What was the number of each type of gender in each study? Why do you think the authors selected this distribution of genders, or, why did they not care about the gender issue? (

Neuropsychology The Life Span Distribution of Autobiographical Memory in Alzheimer’s Disease Marie Kirk and Dorthe Berntsen Online First Publication, July 26, 2018. http://dx.doi.org/10.1037/neu0000486

CITATION Kirk, M., & Berntsen, D. (2018, July 26). The Life Span Distribution of Autobiographical Memory in Alzheimer’s Disease. Neuropsychology. Advance online publication. http://dx.doi.org/10.1037/neu0000486

The Life Span Distribution of Autobiographical Memory in Alzheimer’s Disease

Marie Kirk and Dorthe Berntsen Aarhus University

Objective: The literature on the temporal distribution of autobiographical memory in Alzheimer’s disease (AD) is characterized by mixed findings concerning the presence of a temporal gradient in the loss of autobiographical memory. Some studies show a gradient, implying better access to more remote autobiographical memories, whereas others do not. These conflicting results likely reflect differences in the test methodologies, accentuating the need for replications and extensions. Method: Forty-five older adults diagnosed with AD (via Mini-Mental State Examination, M � 19.89, SD � 4.05) and a matched sample of 44 healthy older adults were assessed on two different autobiographical memory measures: the Autobiographical Memory Interview (Kopelman, Wilson, & Baddeley, 1990) and the Galton–Crovitz task (word and object cueing) to examine the temporal distribution of personal autobiographical memories across the life span. Results: The impairment of episodic and personal semantic remembering, as indexed by the Autobiographical Memory Interview, was associated with a negative temporal gradient with better preservation of memories from the remote past, relative to the recent one. The results from the word- and object-cueing task replicated the finding that AD is associated with markedly impaired recall of recent events. In addition, both groups showed a peak in the recollection of events from middle childhood and adolescence, consistent with research on the reminiscence bump. Conclusions: Older adults diagnosed with AD demonstrate increased recollection of personal semantic and episodic events from the remote past relative to the recent one. The findings are discussed in relation to prominent models of memory consolidation.

General Scientific Summary The finding that Alzheimer’s disease patients demonstrate better recall of personal significant events from their younger years relative to the recent past indicates that stimulating remote memories in psychosocial interventions may be beneficial to this population.

Keywords: autobiographical memory, episodic memory, Alzheimer’s disease, temporal gradient, reminiscence bump

One of the most prominent hallmarks of Alzheimer’s disease (AD) is impairment of autobiographical memory, and hence the ability to recall memories of personal events. As autobiographical memory and our sense of self and identity are intrinsically related (Conway, 2005), impairment to this type of memory has been

associated with a weakened sense of self in AD (Addis & Tippett, 2004; El Haj & Antoine, 2017; Klein, Cosmides, & Costabile, 2003; Martinelli, Anssens, Sperduti, & Piolino, 2013). Although there is evidence that individuals diagnosed with AD demonstrate impoverished autobiographical recall across the life span relative to healthy controls (HCs; El Haj, Antoine, Nandrino, & Kapogi- annis, 2015), the exact nature of the impairment has been a matter of debate.

Two theoretical frameworks suggest different involvement of the medial temporal lobes, including the hippocampus, in episodic remembering and therefore predict different consequences of the medial temporal lobe atrophy observed in AD. According to the standard consolidation model (Alvarez & Squire, 1994; Squire & Alvarez, 1995), semantic and episodic memories are only tempo- rarily dependent on the hippocampi and medial temporal lobes during consolidation, where upon completion they become repre- sented in neocortex. According to this view, medial temporal lobe atrophy, as observed in AD, will impact negatively on recent episodic memories only, resulting in a temporally graded memory loss, consistent with Ribot (1881). In contrast, the multiple trace

Marie Kirk and Dorthe Berntsen, Center on Autobiographical Memory Research (Con Amore), Department of Psychology and Behavioural Sci- ences, Aarhus University.

This work was supported by the Velux Fonden (Grant 13481) and the Danish National Research Foundation (Grant DNRF89). We thank Katrine Willemoes Rasmussen, Susanne Bollerup Overgaard, Anne Marie Tofte- gaard Kuhr, Tine Bennedsen Gehrt, and Niels Peter Nielsen for their contributions during earlier parts of this project. We thank Ove Dahl and Tove Engelhardt Mathiassen for their help with selecting the objects.

