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Levels of Processing and Single Word Priming in Amnesic and Control Subjects
LEVELS OF PROCESSING AND SINGLE WORD PRIMING IN AMNESIC AND CONTROL SUBJECTS Valerie Jenkins1, Riccardo Russo2 and Alan J. Parkin1 (1Laboratory of Experimental Psychology, University of Sussex, Brighton; 2Department of Psychology, University of Essex, Colchester)
ABSTRACT This paper describes an experiment which examined how levels of processing (LOP) affected word fragment completion in a group of Wernicke-Korsakoff patients, a group of patients with closed head injury, and matched controls. The data showed that both the memory-impaired groups and the controls showed a LOP effect but that the effect was larger in controls. Data from other studies are reviewed and, in conjunction with the present findings, it is concluded that LOP effects obtained when memory-impaired individuals are tested using implicit memory tasks arise mainly from the contribution of lexical processing of targets and from contamination by explicit recollection. Key words: amnesia, word priming
INTRODUCTION Recently, the Levels of Processing (LOP) framework has been applied to the area of implicit memory research. A number of studies have shown that levels of processing manipulations at study produce a dissociation between explicit and implicit memory (e.g. Challis and Brodbeck, 1992; Craik, Moscovitch and McDowd, 1994). A typical LOP manipulation involves rating the meaningfulness of a word (semantic processing), compared to counting the number of vowels contained in a word (physical processing). There are numerous demonstrations that encoding manipulations, while producing a strong effect on performance of direct/explicit tests, do not affect priming on indirect/implicit tests in normal and elderly subjects (e.g. Jacoby and Dallas, 1981; Schacter, 1985; Java and Gardiner, 1991). Reliable priming effects have also been found on indirect tasks involving semantic knowledge, for example generating category exemplars following exposure to a list of items (e.g. Gardener et al., 1973). In addition, a number of study manipulations appear to have a dissociative effect on perceptual versus conceptual forms of indirect tasks. Srinivas and Roediger (1990) demonstrated that category association (an indirect conceptual test) responded like free recall by showing a levels of processing effect whereas fragment completion did not. According to the processing view (e.g. Roediger, Weldon and Challis, 1989), the majority of direct memory tests and conceptually driven indirect memory tests rely on conceptually driven processing for their completion, whereas data driven indirect memory tests (e.g. fragment completion) depend on perceptual processes. For this reason, an indirect perceptual task such as fragment completion should not show a LOP effect. The explanation given is that Cortex, (1998) 34, 577-588
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semantic orienting tasks should not promote more perceptual processing than orienting tasks focusing on the structural characteristics of the targets, therefore a similar amount of perceptual processing is assumed to occur for both semantic and physical encoding tasks. On the other hand, given that conceptually driven tasks rely on elaborative processing, LOP should affect performance on both direct and conceptual priming tests. However, while it is generally suggested that indirect memory tests are more sensitive to data driven processing and direct memory tests to conceptually driven processing, Roediger and Blaxton (1987), point out that no necessary correlation between processing mode and type of test exists. Rather, as Srinivas and Roediger (1990) state, it is more useful to acknowledge that tests may involve both types of processes. Challis and Brodbeck (1992) investigated the claim that LOP does not affect priming in perceptual forms of indirect tests. They recorded the effect of different levels of processing on a word fragment completion test in normal subjects. In the experiments, subjects studied words under semantic and physical learning conditions and, following a five minute interval, were instructed to complete each fragment so that it made an English word. The results revealed a reliable priming effect and, unlike other studies (e.g. Graf et al., 1982; Schacter, 1985), a LOP effect occurred on this indirect memory task. These findings led Challis and Brodbeck to review the literature on LOP effects in tests of word fragment completion, word stem completion and perceptual identification. In their review, Challis and Brodbeck (see also Brown and Mitchell, 1994; Thapar and Greene, 1994) reported that a number of studies demonstrated significant LOP effects in perceptual indirect tests of memory (e.g. Squire, Shimamura and Graf, 1987). In other cases the amount of priming, although not significantly different, was greater in the semantic than in the physical condition. Challis and Brodbeck proposed three explanations for the findings. The first was that performance on the indirect perceptual task was contaminated by explicit retrieval. According to this explanation, when completing the indirect task normal subjects may realise that some of the test items had appeared at study. The subjects then continue to complete the task as one of cued recall. This complements a study by Bowers and Schacter (1990) with test aware and test unaware subjects. Bowers and Schacter obtained a LOP effect with test aware subjects and suggested that these subjects had adopted an explicit retrieval strategy. One way to try and resolve the issue of whether indirect tasks are contaminated by explicit retrieval strategies is to work with amnesic patients. The absence of a LOP effect in this subject group would strengthen the view that normal subjects use explicit memory strategies to complete indirect tasks. The second explanation proposed by Challis and Brodbeck (1992) is that LOP affects perceptual processes during encoding. This assumption is derived from Weldon (1991), who suggested that lexical processing facilitates repetition priming in indirect perceptual tests. Therefore, in the shallow processing conditions, for example counting vowels in a word, less priming should occur because the task discourages lexical processing. The third explanation follows on from the second and rests on the assumption that indirect perceptual tests reflect conceptual as well as perceptual processes. It is known that some tasks are sensitive to semantic or conceptual encoding procedures, for example, generating
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a target item from a conceptual cue produces priming on a perceptual identification and a word fragment completion task (Weldon, 1991). If priming tasks reflect different aspects of encoding, then one would expect to find a LOP effect on those that are more sensitive to the conceptual nature of the task. The following experiment was developed to examine whether single word priming in word fragment completion is affected by different levels of processing. A prediction that follows from the previous account is that if LOP effects in perceptual implicit tasks are a by-product of explicit memory contamination, then one may expect to observe a LOP effect in control subjects but not in amnesic patients. In the following experiment the performance of two groups of memory impaired subjects was compared with two matched control groups. The control groups differed significantly by age but not IQ, which was similar to the amnesic groups. The inclusion of two control groups allowed for the comparison of test performance and specifically examined whether normal controls would show a semantic enhancement effect on this indirect memory task. MATERIALS
AND
METHODS
Subjects The subjects were nine Wernicke Korsakoff (WKS) and nine Closed Head Injured (CHI) adult patients. All the Korsakoff patients had a history of chronic alcoholism, were unable to recall day-to-day events, and had extensive retrograde amnesia. The closed head injured subjects had all sustained their injuries through road traffic accidents, which left them with differing degrees of memory loss. Table I gives the mean performance of each group in terms of age, IQ and memory impairment. The groups did not differ significantly from one another on scores of both current and pre-morbid intelligence (NART; Nelson and O’Connell, 1978). However, the closed head injured subjects were significantly different from the Korsakoff group on three counts, age [t (16) = 3.83, p < 0.001], degree of memory loss – General Memory Index of WMS - [t (16) = 2.57, p < 0.02], and recognition ability words [t (14) = 2.62, p < 0.02]. Therefore the WKS were both older and had a more profound amnesia than the CHI group. Two control groups were also used, matched to each amnesic group by age and IQ (using the NART). The control subjects were recruited from the University of Sussex subject pool and were paid a small amount of money for their time. The Korsakoff control group did not differ from the Korsakoff subjects by age [t (16) = 1.35, p > 0.10] or NART score [t (16) = 0.72, p > 0.10] and neither did the Closed Head Injured and their
TABLE I
Comparison of the Two Patient Groups in Terms of Age, Intelligence and Severity of Memory Impairment
AGE NART FSIQ GMI RMT (words)
WKS (n = 9) Mean (S.D)
CHI (n = 9) Mean (S.D)
58.0 (1.1) 103.33 (12.5) 88.22 (10.04) 57.44 (10.40) ~ 31.42 (5.5)
33.77 (12.6) 103.4 (14.4) 91.37 (7.81) 73.88 (15.69) 39.0 (5.83)
NART = National Adult Reading Test; FSIQ = Full Scale Intelligence Quotient; GMI = General Memory Index; RMT = Recognition Memory Test (Warrington, 1984); ~ = mean based on seven subjects.
