John F. Kihlstrom
University of California, Berkeley
One of the persisting puzzles in cognitive neuropsychology is that amnesic patients can recognize items that they cannot recall. Early findings in this regard by Huppert and Piercy (Huppert & Piercy, 1976; Huppert & Piercy, 1977; Piercy & Huppert, 1972) went generally unremarked until they were confirmed by Hirst, Johnson, and their colleagues almost a decade later (Hirst et al., 1986; Hirst, Johnson, Phelps, & Volpe, 1988; Hirst, 1989). Hirst's reports garnered somewhat more attention, including a vigorous denial by Squire and his associates (Haist, Shimamura, & Squire, 1992; Shimamura & Squire, 1988b; Squire & Shimamura, 1986). More recently, the superiority of recognition to recall was confirmed by Aggleton and Shaw (Aggleton & Brown, 1999; Aggleton & Shaw, 1996), at least for some kinds of amnesic patients, so it seems to be something that we have to take seriously.
What makes the relative sparing of recognition puzzling is that under many theories of amnesia it should not occur.
|If amnesia entails a dissociation between episodic and semantic memory (Schacter & Tulving, 1982), the problem is that recall and recognition are both episodic memory tasks.|
|If amnesia entails a dissociation between declarative and procedural (or nondeclarative) memory (Cohen & Squire, 1980; Squire & Knowlton, 1995), the problem is that both recall and recognition involve declarative memory.|
|If amnesia entails a dissociation between explicit and implicit memory (Schacter, 1987; Schacter & Tulving, 1994; Schacter, Wagner, & Buckner, 2000; Tulving & Schacter, 1990), both recall and recognition are expressions of explicit memory.|
No matter how you cut the memory pie, recall and recognition should both be severely impaired in amnesic patients. The possibility that amnesic patients can recognize items that they cannot recall has been especially challenging for those multiple-systems theories of memory which, based on a strong view of modularity, claim that all explicit expressions of episodic (or declarative) memory are mediated by the same brain system, which differs from the brain system(s) responsible for implicit, semantic, and procedural memory.
Perhaps for this reason, the claim that recognition is relatively superior to recall in amnesia has not gone unchallenged. For example, some investigators have suggested that the patients in the Hirst et al. (Hirst et al., 1986) study may not have been severely amnesic (Squire & Shimamura, 1986), but the fact is that both their Korsakoff's syndrome patients and their nonalcoholic patients were severely amnesic by any standard.
However, the comparison of recall and recognition may not be that simple. Amnesic patients recognize more than they can recall, but so of course do neurologically intact individuals who are not amnesic. Squire and Shimamura (Squire & Shimamura, 1986) argued that the proper question is not whether amnesics can recognize items that they cannot recall, but rather whether the relationship between recall and recognition is any different in amnesics than it is in normals -- that is, whether "recognition memory is disproportionately spared in amnesia" (p. 874, emphasis added). In fact, two studies by Shimamura and Squire argued that recognition was in fact no less impaired than free recall (Squire & Shimamura, 1986) or cued recall (Shimamura & Squire, 1988a). When recognition by amnesics and controls was equated by increasing the retention interval for controls, amnesic recall was found to be impaired compared to that of controls, and amnesics' performance on the recognition tests paralleled their performance on the recall tests. Similar findings were obtained in a later study, which concluded that "The striking similarity of recall [and] recognition… in both amnesic patients and normal subjects during the course of forgetting suggests that these measures of memory function are equivalently affected in amnesia (Haist et al., 1992, p. 699). Recognition memory is "closely linked" (p. 691) to recall, because recall and recognition are both products of a single brain system supporting explicit (or, in Squire's terms, declarative) memory.
Hirst et al. (1986) had actually anticipated this proposal in their study, which sought to simulate amnesia among neurologically intact subjects by increasing the rate of presentation during the study phase to a point (a mere half a second per item) where the items are poorly encoded; similarly, by slowing the rate of presentation (to an excruciating 8 seconds per item), they hoped to maximize the likelihood that, despite their poor encoding abilities, amnesic patients would nevertheless be able to remember something of their experience. When the patients were given 8 seconds to encode each item and the controls only half a second, recognition performance was essentially equated between both groups of amnesics and their respective controls. Working backward, Hirst et al. found that, with levels of recognition equated, recall was even more impaired among the amnesic patients than it was in the nonamnesics. Put another way: compared to recall, recognition is relatively spared in amnesia. A recent study by Sullivan Giovannello found that recall was disproportionately impaired when amnesic and control recognition was equated by giving amnesics more study time, as in the first Hirst study, but not by giving controls longer retention intervals, as in the Squire studies (Sullivan Giovanello & Verfaellie, 2001). This obviously complicates matters, but there is a way out of the complication (see below).
