Priming Effects in Amnesia: Evidence for a Dissociable Memory Function

Transcription

1 The Quarterly Journal of Experimental Psychology (1986) 38A, Priming Effects in Amnesia: Evidence for a Dissociable Memory Function Arthur P. Shimamura Department of Psychiatry, University of California, San Diego, California, U.S.A. Amnesic patients are impaired on tests of recall and recognition memory, yet they exhibit intact priming effects. That is, their performance can be facilitated or biased by recently encountered information. This paper reviews the phenomenon of preserved priming effects in amnesia, describes relationships between priming and other memory functions, and comments on what this spared memory function tells us about the organization of memory. Introduction Neuropsychology provides a vital bridge between experimental psychology and neuroscience. Careful studies of patients with brain damage have found that cognitive impairment can often be relatively circumscribed-affecting certain cognitive functions while leaving others intact (see Broadbent and Weiskrantz, 1982; Heilman and Valenstein, 1979; Luria, 1973). This fact has led to the view that brain organization can be characterized as a set of separable, yet highly interactive information processing systems (Gardner, 1983; Luria, 1973; Mishkin, 1982; Shallice, 1979). Studies of the neuropsychology of learning and memory have corroborated this view of brain organization. Amnesic patients exhibit impairment on tests of recall and recognition memory, even when testing is conducted only minutes after learning. This impairment has been linked to damage in the diencephalic midline or in the medial temporal region (for reviews see Mair, Warrington and Weiskrantz, Requests for reprints should be sent to Arthur P. Shimamura, Department of Psychiatry (V116), Veterans Administration Medical Center, 3350 La Jolla Village Drive, San Diego, CA Supported by the National Institute of Mental Health (MH2 4600). I thank Larry Squire and Nelson Butters for helpful discussions and comments The Experimental Psychology Society 93

2 620 A. P. Shimamura 1979; Mishkin, 1982; Squire and Zola-Morgan, 1983). Nevertheless, amnesic patients can exhibit normal performance on tests of intellectual and language functions. Moreover, certain memory functions are also preserved, as indicated by good performance on tests of short-term memory (Baddeley and Warrington, 1970; Drachman and Arbit, 1966), simple classical conditioning of the eyelid response (Weiskrantz and Warrington, 1979), and skills (Brooks and Baddeley, 1976; Cohen and Squire, 1980; Corkin, 1968; Milner, 1962; Squire, Cohen and Zouzounis, 1984). In addition, amnesic patients exhibit preserved priming effects. That is, their performance can be facilitated or biased by recently encountered information. This paper presents a review of the phenomenon of preserved priming in amnesia, with commentary on what this spared memory function tells us about the organization of memory. Preserved Learning in Cued Recall Tests: Preliminary Evidence of Priming Effects in Amnesia The seminal work of Warrington and Weiskrantz with the cued recall procedure provided the impetus for much of the research that will be discussed. They were the first to demonstrate that amnesic patients could exhibit normal or close-to-normal cued recall performance when the cues were fragmented words or pictures (cf. Gollin, 1960). In this task, subjects were presented with fragmented words or pictures and were asked to name the stimuli. If a stimulus could not be named, then a succession of less fragmented versions of the stimulus was shown until the subjects could name it. In the retention test this cueing procedure was repeated, and subjects were asked to use the fragmented cues as aids to facilitate identification of previously presented items. When testing occurred 1 min after presentation, amnesic patients and control subjects exhibited similar levels of cued recall performance, yet amnesic patients were more impaired on tests of free recall and recognition (Warrington and Weiskrantz, 1970a). At longer retention intervals (e.g., 1-hr or 24- hr), amnesic patients exhibited savings in relearning by performing better than they had done during the initial study phase, but they still performed worse than control subjects (Warrington and Weiskrantz, 1968; 1970b). Initially, these findings were used to support the view that amnesia produces a deficit in retrieval. Specifically, it was suggested that cued recall tasks provide a more effective method for retrieving memories, because test cues reduce interference from competing responses (Warrington and Weiskrantz, 1970a, 1974). However, this interpretation was 94

3 Priming Effects in Amnesia 621 later rejected (Warrington and Weiskrantz, 1978), because amnesic patients were not sensitive to manipulations of response competition. For example, when response competition was completely eliminated by using stems that uniquely specify study words (e.g., ank for ankle), amnesic patients exhibited about the same cued recall level as compared to conditions of higher response competition-that is, when word stems could be completed with many possible responses (e.g., mot for motel). In another cued recall experiment, an attempt was made to increase response competition by giving multiple study/test trials in which the words used on the first trial could be cued with the same three-letter beginnings as words used in subsequent trials (e.g., cycle, cyclone). Firstlist learning did interfere with later learning, but on the first reversal trial, amnesic patients did not exhibit disproportionately greater response interference than control subjects (Warrington and Weiskrantz, 1978). This finding was not consistent with a retrieval deficit caused by increased response competition, because if it were then the greatest amount of interference should have occurred on the first reversal trial. In a later study, Warrington and Weiskrantz (1982) offered a different hypothesis of amnesia in which they explained good cued recall performance in terms of an automatic facilitatory effect that occurs as a result of stimulus repetition (see below for details). Although amnesic patients exhibited normal cued recall performance in amnesic patients in some studies (Warrington and Weiskrantz, 1970a, 1974,1978), they often performed significantly more poorly than control subjects in others (Mayes, Meudall and Neary, 1978; Mortensen, 1980; Squire, Wetzel and Slater, 1978; Warrington and Weiskrantz, 1968, 1970b). In the latter studies, cued recall tests did produce better performance than tests of free recall and yes/no recognition, but as both amnesic patients and control subjects exhibited improved cued recall performance, the difference between groups was maintained. More importantly, it was shown that the same pattern of performance exhibited by amnesic patients-that is, preserved cued recall and poor yes/no recognition memory-could be simulated in control subjects if testing occurred after long retention intervals (Mayes and Meudell, 1981; Mortensen, 1980; Squire et al., 1978; Woods and Piercy, 1974). For example, Woods and Piercy (1974) found that recognition performance of control subjects fell from 83% correct after a 1-min delay to 63.7% correct after a 1-wk delay. Yet cued recall performance across these two retention intervals was similar-62.4% correct after a 1-min delay, vs. 64.4% correct after a 1-wk delay. This finding showed that control subjects who are tested at a time when memory is weak exhibit good cued recall performance relative to yes/no recognition performance. Because of such results, the possibility had to be considered that the 95