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control group [t (16) = 1.16, p > 0.10 for age; t (16) = 1.42, p > 0.10 for NART). Materials and Design A list of forty words was extracted from the set used by Blaxton (1989). The words varied in length from five to eight letters and the corresponding fragments could be completed with only one English word. The mean frequency of the words was 34.5 per million (Kucera and Francis, 1967). The forty words were divided into four equal sets and labelled A, B, C, and D. Three sets were presented at study and each incorporated a different orienting task in the incidental study of the target words. The tasks were: 1: Rating pleasantness (Semantic) 2: Counting syllables (Syllable Judgement) 3: Counting ascending and descending letters (Physical). The study list comprised three sets of words presented in a blocked fashion with, the orienting tasks counterbalanced across the study lists, for example, A1B2C3, B2C3D1, with the unstudied set forming the baseline in each condition. The test list comprised the fragments of all forty words presented in a random order, plus four easy to complete fragments at the start. This was to encourage the amnesic subjects to get into a positive frame of mind, because as a group they are easily discouraged by failure. Procedure Subjects were tested individually and the stimuli were presented one at time on an Apple Macintosh Powerbook using the “Experimenter” package (Wathanasin, Birkett, Russell et al., 1991). Study words and test fragments were presented in lower case and the orienting task commands were given at the start of each set of words. In the semantic study condition, the subjects were asked to: “Please read the word aloud and rate the pleasantness of the word using a seven point scale. Seven indicates that you find the meaning of the word very pleasant and one very unpleasant.” In the syllable judgement condition the subjects were asked to: “Please read the word aloud and count the number of syllables contained in each word, for example, the word egg contains one syllable and butter contains two”. In the physical condition the subjects were asked to: “Please read the word aloud and count the number of ascending and descending letters present in each word. These are the letters that extend above or below the main body of the word.” An example was given to clearly explain this point. The word biology was presented visually on a piece of paper and the instructions were repeated. A short trial was administered to each subject, comprising six words, to ensure that they understood the instructions. Each word was presented for ten seconds with a three second inter-stimulus interval. The distractor phase lasted five minutes during which time the amnesic subjects completed the Wisconsin Card Sort Task. The control groups were asked to try and name a series of photographs of famous faces throughout the decades. The test phase of the experiment comprised the presentation of the studied and non studied word fragments in a random order and the subjects were presented with the following instructions: “Please try and complete each fragment with the first word that comes to mind”. The test was indirect in that no reference was made to the study episode. The fragments were presented in lower case and appeared on the screen for ten seconds, then were replaced by the next fragment. There was an inter-stimulus interval of three seconds between each fragment presentation. The study and test conditions were maintained equally throughout for both the amnesic and control groups.
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RESULT Fragment Completion
Table II shows the percentage of fragments correctly completed for the words studied under the three orienting tasks and for the baseline words. TABLE II
Scores from the Word Fragment Completion Task (percentage correct) Groups WKS Controls-WKS CHI Controls-CHI
Semantic
Syll.Judg.
Physical
Baseline
35% 63% 40% 65%
47% 47% 38% 57%
35% 33% 31% 36%
22% 17% 18% 27%
Priming
A measure of priming was calculated for each subject by subtracting the baseline measure from each score for each condition, and these results are illustrated in Figure 1. In order to assess the affect of LOP on priming a 4 × 3 mixed analysis of variance (ANOVA) and a series of planned comparisons was performed on these scores. The between subjects factor had four levels corresponding to the four groups (wks, chi, control-wks, control-chi), and the within subjects factor had three levels corresponding to the semantic, syllabic and physical processing conditions. This analysis showed no differences in the overall fragment completion performance across the four groups, F (3, 32) < 1, neither a significant difference in the overall performance between patients and controls, F (1, 32) = 2.05, (Mean Square Error) MSe = .142, p > .10. The LOP effect was significant (semantic = 29.4%, (Standard Error) SE = 4.5%; syllabic = 26.4%, SE = 4.3%; physical = 12.5%, SE = 3.9%), F (2, 64) = 11.69, MSe = .025, p < .01, and priming was significantly larger than chance in all study conditions, ts (35) > 3.2, ps < .01 (one-tail). There was a significant interaction, F (6, 64) = 2.33, MSe = .025, p < .05, suggesting that the LOP effect differed in the various groups. More specifically a planned contrast indicated, in line with the predictions, that the LOP effect was larger among controls compared to patients, F (2, 64) = 5.86, MSe = .025, p < .01 (see Figure 1). Further analyses were carried out to assess the magnitude of the LOP effect in both controls and patients. A 2 (control-wks vs control-chi) × 3 (processing levels) mixed ANOVA produced only a significant main effect of LOP, F (2, 32) = 11.96, MSe = .033, p < .01 (semantic = 41.7%, SE = 5.5%; syllabic = 30.0%, SE = 7.2%; physical = 12.2%, SE = 5.9% - priming was significantly larger than chance in all study conditions, ts (l7) > 2.06, ps < .05, one-tail). Moreover it appeared that priming under syllabic processing was significantly
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.5 .45 .4 .35 .3
sem
.25
syll phys
.2 .15 .1 .05 .0 Amnesics
Controls
Fig. 1 – Graph showing the interaction between subject groups (Amnesics vs Controls) and levels of processing. Keys: sem = semantic processing, syll = syllabic processing, phys = physical processing. The dependent variable used is the difference in the percentage of completed target fragments minus new fragments.
