

Cued recall Production

.21 .14

Controls G NS .67 .27

0 .15

Amnesia patients R

G

NS

.11 .08

.14 .17

.04 .13

Note. Experiment 2B findings only.

Experiment 2B: Semantic Tasks Method Materials and design. Stimuli for this experiment consisted of 64 words, ranging in frequency from 1 to 424 per million with a mean of 34 per million (Francis & Kucera, 1982). Forty-eight of these words, different than those used in Experiment 2A, were selected from the stimulus set of Blaxton (1992). The remaining words were selected to substitute for stimuli from the Blaxton set that were deemed too difficult for target generation. For each stimulus, a semantically related word was chosen as a cue for the test phase of the experiment. The stimuli were divided into four lists of 16 items each. Two of these lists were used as targets and fillers for the cued-recall task and the other two were used as targets and fillers for the production task. Each test list consisted of 32 semantically related cue words, 16 of which corresponded to previously read or generated items and the other 16 corresponded to filler items. As in Experiment 2A, half of the target stimuli presented during the study phase were assigned to the read condition and the other half to the generate condition, with read and generate items randomly intermixed within the study list. In the generate condition, each target was generated on the basis of a sentence in which only the first letter of the target word was presented. Procedure. The procedure was the same as in Experiment IB, except that the generation task required participants to generate target words on the basis of a sentence. Also, read and generate items were randomly intermixed within the study list. Care was taken to ensure that for each amnesic patient words that had been presented in the read condition in Experiment 1 would then be presented in the generate condition and vice versa. The semantic cued-recall and the semantic production task were administered in random order during the same session, and the instructions were identical to those used in Experiment IB.

Results The proportion of words correctly generated at study was again significantly higher for the controls than for the amnesic patients across both the cued-recall and production tasks; amnesic patient mean = .89; controls mean = .98, F(l, 22) = 16.90, MSE = .007, p < .01. For each participant, we computed the proportion of correct responses conditionalized on generation as a function of task (cued recall or production) and study condition (read, generated or nonstudied). Table 4 presents the proportion of correct baseline responses to nonstudied words, as well as the corrected cued recall and priming scores in the read and generate condition. These scores were obtained by subtracting baseline scores from target scores. Cued recall. Baseline response rates were marginally higher for the amnesic patients than for the controls, /(22) = 2.03,

p < .10, suggesting that amnesic patients may have used a more lenient response criterion. An analysis of the cued-recall scores corrected for guessing revealed a significant main effect of group, F(l, 22) = 28.07, MSE = .044, p < .01, encoding, F(l, 22) = 22.8, MSE = .032,p < .01, and Group X Encoding, F(l, 22) = 18.3, MSE = .032, p < .01. These effects indicated that the performance of amnesic patients and controls did not significantly differ in the read condition, F(l, 43) = 1.56, MSE = .038, whereas controls performed significantly better than the amnesic patients in the generate condition, F(l, 43) = 46.33, MSE = .038, p < .01. This again was due to the absence of a generation effect in amnesic patients, F(l, 22) < 1, an effect that was marked in controls, F(l, 22) = 40.97, MSE = .032,^ < .01. Production. As shown in Table 4, baseline response rates to nonstudied items were equivalent across groups, /(22) = .52, ns. In a first analysis, response rates to studied and nonstudied items were compared separately for each group. Controls showed significant priming in both the read, f(ll) = 3.53,p < .01, and the generate condition, *(11) = 5.75, p < .01. Likewise, amnesic patients showed significant priming in both conditions; read: r(ll) = 2.53,p < .05; generate: t(ll) = 3.37, p < .01. To compare the magnitude of priming across encoding conditions and groups, we performed an ANOVA on the priming scores. A significant effect of encoding was obtained, F(l, 22) = 7.89, MSE = .020, p < .05, which indicated larger priming in the generate than in the read condition. The effects of group, F(l, 22) = 2.71, MSE = .025, and Group x Encoding, F(l, 22) < 1, were nonsignificant. These findings were confirmed in an ANOVA that combined the results of the cued-recall and production tasks. All effects involving the variable task were significant. These included a main effect of task, F(l, 22) = 8.30, MSE = .039, p < .01, a Group x Task, F(l, 22) = 9.26, MSE = .039, p < .01, Task x Encoding F(l, 22) = 5.14, MSE = .020,p < .01, and Group x Task x Encoding interaction, F(l, 22) = 11.49, MSE = .020, p < .01. These effects indicated that amnesic patients' performance was impaired only in the generate condition of the cued-recall task. Discussion Amnesic patients as well as controls were much more successful in generating target words during the study phase of

