Abstract

Episodic autobiographical memory (ABM) is important for social functioning. Loss of specificity in ABM retrieval has been observed in people with mild to moderate Alzheimer's disease (AD). Our aim was to extend these findings to subjects with amnestic mild cognitive impairment (aMCI) and very early AD. We performed a cued ABM task with both subject groups and healthy elderly controls. Although aMCI participants performed better than early AD subjects both showed reduced specificity of ABM retrieval when compared with controls. We conclude that qualitative memory retrieval deficits could contribute to social functioning impairment in people with aMCI and early AD, and highlight the complexity of symptoms already present in early stages of cognitive impairment.

Introduction

People with amnestic mild cognitive impairment (aMCI) show high conversion rates (10%–12% per year, Petersen et al., 1999) to Alzheimer's disease (AD). According to the widely used diagnostic criteria, subjects with aMCI have subjective memory complaints and abnormal memory performance for their age, but normal general cognitive function and intact activities of daily living (Petersen, 2004). But in line with how both groups present clinically, there is evidence that AD and aMCI subjects may already have performance deficits in social interaction-related daily routines, such as conversation, telephone use, or household activities (Reisberg, 2001; Reisberg et al., 2007).

Specific autobiographical memories (ABMs) are important for social functioning (Arie, Apter, Orbach, Yefet, & Zalzman, 2008; Beaman, Pushkar, Etezadi, Bye, & Conway, 2007; Williams, 1996) as they are a source to provide useful analogues in a process of generating alternative solutions to social problems (Beaman et al., 2007). First reported by Williams and Broadbent (1986) in parasuicidal subjects and mainly observed in depressed patients (van Vreeswijk & de Wilde, 2004), the phenomenon of reduced ABM retrieval specificity (overgenerality) describes the inability to report a single event referring to a specific time and place when given a cue word. People tend to report extended-timeframe or categorial memories. These nonspecific responses could represent a truncation of a hierarchical search (“mnemonic interlock,” Williams, 1996), resulting in an omission or output of an intermediate description that would normally be used to aid the retrieval process (Williams, 2006). After a number of failed retrievals, cues will activate a network of intermediate information, so that the search moves “sideways” and not “downward” in the hierarchy (Barnhofer, de Jong-Meyer, Kleinpass, & Nikesch, 2002; Williams, 2006). The CaRFAX model (Williams, 2006) proposes three mechanisms underlying ABM specificity reduction: The subject (a) captures and ruminates thus processing the memories in a global, undifferentiated way (see also Teasdale & Barnard, 1993), (b) avoids memory retrieval and aborts the retrieval process due to learned passive avoidance strategies, (c) is impaired in executive control due to reduced cognitive resources, individual effort, or initiative.

Research regarding ABM specificity reduction has focused largely on traumatic life events to explain the development of overgeneral retrieval in depression (Williams, 2006). Moore and Zoellner (2007) reviewed the literature and showed that there was no consistent association between trauma exposure and overgenerality and that theories emphasizing underlying psychopathological processes may better explain overgenerality findings. One group of theories (cognitive resource allocation theories) suggests that declining cognitive resources may lead to difficulties in the retrieval of specific memories. In this case, other resource-consuming processes, such as intrusions or suppression of thoughts, could interfere with the cognitively challenging task of ABM retrieval (van Vreeswijk & de Wilde, 2004; Moore & Zoellner, 2007). The strategic inhibition theory suggests that impaired emotion regulation could contribute to overgenerality due to intense emotions hampering ABM specificity (Philippot, Schaefer, & Herbette, 2003). Watkins & Teasdale (2004) argue that overgenerality is associated with self-focused and ruminative “analytical” cognitive processing of past events, not with the “traumatic” nature or severity of the events itself. These hypotheses are in line with the CaRFAX model. But they also emphasize the impact of individual cognitive abilities on the quality of autobiographical retrieval in general.

Moses, Culpin, Lowe, and McWilliam (2004) reported reduced specificity of ABM retrieval in people with mild to moderate AD and suggested that this could reflect executive control impairment due to reduced cognitive resources. This interpretation is consistent with theories referring to cognitive resource allocation (Moore & Zoellner, 2007). Executive functions, involved in process planning, control, and evaluation, are known to be impaired in the earliest stages of AD (Greene, Hodges, & Baddeley, 1995).