Setting the issue of proportionality aside, temporarily, it's possible that the apparent superiority of recognition to recall may be illusory in another way, because subjects can appear to recognize old, target items simply by saying "yes" to every item that is presented to them, whether target or lure. In this case, of course, they would also show an equal number of false alarms -- "recognizing" items that had not, in fact, been presented during the study phase. Of course, this possibility can be addressed through analyses of recognition performance that are informed by signal-detection theory -- as in a study by Snodgrass and Corwin (1988), who analyzed recognition data collected by Butters and his colleagues (Butters, Wolfe, Martone, Granholm, & Cermak, 1985). Compared to controls, amnesic patients had both fewer hits and more false alarms -- not a pattern that could occur if they were saying "yes" to everything. While their recognition performance was indeed worse than that of the controls, the amnesics nevertheless proved to make valid, if imperfect, discriminations between old and new items, resulting in levels of d' that were substantially above zero. Moreover, if anything, the amnesics turned out to be somewhat conservative in their decision-making processes.
Assuming then that recognition is relatively spared in amnesia, compared to recall, after all, how do amnesic patients accomplish it? One possible mechanism was suggested by Mandler's two-process theory of recognition (Mandler, 1980; Mandler, Graf, & Kraft, 1986), which holds that recognition is a judgment of prior occurrence that can be based on two quite different processes: retrieval and familiarity. While retrieval reflects the conscious recollection of a previous event in all its episodic glory, familiarity is related to priming-based experiences of perceptual and conceptual salience and fluency. Because priming is spared in amnesia, along with other facets of implicit memory, Mandler's theory suggests that some degree of recognition should be preserved as well, provided that the amnesics are encouraged to capitalize on the phenomenal salience which is part and parcel of what priming is all about.
The contribution of priming to recognition is directly illustrated by an experiment conducted by Jennifer Dorfman and her colleagues, on the retrograde amnesia associated with electroconvulsive therapy (Dorfman, Kihlstrom, Cork, & Misiaszek, 1995). A group of patients receiving ECT for depression studied a wordlist immediately before one of their treatments. Once they regained consciousness in the recovery room, they were presented with three-letter stems of list items and matched controls. For the explicit test, they were asked to recall an item from the previously studied wordlist that began with the stem. For the implicit test, they were asked simply to report the first word that came to mind that began with that stem. As expected, the patients showed a dissociation between explicit and implicit memory: a profound deficit on stem-cued recall (compared to controls who did not receive ECT), but strong priming on a test of stem completion. Dorfman's finding extended to the retrograde component of ECT-induced amnesia the dissociation between explicit and implicit memory found in the anterograde component in an earlier study by Squire and his colleagues (Squire, Shimamura, & Graf, 1985).
In the next phase of Dorfman's experiment the patients received a test of recognition: for half the items, they were instructed to adopt a very conservative criterion, saying yes only if they were fairly sure that the item was on the study list; for the other half, they were encouraged to adopt a more liberal criterion, saying yes if the item rang a bell, even if they were uncertain. When the subjects shifted criterion, hits went up but false alarms stayed constant, resulting in a fourfold increase in d', from 0.41 to 1.70. This genuine improvement in recognition memory occurred, Dorfman et al. concluded, because the subjects were encouraged to capitalize on the experience of perceptual and conceptual fluency that is the phenomenal accompaniment to priming. The notion that amnesic patients can strategically capitalize on the experience of priming to aid their performance on a recognition test is in line with Mandler's two-process theory of recognition. Further, it appears to challenge the strong view that recognition (an expression of explicit memory) and priming (an expression of implicit memory) are independent of each other because they are mediated by separate and independent memory systems in the brain (Kihlstrom, 1998).
If priming can contribute to recognition performance, then the memory systems underlying explicit and implicit memory are not independent after all. Implicit memory may be independent of explicit memory, at least in the limited sense that implicit memory is spared even when explicit memory is grossly impaired. But if amnesic patients can make use of priming-based fluency to enhance their performance on recognition tasks, it would seem that explicit memory is not independent of implicit memory. It is no surprise, then, that Dorfman's experiment, and its implications, came under challenge from some proponents of the multiple-systems theory of implicit memory.