larger than under physical processing, F (1, 17) = 7.49, MSe = .038, p < .025, and that priming under semantic processing was larger than under syllabic processing, F (1, 17) = 6.46, MSe = .019, p < .025. The remaining main effect and interaction were not significant, Fs < 1, overall indicating that an equivalent LOP effect occurred in both control groups. A similar analysis was performed on the patient groups. Neither the main effect of group nor the interaction were significant, Fs < 1.22, ps > .10. However the LOP effect approached significance, F (2, 32) = 2.64, MSe = .017, p = .087 (semantic = 17.2%, SE, = 6.1%; syllabic = 22.8%, SE = 4.8%; physical = 12.8%, Se = 5.0% - priming was significantly larger than chance in all study conditions, ts (17) > 2.54, ps < .05, one-tail). It also appeared that priming under syllabic processing was significantly larger than priming under physical processing, F (1, 17) = 5.67, MSe = .016, p < .03. Priming under semantic processing did not differ from priming under physical processing, F (1, 17) = 1.11, MSe = .016, p > .10, or syllabic processing, F (1, 17) = 1.38, MSe = .02, p > .10. A comparison of the overall priming supported by the two deepest processing conditions (i.e. semantic and syllabic) with the amount of priming obtained under the physical processing condition showed a marginally significant advantage of deeper vs shallow processing, F (1, 17) = 4.30, MSe = .054, p = .054. Using a slightly different way to assess the effect of processing on priming, it appeared that no differences occurred between controls and patients in their priming scores for item studied at physical or syllabic processing, Fs < 1, while
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controls showed larger priming scores compared to patients under semantic processing, F (1, 34) = 8.87, MSe = .06, p < .01. GENERAL DISCUSSION Summarising, it appeared that both controls and amnesic patients showed a reliable priming effect in a word fragment completion task. A reliable overall LOP effect was also detected indicating that deeper levels of processing at study induced larger priming. However, the LOP effect was significantly larger in the controls than in the amnesic groups. Since it has been shown that there are no differences in encoding abilities between amnesics and controls (e.g. Mayes, Downes, Shoqeirat et al., 1993) the presence of a larger LOP effect in the control groups is unlikely to be due to better semantic or lexical processing of targets, but it is more likely to be a by-product of an explicit memory contribution to a nominally implicit memory task. As suggested by Challis and Brodbeck (1992) this type of result may reflect the use by normal subjects of explicit memory strategies to complete the indirect task. The words that had been encoded at a “deeper” level would be more accessible to the subject, especially if he or she became aware of the relationship between the study episode and test situation. Test awareness was not specifically examined in the control groups, but a couple of subjects commented that toward the end of the task they recognised some of the words. However, Bowers and Schacter (1990) realised during their own study that they could not determine whether test awareness was a necessary condition for priming or a consequence of priming (for a similar view see also Richardson-Klavehn, Gardiner and Java, 1994). The substantial LOP effect shown by control subjects, i.e. 29.5% difference between semantic and physical processing conditions, is by no means an isolated finding. Differences in performances between physical and semantic processing equal or larger than 25% have been already reported in other studies measuring LOP effects in implicit memory as measured by fragment completion (e.g. Hamman and Squire, 1996, Experiment 1; Squire et al., 1987, Experiment 3). These large effects, as the present one, could be interpreted as an indication that subjects used the available explicit memory of the learning episode to aid the word completion task. We think that this is a plausible suggestion for two reasons. First, we employed a relatively small number of target items (i.e., thirty), and 68% of the items in the test list were targets from the learning phase (similar figures apply also to Hamman and Squire, 1996; and Squire et al., 1987, studies). As suggested by Roediger and McDermott (1993) under these conditions it is likely that healthy normal controls use explicit strategies to perform implicit memory tasks. Second, we tested a group of twelve undergraduates in a pilot experiment comparing an implicit version with an explicit version of the word fragment completion task used in the previously described experiment. The only difference between the two versions of the completion task was in the test instructions. In the explicit version subjects were asked to use the provided fragments as cues to recall the previously processed items. Results indicated, apart from a lower performance for new/baseline
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fragments in the explicit task (i.e., .07 implicit vs .41 explicit), the presence of a significant LOP effect of an equivalent magnitude in both implicit and explicit tests. The difference between semantic and physical processing conditions completion rate was .11 in the implicit task, t (11) = 2.59, p <.05, and .14 in the explicit task, t (11) = 2.84, p < .05. The LOP effect did not differ significantly in the two tasks, t (11) < 1. In addition, it must also be stressed that the essential point here is that large LOP effects can only be obtained in fragment completion priming when subjects have intact explicit memory. This may arise as a direct consequence of explict influences on task performance or because the brain damage found in the memory-impaired group somehow impairs factors which allow a LOP type of influence on implicit memory for fragment completion. This point, however, must await future research – not in the least the development of an unambiguous means of assessing implicit memory free of putative explicit influences. A marginally significant LOP effect was also present in the amnesic subjects. This may be caused, as suggested in the case of normal control subjects, by an explicit memory contribution to the implicit task. This would also explain the reduced LOP effect in the amnesics compared to the control subjects. Since among the amnesics the available explicit memory for the study episode is generally reduced compared to controls, and given that this occurs especially for deep/semantic level of processing (e.g. Graf, Squire and Mandler, 1984), an explicit contribution to fragment completion is expected to be reduced compared to controls. Another possible explanation for the significant LOP effect in the amnesic patients may relate to the view that lexical processing is a factor that positively affects priming (e.g. Weldon, 1991; Richardson-Klavehn and Gardiner, 1998). Lexical access for each target was induced at study by the request to read aloud each presented item. However, syllabic and semantic orienting tasks, focusing the analysis on the items as a whole, may have boosted lexical processing of targets compared to the physical orienting task that could be performed without further analysing target words in their entirety. Therefore this extra lexical processing in the syllabic and semantic orienting tasks could be held responsible for the LOP effect in the amnesics. The present data seem to rule out the third possible explanation suggested by Challis and Brodbeck (1992) to explain LOP effects in implicit tasks. According to this account semantic processing should boost the conceptual analysis of items, which should then benefit priming in perceptual implicit tasks. That conceptual processes could have positively affected priming in the amnesics subjects over and above lexical processing seems unlikely. This is suggested because priming under semantic processing did not benefit any extra increment over that provided by lexical/syllabic processing at study. A fuller account of LOP effects in implicit memory tasks among memory impaired patients can arise from a closer analysis of the amnesics’ data in the current study, and from a review of the relevant published studies on this topic. To this respect it is important to note that while our amnesic patients showed a LOP effect in the present study, such an effect was different from the one displayed by normal controls. In fact, while normal controls’ completion