It has been shown that in people diagnosed with aMCI neuronal pathology primarily affects medial temporal lobe regions in an AD-like pattern (Small et al., 2006). Although there is an ongoing debate about the medial temporal lobe's exact contributions, which may differ depending on the quality or richness of the recollective experience (Hassabis & Maguire, 2008; Moscovitch et al., 2005), there is evidence that the hippocampus supports scene construction, processes spatial information (Burgess, Maguire, & O'Keefe, 2002; Lee, 2005) and is therefore crucial for imagining new experiences as well as recollecting the past (Eichenbaum, 2004; Hassabis & Maguire, 2008). This could contribute to the finding that aMCI subjects present with increased semantic and reduced episodic ABM performance when compared with healthy controls (Murphy, Troyer, Levine, & Moscovitch, 2008).

Furthermore, the episodic memory system has been shown to be affected by aging itself (Craik, 2000; Nyberg et al., 2003). Older people experience a decrease in their ability to recall sensory-perceptive, affective, or spatiotemporal-specific details, tend to hold an “observer point of view” instead of being an “actor,” and compensate with an increase of semanticized memories (semantic–episodic dissociation, Piolino et al., 2006). Although reduced specificity of ABM can therefore be detected in elderly when compared with younger people (Piolino, Desgranges, Benali, & Eustache, 2002), an overgeneral retrieval style is considered pathologic (Burgess & Shallice, 1996; Conway & Pleydell-Pearce, 2000).

We hypothesize that due to reduced cognitive resources early AD and also aMCI subjects would show impairment in ABM retrieval specificity that could contribute to social functioning deficits in both groups. These findings would further extend our insight into the complexity of symptoms already present in early stages of cognitive impairment. We investigated three groups of subjects: People diagnosed with aMCI, early AD, and healthy elderly controls to expand the findings of Moses and colleagues (2004) to the earlier stage of AD and putative prodromal AD as suggested for aMCI.

Materials and Methods

All aMCI and AD subjects were patients recruited from our Memory Disorder Clinic and the control subjects responded to public advertisements. Participants underwent diagnostic procedures up to 3 months prior to this study. Informed consents were obtained and the Ethics committee for Medical Research (University of Dresden) approved the study. We included three groups of participants: 16 subjects diagnosed with aMCI (meeting criteria by Petersen, 2004), 16 subjects diagnosed with early AD (meeting NINCDS-ADRDA criteria, McKhann et al., 1984), and 16 healthy controls. Whereas CVLT group mean scores were in the average range for aMCI subjects, all participants diagnosed with aMCI had at least one CVLT score that was >1 SD below the mean. There has been controversy whether a cutoff score of 1.5 SD below age norms should be used to attest impaired memory performance in aMCI. Petersen underlines that 1.5 SD was not a cutoff score in the original description of an MCI cohort with nearly half of that group falling below 1.5 SD (Petersen, 2004; Petersen et al., 1999). He states that no particular test or cutoff score was specified and the criterion is left to the judgment of the clinician and should be interpreted in conjunction with the subject's subjective memory complaints (Petersen, 2004). Since we were interested in aMCI subjects in an early clinical stage of memory impairment, we decided to apply the rather strict cutoff of greater 1 SD below age norms.

Magnetic resonance imaging of the brain was obtained and examined by a neuroradiologist. The degree of white matter lesions was rated using the ARWMC scale (Wahlund et al., 2001). Only subjects free of white matter lesions or with focal lesions only (<2 patients on ARWMC) were included. Except stable (12 weeks or longer) acetylcholine esterase inhibitor treatment in all individuals of the AD group, participants were free of psychotropic medications. Other study exclusion criteria were education less than 8 years, history of alcohol or substance abuse, history of psychiatric or neurological disorder preceding MCI and AD onset, epilepsy, and major systemic disease with disturbance of brain function. According to our study protocol, all subjects performed the ABM task (Williams & Broadbent, 1986) as well as MMSE (Folstein, Folstein, & McHugh, 1975), HAMD (Hamilton, 1967), and CVLT (Delis, Kramer, Kaplan, & Ober, 1987) for correlation analyses. Demographic and clinical characteristics of the study subjects are given in Table 1.

Table 1.