For example, Reber and Squire reported a series of three experiments on patients with the amnesic syndrome that sought to cast doubt on Dorfman et al.'s ECT findings and conclusions (Reber & Squire, 1999). They concluded that "the phenomenon reported by Dorfman et al. does not generalize well" and that "nondeclarative memory (priming) is independent of recognition memory and does not contribute to recognition memory scores" (p. 510). Despite the fact that Reber and Squire worded their conclusions rather strongly, their actual empirical findings on which their conclusions are based are anomalous at best. In the first place, their first two experiments did not replicate Dorfman et al.'s procedures -- particularly with regard to the order in which the priming and recognition tests were conducted, though there were other problems as well. If you don't replicate someone's procedures, you shouldn't be surprised if you don't replicate someone's results. Their third experiment did replicate her procedures, and also failed to find improved recognition in amnesics, but it failed to get priming as well. Because the two-process theory predicts that recognition will be spared only when priming is spared, the failure to observe priming in amnesic patients vitiates the failure to observe recognition in them.
In her study, Dorfman employed a specific test order so as to encourage a familiarity-based mode of response on the low-criterion recognition test and a retrieval-based mode of response on the high-criterion test. Specifically, the stem-completion test of implicit memory preceded the low-criterion recognition test, and the stem-cued-recall test of explicit memory preceded the high-criterion recognition. In contrast, Reber and Squire conducted both recognition tests first, before the priming test. In fact, the two tests were conducted in separate experiments conducted almost a year and a half apart (p. 505)! Reber and Squire's failure to replicate Dorfman's procedures makes it impossible to interpret their failure to replicate her results. Reber and Squire's third experiment did replicate Dorfman's procedures, but unaccountably failed to produce priming on the stem completion test. Because the hypothesis of recognition by familiarity assumes that priming will be at least relatively spared, the failure to observe priming in Reber and Squire's third experiment vitiates that experiment as a test of Dorfman et al.'s hypothesis.
The priming-recognition hypothesis is apparently contradicted by the amnesic patient, E.P., who shows intact levels of priming but only chance levels of recognition (Hamann & Squire, 1997). The case is interesting, because Squire has pointed out that most amnesic patients are not completely amnesic, and that residual explicit memory may be responsible for the apparent sparing of recognition. E.P. doesn't just have relatively impaired recognition, compared to controls. He doesn't have any recognition at all -- though he does have spared implicit memory. In a new study (which, remarkably, did not even cite the Dorfman et al. study in its reference list), Stark and Squire presented a series of five experiments suggesting that shifting criteria failed to improve E.P.'s recognition memory, and thus that priming makes no contribution to recognition performance (Stark & Squire, 2000).
However, like the earlier studies of Reber and Squire, this new evidence is ambiguous at best, partly because of problems with the instructions given to their subjects. It's not enough simply to ask subjects to make their recognition judgments quickly, or to loosen their standards for recognition. You've got to get them to change their criterion qualitatively from one set of considerations to another. If you don't encourage subjects to shift their criterion for recognition from recollection to familiarity, you can't expect their recognition performance to change. But there is another problem as well, which stems from the fact that E.P. knows he's amnesic. In their critique of the Dorfman et al. paper, Reber and Squire (1999) had suggested (p. 509) that our findings were due to the fact that "ECT patients are unaccustomed to their memory dysfunction" while "Amnesic patients are accustomed to their condition" (see below). Patients like E.P., for whom amnesia has become part of their identity, may simply not be motivated to capitalize on priming-based familiarity when making recognition judgments. So the fate recognition in amnesia isn't just a matter of brain modules and cognitive processes; there's a social-psychological dimension that is important as well.
· In their Experiment 1, speeded recognition judgments did not improve E.P.'s recognition performance (or that of other amnesic subjects). The rationale for this experiment was that priming is automatic, and automatic judgments should be made rapidly -- "off the top of the head", as it were. But this ignores Mandler's point that familiarity-based recognition is an inferential judgment -- a judgment that may require time for reflection. Priming is automatic, but making an inference about the past based on feelings of familiarity takes time, as our studies showed using the tripartite remember/know/feel distinction (Kihlstrom, Kim, & Dabady, 2002).
· In Experiment 2, the recognition test was modified so as to remove any reference to the study phase; instead, E.P. and other amnesic subjects were simply asked which of two words was "more familiar". Again, E.P.'s recognition remained at chance levels. While on the surface such an instruction would seem to enhance familiarity-based recognition, in fact it changes the task entirely. Rather than making judgments about prior occurrence during a study phase, as would be essential for an episodic memory test, the subjects are simply asked to make judgments about the subjective frequency of the word in spoken and written English -- a semantic memory task.