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performance was at its best after semantic processing, intermediate after syllabic processing, and lowest after physical processing, the performance of amnesic patients in the semantic condition was not better than in the syllabic condition. This finding suggests that the LOP effect displayed by our amnesic sample was more likely due to lexical processing of the stimuli than due to an explicit memory contribution to the implicit task, as in the case of the control subjects. In fact, if explicit memory had primarily contributed over and above lexical processing to the LOP effect in the amnesic sample, then amnesics should have performed significantly better in the semantic than in the lexical processing condition. This pattern of performances should have occurred in the case of an explicit contribution to the word completion test because semantic orienting tasks normally induce better explicit memory performance than lexical orienting tasks. A comparable performance after lexical and semantic orienting tasks suggests that lexical processing of stimuli, equivalently activated by the two processing tasks, should be held responsible for the observed LOP effect among our amnesics (for a similar discussion and findings on normal subjects see Richardson-Klavehn and Gardiner, 1998). The above conclusion does not preclude the relevance of an explicit memory contribution to LOP effect in implicit memory tasks among amnesics. Indications that this can be the case can be gathered from a review of the relevant literature on this topic. There are six published studies where the LOP manipulation was used in conjunction with amnesic patients (Graf et al., 1984; Squire, Shimamura and Graf, 1987; Carlesimo, 1994; Carlesimo, Marfia, Loasses and Caltagirone, 1996; Brunfaut and d’Ydewalle, 1996; Hamman and Squire, 1996). In these studies patients were tested in either word fragment or word stem completion tasks only after physical and semantic processing at study. No lexical processing tasks were used. In the first study (Graf et al., 1984), two experiments assessed the effect of LOP in a word stem completion task using amnesics. The results of the first experiment are, however, difficult to interpret. Implicit testing occurred after learning, but a free recall task on the targets used in the implicit task was administered just before stem completion. Since amnesics showed a LOP effect in both the implicit and the explicit task it is difficult to rule out an explanation in term of explicit memory contamination in the implicit task. In the second experiment the intervening free recall was removed and stem completion was assessed at three different study test delays: no delay, 15 min, and 2 hours. No statistical analyses are provided on the LOP effect in the amnesics. However, inspecting Figure 2 at p. 171, it appears that a LOP effect of about 5% was present at zero delay, while the LOP effect basically disappeared at 15 min and at 2 hours delays. A plausible interpretation of this result could be that a LOP effect occurred only when amnesics were capable of linking the test phase of the fragment completion task to the study phase. At longer delays the link between the study and test might not have been apparent to the amnesics, given their poor memory for past episodes, therefore the probability of explicit contamination in the implicit tasks was reduced. Concurrent to this the LOP effect in the implicit task disappeared. Congruent with this interpretation of the LOP effect in implicit tasks is a
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study by Squire et al. (1987). In two experiments using word stem and word fragment completion a LOP effect of 8% (no statistical analysis are available) in the amnesic patients was only present when testing was carried out at no delay, and this only in the word stem completion task. When the delay between study and test was either two hours or four days no LOP effect was present. It is relevant to notice that amnesic patients showed a LOP effect of comparable magnitude in a yes/no recognition memory task at immediate and two hours delay. This suggests that conceptual and lexical processing of targets, assuming the relevance of lexical processing to recognition memory, should have been similarly available at both intervals to support the LOP effect in the implicit task. However such an effect was absent at the two-hour delay in the implicit tasks (– 10% in stem completion and 0% in fragment completion). This result rules out conceptual and lexical processing as factors supporting LOP effects in implicit word completion tasks at least in Squire et al. study. The similar in magnitude LOP effect in recognition memory among amnesics at immediate and two hour delays is compatible with an account of the LOP effect in the implicit task performance being due to explicit memory contamination. In fact, even if a similar amount of explicit memory for the study episode was available to amnesics immediately and after a two hour delay, it is likely that, given the nature of the implicit task (i.e. say the first word that pop to mind in response to a cue), only after no delay the link between the study and test would be apparent, thus allowing patients to use the available explicit memory of the learning episode in the implicit task. Congruent with this account of LOP effects in implicit tasks in amnesia are the results obtained by Carlesimo (1994), Carlesimo, Marfia, Loasses et al. (1996), and Hamman and Squire (1996). In these studies amnesics were either tested immediately or 5 min after learning using word stem and/or word fragment completion tasks. Here too larger priming effects, often marginally significant, were obtained under semantic than physical processing of targets. Finally, Brunfaut and d’Ydewalle (1996) tested a sample of Korsakoff patients using a word stem completion task. No apparent LOP effect was detected in both amnesic and control subjects. It is relevant to note that Korsakoff patients did not show a LOP effect in a cued memory task where word stems acted as cues. This finding is compatible with the view that LOP effects in implicit memory, when present, arise from the contribution of explicit recollection. From the above review of the relevant literature on LOP effects in implicit memory tasks among amnesic patients it then appears that explicit memory contamination is a plausible factor in contributing to the appearance of significant LOP effects in implicit word completion tasks among amnesics (for a similar view see also Hamman and Squire, 1996). It is however important to note that none of the reviewed studies used a lexical processing task in conjunction with semantic and physical orienting tasks. Therefore, it is somehow difficult to assess the differential contribution of lexical processing and explicit memory contamination on LOP effects in implicit tasks (but see the above discussion in relation to the methodology employed by Squire et al, 1987). If after a lexical orienting task patients had displayed an equivalent amount of repetition priming as under the semantic orienting task, then the role of explicit
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memory contamination in originating the LOP effect among amnesics would have been undermined. The present study in conjunction with Graf et al.’s (1984), Squire et al.’s (1987), Carlesimo (1994), and Hamman and Squire (1996) studies showed that LOP effects in implicit memory tasks are present not only in normal controls (for reviews see Challis and Brodbeck, 1992; Brown and Mitchell, 1994) but also in amnesic subjects. A closer analysis of the results of the present experiment suggests that the lexical processing of targets is the most plausible contributing factor the LOP effect in word completion implicit tasks. On the other hand a literature review suggests that explicit memory contamination can also have an important role in the origin of LOP effects in implicit memory tasks among amnesic patients. Limitations of the methodology used in the reviewed studies did not allow to clearly assess the contribution of lexical processes to the LOP effects detected in the reviewed studies. While the results obtained in the present experiment provide evidence for a critical role of lexical processing in originating the LOP effect in implicit memory tasks among amnesic patients, we recognise the need of further studies to clearly assess the respective role of lexical processing and explicit memory contamination as causes of LOP effects in implicit memory tasks among amnesics. However, as this study suggests (see also Richardson-Klavehn and Gardiner, 1998), only the use of a lexical orienting task in combination with semantic and physical orienting tasks will provide clearer evidence on the role of the above factors in LOP effects in implicit memory tasks among amnesics. Finally we would like to point out that our discussion of LOP effects in implicit tasks applies when LOP is manipulated between subjects or within subjects in a blocked way. Further studies are required to explain the effect of LOP in implicit tasks when different orienting tasks are randomly mixed in the study list (see Thapar and Green, 1994). Acknowledgements. Valerie Jenkins was supported by a scholarship and Alan Parkin was supported by a grant (G9433211N) from the UK Medical Research Council. Riccardo Russo was supported by a grant from The Nuffield Foundation. REFERENCES BLAXTON, T.A. Investigating dissociation among memory measures: Support for a transfer appropriate processing framework. Journal of Experimental Psychology: Learning, Memory and Cognition, 15: 657-668, 1989. BOWERS, J.S., and SCHACTER, D.L. Implicit memory and test awareness. Journal of Experimental Psychology: Learning, Memory and Cognition, 16: 404-413, 1990. BRUNFAUT, E., and D’YDEWALLE, G. A comparison of implicit memory tasks in Korsakoff and alcoholic patients. Neuropsychologia, 34: 1143-1150, 1996. BROWN, A.S., and MITCHELL, D.B. A reevaluation of semantic versus nonsemantic processing in implicit memory. Memory and Cognition, 22: 533-541, 1994. CARLESIMO, G. Perceptual and conceptual priming in amnesic and alcoholic patients. Neuropsychologia, 32: 903-921, 1994. CARLESIMO, G., MARFIA, G.A., LOASSES, A., and CALTAGIRONE , C. Perceptual and conceptual components in implicit and explicit stem completion. Neuropsychologia, 34: 785-792, 1996. CHALLIS, B.H., and BRODBECK, D.R. Levels of processing affects priming in word fragment completion. Journal of Experimental Psychology: Learning, Memory and Cognition, 18: 595-607, 1992. CRAIK, F.I.M., and LOCKHART, R.S. Level of processing: a framework for memory research. Journal of Verbal Learning and Verbal Behaviour, 11: 671-684, 1972. CRAIK, F.I.M., MOSCOVITCH, M., and MCDOWD, J.M. Contributions of surface and conceptual