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this experiment than they had been in Experiment 1, suggesting that our modification of the generation task had its desired effect. Additionally, by intermixing the two encoding conditions during study, the effects of encoding manipulation became more pronounced. In both the semantic cued-recall and production tasks, controls now showed a significant advantage of generate over read encoding. This finding is consistent with the notion that performance in these tasks is primarily conceptually driven. As in Experiment IB, the performance of amnesic patients on the semantic production task did not reliably differ from that of the controls. Moreover, amnesic patients showed conceptually driven transfer effects similar to those obtained by normal controls. Amnesics' ability to benefit from conceptually driven processing in an implicit semantic task again contrasts with the predictions of Blaxton's (1992) processing account and suggests that amnesic patients are not impaired on all conceptually driven tasks. Instead, the implicit or explicit nature of the task seems to be the determining factor. Patients performed normally on the implicit semantic production task, but they were severely impaired on the explicit semantic cued recall task. This was due largely to the fact that the amnesic patients failed to show the expected advantage of conceptual over data-driven processing in the semantic cued-recall task. In fact, they did not perform significantly worse than did the controls in the read condition. It must be noted that their normal performance in the read condition, however, was due primarily to the suppression of the controls' performance in that condition; a finding that has commonly been observed when comparing mixed to blocked list conditions (Begg & Snider, 1987; Slamecka & Katsaiti, 1987). As in Experiment 1 A, the results of the graphemic tasks are also inconsistent with this processing account because the amnesic patients performed normally on the graphemic production task but were significantly impaired in the graphemic cued-recall task. The latter task was designed to be a datadriven processing task; whether this is, in fact, the case is questionable, however, given that the controls again did not demonstrate the expected advantage of a data-driven encoding manipulation. We consider possible reasons for this outcome in the General Discussion.

General Discussion The results of these two experiments demonstrate that amnesic patients are impaired on explicit tests of cued recall, whereas they perform normally on implicit tests of production, regardless of whether these tasks require primarily data-driven or conceptually driven processing. These findings suggest that the processing distinction between data-driven and conceptually driven processing (Blaxton, 1989; Roediger, Srinivas, & Weldon, 1989; Roediger, Weldon, & Challis, 1989) does not provide a plausible account of task dissociations in amnesia. Instead, the distinction between implicit and explicit tasks, as originally advanced by Graf and Schacter (1985), provides a better taxonomy of the amnesic patients' performance. Systems theories have tended to interpret these dissociations between implicit and explicit task performance in amnesia as evidence for the existence of separate underlying neural

systems. In doing so, they have stressed the nonoverlapping nature of these different forms of memory on the assumption that each reflects the operation of a distinct set of underlying processes. However, findings in normal participants of associations between implicit and explicit tasks with similar processing demands argue against this direct mapping of processes onto task (Blaxton, 1989; Weldon & Roediger, 1987). Furthermore, the present findings indicate that a data-driven, conceptually driven distinction does not accurately characterize the task dissociations observed in amnesia. Therefore, the question is still open as to how best to define the processing characteristics of implicit versus explicit retrieval. A framework the first and second authors (Cermak & Verfaellie, 1992) have favored to describe these processing dissociations in amnesia is based on the proposal that performance on any memory task reflects a combination of automatic and controlled processes (Jacoby, 1991; Jacoby & Kelley, 1992). We have suggested that amnesic patients are capable of using the fluency with which items are processed as an automatic basis of responding but are severely impaired in using the controlled processes necessary for conscious recollection. Importantly, even though implicit and explicit memory tests draw preferentially on automatic and controlled processes respectively, we have also demonstrated that amnesics can use fluency normally in the context of an explicit recognition task (Verfaellie & Treadwell, 1993) and are impaired in an implicit task that allows for the contribution of conscious recollective processes (Cermak, Verfaellie, Letourneau, & Jacoby, 1993). The present study was not designed to test the validity of this processing framework in amnesia; nevertheless, it can accommodate the current findings. Optimal performance on both the graphemic and semantic cued-recall tasks requires conscious retrieval of study items, whereas performance on both the graphemic and semantic production task reflects primarily,1 if not exclusively, automatic consequences of fluency. In the graphemic production task, this fluency is based on the match between the perceptual characteristics of a stimulus at study and test. In the semantic production task, the superior performance in the generate compared with the read condition suggests that fluency reflects primarily the ease with which conceptual processes are reinstated across presentations. This being the case, the present findings indicate that amnesic patients not only have intact perceptual fluency but also intact conceptual fluency. It is this fluency that probably provides the support for their normal performance on implicit tasks. The notion that under certain conditions, conceptual processing can contribute to amnesics' performance may at first sight appear contradictory to the long held view that amnesia is 1 Although the performance of amnesic patients on the graphemic and semantic production tasks was statistically equivalent to that of controls, their performance in Experiment 2 was numerically lower than that of the controls. The present study did not allow us to assess the separate contribution of automatic versus controlled processes to performance of the graphemic and semantic production tasks. However, we hypothesize that small differences in the level of performance of the amnesics and controls may reflect the contribution of controlled processes to the performance of controls on these tasks.

