Alzheimer's disease and memory-monitoring impairment: Alzheimer's patients show a monitoring deficit that is greater than their accuracy deficit

Much research has documented the costs to memory from Alzheimer’s disease (AD). Individuals with AD are less likely than age- and education-matched controls to recognize or recall previously encountered events (Budson, Wolk, Chong, & Waring, 2006). AD patients also show difficulty remembering source information – specific information about the exact circumstances under which an event was encountered (e.g., Johnson, Hastroudi & Lindsay, 1993). They are less able than controls to remember: (a) whether an item was previously seen or imagined (e.g., Dalla Barba et al., 1999), (b) whether a sentence was completed by oneself or by another (e.g., Multhaup & Balota, 1997), (c) whether words had been previously presented in a red or green color (Tendolkar et al., 1999), (d) whether a fact was said by a man or a woman (Mitchell, Sullivan, Schacter, & Budson, 2006), (e) whether a word was presented during one task or another (Pierce, Sullivan, Schacter, & Budson, 2005; Pierce, Waring, Schacter, & Budson, 2008), (f) whether an item was presented during the study or test session (Budson, Dodson, Daffner, & Schacter, 2005), and (g) source information outside of the laboratory (Budson et al., 2004; Budson, Simons, Waring, Sullivan, Hussion, & Schacter, 2007; see Souchay & Moulin, 2009, for a review). Although the memory deficit from AD is increasingly clear, what is not clear is the extent to which AD patients are aware of this memory deficit. In other words, how well can AD patients monitor and judge the likely accuracy of memories? To foreshadow our results, this paper shows that AD patients are strikingly unaware of the accuracy of their memories. Even when their recognition performance is comparable to that of an older control group, AD patients are unable to distinguish between correct and incorrect recognition responses. Reliably monitoring one’s memory is critically important for knowing how much to trust a particular memory. One problem in particular that patients with AD experience is a high percentage of false memories, both in the laboratory (Budson, Daffner, Desikan, & Schacter, 2000) and in the real world (Budson et al., 2007). For instance, patients who falsely remember that they have already turned off the stove or have taken their medications when they have not will no longer be able to live independently. However, accurately monitoring memories is a potential mechanism for counteracting the influence of false memories when, for example, individuals are aware that a particular memory is likely to be false. Thus, understanding the extent to which patients with AD can monitor and judge the accuracy of their memories is an important clinical issue in addition to being of great theoretical interest. The small literature that has examined memory-monitoring on the part of Alzheimer’s patients has produced conflicting findings (see Pannu & Kaszniak, 2005, and Souchay, 2007 for reviews). On the one hand, patients with mild AD appear no different from healthy controls in using confidence ratings to judge the likely accuracy of answers to general knowledge questions (e.g., Who wrote Alice in Wonderland?) that assess well-learned or semantic information (Backman & Lipinska, 1993; Lipinska & Backman, 1996; see also Cosentino et al., 2007). Similarly, Moulin et al. (2003) observed no differences between AD participants and healthy older controls in monitoring the accuracy of recognition judgments. On the other hand, Souchay et al (2002) showed that AD patients were impaired in monitoring episodic memories. When completing a cued-recall test of recently-learned material, AD patients were much less accurate than older controls in providing feeling-of-knowing (FOK) judgments about the likelihood of recognizing an unrecallable item (Souchay et al., 2002). To our knowledge, no one has examined AD patients’ ability to monitor the likely accuracy of source judgments. In general, this pattern of AD patients – when compared to healthy older adults – showing a preserved ability to monitor the accuracy of semantic memories but an impaired ability to monitor the accuracy of episodic memories parallels a similar pattern that exists when healthy older adults are compared to younger adults. Older adults are either no different from or better than younger adults in monitoring the accuracy of responses to general knowledge questions – either with confidence ratings or by providing FOK judgments (e.g., Allen-Burge & Storandt, 2000; Butterfield, Nelson, & Peck, 1988; Dodson, Bawa, & Krueger, 2007; Perlmutter, 1978; Pliske & Mutter, 1996). However, older adults are much worse than younger adults in monitoring the accuracy of recently-learned (episodic) material: a) they provide less accurate FOK judgments on cued-recall tests (Souchay et al, 2000); and b) their confidence ratings are less well calibrated on both cued-recall tests and source memory tests because of the occurrence of high-confidence errors (Dodson et al., 2007a, 2007b; see also Dodson & Krueger, 2006). Dodson and colleagues proposed a misrecollection account to explain the pattern of older adults’ monitoring performance (Dodson et al., 2007a, 2007b). They suggested that advancing age is associated with an increased susceptibility of miscombining features of different events that in turn produce confidently-held misrecollections – memory problems that are likely caused by deterioration of the hippocampus and surrounding tissue (e.g., Shimamura & Wickens, 2009; Squire et al., 2004; and see Raz et al., 2005 for evidence of accelerated shrinkage of the hippocampus with healthy aging). This account predicts age-related differences in monitoring performance – because of the occurrence of high confidence errors – on all tests that require memory for specific details about recently-learned past events, such as source memory tests. The goals of the present study are twofold. First, given the similarity between older adults and AD patients in that both show relatively preserved monitoring of semantic memories and impaired monitoring of episodic memories (when compared to their respective control groups), we sought to test the misrecollection account as an explanation of the monitoring performance on the part of AD patients. Specifically, if AD patients show a more severe version of the same misrecollection impairment that is exhibited by older adults then we should observe that on a source memory test AD patients are more prone than older adults to make high confidence errors. The second goal is to examine whether the memory-monitoring deficit in AD patients is a byproduct of their overall weaker memory performance or whether this memory-monitoring deficit is a byproduct of a more specific, malfunctioning memory-monitoring mechanism. The answer to this question is unknown because in all extant studies AD patients show worse memory performance than their healthy older counterparts. Thus, worse memory-monitoring by AD patients may be a byproduct of their worse accuracy (see Hertzog et al., 2010 for a similar argument about differences in memory-monitoring between older and younger adults). No study has sought to compare the memory-monitoring abilities of AD patients and healthy older adults when both groups show comparable memory performance. To address these goals, we used a combination recognition and source identification paradigm that involves collecting confidence ratings for both memory judgments (e.g., Dodson, Bawa, & Krueger, 2007; Simons, Peers, Mazuz, Berryhill & Olson, 2010). At encoding, participants heard sentences that were presented by either a female or a male. At test, participants were presented with sentences and made an initial old-new recognition judgment (i.e., Did you encounter it before or is it new?) and for items receiving a judgment of old, participants made a source judgment about who presented the item earlier (i.e., male or female?). For both the recognition and the source judgments, participants rated the likely accuracy of their responses on a confidence scale from 50 (guessing) to 100 (certain). According to our misrecollection account, we should observe that AD patients make more high confidence errors than healthy older adults on the source judgment. Critically, if the monitoring impairment on the part of AD patients is not merely a byproduct of their worse accuracy then we should observe that even when AD patients and healthy older adults show comparable source identification accuracy, the AD patients still will exhibit a monitoring impairment. In other words, matching the AD patients and the older adults on source memory accuracy avoids a potential confound and so any observed differences in monitoring performance on this judgment cannot be attributed to differences in source accuracy.