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information to performance on implicit and explicit memory tasks. Journal of Experimental Psychology: Learning, Memory and Cognition, 20: 864-875, 1994. CRAIK, F.I.M., and TULVING, E. Depth of processing and the retention of words in episodic memory. Journal of Experimental Psychology: General, 104: 268-294, 1975. GARDENER, H., BOLLER, F., MORIENES, J., and BUTTERS, N. Retrieving information from Korsakoff patients: Effects of categorical cues and references to the task. Cortex, 9: 165-175, 1973. GRAF, P., MANDLER, G., and HADEN, P. Simulating amnesic symptoms in normal subjects. Science, 218: 1243-1244, 1982. GRAF, P., SQUIRE, L.R., and MANDLER, G. The information that amnesic patients do not forget. Journal of Experimental Psychology: Learning, Memory and Cognition, 10: 164-178, 1984. HAMMAN, S.B., and SQUIRE, L.R. Levels-of-processing effects in word-completion priming: A neuropsychological study. Journal of Experimental Psychology: Learning, Memory and Cognition, 22: 933-947, 1996. JACOBY, L.L., and DALLAS, M. On the relationship between autobiographical memory and perceptual learning. Journal of Experimental Psychology: General, 110: 306-40, 1981. JAVA, R.I. Priming and ageing: Evidence of preserved memory function in an anagram solution task. American Journal of Psychology, 105: 541-548, 1992. JAVA, R.I., and GARDINER, J.M. Priming and ageing: Further evidence of preserved memory function. American Journal of Psychology, 104: 89-100, 1991. KUCERA, H., and FRANCIS, W.N. Computation Analysis of Present Day American English. Brown University Press, 1967. MAYES, A.R., DOWNES, J.J., SHOQEIRAT, M., HALL, C., and SAGAR, H.J. Encoding ability is preserved in amnesia: Evidence from a direct test of encoding. Neuropsychologia, 31: 745-759, 1993. NELSON, H.E. A modified card sorting test sensitive to frontal lobe deficits. Cortex, 12: 313-324, 1976. NELSON, H.E., and O’CONNELL. Dementia: the estimation of premorbid intelligence levels using the National Adult Reading Test. Cortex, 14: 234-244, 1978. RICHARDSON -KLAVEHN, A., and GARDINER, J.M. Depth-of-processing effects on priming in stem completion: Test of the voluntary contamination, conceptual processing, and lexical procesing hypothesis. Journal of Experimental Psychology: Learning, Memory and Cognition, 1998 (in press). RICHARDSON-KLAVEHN, A., GARDINER, J.M., and JAVA, R.I. Involuntary conscious memory and the method of opposition. Memory, 2: 1-29, 1994. ROEDIGER, H.L., and BLAXTON, T.A. Effects of varying modality, surface features and retention interval on priming in word fragment completion. Memory and Cognition, 15: 379-388, 1987. ROEDIGER, H.L., and MCDERMOTT, K.B. Implicit memory in normal human subjects. In H. Spinnler and F. Boller (Eds.), Handbook of Neuropsychology, Amsterdam: Elsevier, 1993, vol 8, pp. 63-131. ROEDIGER, H.L., WELDON, M.S., and CHALLIS, B.H. Explaining dissociations between implicit and explicit measures of retention: A processing account. In H.L. Roediger and F.I.M. Craik (Eds.), Varieties of Memory and Consciousness: Essays in Honour of Endel Tulving. Hillsdale, NJ: Erlbaum, 1989, pp. 3-41. SCHACTER, D.L. Priming of old and new knowledge in amnesic patients and normal subjects. Annals of New York Academy of Science, 444: 44-53, 1985. SQUIRE, L.R., SHIMAMURA, A.P., and GRAF, P. Strenght and duration of priming effects in normal subjects and amnesic patients. Neuropsychologia, 25: 195-210, 1987. SRIVINAS, K., and ROEDIGER H.L. Classifying implicit memory tests: category association and anagram solution. Journal of Memory and Language, 29: 389-412, 1990. THAPAR, A., and GREENE, R.L. Effects of level of processing on implicit and explicit memory tasks. Journal of Experimental Psychology: Learning, Memory and Cognition, 17: 526-541, 1991. WATHANASIN, S., BIRKETT, T.E., RUSSELL, P.T., and ALTMANN, G.T.M. Experimenter Package for the Apple Macintosh Computer, 1991. WECHSLER, D. Manual for the Wechsler Adult Intelligence Scale - Revised. New York: Psychological Society, New York, 1981. WECHSLER, D. The Wechsler Memory Scale - Revised. San Antonio: Psychological Corporation, 1987. Alan J. Parkin, Laboratory of Experimental Psychology, University of Sussex, Brighton BN1 9QG. E-mail: [email protected] Dr. Riccardo Russo, Dept. of Psychology, University of Essex, Colchester C04 3SQ, VK. E-mail: [email protected]
(Received 28 December 1996; accepted 2 December 1997)
ABSTRACT This paper describes an experiment which examined how levels of processing (LOP) affected word fragment completion in a group of Wernicke-Korsakoff patients, a group of patients with closed head injury, and matched controls. The data showed that both the memory-impaired groups and the controls showed a LOP effect but that the effect was larger in controls. Data from other studies are reviewed and, in conjunction with the present findings, it is concluded that LOP effects obtained when memory-impaired individuals are tested using implicit memory tasks arise mainly from the contribution of lexical processing of targets and from contamination by explicit recollection. Key words: amnesia, word priming
INTRODUCTION Recently, the Levels of Processing (LOP) framework has been applied to the area of implicit memory research. A number of studies have shown that levels of processing manipulations at study produce a dissociation between explicit and implicit memory (e.g. Challis and Brodbeck, 1992; Craik, Moscovitch and McDowd, 1994). A typical LOP manipulation involves rating the meaningfulness of a word (semantic processing), compared to counting the number of vowels contained in a word (physical processing). There are numerous demonstrations that encoding manipulations, while producing a strong effect on performance of direct/explicit tests, do not affect priming on indirect/implicit tests in normal and elderly subjects (e.g. Jacoby and Dallas, 1981; Schacter, 1985; Java and Gardiner, 1991). Reliable priming effects have also been found on indirect tasks involving semantic knowledge, for example generating category exemplars following exposure to a list of items (e.g. Gardener et al., 1973). In addition, a number of study manipulations appear to have a dissociative effect on perceptual versus conceptual forms of indirect tasks. Srinivas and Roediger (1990) demonstrated that category association (an indirect conceptual test) responded like free recall by showing a levels of processing effect whereas fragment completion did not. According to the processing view (e.g. Roediger, Weldon and Challis, 1989), the majority of direct memory tests and conceptually driven indirect memory tests rely on conceptually driven processing for their completion, whereas data driven indirect memory tests (e.g. fragment completion) depend on perceptual processes. For this reason, an indirect perceptual task such as fragment completion should not show a LOP effect. The explanation given is that Cortex, (1998) 34, 577-588
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semantic orienting tasks should not promote more perceptual processing than orienting tasks focusing on the structural characteristics of the targets, therefore a similar amount of perceptual processing is assumed to occur for both semantic and physical encoding tasks. On the other hand, given that conceptually driven tasks rely on elaborative processing, LOP should affect performance on both direct and conceptual priming tests. However, while it is generally suggested that indirect memory tests are more sensitive to data driven processing and direct memory tests to conceptually driven processing, Roediger and Blaxton (1987), point out that no necessary correlation between processing mode and type of test exists. Rather, as Srinivas and Roediger (1990) state, it is more useful to acknowledge that tests may involve both types of processes. Challis and Brodbeck (1992) investigated the claim that LOP does not affect priming in perceptual forms of indirect tests. They recorded the effect of different levels of processing on a word fragment completion test in normal subjects. In the experiments, subjects studied words under semantic and physical learning conditions and, following a five minute interval, were instructed to complete each fragment so that it made an English word. The results revealed a reliable priming effect and, unlike other studies (e.g. Graf et al., 1982; Schacter, 1985), a LOP effect occurred on this indirect memory task. These findings led Challis and Brodbeck to review the literature on LOP effects in tests of word fragment completion, word stem completion and perceptual identification. In their review, Challis and Brodbeck (see also Brown and Mitchell, 1994; Thapar and Greene, 1994) reported that a number of studies demonstrated significant LOP effects in perceptual indirect tests of memory (e.g. Squire, Shimamura and Graf, 1987). In other cases the amount of priming, although not significantly different, was greater in the semantic than in the physical condition. Challis and Brodbeck proposed three explanations for the findings. The first was that performance on the indirect perceptual task was contaminated by explicit retrieval. According to this explanation, when completing the indirect task normal subjects may realise that some of the test items had appeared at study. The subjects then continue to complete the task as one of cued recall. This complements a study by Bowers and Schacter (1990) with test aware and test unaware subjects. Bowers and Schacter obtained a LOP effect with test aware subjects and suggested that these subjects had adopted an explicit retrieval strategy. One way to try and resolve the issue of whether indirect tasks are contaminated by explicit retrieval strategies is to work with amnesic patients. The absence of a LOP effect in this subject group would strengthen the view that normal subjects use explicit memory strategies to complete indirect tasks. The second explanation proposed by Challis and Brodbeck (1992) is that LOP affects perceptual processes during encoding. This assumption is derived from Weldon (1991), who suggested that lexical processing facilitates repetition priming in indirect perceptual tests. Therefore, in the shallow processing conditions, for example counting vowels in a word, less priming should occur because the task discourages lexical processing. The third explanation follows on from the second and rests on the assumption that indirect perceptual tests reflect conceptual as well as perceptual processes. It is known that some tasks are sensitive to semantic or conceptual encoding procedures, for example, generating