Correspondence concerning this article should be addressed to Marie Kirk, Center on Autobiographical Memory Research (Con Amore), De- partment of Psychology and Behavioural Sciences, Aarhus University, Bartholins Allé 9, Aarhus C 8000, Denmark. E-mail: [email protected]

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Neuropsychology © 2018 American Psychological Association 2018, Vol. 1, No. 999, 000 0894-4105/18/$12.00 http://dx.doi.org/10.1037/neu0000486

1

theory (Nadel & Moscovitch, 1997) states that episodic memories continue to be dependent on the medial temporal lobe structures and hippocampus. The hippocampus is what binds the different parts of an episode, such as sensory-perceptual features, contextual information and emotional content, into a coherent and detailed memory of an experience (Moscovitch, Cabeza, Winocur, & Na- del, 2016). As a result, this model predicts a flat, or minimal, gradient in the temporal distribution of both personal semantic and episodic memories, following medial temporal lobe damage, where memories across all lifetime periods are equally impaired.

In research with AD patients, these conflicting views have been examined using two different semistructured interviews, the Au- tobiographical Memory Interview (AMI; Kopelman, Wilson, & Baddeley, 1990) and the Autobiographical Interview (AI; Levine, Svoboda, Hay, Winocur, & Moscovitch, 2002). In both the AMI and the AI, participants are probed by specific lifetime periods when asked to recall autobiographical events. For example, in the AMI, participants are asked to recall an incident that occurred during secondary school (or high school) or from their wedding, whereas participants during the administration of the AI are pro- vided with a list of lifetime periods, as well as a list of typically occurring events, and required to provide an event from each listed time period.

The two methods differ with respect to how many lifetime periods are included in the test. In the AMI, participants are examined on three lifetime periods (childhood, early adult life, recent adult life). In contrast, the AI involves five lifetime periods (early childhood, adolescent/teenage years, early adulthood, mid- dle age, and the previous year), although some studies have used modified versions (see, e.g., Addis, Sacchetti, Ally, Budson, & Schacter, 2009; Irish, Hornberger, et al., 2011). The two methods are similar in the way they both probe memories for typically occurring events.

Studies using the AMI (or modified versions of it) generally have demonstrated a negative temporal gradient for episodic mem- ory, indicating that memory for remote events, compared with recent events, is better preserved in AD patients (Barnabe, White- head, Pilon, Arsenault-Lapierre, & Chertkow, 2012; De Simone et al., 2016; Graham & Hodges, 1997; Greene, Hodges, & Baddeley, 1995; Irish, Lawlor, O’Mara, & Coen, 2011; Ivanoiu, Cooper, Shanks, & Venneri, 2006; Kopelman, 1989; Leyhe, Müller, Mil- ian, Eschweiler, & Saur, 2009; Müller, Mychajliw, Reichert, Melcher, & Leyhe, 2016). A few studies using the AMI have failed to find statistically significant effects, but report numerical differ- ences in the same directions (Addis & Tippett, 2004; Gilboa et al., 2005; Meeter, Eijsackers, & Mulder, 2006; Nestor, Graham, Bozeat, Simons, & Hodges, 2002). The results for the personal semantic part of the AMI largely follow the same pattern with the majority of studies reporting a negative temporal gradient or finding nonsignificant differences in the same direction (e.g., Ad- dis & Tippett, 2004; De Simone et al., 2016; Ivanoiu et al., 2006; Kopelman, 1989; Leyhe et al., 2009; Nestor et al., 2002, but see Meeter et al., 2006).

In contrast, some studies using the AI (Addis et al., 2009; Irish, Hornberger, et al., 2011) have reported a flat temporal gradient for episodic memories in AD. These conflicting results likely reflect differences in the two test methodologies. In a recent study, Barnabe et al. (2012) showed that the pattern of a temporal gradient varies as a function of how many epochs (i.e., lifetime