4 622 A. P. Shimamura good cued recall performance exhibited by amnesic patients is merely a consequence of weak memory and does not necessarily reflect a feature of preserved memory that is unique to amnesia. To summarize the findings of the cued recall procedure: (1) the amnesic deficit cannot be explained as a simple deficit in retrieval that is circumvented by cued recall procedures, (2) cued recall procedures improve the memory of both amnesic patients and control subjects, and thus entirely normal performance in amnesic patients is not usually observed, and (3) the good cued recall performance relative to yes/no recognition performance may be a consequence of differential sensitivity of test measures rather than an indication of a specific amnesic deficit that affects free recall and recognition but not cued recall. Despite these facts, the finding of entirely normal cued recall performance in amnesic patients in some cases (Warrington and Weiskrantz, 1970a, 1974, 1978) suggested that under certain testing conditions it may be possible to demonstrate preserved performance. The following sections summarize more recent findings and outline the conditions under which intact performance is found. Demonstrations of Preserved Priming Effects in Amnesia There were early hints that a different memory process or strategy was sometimes being used in the cued recall task. It was noted that patients treated the task more as a guessing game than a formal test of memory (Warrington and Weiskrantz, 1968, p. 974). Mortensen (1980) suggested that good cued recall performance by amnesic patients may be explained by the fact that reading a word during study must involve activation of its semantic memory representations... this activation may result in some kind of priming (p. 81). Similarly, Rozin (1976) suggested that the preserved cued recall performance found by Warrington and Weiskrantz and by himself (subsequently published by Diamond and Rozin, 1984) was the result of a transient activation of preexisting representations in memory. Rozin (1976) suggested that activation is preserved in amnesia and that this process can be likened to a hot tubes effect. After a vacuum tube radio is turned off, the tubes remain hot for a while. The idea that memory activation is preserved in amnesia helped to clarify some of the inconsistent results obtained by the cued recall procedure. By this view, amnesia produces a deficit in conscious recollection, a deficit that could be attributed to poor memory storagethat is, poor elaborative encoding, organization, and consolidation during study (Butters and Cermak, 1980; Squire, 1982)-or attributed 96

5 Priming Effects in Amnesia 623 to both poor memory storage and retrieval (Warrington and Weiskrantz, 1982). Thus, amnesic patients are impaired on tests of free recall, recognition, and sometimes cued recall because these tests asked subjects explicitly to recollect material that had previously been presented. The difference between cued recall tests and tests of free recall and recognition is that performance on cued recall tests does not necessarily require subjects to make a familiarity judgement in order to perform well. Subjects may treat the cued recall test as a guessing game and simply say the first word that comes to mind. In such cases, amnesic patients could have performed well if automatic activation of preexisting memory was sufficient to make their performance indistinguishable from that of control subjects. Thus, in order to observe preserved learning in amnesia, it may be necessary to test memory implicitly and dissuade subjects from consciously recollecting previously presented material. When a test assesses memory in an implicit manner by demonstrating that performance is biased by previously presented material, then that test can be construed as a test ofpriming. By this definition, the cued recall test is not a priming test when subjects are told explicitly to use cues as aids to facilitate memory. However, the cued recall test becomes a priming test if subjects are not told to use the cues as aids to memory but simply told to say the first word that comes to mind. The first study that manipulated explicit and implicit testing instructions in amnesic patients was conducted by Gardner, Boller, Moreines and Butters (1973). They presented words with category cues (e.g., The first word is a tree-it is auk") and later asked subjects to use category cues as aids to facilitate memory (cued recall instructions) or simply asked subjects to say the first six exemplars that came to mind when given a category name (implicit memory instructions). Patients with Korsakoff s syndrome were impaired when explicit (cued recall) test instructions were given, but they produced as many previously presented words as control subjects when asked to say the first exemplars that came to mind. Graf, Squire and Mandler (1984) used both implicit and explicit memory instructions in a word completion task. They presented words incidentally by asking subjects to rate words according to how much they liked each one (semantic task) or by asking subjects to determine whether the vowels in a word were the same ones used in the preceding word (nonsemantic task). As words were presented incidentally, subjects did not expect a memory test. Following word presentation, subjects were given three-letter word stems of previously presented words and were told either (1) to use the stems as cues to facilitate memory for previously presented words (cued recall instructions), or (2) to complete EP(A1 38:4-G 97