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a target item from a conceptual cue produces priming on a perceptual identification and a word fragment completion task (Weldon, 1991). If priming tasks reflect different aspects of encoding, then one would expect to find a LOP effect on those that are more sensitive to the conceptual nature of the task. The following experiment was developed to examine whether single word priming in word fragment completion is affected by different levels of processing. A prediction that follows from the previous account is that if LOP effects in perceptual implicit tasks are a by-product of explicit memory contamination, then one may expect to observe a LOP effect in control subjects but not in amnesic patients. In the following experiment the performance of two groups of memory impaired subjects was compared with two matched control groups. The control groups differed significantly by age but not IQ, which was similar to the amnesic groups. The inclusion of two control groups allowed for the comparison of test performance and specifically examined whether normal controls would show a semantic enhancement effect on this indirect memory task. MATERIALS
AND
METHODS
Subjects The subjects were nine Wernicke Korsakoff (WKS) and nine Closed Head Injured (CHI) adult patients. All the Korsakoff patients had a history of chronic alcoholism, were unable to recall day-to-day events, and had extensive retrograde amnesia. The closed head injured subjects had all sustained their injuries through road traffic accidents, which left them with differing degrees of memory loss. Table I gives the mean performance of each group in terms of age, IQ and memory impairment. The groups did not differ significantly from one another on scores of both current and pre-morbid intelligence (NART; Nelson and O’Connell, 1978). However, the closed head injured subjects were significantly different from the Korsakoff group on three counts, age [t (16) = 3.83, p < 0.001], degree of memory loss – General Memory Index of WMS - [t (16) = 2.57, p < 0.02], and recognition ability words [t (14) = 2.62, p < 0.02]. Therefore the WKS were both older and had a more profound amnesia than the CHI group. Two control groups were also used, matched to each amnesic group by age and IQ (using the NART). The control subjects were recruited from the University of Sussex subject pool and were paid a small amount of money for their time. The Korsakoff control group did not differ from the Korsakoff subjects by age [t (16) = 1.35, p > 0.10] or NART score [t (16) = 0.72, p > 0.10] and neither did the Closed Head Injured and their
TABLE I
Comparison of the Two Patient Groups in Terms of Age, Intelligence and Severity of Memory Impairment
AGE NART FSIQ GMI RMT (words)
WKS (n = 9) Mean (S.D)
CHI (n = 9) Mean (S.D)
58.0 (1.1) 103.33 (12.5) 88.22 (10.04) 57.44 (10.40) ~ 31.42 (5.5)
33.77 (12.6) 103.4 (14.4) 91.37 (7.81) 73.88 (15.69) 39.0 (5.83)
NART = National Adult Reading Test; FSIQ = Full Scale Intelligence Quotient; GMI = General Memory Index; RMT = Recognition Memory Test (Warrington, 1984); ~ = mean based on seven subjects.
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control group [t (16) = 1.16, p > 0.10 for age; t (16) = 1.42, p > 0.10 for NART). Materials and Design A list of forty words was extracted from the set used by Blaxton (1989). The words varied in length from five to eight letters and the corresponding fragments could be completed with only one English word. The mean frequency of the words was 34.5 per million (Kucera and Francis, 1967). The forty words were divided into four equal sets and labelled A, B, C, and D. Three sets were presented at study and each incorporated a different orienting task in the incidental study of the target words. The tasks were: 1: Rating pleasantness (Semantic) 2: Counting syllables (Syllable Judgement) 3: Counting ascending and descending letters (Physical). The study list comprised three sets of words presented in a blocked fashion with, the orienting tasks counterbalanced across the study lists, for example, A1B2C3, B2C3D1, with the unstudied set forming the baseline in each condition. The test list comprised the fragments of all forty words presented in a random order, plus four easy to complete fragments at the start. This was to encourage the amnesic subjects to get into a positive frame of mind, because as a group they are easily discouraged by failure. Procedure Subjects were tested individually and the stimuli were presented one at time on an Apple Macintosh Powerbook using the “Experimenter” package (Wathanasin, Birkett, Russell et al., 1991). Study words and test fragments were presented in lower case and the orienting task commands were given at the start of each set of words. In the semantic study condition, the subjects were asked to: “Please read the word aloud and rate the pleasantness of the word using a seven point scale. Seven indicates that you find the meaning of the word very pleasant and one very unpleasant.” In the syllable judgement condition the subjects were asked to: “Please read the word aloud and count the number of syllables contained in each word, for example, the word egg contains one syllable and butter contains two”. In the physical condition the subjects were asked to: “Please read the word aloud and count the number of ascending and descending letters present in each word. These are the letters that extend above or below the main body of the word.” An example was given to clearly explain this point. The word biology was presented visually on a piece of paper and the instructions were repeated. A short trial was administered to each subject, comprising six words, to ensure that they understood the instructions. Each word was presented for ten seconds with a three second inter-stimulus interval. The distractor phase lasted five minutes during which time the amnesic subjects completed the Wisconsin Card Sort Task. The control groups were asked to try and name a series of photographs of famous faces throughout the decades. The test phase of the experiment comprised the presentation of the studied and non studied word fragments in a random order and the subjects were presented with the following instructions: “Please try and complete each fragment with the first word that comes to mind”. The test was indirect in that no reference was made to the study episode. The fragments were presented in lower case and appeared on the screen for ten seconds, then were replaced by the next fragment. There was an inter-stimulus interval of three seconds between each fragment presentation. The study and test conditions were maintained equally throughout for both the amnesic and control groups.
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RESULT Fragment Completion
Table II shows the percentage of fragments correctly completed for the words studied under the three orienting tasks and for the baseline words. TABLE II
Scores from the Word Fragment Completion Task (percentage correct) Groups WKS Controls-WKS CHI Controls-CHI
Semantic
Syll.Judg.
Physical
Baseline
35% 63% 40% 65%
47% 47% 38% 57%
35% 33% 31% 36%
22% 17% 18% 27%
Priming
A measure of priming was calculated for each subject by subtracting the baseline measure from each score for each condition, and these results are illustrated in Figure 1. In order to assess the affect of LOP on priming a 4 × 3 mixed analysis of variance (ANOVA) and a series of planned comparisons was performed on these scores. The between subjects factor had four levels corresponding to the four groups (wks, chi, control-wks, control-chi), and the within subjects factor had three levels corresponding to the semantic, syllabic and physical processing conditions. This analysis showed no differences in the overall fragment completion performance across the four groups, F (3, 32) < 1, neither a significant difference in the overall performance between patients and controls, F (1, 32) = 2.05, (Mean Square Error) MSe = .142, p > .10. The LOP effect was significant (semantic = 29.4%, (Standard Error) SE = 4.5%; syllabic = 26.4%, SE = 4.3%; physical = 12.5%, SE = 3.9%), F (2, 64) = 11.69, MSe = .025, p < .01, and priming was significantly larger than chance in all study conditions, ts (35) > 3.2, ps < .01 (one-tail). There was a significant interaction, F (6, 64) = 2.33, MSe = .025, p < .05, suggesting that the LOP effect differed in the various groups. More specifically a planned contrast indicated, in line with the predictions, that the LOP effect was larger among controls compared to patients, F (2, 64) = 5.86, MSe = .025, p < .01 (see Figure 1). Further analyses were carried out to assess the magnitude of the LOP effect in both controls and patients. A 2 (control-wks vs control-chi) × 3 (processing levels) mixed ANOVA produced only a significant main effect of LOP, F (2, 32) = 11.96, MSe = .033, p < .01 (semantic = 41.7%, SE = 5.5%; syllabic = 30.0%, SE = 7.2%; physical = 12.2%, SE = 5.9% - priming was significantly larger than chance in all study conditions, ts (l7) > 2.06, ps < .05, one-tail). Moreover it appeared that priming under syllabic processing was significantly
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.5 .45 .4 .35 .3
sem
.25
syll phys
.2 .15 .1 .05 .0 Amnesics
Controls
Fig. 1 – Graph showing the interaction between subject groups (Amnesics vs Controls) and levels of processing. Keys: sem = semantic processing, syll = syllabic processing, phys = physical processing. The dependent variable used is the difference in the percentage of completed target fragments minus new fragments.