· Experiment 3 combined the speeded judgment of Experiment 1 with the generic familiarity judgment of Experiment 2. Again E.P.'s recognition performance failed to improve -- but as the old saying goes, two wrongs don't make a right. The fact that E.P. performed poorly on this test says nothing about whether priming can contribute to recognition judgments in episodic memory, under circumstances where amnesic patients are encouraged to rely on intuitive feelings of familiarity.
· In Experiment 4, a trial of stem-completion priming was immediately followed by a test of recognition memory for the targets and lures produced by the stem-completion test -- thus following the spirit of Dorfman's (1995) procedure in a way that Reber and Squire (Reber & Squire, 1999) had not. Again E.P. showed poor recognition despite intact priming -- but then again, contrary to Dorfman's procedures, he was not encouraged to make strategic use of the feeling of familiarity when making recognition judgments.
· Experiment 5A repeated the procedure of Experiment 4 with a yes/no recognition task as opposed to a forced-choice task. The results were the same, but again E.P. was not encouraged to strategically use the feeling of familiarity to make his recognition judgments. (Experiment 5B was concerned with controls, not amnesics.)
Based on the findings of their experiments, Stark and Squire concluded (p. 459) that "although recognition memory judgments may be made on the basis of familiarity, repetition priming is not the source of this feeling of familiarity". On the one hand, then, Stark and Squire seem to be conceding that Dorfman et al. (1995) were right all along, and that a feeling of familiarity can contribute to recognition performance, although they still seem to deny that this strategy is available to amnesic patients. On the other hand, they continue to insist on a strict separation between priming and recognition, reasserting that the feeling of familiarity has nothing to do with priming. All of which leads to the following question: If recognition can be mediated by familiarity, as Stark and Squire concede, and if the feeling of familiarity is unrelated to repetition priming, as they insist, where does the feeling of familiarity come from?
It's possible, we suppose, that amnesic recognition could reflect the operation of yet a third memory system in the brain, separate from the system that mediates aspects of explicit memory, like recall, but also separate from the system that mediates aspects of implicit memory, like priming. For example, there might be some kind of novelty detection system, similar to the mechanism that underlies the orienting reflex or the "oddball" response (Donchin & Coles, 1988; Knight & Scabini, 1998). If this system is also spared in amnesia, then amnesic patients could perform relatively well on recognition tasks by saying yes not to items that elicit a priming-based feeling of familiarity, but rather to items that fail to elicit a novelty response (Habib, McIntosh, Wheeler, & Tulving, 2002). Perhaps this is the case, but the suggestion raises the danger of postulating new memory systems to account for every task dissociation revealed by behavioral experiments. Considerations of parsimony make it seem reasonable to pursue the hypothesis that priming does make a contribution to amnesic recognition after all, by creating the feeling of familiarity.
By the same token, so long as we are in the business of considering additions to the number of memory systems, Aggleton and Shaw (1999) have proposed that the two forms of recognition, one based on recollection and the other based on familiarity, are themselves mediated by two separate brain modules. In their view, recognition-by-recollection is based on a system involving the hippocampus and anterior portions of the thalamus, while recognition-by-familiarity is mediated by a system involving the perirhinal cortex of the temporal lobe and the medial dorsal nucleus of the thalamus. Both of these systems, in turn, are part of an "extended hippocampal system" (p. 425) that mediates explicit or declarative memory. But if the perirhinal system remains intact, amnesic patients could capitalize directly on the feeling of familiarity to recognize events that they cannot recall. It's an open question whether we can see recognition in appropriately instructed amnesics who do not have this perirhinal system intact. Which brings us back to the question: Where does the feeling of familiarity come from?
Evidence supporting this proposition is provided by studies that examine recollective experience, or the phenomenal experience of remembering: Remembering involves the conscious recollection of some past event, as an explicit expression of episodic memory; by contrast, Knowing is the intuition that an event occurred in the past, as an implicit expression of episodic memory. Actually, as I have argued at length elsewhere, what Gardiner calls "knowing" should really be called "feeling", and "knowing" should be reserved for abstract knowledge of an event accessed from semantic memory, but I want to set that issue aside for now.