6 624 A. P. Shimamura the word stems with the first word that came to mind (word completion instructions). As in the Gardner et al. (1973) study, amnesic patients (patients with Korsakoff s syndrome or anoxic encephalopathy) exhibited impaired performance when they were given explicit instructions to remember, but they exhibited normal performance when given word completion instructions. Specifically, amnesic patients exhibited equivalent levels of performance under both cued recall and word completion instruction conditions, whereas control subjects exhibited better performance under cued recall instructions. In addition, the priming effect was not greatly influenced by the type of study task (semantic vs. nonsemantic), though recognition and recall were greatly affected by the study task manipulation (see also Graf, Mandler and Haden, 1982). Finally, the priming effect was transient: it was intermediate after a 10- min delay and disappeared in both amnesic patients and control subjects after a 2-hr delay. Other demonstrations of preserved priming were made by Jacoby and Witherspoon (1 982) and Johnson, Kim and Risse (1 985). Jacoby and Witherspoon (1982) asked patients with Korsakoff s syndrome and normal subjects questions such as, name a musical instrument that employs a reed. Subjects were then asked to spell homophonic words such as reedlread. Korsakoff patients and normal subjects exhibited a similar spelling bias toward the spelling of previously presented words. Amnesic patients) however, were impaired on a recognition test that involved the same words. Johnson et al. (1985) studied preference biases in amnesic patients. They used a paradigm similar to one described by Zajonc (1980), in which preferences for tones could be established by repeated exposures. Johnson et al. (1 985) presented several melodies from Korean songs and asked subjects to rate the melodies as to whether they sounded American or Chinese. Some melodies were repeated up to 10 times in the study phase. Five minutes after presentation, subjects listened to previously presented melodies intermixed with new melodies and were asked to rate how much they liked each melody. Johnson et al. (1 985) demonstrated that patients with Korsakoff s syndrome and control subjects exhibited a similar preference bias for repeated melodies. The amnesic patients, however, were impaired on a recognition memory for the melodies. Thus, amnesic patients exhibit normal priming effects as measured by word completion, spelling, and preference tasks (see Table I). Two important similarities can be found in the testing procedures. First, subjects did not expect a memory test because target words were presented incidentally. Second, rather than asking subjects to recollect study material explicitly, testing was measured as a change in performance. That is, subjects were simply asked to spell words, make 98

7 Priming Effects in Amnesia 625 preference judgments, or complete three-letter word stems with the first word that came to mind. This preserved capacity to prime previously presented material has now been demonstrated in a variety of patients with memory disorders-including patients who developed amnesia due to Korsakoff s syndrome (Gardner et al., 1973; Graf et al., 1984; Jacoby and Witherspoon, 1982; Shimamura and Squire, 1984), electroconvulsive therapy (Squire, Shimamura and Graf, 1985), anoxic or ischaemic episodes (Graf et al., 1984; Graf, Shimamura and Squire, 1985), encephalitis (Warrington and Weiskrantz, 1978) and medial temporal lesions (Nissen, Cohen and Corkin, 1981). Defining the Boundary of Preserved Priming Effects in Amnesia The first critical boundary condition for observing entirely normal priming performance in amnesia is the requirement that memory be tested implicitly, as just described. When amnesic patients were instructed explicitly to recollect previously presented material, they exhibited impaired performance; but when amnesic patients were asked simply to respond with the first word that came to mind, they exhibited normal performance (Gardner et al., 1973; Graf et al. 1984; Shimamura and Squire, 1984). Another feature of priming is that the effects appear to be relatively short-lived in amnesic patients. At immediate testing, both amnesic patients and control subjects completed previously presented words at about two to three times the level of baseline guessing; but when testing was delayed by two hours, completion performance was indistinguishable from baseline levels for all subjects (Graf et al., 1984; Shimamura and Squire, 1984; Squire, Shimamura and Graf, in press). These findings were obtained initially in word completion tests in which the cues consisted of word stems that could be completed with several possible words (e.g., mot for motel, motor, mother, moth), only one of which was presented for study. The finding that priming is a relatively transient phenomenon contrasts with the finding that completion performance can be longlasting in normal subjects (Tulving, Schachter and Stark, 1982). The study of Tulving et al. (1982) differed from the priming studies discussed above in two important ways: (1) explicit (cued recall) instructions were used; and (2) test cues uniquely specified target words (e.g., a - a - in for assassin). Squire et al. (in press, Experiment 3) used the same word cues as Tulving et al. (1982) and assessed word completion performance in amnesic patients and control subjects after delays of 0, 2 hours and 4 days. They replicated the 99

8 626 A. P. Shimamura finding of Tulving et al. (1982) by showing that control subjects exhibit good completion performance after a 4-day retention interval. Amnesic patients, however, exhibited poorer completion performance at immediate testing as compared with control subjects, and their performance fell to baseline levels after a 2-hr delay. Moreover, unlike studies in which word stems could be completed with many possible responses (e.g., Graf et al., 1982), this study found that word completion performance by control subjects was greatly influenced by the learning condition (semantic vs. nonsemantic task). By contrast, amnesic patients were not influenced by the learning condition, and they exhibited poorer completion performance. Thus, elaborative encoding may be used by subjects in cases where completion is tested with word stems that uniquely specify study words. Only one study has reported entirely normal cued recall performance in amnesic patients after a 24-hr delay (Warrington and Weiskrantz, 1978). As in the Tulving et al. (1982) and Squire et al. (in press) studies, Warrington and Weiskrantz (1978) used word cues that could be completed with only one common word (e.g., unk for ankle). However, the learning procedure used by Warrington and Weiskrantz (1 978) was quite different. Subjects first attempted to complete 200 word stems without prior word presentation. The first 20 words that could not be completed on this initial screening phase were then used as study words. Subjects were shown study words on a sheet of paper and were asked to copy the list and read each word aloud. On the following day, amnesic patients and control subjects were given cues for the 20 study words and were asked to use the cue to facilitate memory for the previously presented words (i.e., cued recall memory instructions). Amnesic patients completed 79% of the study words, and control subjects completed 63% of the words. This finding of above-normal cued recall performance after a 24-hr retention is suspect because amnesic patients were much better than control subjects at completing word stems, even before word presentation. During the initial screening phase, amnesic patients completed more words (81% correct) than control subjects (63% correct). Thus, it is not clear to what extent the retention scores reflected baseline completion ability instead of memory for the words having been presented. To compare the retention scores between groups appropriately, word completion performance should also have been assessed for stems that could not be completed on the initial screening test and that were not presented for study. Unfortunately, this baseline measure was not obtained. Squire et al. (in press, Experiment 2) used cues similar to those used by Warrington and Weiskrantz (1978) and adjusted completion performance for differences in baseline rates. In that study, 100