larger than under physical processing, F (1, 17) = 7.49, MSe = .038, p < .025, and that priming under semantic processing was larger than under syllabic processing, F (1, 17) = 6.46, MSe = .019, p < .025. The remaining main effect and interaction were not significant, Fs < 1, overall indicating that an equivalent LOP effect occurred in both control groups. A similar analysis was performed on the patient groups. Neither the main effect of group nor the interaction were significant, Fs < 1.22, ps > .10. However the LOP effect approached significance, F (2, 32) = 2.64, MSe = .017, p = .087 (semantic = 17.2%, SE, = 6.1%; syllabic = 22.8%, SE = 4.8%; physical = 12.8%, Se = 5.0% - priming was significantly larger than chance in all study conditions, ts (17) > 2.54, ps < .05, one-tail). It also appeared that priming under syllabic processing was significantly larger than priming under physical processing, F (1, 17) = 5.67, MSe = .016, p < .03. Priming under semantic processing did not differ from priming under physical processing, F (1, 17) = 1.11, MSe = .016, p > .10, or syllabic processing, F (1, 17) = 1.38, MSe = .02, p > .10. A comparison of the overall priming supported by the two deepest processing conditions (i.e. semantic and syllabic) with the amount of priming obtained under the physical processing condition showed a marginally significant advantage of deeper vs shallow processing, F (1, 17) = 4.30, MSe = .054, p = .054. Using a slightly different way to assess the effect of processing on priming, it appeared that no differences occurred between controls and patients in their priming scores for item studied at physical or syllabic processing, Fs < 1, while
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controls showed larger priming scores compared to patients under semantic processing, F (1, 34) = 8.87, MSe = .06, p < .01. GENERAL DISCUSSION Summarising, it appeared that both controls and amnesic patients showed a reliable priming effect in a word fragment completion task. A reliable overall LOP effect was also detected indicating that deeper levels of processing at study induced larger priming. However, the LOP effect was significantly larger in the controls than in the amnesic groups. Since it has been shown that there are no differences in encoding abilities between amnesics and controls (e.g. Mayes, Downes, Shoqeirat et al., 1993) the presence of a larger LOP effect in the control groups is unlikely to be due to better semantic or lexical processing of targets, but it is more likely to be a by-product of an explicit memory contribution to a nominally implicit memory task. As suggested by Challis and Brodbeck (1992) this type of result may reflect the use by normal subjects of explicit memory strategies to complete the indirect task. The words that had been encoded at a “deeper” level would be more accessible to the subject, especially if he or she became aware of the relationship between the study episode and test situation. Test awareness was not specifically examined in the control groups, but a couple of subjects commented that toward the end of the task they recognised some of the words. However, Bowers and Schacter (1990) realised during their own study that they could not determine whether test awareness was a necessary condition for priming or a consequence of priming (for a similar view see also Richardson-Klavehn, Gardiner and Java, 1994). The substantial LOP effect shown by control subjects, i.e. 29.5% difference between semantic and physical processing conditions, is by no means an isolated finding. Differences in performances between physical and semantic processing equal or larger than 25% have been already reported in other studies measuring LOP effects in implicit memory as measured by fragment completion (e.g. Hamman and Squire, 1996, Experiment 1; Squire et al., 1987, Experiment 3). These large effects, as the present one, could be interpreted as an indication that subjects used the available explicit memory of the learning episode to aid the word completion task. We think that this is a plausible suggestion for two reasons. First, we employed a relatively small number of target items (i.e., thirty), and 68% of the items in the test list were targets from the learning phase (similar figures apply also to Hamman and Squire, 1996; and Squire et al., 1987, studies). As suggested by Roediger and McDermott (1993) under these conditions it is likely that healthy normal controls use explicit strategies to perform implicit memory tasks. Second, we tested a group of twelve undergraduates in a pilot experiment comparing an implicit version with an explicit version of the word fragment completion task used in the previously described experiment. The only difference between the two versions of the completion task was in the test instructions. In the explicit version subjects were asked to use the provided fragments as cues to recall the previously processed items. Results indicated, apart from a lower performance for new/baseline
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fragments in the explicit task (i.e., .07 implicit vs .41 explicit), the presence of a significant LOP effect of an equivalent magnitude in both implicit and explicit tests. The difference between semantic and physical processing conditions completion rate was .11 in the implicit task, t (11) = 2.59, p <.05, and .14 in the explicit task, t (11) = 2.84, p < .05. The LOP effect did not differ significantly in the two tasks, t (11) < 1. In addition, it must also be stressed that the essential point here is that large LOP effects can only be obtained in fragment completion priming when subjects have intact explicit memory. This may arise as a direct consequence of explict influences on task performance or because the brain damage found in the memory-impaired group somehow impairs factors which allow a LOP type of influence on implicit memory for fragment completion. This point, however, must await future research – not in the least the development of an unambiguous means of assessing implicit memory free of putative explicit influences. A marginally significant LOP effect was also present in the amnesic subjects. This may be caused, as suggested in the case of normal control subjects, by an explicit memory contribution to the implicit task. This would also explain the reduced LOP effect in the amnesics compared to the control subjects. Since among the amnesics the available explicit memory for the study episode is generally reduced compared to controls, and given that this occurs especially for deep/semantic level of processing (e.g. Graf, Squire and Mandler, 1984), an explicit contribution to fragment completion is expected to be reduced compared to controls. Another possible explanation for the significant LOP effect in the amnesic patients may relate to the view that lexical processing is a factor that positively affects priming (e.g. Weldon, 1991; Richardson-Klavehn and Gardiner, 1998). Lexical access for each target was induced at study by the request to read aloud each presented item. However, syllabic and semantic orienting tasks, focusing the analysis on the items as a whole, may have boosted lexical processing of targets compared to the physical orienting task that could be performed without further analysing target words in their entirety. Therefore this extra lexical processing in the syllabic and semantic orienting tasks could be held responsible for the LOP effect in the amnesics. The present data seem to rule out the third possible explanation suggested by Challis and Brodbeck (1992) to explain LOP effects in implicit tasks. According to this account semantic processing should boost the conceptual analysis of items, which should then benefit priming in perceptual implicit tasks. That conceptual processes could have positively affected priming in the amnesics subjects over and above lexical processing seems unlikely. This is suggested because priming under semantic processing did not benefit any extra increment over that provided by lexical/syllabic processing at study. A fuller account of LOP effects in implicit memory tasks among memory impaired patients can arise from a closer analysis of the amnesics’ data in the current study, and from a review of the relevant published studies on this topic. To this respect it is important to note that while our amnesic patients showed a LOP effect in the present study, such an effect was different from the one displayed by normal controls. In fact, while normal controls’ completion