In a groundbreaking paper, Tulving (Tulving, 1985) distinguished between two quite different recollective experiences: remembering, or one's concrete awareness of oneself in the past (what Tulving characterized as autonoetic consciousness); and knowing, or one's abstract knowledge of the past (what Tulving called noetic consciousness). Whenever subjects endorsed an item as old on a recognition test, they were asked to indicate the nature of their recollective experience. If recognition of a particular item was accompanied by conscious recollection of the its occurrence on the study list, they were to rate the item as "remembered"; if not, they were to rate it as "known". In his study, Tulving found that not all recognition judgments were accompanied by conscious recollection of the study experience. For some endorsements, the subjects simply "knew" that the item had appeared on the list, much the way they knew that Ontario was a province of Canada (the study was conducted in Canada). More important, Tulving discovered that "remember" judgments were affected by level of processing, but "know" judgments were not. Similar findings were obtained by Gardiner (Gardiner, 1988).
Although Gardiner's development of what has come to be called the remember-know paradigm was inspired by Tulving's 1985 paper, his conception and Tulving's seem to differ in important ways. For Tulving, the remember-know distinction maps onto his earlier (1972) distinction between episodic memory, or the person's awareness that an event "is a veridical part of his own past existence" (1985, p. 3), and semantic memory, or the person's "symbolic knowledge of the world" (1985, p. 3). But for Gardiner, the remember-know distinction maps more closely onto Mandler's (1980) distinction between recognition by retrieval and recognition by familiarity. Recognition by retrieval involves remembering an event as an event, including the personal and spatiotemporal context in which the event occurred; by contrast, recognition by familiarity involves a feeling or intuition that some event occurred in the past, in the absence of conscious recollection of that event. An alternative framework for Gardiner's distinction, of course, is provided by the distinction between explicit and implicit memory, which was just emerging at the time (Schacter, 1987). Explicit memory involves the conscious recollection of an experience from the past, while implicit memory is a memory-based change in behavior that occurs independent of, and in the classic case in the absence of, conscious recollection. For Gardiner, then, remembering reflects explicit memory, while knowing reflects implicit memory.
These alternative interpretations of remembering and knowing are connected, from Mandler's point of view, because both recognition by familiarity and implicit memory are based on the activation by an event of previously stored knowledge. Nevertheless, as I have argued elsewhere, it may be a mistake to conflate semantic memory with implicit memory, and knowing with intuiting. Accordingly, I have suggested that there are at least three varieties of recollective experience -- or, if you will, three different memory qualia:
These memory qualia are familiar to anyone who has ever taken a multiple-choice test. Sometimes, we choose a response because we remember the circumstances under which we learned it -- the particular lecture, or, as sometimes happens, the location on the textbook page where the information appeared (Rothkopf, 1971). On other occasions, we choose a response because we just know the answer -- it's part of our knowledge about the world, and we don't remember the circumstances under which we learned it. On still other occasions, we choose a response because we feel that it is the right one. We don't actually know the answer, and we certainly don't remember where we learned it, but we choose a response because it strikes us intuitively as familiar, and we infer from this feeling of familiarity that, of all the choices available, this is the one that is most likely to be correct. We're guessing, in a way that we're not guessing when we're remembering or knowing, but it's not random guessing; it's guessing informed by the feeling of familiarity (Bowers, 1984) -- a feeling of familiarity that comes from priming.
There is now a considerable amount of experimental evidence that remembering, knowing, and feeling, at least, are distinct recollective experiences (Kihlstrom, Kim et al., 2002). In the first place, subjects can make the distinctions when they are asked to. Recollection by remembering and by knowing is affected by level of processing, while recollection by feeling is not. Recollection by feeling is also associated with longer response latencies, and lower confidence levels, than either of the other two modes. And repeated study trials increase the frequency of recollection by knowing, while decreasing the frequency of recollection by remembering or by feeling. However, the vast bulk of the literature on recollective experience employs only the dichotomous distinction between remembering and knowing. As it happens, however, in this literature "knowing" is usually defined in terms closer to Gardiner's construal than Tulving's. Because "remembering" is tantamount to Mandler's "retrieval" process, while "knowing" is tantamount to "familiarity", studies of memory in amnesia that use the remember-know paradigm can be interpreted as bearing on the role of priming-based feeling of familiarity in recognition. In an effort to make things clearer, in what follows I will use the phrase familiarity-based feeling of "knowing", to indicate that "knowing" is really a euphemism for the feeling of familiarity.