9 Priming Effects in Amnesia 627 completion performance by amnesic patients was at baseline levels after a 2-hr and 4-day retention interval. Thus, priming effects in amnesic patients appear to be relatively short-lasting. Furthermore, the use of implicit tests of memory is not always a sufficient condition for producing preserved learning. Even in a task that is intended to measure priming (e.g., completion of word fragments to form words uniquely specified by the fragments), amnesic patients were impaired when testing occurred after long delays (Squire et al., in press). The long-lasting effects exhibited by normal subjects may be attributed to explicit memory. Note that when a cue can be completed with several possible responses (e.g., mot for motel, moth, mother), subjects may say the first word that comes to mind, whether or not the word was previously presented. In that situation, both amnesic patients and control subjects exhibited short-lasting word completion effects. When cues uniquely specify study words (e.g., jui for juice; a - a - in for assassin), subjects either say the appropriate word or fail to make a response during the alotted time. In this situation, rather than failing to make a response because the appropriate word was not available via activation, normal subjects may retrieve the word from explicit memory. This explanation accounts for the fact that when completion was based on cues that uniquely specified study words, control subjects exhibited initially larger and longer-lasting completion effects than amnesic patients. Further studies are needed to describe more fully the time course of priming effects. Although previous methods have shown that priming effects are relatively short-lasting, it may still be possible that with other stimuli or with other procedures longer-lasting effects could be found. For example, priming may last longer if activation is strengthened by many stimulus repetitions. Or it may be that certain study techniques (e.g., extensive elaborative encoding; mnemonic techniques) could extend the time course of priming effects in amnesia. A third feature of preserved priming effects is that priming extends beyond the sensory modality within which information is presented. Graf et al. (1985) presented words either verbally or visually, and word completion was tested by presenting three-letter word stems (visually) and asking subjects to write the first word that came to mind for each cue. Both amnesic patients and control subjects exhibited priming effects when testing occurred within modality and when testing occurred across modality. Averaged across subject groups, within-modality priming effects (44% words completed) were significantly larger than across-modality effects (32% words completed), but in both cases performance by amnesic patients was indistinguishable from that of control subjects. Nevertheless, amnesic patients were impaired on tests 101

10 628 A. P. Shimamura of free recall. These findings argue against the view that priming effects activate exclusively sensory-specific representations (Jacoby, 1983). Amnesia spares the processes that mediate priming across sensory modalities, as well as the specific sensory and perceptual processes that mediate priming within a modality. Not only can priming effects be found across sensory modalities, they can also operate across semantic representations. Shimamura and Squire (1984) presented word pairs, such as table-chair, in an incidental learning task. After presentation, subjects were shown the first word of each pair and were asked to say the first word that came to mind. That is, subjects were simply asked to free-associate to cue words. Both amnesic patients and control subjects exhibited priming effects that were about two to three times above baseline levels (70% correct vs. 25% baseline). In a similar experiment, Schacter (1985) showed that amnesic patients exhibit preserved priming for idiomatic phrases, such as sour-grapes, when asked to make free association responses to the first word in each pair. This priming effect was not found for nonunitized phrases (e.g., small-grapes). These studies show that after word pair presentation preexisting or unitized semantic associates can be activated. Priming also occurs even when the test cues are never presented during study. Shimamura and Squire (1984) presented single words (e.g., baby) in an incidental learning task and asked subjects to free associate to cues that were related to the study words (e.g., child). Both amnesic patients and control subjects exhibited priming effects that were about twice the level of baseline guessing rates (47% correct vs. 23% baseline). This semantic priming effect (sometimes called related or indirect priming) disappeared in both groups when testing was delayed by two hours. Similarly, Graf et al. (1985) presented related words (e.g., uncle, sister, aunt) intermixed with other words and later asked subjects to produce the first eight exemplars that came to mind in response to category names (e.g., relatives). Amnesic patients exhibited normal priming by category cues, even though the categories were never specified during study (17% correct vs. 5% baseline). Thus, priming is not restricted to activation of sensory or perceptual representations; priming can activate semantic representations as well. However, priming may be restricted to activation of preexisting or unitized representations. Diamond and Rozin (1 984) found that amnesic patients (Korsakoff patients and elderly senile patients) could explicitly recall about 5 of 6 words when cued wtih three-letter stems, but they averaged less than 1 correct recall of 6 presented nonwords when cued by three-letter stems (e.g., num for numdy). Control subjects maintained their high level of cued recall performance even for nonwords. A similar finding was obtained by Cermak, Talbot, Chandler and 102