periods) were included in the analyses, as well as the number of memories included in each epoch (i.e., one or two memories). Barnabe et al. (2012) scored the memories using both the AI and the AMI procedure. Contrasting only two life periods—childhood versus recent adult life—yielded a temporal gradient for both the AMI and the AI, whereas fewer memories per epoch (i.e., one memory per epoch) diminished it. These findings may help to explain the absence of a gradient in some studies using the AI procedure. For example, Addis et al. (2009) reported a flat gradient for autobiographical memory in their study using an adapted version of the AI with five lifetime periods and one memory per epoch. Probing for just one memory per life time period may result in participants reporting a well-rehearsed, and thus, relatively better preserved and more accessible memory, potentially yielding a flat gradient with similar performance across the life span. Irish, Hornberger, et al. (2011) used a shortened version of the AI in which they omitted the childhood life time period (up to age 11). Even if participants may not recall many memories from early childhood due to infantile amnesia (Rubin, 2000; West & Bauer, 1999), work generally shows that AD patients report a high pro- portion of memories from middle childhood (e.g., Greene et al., 1995; Kopelman, 1989). Thus, omitting this life time period when examining the life span distribution of autobiographical memories will most likely influence the results.

A different line of research addressing the temporal distribution of autobiographical memories comes from studies examining the reminiscence bump, that is, the finding that healthy middle-aged and older adults recall a preponderance of memories, clustering around adolescence and early adult life, compared with the sur- rounding lifetime periods, when asked to freely generate memories from across the entire life span (Rubin, Wetzler, & Nebes, 1986). The majority of studies examining the presence of a reminiscence bump for autobiographical memories have relied on the Galton– Crovitz method (Crovitz & Schiffman, 1974; Galton, 1879), in which participants retrieve memories of personal events in asso- ciation to single nouns. Other techniques involve asking the par- ticipants to report their most important memories or tell their life story (see Koppel & Berntsen, 2015, for a review). In contrast to the AMI and the AI, studies addressing the reminiscence bump typically do not use time periods as constraints for memories; that is, participants are not asked to retrieve each memory from within specific lifetime periods. Instead, the memories are freely gener- ated from across the entire life course.

Surprisingly, very few studies have examined the bump using such open-ended recall across the entire life span in dementia populations. Fromholt and Larsen (1991) asked 15 older adults with dementia and 15 healthy older adults to freely tell their life stories. Afterward, events mentioned in the life stories were dated in the life course of the person. Both groups showed a reminis- cence bump (see Fromholt et al., 2003, for similar results). From- holt and Larsen (1991) also found that the life stories told in the dementia group involved more repetitions and more normative events. The latter may suggest that the personal life stories in the dementia group to a larger extent drew upon the cultural life script, which is highly schematized and culturally shared knowledge about the expected order and timing of important transitional life events in a typical life, such as beginning school, getting married, having children, obtaining a major achievement (Berntsen & Ru- bin, 2002, 2004; Rubin & Berntsen, 2003).

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2 KIRK AND BERNTSEN

Although the reminiscence bump is a robust finding, recent work (Koppel & Berntsen, 2015; Koppel & Rubin, 2016) shows that the bump is far from stable across different experimental designs, and that both the size and temporal location of the bump are sensitive to the cueing method employed. Recent reviews (Koppel & Berntsen, 2015, 2016) have shown that the temporal location of the bump varies systematically according to how mem- ories are probed, with the mean range of the bump located from 8.7 to 22.5 years of age for word-cued memories, compared to 15.1 to 27.9 for important memories. Thus, memories generated in re- sponse to word cues yield a bump located during the second decade of life compared with memories for important events showing a peak located in the third life.

In summary, the vast majority of studies examining the life span distribution of autobiographical memories in older adults with AD (and other types of dementia) has employed structured autobio- graphical memory interviews, probing memories by referring to specific lifetime periods. These studies typically find a temporal gradient, but several exceptions are identified, most likely reflect- ing methodological differences in the number of lifetime periods employed and the number of memories requested. Surprisingly, only few studies have attempted to integrate this research with research on the reminiscence bump in the broader autobiographical memory literature (Kopelman, 2008). In contrast to the structured autobiographical interviews, this research examines the temporal distribution of memories by using open-ended memory retrieval from across the entire life span, that is, with no temporal con- straints for each memory trial. Using this open-ended approach, a few studies involving dementia patients have examined the tem- poral distribution of events mentioned in life stories, but we were unable to identify any studies using the Galton–Crovitz word cue task, unconstrained by time period, in older adults with dementia.