Setting that issue aside, there is now a considerable amount of experimental evidence that recognition by amnesics is mediated by a familiarity-based "feeling of knowing" rather than conscious recollection. For example, a pioneering study by Knowlton and Squire (Knowlton & Squire, 1995) found that both retrieval-based "remembering" and familiarity-based "knowing" were impaired in amnesic patients, compared to controls. However, the two-way interaction was also significant: for amnesics, recognition by remembering was more impaired than recognition by feeling-based knowing. This is exactly what we would expect if amnesic patients based their recognition judgments on priming-based feelings of familiarity.
Similarly, two studies of the associative memory illusion (Roediger & McDermott, 1995) by Schacter, Verfaellie, and their colleagues indicated that amnesics have severely impaired "remember" processes and fairly normal "familiarity" processes (Schacter, Verfaellie, & Anes, 1997; Schacter, Verfaellie, & Pradere, 1996). Similarly, a study by Verfaellie and colleagues (Verfaellie, Giovanello, & Keane, 2001) found that most (approximately 71%) of the amnesics' hits were associated with knowing (i.e., feeling), whereas most of the controls' hits (approximately 70%) were associated with remembering.
Taking account of recollective experience may help resolve the discrepancy between the studies of Hirst et al. and those of Squire and his colleagues on the issue of proportionality discussed earlier. Recall that when Hirst and his colleagues matched amnesic and control recognition performance by giving amnesics more study time, they found that amnesic recall was disproportionately impaired (Hirst et al., 1986; Hirst et al., 1988). However, when Squire and his colleagues achieved the same end by extending the retention interval by controls, they showed that amnesic recall was impaired to the same degree as recognition (Haist et al., 1992; Shimamura & Squire, 1988a; Squire & Shimamura, 1986). However, it is known that after long retention intervals, even controls favor recognition by familiarity-based "knowing" rather than conscious recollection. Because recall (almost by definition) depends solely on conscious recollection processes that are apparently unavailable to amnesics, matching by study time will perforce yield worse recall in amnesics by controls, while matching by retention interval will put both amnesics and controls on an equal footing.
In a test of this hypothesis, Sullivan Giovanello and Verfaellie found that, in fact, "the differential contribution of recollection and familiarity to the performance of amnesic patients" (p. 444) could account for the disparate findings in the two conditions (Sullivan Giovanello & Verfaellie, 2001). In other words, recognition is relatively spared in amnesics precisely because they can rely on the priming-based feeling of familiarity to mediate successful performance.
Another perspective on priming and recognition comes from a sizeable literature from studies of normal subjects, indicating that priming can influence recognition judgments by giving rise to perceptual and conceptual (e.g., Dorfman & Mandler, 1994; Graf & Mandler, 1984; Johnston, Dark, & Jacoby, 1985; Mandler, Hamson, & Dorfman, 1990). In studies of normal memory, it is now taken as a given that a priming-based fluency heuristic can mediate successful recognition by neurologically intact, nonamnesic subjects (Jacoby & Dallas, 1981; Jacoby, Kelley, & Dywan, 1989; Lloyd, Westerman, & Miller, 2002; Whittlesea, 1993; Whittlesea & Williams, 2000, 2001a, 2001b). Given that priming is spared in amnesia, why shouldn't amnesics take advantage of the fluency heuristic as well.
Even more important, there are other neuropsychological studies, besides Dorfman's, which indicate that priming does in fact contribute to recognition in amnesic patients. For example, Verfaellie and Treadwell used Jacoby's (1991) process dissociation procedure to identify the contributions of fluency and recollection to recognition (Verfaellie & Treadwell, 1993). Amnesics were impaired only on recognition by the conscious recollection process. With respect to recognition by the automatic familiarity process, they were indistinguishable from nonamnesic controls. Put another way, recognition-by-recollection differed greatly between levels of processing, and between amnesics and controls, as it should if recollection is closely tied to explicit memory. But recognition-by-familiarity was unaffected by levels of processing, and did not differ between amnesics and controls, as we would expect if familiarity were closely tied to priming and implicit memory. Almost all of the correct recognition judgments by amnesics were mediated by priming-based familiarity -- exactly the pattern of performance predicted by Dorfman et al. (Dorfman et al., 1995). Amnesics do not remember much, but because of their spared implicit memory, they can strategically rely on priming-based feelings of familiarity to make relatively accurate judgments about the past, and thus improve their performance on explicit memory tasks (see also Verfaellie & Cermak, 1999).
If recognition by amnesics were mediated by priming-based feelings of familiarity, as both these studies and the studies of recollective experience suggest, we would also expect that the levels of confidence attached to these judgments would be relatively low, compared to those of normals whose recognition is mediated by retrieval or remembering. Studies of normal memory show that recognition by the priming-based feeling of "knowing" is accompanied by relatively low confidence levels, compared to recognition by remembering (Kihlstrom, Kim et al., 2002), and this is true for recognition by amnesics as well (Haist et al., 1992; Shimamura & Squire, 1988b).