11 Priming Effects in Amnesia 629 Wolbarst (1985), who studied patients with Korsakoffs syndrome in a perceptual identification task. Words and nonwords were presented for study and were later tested by presenting them again, first briefly (35 msec) and then at longer exposure durations, until subjects could name the word or nonword. Patients with Korsakoff s syndrome identified previously presented words at significantly shorter exposure durations than nonpresented words (53 msec vs. 63 msec), and the magnitude of this difference was comparable to that of control subjects (39 msec vs. 45 msec). However, patients with Korsakoff s syndrome did not perform as well as control subjects when perceptual identification was assessed for nonwords. Korsakoff patients required 140 msec of exposure time to identify previously presented nonwords (158 msec for nonpresented nonwords), whereas control subjects required only 69 msec of exposure time to identify previously presented nonwords (1 24 msec for nonpresented nonwords). Apparently, amnesic patients did not exhibit priming of nonwords because nonwords had no prior semantic representation in memory. Thus, although amnesic patients can prime words and preexisting semantic associates, they cannot prime recently presented nonwords. One possibility is that priming of semantic associates may occur only for items that are already highly associated to presented items. Cutting (1978) showed that amnesic patients exhibited good paired-associate learning only for the highest word associates. However, there is evidence to suggest that amnesic patients can exhibit priming of more complex representations. As mentioned previously, Johnson et al. (1985) demonstrated that amnesic patients preferred recently presented (but previously unfamiliar) Korean melodies over totally new Korean melodies. This finding suggests that a repeated melody formed a unitized representation (at least temporarily) and that priming of this representation was the basis for performance in the preference task. In another study, Moscovitch (1984) showed that amnesic patients exhibited faster reading rates for previously read sentences than for new sentences. One possiblity is that that priming of such complex representations or unitizations depends on preexisting knowledge about melodies and sentence structure. If this interpretation is correct, then it should not be possible to demonstrate priming for random sequences of tones or words. The boundary conditions of preserved priming effects can be summarized as follows: 1. Priming effects depend on implicit testing of information, though implicit testing is not sufficient for producing preserved priming effects. 103

12 630 A. P. Shimamura Priming effects, at least as measured so far, are relatively transient, lasting on the order of minutes and hours rather than days. Priming effects can be found for both within-modality and acrossmodality conditions, though within-modality effects are larger. Priming is not restricted to repetition or direct priming conditions. Amnesic patients exhibit normal priming even when cues are related semantically to previously presented material-i.e., the cues were never themselves presented during study. Priming reflects activation of preexisting or unitized representations. Relationships Between Priming and Other Phenomena What is the relationship between priming and explicit memory tests (e.g., recall and recognition tests)? Some theorists have argued that priming operates independently and does not affect conscious or explicit remembering (Tulving et al., 1982). Others have suggested that priming facilitates or contributes to explicit remembering (Jacoby, 1983; Mandler, 1980). Studies of normal subjects have attempted to identify behavioural dissociations between measures of priming and measures of explicit memory. One strategy is to demonstrate that certain independent variables affect one measure but not another. Yet, problems can arise because behavioural measures may not tap one memory process exclusively. For instance, explicit or conscious memory may artifactually influence putative measures of priming. Another strategy is to demonstrate stochastic independence between measures (e.g., Tulving et al., 1982), though methodological problems can also occur with this approach (see Shimamura, 1985). Neuropsychological evidence could help to corroborate the view that priming and explicit memory operate independently from one another, because amnesic patients typically fail to recall information after even a short delay, and thus their performance is less likely to be confounded by explicit remembering. One way to assess the independence between priming and explicit memory is to demonstrate that amnesic patients exhibit preserved priming at a time when performance on sensitive explicit memory tests is at chance levels. Squire et al. (1985) addressed this issue in a test of patients who were prescribed bilateral ECT for relief of depressive illness. Pilot tests showed that bilateral ECT patients exhibit near-chance levels on recognition tests when testing is conducted within the first hour after treatment. Squire et al. (1985) gave tests of three-alternative forced-choice recognition memory at four different times (45 min, 65 min, 85 min, 9 hr) after treatment. In addition, tests of 104

13 Priming Effects in Amnesia 63 1 word completion were given on another treatment day, at 45 min, 65 min and 85min after treatment. For each study/test trial, ten words were presented at the scheduled times after treatment, and retention was always tested 15 min later. When word presentation occurred at 45 min after treatment, ECT patients performed at or near chance levels (average score=3.8 words recognized out of 10 words; chance = 3.3 words). In fact, 7 of 13 ECT patients scored below the level of chance performance on the test. Yet word completion performance was the same as that of control subjects when testing occurred at this same time after treatment (amnesic patients = 26% correct; control subjects = 25% correct). In addition, during the hours after treatment, recognition memory performance improved markedly, to 7.5 words correct, yet word completion performance was stable. These findings demonstrated that priming can be fully intact at a time when recognition memory was near or at chance levels. Apparently, in amnesic patients priming does not contribute to recognition memory performance in any significant way. These findings, however, do not rule out the possiblity that priming facilitates explicit remembering in normal subjects (e.g., Johnston, Dark and Jacoby, 1985). For example, the brain areas damaged in amnesia may permit information that comes to mind via priming to be recognized as familiar and otherwise used in conscious remembering. Morever, the findings do not rule out the possibility that conscious remembering itself depends on priming. That is, activation of memory representations may be necessary for explicit memory, and thus an impairment in priming should always be accompanied by an impairment in explicit memory. One frequent observation is that amnesic patients are good at learning related paired-associates (Cutting, 1978; Warrington and Weiskrantz, 1982; Wechsler, 1917; Winocur and Weiskrantz, 1976). Shimamura and Squire (1984) tested the hypothesis that good paired-associate learning of related word pairs is related to semantic priming effects. They found that at immediate testing, patients with Korsakoff s syndrome exhibited good, but not quite normal, memory for highly related word pairs (patients = 70% correct; controls = 94% correct). Like priming effects, the paired-associate memory exhibited by the patients decayed and was not different from baseline guessing rates after a two-hour delay. Control subjects maintained their good performance after a two-hour delay. Moreover, the small but reliable difference between amnesic patients and control subjects on immediate tests of paired-associate memory was attributed to the fact that these tests required explicit memory instructions. When paired-associate memory was tested using implicit, free-association instructions, amnesic patients and control subjects exhibited the same level of performance-70% and 69% 105