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performance was at its best after semantic processing, intermediate after syllabic processing, and lowest after physical processing, the performance of amnesic patients in the semantic condition was not better than in the syllabic condition. This finding suggests that the LOP effect displayed by our amnesic sample was more likely due to lexical processing of the stimuli than due to an explicit memory contribution to the implicit task, as in the case of the control subjects. In fact, if explicit memory had primarily contributed over and above lexical processing to the LOP effect in the amnesic sample, then amnesics should have performed significantly better in the semantic than in the lexical processing condition. This pattern of performances should have occurred in the case of an explicit contribution to the word completion test because semantic orienting tasks normally induce better explicit memory performance than lexical orienting tasks. A comparable performance after lexical and semantic orienting tasks suggests that lexical processing of stimuli, equivalently activated by the two processing tasks, should be held responsible for the observed LOP effect among our amnesics (for a similar discussion and findings on normal subjects see Richardson-Klavehn and Gardiner, 1998). The above conclusion does not preclude the relevance of an explicit memory contribution to LOP effect in implicit memory tasks among amnesics. Indications that this can be the case can be gathered from a review of the relevant literature on this topic. There are six published studies where the LOP manipulation was used in conjunction with amnesic patients (Graf et al., 1984; Squire, Shimamura and Graf, 1987; Carlesimo, 1994; Carlesimo, Marfia, Loasses and Caltagirone, 1996; Brunfaut and d’Ydewalle, 1996; Hamman and Squire, 1996). In these studies patients were tested in either word fragment or word stem completion tasks only after physical and semantic processing at study. No lexical processing tasks were used. In the first study (Graf et al., 1984), two experiments assessed the effect of LOP in a word stem completion task using amnesics. The results of the first experiment are, however, difficult to interpret. Implicit testing occurred after learning, but a free recall task on the targets used in the implicit task was administered just before stem completion. Since amnesics showed a LOP effect in both the implicit and the explicit task it is difficult to rule out an explanation in term of explicit memory contamination in the implicit task. In the second experiment the intervening free recall was removed and stem completion was assessed at three different study test delays: no delay, 15 min, and 2 hours. No statistical analyses are provided on the LOP effect in the amnesics. However, inspecting Figure 2 at p. 171, it appears that a LOP effect of about 5% was present at zero delay, while the LOP effect basically disappeared at 15 min and at 2 hours delays. A plausible interpretation of this result could be that a LOP effect occurred only when amnesics were capable of linking the test phase of the fragment completion task to the study phase. At longer delays the link between the study and test might not have been apparent to the amnesics, given their poor memory for past episodes, therefore the probability of explicit contamination in the implicit tasks was reduced. Concurrent to this the LOP effect in the implicit task disappeared. Congruent with this interpretation of the LOP effect in implicit tasks is a
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study by Squire et al. (1987). In two experiments using word stem and word fragment completion a LOP effect of 8% (no statistical analysis are available) in the amnesic patients was only present when testing was carried out at no delay, and this only in the word stem completion task. When the delay between study and test was either two hours or four days no LOP effect was present. It is relevant to notice that amnesic patients showed a LOP effect of comparable magnitude in a yes/no recognition memory task at immediate and two hours delay. This suggests that conceptual and lexical processing of targets, assuming the relevance of lexical processing to recognition memory, should have been similarly available at both intervals to support the LOP effect in the implicit task. However such an effect was absent at the two-hour delay in the implicit tasks (– 10% in stem completion and 0% in fragment completion). This result rules out conceptual and lexical processing as factors supporting LOP effects in implicit word completion tasks at least in Squire et al. study. The similar in magnitude LOP effect in recognition memory among amnesics at immediate and two hour delays is compatible with an account of the LOP effect in the implicit task performance being due to explicit memory contamination. In fact, even if a similar amount of explicit memory for the study episode was available to amnesics immediately and after a two hour delay, it is likely that, given the nature of the implicit task (i.e. say the first word that pop to mind in response to a cue), only after no delay the link between the study and test would be apparent, thus allowing patients to use the available explicit memory of the learning episode in the implicit task. Congruent with this account of LOP effects in implicit tasks in amnesia are the results obtained by Carlesimo (1994), Carlesimo, Marfia, Loasses et al. (1996), and Hamman and Squire (1996). In these studies amnesics were either tested immediately or 5 min after learning using word stem and/or word fragment completion tasks. Here too larger priming effects, often marginally significant, were obtained under semantic than physical processing of targets. Finally, Brunfaut and d’Ydewalle (1996) tested a sample of Korsakoff patients using a word stem completion task. No apparent LOP effect was detected in both amnesic and control subjects. It is relevant to note that Korsakoff patients did not show a LOP effect in a cued memory task where word stems acted as cues. This finding is compatible with the view that LOP effects in implicit memory, when present, arise from the contribution of explicit recollection. From the above review of the relevant literature on LOP effects in implicit memory tasks among amnesic patients it then appears that explicit memory contamination is a plausible factor in contributing to the appearance of significant LOP effects in implicit word completion tasks among amnesics (for a similar view see also Hamman and Squire, 1996). It is however important to note that none of the reviewed studies used a lexical processing task in conjunction with semantic and physical orienting tasks. Therefore, it is somehow difficult to assess the differential contribution of lexical processing and explicit memory contamination on LOP effects in implicit tasks (but see the above discussion in relation to the methodology employed by Squire et al, 1987). If after a lexical orienting task patients had displayed an equivalent amount of repetition priming as under the semantic orienting task, then the role of explicit
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memory contamination in originating the LOP effect among amnesics would have been undermined. The present study in conjunction with Graf et al.’s (1984), Squire et al.’s (1987), Carlesimo (1994), and Hamman and Squire (1996) studies showed that LOP effects in implicit memory tasks are present not only in normal controls (for reviews see Challis and Brodbeck, 1992; Brown and Mitchell, 1994) but also in amnesic subjects. A closer analysis of the results of the present experiment suggests that the lexical processing of targets is the most plausible contributing factor the LOP effect in word completion implicit tasks. On the other hand a literature review suggests that explicit memory contamination can also have an important role in the origin of LOP effects in implicit memory tasks among amnesic patients. Limitations of the methodology used in the reviewed studies did not allow to clearly assess the contribution of lexical processes to the LOP effects detected in the reviewed studies. While the results obtained in the present experiment provide evidence for a critical role of lexical processing in originating the LOP effect in implicit memory tasks among amnesic patients, we recognise the need of further studies to clearly assess the respective role of lexical processing and explicit memory contamination as causes of LOP effects in implicit memory tasks among amnesics. However, as this study suggests (see also Richardson-Klavehn and Gardiner, 1998), only the use of a lexical orienting task in combination with semantic and physical orienting tasks will provide clearer evidence on the role of the above factors in LOP effects in implicit memory tasks among amnesics. Finally we would like to point out that our discussion of LOP effects in implicit tasks applies when LOP is manipulated between subjects or within subjects in a blocked way. Further studies are required to explain the effect of LOP in implicit tasks when different orienting tasks are randomly mixed in the study list (see Thapar and Green, 1994). Acknowledgements. Valerie Jenkins was supported by a scholarship and Alan Parkin was supported by a grant (G9433211N) from the UK Medical Research Council. Riccardo Russo was supported by a grant from The Nuffield Foundation. REFERENCES BLAXTON, T.A. Investigating dissociation among memory measures: Support for a transfer appropriate processing framework. Journal of Experimental Psychology: Learning, Memory and Cognition, 15: 657-668, 1989. BOWERS, J.S., and SCHACTER, D.L. Implicit memory and test awareness. Journal of Experimental Psychology: Learning, Memory and Cognition, 16: 404-413, 1990. BRUNFAUT, E., and D’YDEWALLE, G. A comparison of implicit memory tasks in Korsakoff and alcoholic patients. Neuropsychologia, 34: 1143-1150, 1996. BROWN, A.S., and MITCHELL, D.B. A reevaluation of semantic versus nonsemantic processing in implicit memory. Memory and Cognition, 22: 533-541, 1994. CARLESIMO, G. Perceptual and conceptual priming in amnesic and alcoholic patients. Neuropsychologia, 32: 903-921, 1994. CARLESIMO, G., MARFIA, G.A., LOASSES, A., and CALTAGIRONE , C. Perceptual and conceptual components in implicit and explicit stem completion. Neuropsychologia, 34: 785-792, 1996. CHALLIS, B.H., and BRODBECK, D.R. Levels of processing affects priming in word fragment completion. Journal of Experimental Psychology: Learning, Memory and Cognition, 18: 595-607, 1992. CRAIK, F.I.M., and LOCKHART, R.S. Level of processing: a framework for memory research. Journal of Verbal Learning and Verbal Behaviour, 11: 671-684, 1972. CRAIK, F.I.M., MOSCOVITCH, M., and MCDOWD, J.M. Contributions of surface and conceptual
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(Received 28 December 1996; accepted 2 December 1997)