Bringing all these strands together, Yonelinas and his colleagues combined Jacoby's process dissociation procedure and the Tulving-Gardiner remember-know paradigm with confidence ratings and signal detection theory to uncover the components of recognition in amnesia (Yonelinas, Kroll, Dobbins, Lazzara, & Knight, 1998). Their re-analysis of four previous studies (Knowlton & Squire, 1995; Schacter et al., 1997; Schacter, Verfaellie, Anes, & Racine, 1998; Verfaellie & Treadwell, 1993) confirmed the original conclusion of Verfaellie and Treadwell (Verfaellie & Treadwell, 1993) that amnesia severely impairs recognition by remembering (recollection, in Jacoby's terms), but leaves recognition by familiarity (Jacoby's fluency) relatively spared. In a new experiment, Yonelinas et al. tested a dual-process theory of recognition similar to those proposed by Mandler (1980) and Jacoby (Jacoby, 1991). The overall pattern of findings strongly suggested that recognition by amnesics is primarily mediated by familiarity, while recognition by controls is mediated by recollection as well. Amnesia impaired both processes, compared to controls; but there was some recognition spared in the amnesics, and almost all of it was based on a feeling of familiarity -- a feeling of familiarity that is a product of priming (see also Khoe, Kroll, Yonelinas, Dobbins, & Knight, 2000). A later study added evidence supporting the conclusion that the familiarity component in the process dissociation procedure is closely related, if not identical, to the recollective experience of "knowing" -- that is, of feeling" (Yonelinas, 2001, p. 361), and that both, in turn, are reflected in the familiarity-based ROC curve derived from confidence ratings. Priming underlies all three aspects of recognition.
As its name suggests, Yonelinas' two-process model holds that recognition can be mediated by two processes:
The model further specifies that recollection is a threshold, or qualitative, process: a person either remembers an item consciously or not. By contrast, familiarity varies along a continuum: items can seem more or less familiar, presumably reflecting their underlying level of activation.
Finally, the model specifies a particular relation between remembering and familiarity: subjects either recognize items based on familiarity, or they recognize items by adding recollection to familiarity.
Yonelinas' dual-process model is a formal, mathematical model that generates quantitative predictions represented by a set of "receiver operating characteristic" (ROC) curves generated according to the principles of signal-detection theory (see also Yonelinas, 2001). The model yields theoretical ROC curves of the sort generated by the model. Chance performance, with hits equaling false alarms, is represented by a straight line running along the diagonal. Performance above chance, with hits exceeding false alarms, is represented by lines above the diagonal -- the better the performance, the further the curve is from the diagonal. Note that the theoretical ROC curve for recognition by familiarity (fluency or feeling) alone is lower than that for familiarity plus recollection. This is because fluency alone is somewhat less reliable than recollection, for reasons discussed earlier. Moreover, the familiarity curve is symmetrical, while the curve for familiarity plus recollection (retrieval or remembering) is asymmetrical. This follows from the assumption that familiarity is a continuous process, while recollection is a threshold process. At the high levels of confidence represented by the left-hand side of the graph, where subjects have relatively few hits but also very few false alarms, recollection makes memory more accurate than it would be if the subject relied on familiarity alone.
The point of all of this is that recognition by familiarity is mediated by an experience of perceptual and conceptual fluency that in turn reflects the priming effects of past experience. And it is familiarity -- feeling, not knowing, which seems to underlie successful recognition by amnesics. Heuristic reliance on the feeling of familiarity, in turn based on the perceptual and conceptual fluency that comes with priming, permits amnesic patients to recognize items that would not be recognized if they relied on conscious recollection. Because familiarity does not help much when it comes to free recall, amnesics perform better on tests of recognition tests than they do on tests of recall. Because the feeling of familiarity is based on the perceptual and conceptual fluency that comes with priming, recognition in amnesia constitutes a case where implicit memory interacts with explicit memory.