14 632 A. P. Shimamura Table I Examples of Preserved Learning in Amnesia Task Study 1. Fragmented Picture Completion Warrington & Weiskrantz (1968) 2. Word Completion 3. Lexical Decision 4. Perceptual Identification 5. Spelling of Homophones 6. Preference Judgments 7. Free Association of Related Information Warrington & Weiskrantz (1968) Warrington & Weiskrantz (1970a) Warrington & Weiskrantz (1978) Diamond & Rozin (1984) Graf et al. (1984) Graf et al. (1985) Shimamura & Squire (1984) Squire et al. (1985; in press) Shimamura et al. (submitted) Moscovitch (1982) Glass & Butters (1985) Nissen et al. (1981) Cermak et al. (1985) Jacoby & Witherspoon (1982) Johnson et al. (1985) Gardner et al. (1973) Shimamura & Squire (1984) Graf et al. (1985) Schacter (1985) Mayes et al. (in press) 8. Word Comptetion with New Associates Graf & Schacter (1985) correct, respectively (Shimamura and Squire, 1984). Thus, the good memory for related paired associates exhibited by amnesic patients appears to be a function of preserved priming ability. Mayes, Pickering and Fairbairn (in press) further investigated priming effects and paired-associate learning. They discovered a relationship between priming effects and the higher susceptibility to proactive interference exhibited by amnesic patients. In an A-B, A-C pairedassociate learning paradigm (e.g., soldier-rifle; soldier-army), amnesic patients tend to produce more prior list intrusions when testing for A-C pairs than do normal subjects (Cermak and Butters, 1972; Warrington and Weiskrantz, 1974; 1978; Winocur and Weiskrantz, 1976). Mayes et al. (in press) investigated this phenomenon in a priming paradigm. During the presentation phase, subjects were shown 12 word pairs and were asked to rate each word pair according to the strength of the association between the two words. Subjects first rated 12 A-B pairs and then 12 A-C pairs. Following a 2-min delay, subjects were shown the 106

15 Priming Effects in Amnesia 633 first word in each pair and asked to make free association responses. In this priming paradigm, control subjects made about as many first-list intrusions (3.6 intrusions) as amnesic patients (4.3 intrusions). In fact, amnesic patients produced about as many intrusions in this task as in separate tests of paired-associate memory done with explicit instructions. Moreover, when presentation of the second (A-C) list was delayed by 2 hr-a time after learning when activation of A-B pairs should have decayed-paired-associate (i.e., explicit) memory for A-C word pairs in amnesic patients was as good as it was when no prior list had been presented. Thus, proactive interference effects followed the same time course as priming effects. Apparently, the greater susceptibility to proactive interference in paired-associate learning tasks by amnesic patients can be attributed to activation of first-list word pairs. Even in explicit tests of memory, amnesic patients based their responses on activation, whereas control subjects had the capacity to recollect other cues consciously such as spatial-temporal context information that could have facilitated memory for A-C pairs. It is worth considering one other major test procedure-the lexical decision task-that has been commonly used to study priming in normal subjects (see Meyer and Schvaneveldt, 1976; Scarborough, Cortese and Scarborough, 1977). One difference between this task and the others discussed here is the use of reaction time as a dependent variable. Moscovitch (1982) demonstrated a repetition priming effect in two amnesic patients in a lexical decision task, though baseline reaction times were slower for amnesic patients than for control subjects. Glass and Butters (1985) found a priming effect in patients with Korsakoffs syndrome, using a lexical decision task based on procedures described by Neely (1977). Subjects were told to expect a word corresponding to a body part (e.g., arm) on trials chat were preceded by three x s (e.g., xxx ), and on 75% of these trials such a word actually appeared. Like control subjects, amnesic patients made faster lexical decisions on trials when they were shown an expected word as compared to trials when they were shown an unexpected word. However, when the three x s were replaced with an unrelated word (e.g. when the word furniture precedes a stimulus, expect a body part ), patients with Korsakoff s syndrome were neither facilitated nor inhibited by the priming word. Thus, findings from lexical decision tasks have shown that priming effects in amnesic patients can sometimes be reflected in response latencies. It should be mentioned, however, that findings from reaction time Faradigms, such as those borrowed from experimental psychology, must be conducted with care when testing neuropsychological popula- tions. Baseline response latencies are often slower in patients than in control subjects-sometimes by hundreds of milliseconds. Moreover, 107

16 634 A. P. Shimamura patients tend to make more errors than control subjects. These facts make interpretation of reaction time data difficult, because the level of baseline performance may affect the magnitude of a latency effect (e.g., a difference in reaction time between primed and unprimed trials). Moreover, differences in accuracy rates across subject groups or across test conditions can also make interpretations difficult. The best control for these artifacts is to match patients and control subjects on baseline response latency (e.g., simple reaction time) and accuracy. Priming Effects and Theories of Memory Evidence of preserved priming effects in amnesia has led to a growing consensus that preexisting or unitized memory representations can be automatically activated. Amnesic patients, however, cannot explicitly or consciously recollect information learned since the onset of amnesia. Some interpretations have made use of the term, conscious recollection, to describe the process that is impaired in amnesia (Baddeley, 1982; Moscovitch, 1982; Squire, 1986). The conscious vs. automatic distinction shares features of the reflective vs. sensory/perceptual process distinction of Johnson (1983) and the elaboration vs. integration distinction of Mandler (1979). These views of memory differ in some ways, but they all share the idea that preserved learning in amnesia is found only when memory is tested implicitly-that is, without conscious knowledge that memory is being tested. One often cited dichotomy that incorporates the conscious vs. automatic distinction is the view that amnesia impairs declarative memory and spares procedural memory (Cohen, 1984; Cohen and Squire, 1980; Squire, 1982, 1986). Declarative memory is available to conscious awareness and includes the facts and episodes of everyday experiences. Procedural memory is implicit and is available only by engaging the specific operations in which the memory is embedded. The ability to acquire new declarative memory is impaired in amnesia, and this ability depends on the integrity of the medial temporal and diencephalic regions. In particular, the circuitry of the hippocampus and its associated input and output connections are critical for the establishment of long-term, declarative memory (Squire, 1986). Procedural memory (e.g. skills and simple classical conditioning) is not dependent upon this circuitry and is considered to be a phylogenetically (and possibly ontogenetically) early memory system. Priming is seen as an example of procedural memory because it reflects facilitation of a cognitive operation or procedure (Crowder, 1985; Squire, 1986). The operations that can be facilitated include the tendency to activate both perceptual and 108