The Present Study

In the present study, we examine the temporal distribution of autobiographical memories in a large sample of AD patients and matched HCs. We employ two different episodic autobiographical measures. First, we use the AMI (Kopelman et al., 1990) to examine whether episodic and personal semantic memories yield differences in the patterns of a temporal gradient. Second, we use the Galton–Crovitz task with two different conditions, a word- and an object-cueing condition, where participants are cued with con- crete everyday objects historically dated to the participants’ youth, or the verbal signifiers for the objects, respectively.

In line with the majority of previous studies using the AMI, we expected to find that AD patients overall demonstrate a temporal gradient with better memory for remote events, relative to recent ones, on both the personal semantic and episodic subscales of the test. We furthermore predicted that the healthy, older control participants would demonstrate similar performances across the three lifetime periods. For the Galton–Crovitz tasks, we expected patients to show increased recollection of events dated during middle childhood and early adult life compared to the surrounding lifetime periods, when cued by both words and objects (Koppel & Berntsen, 2015). In line with the vast amount of studies that have demonstrated a reminiscence bump for healthy, middle-aged and older adults, we also expected the control participants to demon-

strate a bump in the recollection of memories, when cued by words and objects.

Thus, we expected AD patients to demonstrate increased recol- lection of memories from the earlier parts of life irrespective of method of testing, whereas for healthy older adults, we expected to find this only for the Galton–Crovitz tasks.

Method

Participants

Eighty-nine participants were included in the study: 45 (32 females) AD patients and 44 HCs (24 females). These participants were drawn from the samples used in Kirk and Berntsen (2018) to examine different aspects of autobiographical memory in AD.1,2

The AD and HC groups were matched on age and years of education, see Table 1. All 45 AD patients had been formally diagnosed at a memory clinic according to the international guide- lines by the National Institute on Aging and Alzheimer’s Associ- ation clinical criteria (McKhann et al., 2011). AD patients were recruited with the assistance of regional dementia workers, who established the initial contact to the patients through their primary care takers. Trained psychologists then assessed and screened eligible patients according to the inclusion criteria. Inclusion cri- teria for both groups involved fluency in Danish, no history of severe head injury, substance abuse, or any other major psychiatric disorder. Participants were not eligible for participation if they demonstrated substantial vision or hearing disability. Use of anti- depressants and medication used to treat AD was not an exclusion criterion.

Additional exclusion criteria for the HC participants included signs of dementia, as indexed by a score of 26 or below on the Mini-Mental State Examination (MMSE; Folstein, Folstein, & McHugh, 1975). HC participants were recruited through senior’s organizations, and from the research center’s participant database. The study was approved by the Central Denmark Region Com- mittees on Health Research Ethics, and all participants gave in- formed consent to participate in the study, the AD patients always in the presence of their primary caretakers.

Materials

Neuropsychological assessment. All participants were as- sessed on Addenbrooke’s Cognitive Examination (ACE; Mathuranath, Nestor, Berrios, Rakowicz, & Hodges, 2000), which includes the MMSE (Folstein et al., 1975), to assess global cog- nitive ability.3 Maximum scores on both measure index better

1 Of the 50 AD patients included in Kirk and Berntsen (2018), only 46 were included in the present study, as four participants did not complete or perform the AMI and one participant was excluded from analysis due to confabulation. Of the original 50 HC participants, four participants were excluded from analysis, as they scored �88 on the Addenbrooke’s Cog- nitive Examination.

2 The Kirk and Berntsen (2018) article does not address the temporal distribution of autobiographical memories.

3 All the AD participants were furthermore included in a prospective study (Kirk, Rasmussen, Overgaard, & Berntsen, 2017) that included a more extensive test battery not limited to the measures included in the present study.

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3AUTOBIOGRAPHICAL MEMORIES IN AD

cognitive ability. As part of the ACE, participants were further- more assessed on verbal fluency, that is, phonemic (letter S) and semantic fluency (animal category; Lezak, Howieson, Bigler, & Tranel, 2012). Participants were also screened for depressive symptoms with the Geriatric Depression Scale (Brink et al., 1982). The self-report scale consists of 15 items that can be answered with a yes or no in reference to how the respondent felt over the past week. Higher scores are indicative of depression with scores below 5 considered to be within the normal range.