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caused by a deficit in semantic encoding (Cermak, 1979). However, this view was forwarded only as an explanation of amnesics' performance on explicit memory tasks. There, it was demonstrated that amnesic patients failed to benefit from semantic encoding when the retrieval cues provided at test did not guide access to the same processing performed at encoding. In contrast, when the same associative encoding performed at study was reestablished at test, as is the case in an encoding specificity paradigm, then amnesic patients' performance was greatly enhanced (Cermak, Uhly, & Reale, 1980). Thus, these findings are consistent with the theoretical framework advanced here and suggest that amnesic patients can benefit from conceptual processing (see also Cermak & Stiassny, 1982), provided this processing can be automatically reinstated at the time of testing, as is often the case in implicit memory tasks. Although our current data demonstrate that an implicit task can be conceptually driven, it is less clear to what extent the opposite pattern can be obtained; namely that of an explicit task that is primarily data driven. In the graphemic cued-recall task, we failed to replicate Blaxton's (1992) finding of superior performance in the read compared with the generate condition. This finding is essential in demonstrating that this task is data driven. Although we used the same materials as Blaxton, one major difference in the two studies was that the list length was significantly shorter in the present study. Given the shorter list, the participants might have been able to process aspects of a stimulus other than its perceptual characteristics, even when the retrieval demands emphasized perceptual processing. However, this is unlikely to be the sole explanation because Challis (1993) also failed to confirm the data-driven nature of this task with a study list even longer than that used by Blaxton. This raises the question as to whether an explicit task can ever be purely data driven. It is possible that normal individuals use the graphemic cues to generate potential alternatives and then check the adequacy of these responses on the basis of recollection of the semantic and contextual aspects of the stimulus. In the context of such a generate-recognize strategy, the generation component might be primarily data driven, but the recognition component might rely on conscious recollection processes that are primarily conceptual in nature. Finally, although the distinction between data-driven and conceptually driven processes does not explain the task dissociations observed in amnesia, it remains a useful heuristic. The belief that implicit memory consists of two dissociable components that respond to the reinstatement of perceptual and conceptual aspects of a stimulus respectively, has important implications for examining different sources of priming in a variety of neuropsychological populations. The present study and several others (Graf, Shimamura, & Squire, 1985; Shimamura & Squire, 1984) indicate that perceptual and conceptual priming are both preserved in amnesia. Thus, neither form of implicit memory must depend on the integrity of the limbic-diencephalic brain system that is damaged in global amnesia. However, dissociations between perceptual and conceptual priming have been obtained in other patient populations. For instance, patients with Alzheimer's disease have been found to perform normally on tasks of perceptual priming, such as perceptual identification (Keane, Gabrieli,

Fennema, Growdon, & Corkin, 1991; Keane, Gabrieli, Growdon, & Corkin, 1994; Gabrieli, Keane et al., 1994) and picture naming (Gabrieli, Francis et al., 1995) but are impaired on tasks of conceptual priming, such as word association priming (Brandt, Spencer, McScorley, & Folstein, 1988; Huff, Mack, Mahlman, & Greenberg, 1988; Salmon, Shimamura, Butters, & Smith, 1988). Precisely the opposite pattern has been described (Grosse, Gabrieli, & Reminger, 1992; Keane, Clarke, & Corkin, 1992) in 2 patients with lesions in the occipital cortex who were impaired on a perceptual identification task but performed normally on a category generation task. Taken together, these findings suggest that performance on data-driven and conceptually driven implicit memory tasks might be mediated by distinct neuroanatomical systems, both residing outside the limbic-diencephalic area.

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Received September 28,1994 Revision received November 30,1994 Accepted December 7,1994