17 Priming Effects in Amnesia 635 semantic processes. Like skill learning, priming effects can be tested implicitly. The memory/habit distinction (Mishkin, Malamut and Bachevalier, 1984) and the vertical/horizontal distinction (Wickelgren, 1979) are similar views that also emphasize the importance of the medial temporal and diecephalic brain regions to one kind of memory functioning. Warrington and Weiskrantz (1982) suggested a related view. They proposed that amnesia is best characterized as a disconnection syndrome that severs communication between the temporal and frontal lobes. The temporal lobes are thought to subserve semantic memory functions, such as verbal knowledge and object recognition. The frontal lobes engage in cognitive mediation, which includes processes such as elaboration, imagery and organization. Amnesia occurs as a result of disconnecting the pathways between these areas. Priming is seen as a function of semantic memory that is not dependent on the cognitive mediational system. Priming effects reflect automatic activation of previously presented information, which can occur as a result of mere repetitive exposure of stimuli. The cognitive mediation system is required for explicit recall or recognition of information. This view of memory shares many features with the procedural/declarative and habit/memory distinctions. In particular, all of these views consider priming effects and skill learning to reflect modes of memory that are not affected by amnesia. There are two other views of memory that should be discussed. First, it has been suggested that preserved learning in amnesia reflects selective activation of sensory and perceptual processes (Jacoby, 1983; Jacoby and Witherspoon, 1982). That is, amnesic patients can exhibit normal perceptual enhancement as a result of stimulus presentation, and this perceptual jkency enables amnesic patients to perform well on priming tests. Although this view was supported by preserved performance on tests of repetition priming (e.g., Graf et al., 1984; Jacoby and Witherspoon, 1982), other findings suggest that it is too narrow. Amnesic patients exhibit preserved performance not only on tests of repetition priming, but also on tests of indirect or semantic priming (e.g., Graf et al., 1985; Shimamura and Squire, 1984). That is, the activation process that is spared in amnesia includes semantic processes, not just perceptual ones. For example, amnesic patients can be primed by presenting semantic associates of recently presented stimulus words, even when the associates were never presented during study. A second view has been that amnesia spares semantic memory but impairs episodic memory (Cermak et al., 1985; Kinsbourne and Wood, 1975, 1982; see also Tulving, 1983). Semantic memory includes facts and general knowledge. Episodic memory is autobiographical 109

18 636 A. P. Shimamura memory-i.e., memory associated with time and place information. By this view, preserved priming effects provide evidence in support of the semantic/episodic distinction, because priming reflects intact activation of semantic representations. One problem with taking priming effects as evidence for preserved semantic memory is that priming operates on both perceptual and semantic processes. The finding of greater priming effects for within- than across-modality conditions is difficult to interpret if priming is considered to be a function of only semantic memory. Another problem is that not all semantic memory functions are preserved in amnesia. Amnesic patients are impaired on tests of recently acquired semantic memory just as they are impaired on tests of episodic memory. For example, amnesic patients exhibit impaired memory for recently learned facts (Cermak and O Connor, 1983; Shimamura and Squire, in press) and for new vocabulary words (Gabrieli, Cohen and Corkin, 1983). Finally, priming effects may deserve a special classification, in addition to the classifications of memory described thus far. For instance, there may be characteristics of priming effects, as yet uncovered, that prevent them from being classified as either declarative or procedural. Priming could constitute a third category of memory phenomena. As research continues, other classification schemes may more adequately define priming effects. At the moment, however, there appears to be more consensus than disagreement among present views of memory on the issue of preserved priming effects in amnesia. The following section offers some perspectives for new directions in research on the phenomenon of priming. New Directions Recently, Graf and Schacter (1985) reported a priming phenomenon unlike any of the effects described thus far. They presented unrelated word pairs (e.g., window-reason) to subjects in an incidental learning task and then asked them to make word completion responses in the context of the same word that had been presented during study (e.g., window-rea) or in the context of a different word (e.g., mold-rea). Amnesic patients (e.g., patients with closed-head injury, encephalitis, or ruptured anterior communicating artery) exhibited facilitation in completion performance when the three-letter cue was associated with the word that had been presented during study. What makes this finding unique is that it demonstrated priming for newly associated information. Thaz is, the associative link between two unrelated words, such as 110