There is now abundant evidence that a priming-based feeling of familiarity can mediate recognition judgments of both normal subjects and amnesic patients, and that the recognition judgments of amnesic patients, in contrast to those of normal subjects, are mediated more by familiarity than by recognition. Nevertheless, recognition is not always improved by relaxing decision criteria (Reber & Squire, 1999; Stark & Squire, 2000; Sullivan & Verfaellie, 1999). Why the difference in outcome? In the first place, it should be understood that the process proposed here is not simply one of "relaxing" decision criteria. It is not necessarily enough for subjects just to lower their standards for what they are willing to judge to be "old" rather than "new". Rather, they may need to apply a qualitatively different set of standards. It is one thing to judge that someone is familiar because you can remember the circumstances under which you initially, or most recently, encountered them. This is what Mandler means by retrieval, Jacoby by recollection, and both Tulving and Gardiner mean by remembering. It is quite another thing to make the same judgment based on the fact that the person's face or name "rings a bell". That is what Mandler means by familiarity, Jacoby by familiarity or fluency, Gardiner means by knowing, and I mean by feeling. To shift from one to the other as the standard for making the "judgment of previous occurrence" (Mandler, 1980, p. 252), is not to raise or lower the threshold on a single continuum. Rather, it is to shift from one standard to another. Instructions to subjects must make this clear.
But there is more to shifting criteria than simply giving subjects carefully worded instructions. Subjects have to believe that they can comply with them -- a problem known in personality and social psychology as self-efficacy (Bandura, 1977, 2000). If subjects don't think they'll succeed, they may not be motivated to try, and instead respond randomly. Reber and Squire suggested as much when they noted (p. 509), "ECT patients are unaccustomed to their memory dysfunction…", while "Amnesic patients… are accustomed to their condition…." This is certainly true of college students experiencing posthypnotic amnesia as well. Perhaps Dorfman's patients, for whom amnesia is an acute problem rather than a chronic condition, were simply trying harder to remember, and were thus more motivated to capitalize on priming-based familiarity. We know that, despite their impairments in explicit episodic memory, amnesic patients can incorporate new "semantic" self-knowledge into their self-concepts (Kihlstrom, Beer, & Klein, 2002; Klein & Kihlstrom, 1998; Klein, Loftus, & Kihlstrom, 1996), and amnesia may be one of those facts. Although it might seem paradoxical to say that amnesic patients "remember" that they can't remember, even H.M. is aware that he is amnesic (Hilts, 1995). Although some amnesic patients may be unaware of their memory deficits (McGlynn & Schacter, 1989; Prigatano & Schacter, 1991), a condition generally called anosognosia, many patients for whom amnesia is part of their identity may just not try to remember anymore.
The fact that H.M. himself shows some recognition (Huppert & Piercy, 1977) does not contradict this hypothesis. H.M. knows he is amnesic, but he is also a highly experienced and cooperative experimental subject. Accordingly, his motivation to remember may differ from that of other amnesic patients.
It may also be that, in severe cases, the amnesic syndrome itself prevents amnesic patients from strategically capitalizing on the experience of fluency that gives rise to the feeling of familiarity. This is because fluency is not absolute. It is not the case, for example, that items identified in less than 750 milliseconds are experienced as more familiar than those which require more time. Rather, fluency is relative: the fluency to which priming gives rise is only experienced in comparison to the relative difficulty of processing other items. This comparison itself requires memory -- at least the ability to remember, over a relatively short term, how easy or difficult it was to process one item when processing another item. Amnesia normally spares such primary or "short-term" memory, of course (Talland, 1965), so under ordinary circumstances amnesic patients retain the capacity to make such a comparison -- provided that they are encouraged to do so. At the same time, it is possible to imagine experimental procedures that would tax this capacity severely: blocking the presentation of primed and unprimed items at the time of the test, for example, or increasing the interval between items, or inserting a distracting task. Anything that compromises primary or "short-term" memory would impair the ability of anyone -- amnesic or not -- to appreciate the relative fluency, created by priming, that gives rise to the feeling of familiarity that can mediate recognition.
Explicit and implicit memory may well prove to be mediated by a number of separate systems, as dogma in contemporary cognitive neuroscience insists. But at the same time, theory has to find a way for these systems to interact -- to combine and communicate with each other to support the individual's performance of the task at hand. Similar considerations apply to single-system theories, all of which assume that different processes play different roles in explicit and implicit memory. Because there are no process-pure tasks, these processes must be able to interact to support the subject's performance of each and every one of them. In the final analysis, it's a whole, sentient, intelligent, conscious person who performs the task, using all the information that is available to him or her, whether those influences arise from conscious or unconscious memory. This is true whether that person is a neurologically intact college sophomore or a brain-damaged amnesic patient.
Expanded version of a paper delivered at a symposium on "Recognition in Amnesia" presented at the annual meeting of the Memory Disorders Research Society, October 2002.
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