Demographic and clinical characteristics of subject groups and correlation with ABM task performance

Characteristic (mean ± SDControls (n = 16) aMCI (n = 16) AD (n = 16) Pearson's ra 
Age (years) 62.94 ± 5.73 63.13 ± 5.78 64.67 ± 7.3 .15 
School education (years) 9.82 ± 4.22 9.0 ± 4.3 9.52 ± 3.94 .07 
Female sex (numbers) 11 .07 
HAMD-21 (0–65 patients) 1.38 ± 1.67 3.38 ± 2.22 1.53 ± 2.06 .04 
MMSE (0–30 patients) 30.0 ± 0.0 28.56 ± .81 24.19 ± 2.95 .69*** 
CVLT (z-scores) 
 Short delay free recall 0.25 ± 0.86 −0.7 ± 1.39 −2.64 ± 0.63 .65*** 
 Short delay cued recall 0.13 ± 0.86 −0.57 ± 1.28 −1.93 ± 0.92 .55*** 
 Long delay free recall 0.31 ± 0.95 −0.43 ± 1.22 −2.71 ± 0.91 .73*** 
 Long delay cued recallb 0.44 ± 0.89 −0.57 ± 1.34 −2.57 ± 1.02 .65*** 
 Recognition hits 0.81 ± 0.54 0.36 ± 0.84 −1.0 ± 1.66 .53*** 
 false positiveb,c 0.56 ± 0.63 −0.43 ± 1.79 −1.57 ± 1.79 .43** 
 List B −0.5 ± 0.73 −0.67 ± 0.82 −1.71 ± 0.91 .40** 
Characteristic (mean ± SDControls (n = 16) aMCI (n = 16) AD (n = 16) Pearson's ra 
Age (years) 62.94 ± 5.73 63.13 ± 5.78 64.67 ± 7.3 .15 
School education (years) 9.82 ± 4.22 9.0 ± 4.3 9.52 ± 3.94 .07 
Female sex (numbers) 11 .07 
HAMD-21 (0–65 patients) 1.38 ± 1.67 3.38 ± 2.22 1.53 ± 2.06 .04 
MMSE (0–30 patients) 30.0 ± 0.0 28.56 ± .81 24.19 ± 2.95 .69*** 
CVLT (z-scores) 
 Short delay free recall 0.25 ± 0.86 −0.7 ± 1.39 −2.64 ± 0.63 .65*** 
 Short delay cued recall 0.13 ± 0.86 −0.57 ± 1.28 −1.93 ± 0.92 .55*** 
 Long delay free recall 0.31 ± 0.95 −0.43 ± 1.22 −2.71 ± 0.91 .73*** 
 Long delay cued recallb 0.44 ± 0.89 −0.57 ± 1.34 −2.57 ± 1.02 .65*** 
 Recognition hits 0.81 ± 0.54 0.36 ± 0.84 −1.0 ± 1.66 .53*** 
 false positiveb,c 0.56 ± 0.63 −0.43 ± 1.79 −1.57 ± 1.79 .43** 
 List B −0.5 ± 0.73 −0.67 ± 0.82 −1.71 ± 0.91 .40** 

Notes: MMSE = Mini-Mental State Examination (Folstein et al., 1975); HAMD = Hamilton Depression Rating Scale (Hamilton, 1967); CVLT = California Verbal Learning Test (Delis et al., 1987); aMCI = amnestic mild cognitive impairment; AD = Alzheimer's disease; SD = standard deviation; ABM = autobiographical memory.

aPearson's correlation analyses, r(48), between ABM task performance and demographic/clinical variables: **p < .01, ***p < .001, one-tailed.

bSignificant between group differences for control versus aMCI group (ANOVA, post-hoc t-tests, p < .05).

cDifference for aMCI versus AD subjects not significant (differences for control-AD and aMCI-AD groups were significant for all other cognitive variables).

In the ABM task, participants were instructed to report a single-event memory with particular time and place, lasting no longer than 1 day, when given a cue word. In the literature, there are different modifications of the original cued ABM task, for example, extending the classification from a two-categorial (categoric-specific) to a three-categorial (categoric-extended-specific, Barnhofer et al., 2002; Moses et al., 2004) model. We used the three-categorial version with the German translation (Andor, 2000) of 10 cue words (five positive: Happy, surprised, interested, successful, and safe; five negative: Hurt, clumsy, lonely, angry, and sorry), presented in pseudorandom order printed on a card. A practice trial was performed in advance with two cues (curious and proud). A time limit of 60 s was used for each trial. If there was no response within 60 s, this was rated as omission. If participants responded with a categoric memory, a prompt (“Could you describe a specific situation”) was given once to ensure that the categoric response was used due to the inability of being specific rather than due to a usual narrative reporting style. Responses were rated according to three categories, depending on the level of specificity of ABM retrieval: 1 = categoric (“… if I go shopping …”); 2 = extended (“… on my last vacation …”); 3 = specific (subject reports a single event with particular time and place). The answers were recorded on audiotape and then rated by two independent raters. The second rater was blind to the diagnoses. The overall inter-rater agreement (Spearman's rank correlation) was .96.