19 Priming Effects in Amnesia 637 Lwindow and reason, was primed after these two words were presented together during study. Previous studies had suggested that only highly associated information (e.g., highly related word pairs; linguistic idioms) could be successfully primed. Priming of newly associated information broadens the scope of preserved functions in amnesia and offers a new direction for further research. In fact, several findings suggest that priming of newly associated information represents a different type of priming. In a study of normal subjects, Schacter and Graf (1986) showed that this priming effect occurred only if the study task ensured elaborative encoding of the new associations. For example, priming of new assocations occurred if subjects were required during study to generate a sentence that used the two words together. No priming occurred if subjects made individual linking judgments for each word in a pair. The importance of elaborative encoding during study distinguishes this type of priming effect from the others mentioned above. Previous studies have shown that manipulations of elaborative encoding do not affect or only slightly affect word completion performance. Specifically, manipulations of orienting task (semantic vs. nonsemantic) often had no effect on word completion performance (Graf et al., 1982; Squire et al., in press). Other studies have shown a small but reliable effect of orienting task on word completion performance, even in amnesic patients (Graf et al., 1984). It is conceivable that increased elaborative encoding could facilitate priming performance, because it directs more attention to semantic features and thus enables more representations to be activated. However, these effects of elaborative encoding presumably differ from those found for priming of new associations. In order to obtain priming of new associations, it is necessary to establish explicit associations between words during study. Thus, unlike the priming effects cited earlier, priming of new associations depends on elaborative encoding. Another critical feature of this phenomenon is that not all amnesic patients exhibit this capacity to prime new associations. Upon reexamination of their data, Schacter and Graf (in press) found that of 12 amnesic patients studied, 7 patients considered to be moderately impaired exhibited normal priming of new associations, whereas 5 severely impaired patients did not exhibit any priming of new associations (the moderately impaired patients averaged 89.4 on the Wechsler Adult Intelligence Scale-Revised [WAIS-R] and 82.4 on the Wechsler Memory Scale [WMS], and the 5 severely impaired patients averaged 99.6 on the WAIS-R and 80.0 on the WMS). Presumably, performance 111

20 638 A. P. Shimamura on this priming test depends in part on the brain regions damaged in amnesia, neural systems that play a role in conscious or declarative memory. Thus, the priming of new associations can be distinguished in two ways from the priming of preexisting associations. First, priming of new associations requires elaborative encoding at the time of study. Second, it requires some part of the memory system that is impaired in amnesia. One possibility is that tests of new associations simply depend on declarative memory and that the memory capacity of moderately impaired patients is adequate for good performance on these tests. By this view, performance on these tests should always be correlated with performance on explicit memory tests. Another more interesting possibility is that the priming of new associations reflects a process that is truly intact-once elaborative encoding has been established at the time of study. That is, declarative memory is required to establish new associations, but once they are established, priming may proceed automatically and implicitly at the time of retrieval. Further studies are required to distinguish between these two possibilities. Studies of patients prescribed ECT may provide one way of distinguishing between these possibilities, because these patients could be asked to establish new associations prior to treatment-that is, prior to the onset of amnesia. If priming of new associations is intact once elaborative encoding has been established, then even ECT patients who are severely amnesic following treatment may exhibit intact priming of new associations. Unlike priming of new associations, priming of preexisting semantic associates (e.g., related words and idioms) and priming of single words are completely independent of the brain regions damaged in amnesia. Even the severely amnesic patient H. M., who sustained bilateral resection of the medial temporal lobes (Scoville and Milner, 1957), exhibited priming in a perceptual identification task (Nissen et al., 1981). Thus for H. M., priming did not depend on the integrity of the medial temporal region. Priming may depend on other cortical regions, as indicated in a recent study of a group of patients with the clinical diagnosis of early-stage Alzheimer s disease (Shimamura, Salmon, Squire and Butters, submitted). On tests of recall and recognition, these patients exhibited memory deficits comparable to patients with Korsakoff s syndrome. Yet their word completion performance was grossly impaired compared to the performance of Korsakoff patients or to agematched control subjects. Patients with dementia due to Huntington s disease exhibited impaired verbal memory, but their priming ability was intact. These findings suggest that Alzheimer s disease may disrupt activa- 112

21 Priming Effects in Amnesia 639 tion of cortical processes or representations. This interpretation is consistent with neuropathological evidence indicating involvement of neocortex in Alzheimer s disease (Pearson, Esiri, Hiorns, Wilcox and Powell, 1985). Also, impaired activation may account for poor performance on tests of word finding and semantic memory; these processes are critical features of the disease, particularly at later stages (see Martin and Fedio, 1983; Warrington, 1974; Weingartner, Grafman, Boutelle, Kaye and Martin, 1983). Further studies of priming in patients with more focal cortical damage (e.g., patients with aphasia or anomia) may help define the cortical areas that contribute to priming. There is still much to be learned about the phenomenon of priming in amnesic patients. Can priming be made to last longer in amnesic patients? What is the relationship between priming effects and shortterm memory? What is the relationship between the priming tasks described here and others that have been used in cognitive studies of normal subjects (e.g., Feustel, Shiffrin and Salasoo, 1983; Loftus, 1973; McKoon and Ratcliff, 1979; Meyer and Schvaneveldt, 1976; Warren and Morton, 1982)? What is the relationship between priming effects and skill learning? Progress in a scientific area is not only related to the number of facts that have been accumulated, but it is also related to the number of new questions and new directions that can be generated. In terms of the phenomenon of spared priming effects in amnesia, much has been learned, but there are still many questions to be answered. REFERENCES Baddeley, A. D. (1982). Domains of recollection. Psychological Review, 89, Baddeley, A. D. and Warrington, E. K. (1970). Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, Broadbent, D. E. and Weiskrantz, L. (Eds.) (1982). The neuropsychology of cognitive function. London: The Royal Society. Brooks, D. N. and Baddeley, A. D. (1976). What can amnesic patients learn? Neuropsychologia, 14, Butters, N. and Cermak, L. S. (1980). Alcoholic Korsakofs syndrome: An information processing approach. New York: Academic Press. Cermak, L. S. and Butters, N. (1972). The role of interference and encoding in the short-term memory deficits of Korsakoff patients. Neuropsychologia, 10, Cermak, L. S. and O Connor, M. (1983). The retrieval capacity of a patient with amnesia due to encephalitis. Neuropsychologia, 21, Cermak, L. S., Talbot, N., Chandler, K. and Wolbarst, L. R. (1985). The perceptual priming phenomenon in amnesia. Neuropsychologia, 23,

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