The Autobiographical Memory Interview. The AMI (Ko- pelman et al., 1990) is a semistructured interview that assesses autobiographical memory and personal semantic memory across three broad time bins that span from childhood, early adult life to recent life. More specifically, the interview consists of two sched- ules; a personal semantic schedule, which assesses recall of per- sonal semantic information (e.g., name of the first school that one attended), and an autobiographical incident schedule, which as- sesses recall of specific events (e.g., recall of an incident that occurred while one was at primary school). Both schedules gen- erate a composite score (range � 0–27 for the autobiographical incidents schedule; range � 0–63 for personal semantic informa- tion), as well as subdomain scores for the three individual time bins (range � 0–9 for each time bin on the autobiographical incident memory schedule; range � 0–21 for each time bin on the personal semantic memory schedule). Participants are required to recall three autobiographical incidents from each of the three time bins, adding to a total of nine episodic incidents. Each reported incident is then scored according to the scoring criteria outlined in Kopelman et al. (1990). Responses are rated on a scale of 0 (no response, or response based on semantic memory), 1 (vague personal memory), 2 (personal but nonspecific event, but time and place not recalled), or 3 (episodic memory, specific in time and place). Higher scores on both the autobiographical incident mem- ory schedule and the personal semantic memory scale index better recall function.

The Galton–Crovitz cueing technique. To examine autobi- ographical memory recall, we included the Galton–Crovitz task (Crovitz & Schiffman, 1974; Galton, 1879) with two different conditions: an object-cueing condition and a word-cueing condi- tion.4

In the object-cued recall condition, participants were presented with concrete objects with a clear reference to the participants’ younger years, such as a skipping rope or a bottle of perfume (see Appendix A for a list of stimuli). Two experts (a historian and a social anthropologist and museum curator) with extensive knowl- edge of 20th-century history assisted in the selection of the object cues. All the object stimuli were piloted prior to the commence- ment of the study with nine AD patients to ensure that the stimuli were relevant to a broad group of participants. As an example, some object cues were omitted from the final study as it was found that specific brands of soaps and washing powder were only familiar to a few participants due to large variations in regional use of these goods during the 1950s. Similarly, a handheld chalkboard did not match the age group of the participants as the majority of these used paper and pencils during their time of education. In the object-cued condition, participants were handed a concrete object, which they were encouraged to explore with their hands.

In the word-cueing condition, participants were presented with the verbal signifiers of the objects, such as the word “skipping rope” or “perfume.” Word cues were presented in black font, size 36 point, on a 210- � 297-mm (8.3- � 11.7-in.) white card.

In both conditions, participants were presented with a cue and then requested to retrieve a memory in response to each word. Participants were presented with a total of five verbal cues and five object cues. Stimuli were presented in blocks of modalities (i.e., words vs. objects) with the order of presentation counterbalanced across participants to prevent order effects. In both conditions, participants were presented with one cue at a time. Each cue was named out loud by the interviewer. Participants were then required to report the first memory of a personally experienced event that came to mind, if any, and were informed that the recalled memory did not need to be specifically related to the cue, the test instruc- tions are provided in Appendix B. To minimize variation in prompting and wording of questions, all interviewers followed a standardized test protocol. The participants were not interrupted during recall but were asked to provide more details, such as time and place of the event, if this was not naturally provided.

4 The task has been described in detail in Kirk and Berntsen (2018).

Table 1 Descriptive Statistics and Independent t-Test Results for Age, Education, Cognitive Ability, and Executive Functioning

Variables

Alzheimer Control

t(87) 95% CIM SD M SD

Age (years) 80.67 7.52 80.18 6.02 .34 [�2.39, 3.36] Education (years) 9.96 3.05 11.09 3.58 �1.99 [�2.80, .00] Geriatric Depression Scale/15 2.96 2.06 1.36 1.30 �4.36��� [.87, 2.32] MMSE/30 19.89 4.05 28.98 .95 �14.51��� [�10.33, �7.84] ACE/100 58.31 11.41 91.10 4.74 �17.63��� [�36.48, �29.08] Semantic fluency 9.82 4.96 21.10 6.35 �9.34��� [�7.33, �3.55] Phonemic fluency 7.38 4.22 12.82 4.72 �5.74��� [�13.66, �8.87]

Note. MMSE � Mini-Mental State Assessment; ACE � Addenbrooke’s Cognitive Examination; CI � confidence interval. The MMSE is included in the ACE. Fluency scores are presented as total number of items recalled. The numbers after the slash indicate max score on the scale. ��� p � .001.

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