Results

We performed a two-way mixed-design ANOVA, post hoc t-tests and effect size measures using Cohen's d. No significant group differences could be detected in the demographic variables given in Table 1.

Results were significant for both between (cognitive status), F(2,45) = 8.98, p < .001, and within (responded memory type), F(2,90) = 97.0, p < .001, group factors and their interaction, F(4,90) = 29.1, p < .001. Compared with AD subjects, controls reported fewer categoric (p < .001, Cohen's d = 1.63, controls: Mean [M] = 0.62, SD = 0.81 and AD: M = 3.44, SD = 2.31) and extended (p = .01, d = 0.94, controls: M = 0.69, SD = 1.01 and AD: M = 2.19, SD = 2.01) memories and a higher number of specific memories (p < .001, d = 2.87, controls: M = 8.38, SD = 1.26 and AD: M = 2.75, SD = 2.47).

When comparing controls and aMCI subjects, controls reported fewer extended (p = .004, d = 1.09, controls: M = 0.69, SD = 1.01 and aMCI: M = 1.81, SD = 1.05) memories and a higher number of specific memories (p < .001, d = 1.23, controls: M = 8.38, SD = 1.26 and aMCI: M = 6.62, SD = 1.58). No significance could be found for categoric memories (p = .5, d = 0.25, controls: M = 0.62, SD = 0.81 and aMCI: M = 0.88, SD = 1.2).

When compared with people diagnosed with AD, aMCI subjects reported fewer categoric (p < .001, d = 1.39, aMCI: M = 0.88, SD = 1.2 and AD: M = 3.44, SD = 2.31) and a higher number of specific (p < .001, d = 2.72, aMCI: M = 6.62, SD = 1.26 and AD: M = 2.75, SD = 1.57) memories. The number of extended memories did not differ significantly (p = .5, d = 0.24, aMCI: M = 1.81, SD = 1.05 and AD: M = 2.19, SD = 2.01).

Interactions between cognitive status and cue's emotional valence, or memory type and cue's emotional valence did not reach significance. Pearson's correlations revealed significant relationships between cognitive status measures and ABM task performance. Results are given in Table 1. Age, gender, years of education, and HAMD score did not significantly correlate with ABM specificity.

Discussion

In this study, we found evidence for reduced specificity of ABM retrieval not only in people with very early AD but also in subjects diagnosed with aMCI. Episodic ABM is important for social functioning (Welzer & Markowitsch, 2005) as it gives us the sense of a subjective timeline we can mentally travel back and a “self,” existing in this subjective time (Tulving, 2002). Although there is age-related decrease in autobiographical retrieval specificity (Piolino et al., 2002), the phenomenon of overgenerality has been seen as a pathologic truncation in the search for memories, referring to a “top-down” model of episodic memory retrieval—a staged search starting with a semantic elaboration, followed by generic descriptions to specific mnemonic material in the end (Burgess & Shallice, 1996; Conway & Pleydell-Pearce, 2000). It has been shown that ABM task performance deficits are not specific for a disease and have been observed in patients with very different disorders such as mood disorders, posttraumatic stress disorder, anxiety disorder, AD, acute stress, trauma, and suicidality (for review seevan Vreeswijk & de Wilde, 2004; see also Moses et al., 2004). The results presented here are in line with the suggestions by Moore and Zoellner (2007) emphasizing the impact of underlying pathology on cognitive processing and on the quality of autobiographical retrieval in general.

We provide evidence that AD subjects already in a very early stage of the disease report significantly more categoric and extended, and significantly fewer specific responses when compared with age-matched control subjects irrespective of the cue's emotional valence. Moses and colleagues (2004) suggested that AD participants may lack the cognitive resources to conduct an efficient search for specific memories. This is in line with proposed mechanisms underlying ABM specificity reduction, for example, cognitive resource allocation (for review seeMoore & Zoellner, 2007). In this study, people with aMCI and controls performed equally in avoiding categoric responses. However, aMCI subjects differed significantly from controls but not AD subjects using extended memories and held a middle position in responding with specific memories. This observation fits well in how aMCI patients present clinically and supports the model of a continuum of cognitive decline with aMCI as an intermediate state. Reisberg and colleagues revealed that people with aMCI already have performance deficits in daily routines, for example, reading, food preparation, or driving abilities but especially in social interaction-related activities, such as conversation and telephone use (Reisberg, 2001; Reisberg et al., 2007). In a problematic social interaction scenario (e.g., decision making based on multiple variables), the ability to generate numerous alternative solutions has been shown to be essential for the social problem-solving process itself and predictive for solution quality (D'Zurilla & Nezu, 1980). ABM is important for establishing these alternative solutions to open-ended social problems (Beaman et al., 2007) and the achievement of interpersonal goals (Pillemer, 2003; Williams, 2006). It has been shown that ABM specificity predicts social problem-solving performance and serves as a guiding and directive function with respect to social behavior across the life-span (Beaman et al., 2007; Pillemer, 2003), whereas categoric recall is associated with poor interpersonal social problem-solving (Pollock & Williams, 2001), negative life events, and hopelessness (Arie et al., 2008). We suggest that ABM retrieval quality (specificity) may be more predictive of dysfunctional social problem-solving than other cognitive deficits, which is in line with a recent study by Beaman and colleagues (2007). The authors found that decline in cognitive ability predicted reduced ABM specificity, which itself predicted reduced social problem-solving performance (Beaman et al., 2007). Interestingly, cognitive ability, as measured with processing speed, inhibitory control, and working memory tasks, did not predict social problem-solving performance directly, and no age differences could be found (Beaman et al., 2007).

Our data also show that performance in cognitive measures is correlated with ABM task performance, suggesting a relationship between ABM specificity and the subjects' cognitive resources. Furthermore, reduced ABM task performance could point to impairment of cognitive processes that may be related to social interaction deficits. Interestingly, it has recently been shown that burden among spousal and child caregivers of MCI subjects is not significantly correlated with performance in standard neuropsychological tests itself (Bruce, McQuiggan, Williams, Westervelt, & Tremont, 2008).

Group differences in cognitive measures (see Table 1 for details) highlight the subtlety of cognitive impairment in aMCI subjects, whereas the group comparison in the study presented here reveals that ABM task performance is already significantly reduced in aMCI subjects when compared with normal controls. This may encourage further studies aimed at analyzing the sensitivity and specificity of ABM task performance in aMCI and early AD diagnostic procedures. It would necessitate a large study sample with sufficient power to determine normal and abnormal ranges for ABM task performance. Standardization of the ABM procedure would be of great importance as individual performance has been shown to be moderated by methodological variables, such as the way of presenting cues (auditory/visually), or the maximum available amount of time to respond to a presented cue (for review seevan Vreeswijk & de Wilde, 2004).

The data presented here are commensurate with the notion that cognitive deficits in aMCI are more widespread than routine neuropsychological testing may reveal in a clinical setting. These deficits may exceed isolated memory impairment (Kramer et al., 2006), and our results could contribute to better recognize the everyday complaints aMCI patients report in the clinic. They may also encourage the clinician during the patients' interviews to look for clinical signs of overgenerality in their answers to his specific questions. Furthermore, it seems feasible to directly perform the ABM task, as described in this study, in the patients' initial examinations by a physician or clinical neuropsychologist (e.g., within the neuropsychological assessment battery). This is neither time-consuming nor difficult to analyze, however, despite applicability diagnostic usefulness would have to be investigated.

One of our study's limitations is that we did not measure social functioning deficits directly, which limits our ability to draw direct conclusions regarding the association of ABM overgenerality and social functioning. Furthermore, we did not directly investigate impairment of executive control. Assessment of executive functioning in people with cognitive deficits is challenging as it is affected by factors such as education, age, cultural background, sensory motor difficulties, and other impairments (Petersen et al., 2001). However, executive control deficits have been demonstrated in early AD (Greene et al., 1995) and MCI (Traykov et al., 2007).

In conclusion, we found reduced specificity of ABM retrieval in aMCI and early AD subjects when compared with healthy elderly controls that could be associated with reduced cognitive resources. This might contribute to social functioning deficits in aMCI and AD subjects and could be investigated more directly in future studies.

Funding

MD was funded by a Young Scientist Grant of the Technische Universität Dresden.

Conflict of Interest

None declared.

Acknowledgements

MD and CB have equally contributed to the study and therefore share first authorship.

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