Abstract
Background:
Alzheimer’s disease (AD) is characterized by severe memory alterations, affecting especially memories of personal past events. Until now, autobiographical memory impairments have been characterized using formal memory assessments, requiring patients to strategically and deliberately recall past events. However, contrary to this highly cognitively demanding mode of memory recall, autobiographical memories frequently come to mind unexpectedly based on automatic associative processes. The involuntary recall of personal memories is effortless and possibly represents a preserved way for AD patients to remember past events.
Objective:
This study aimed to investigate involuntary autobiographical memory in AD patients and compare the characteristics of these memories with those of healthy controls.
Methods:
Involuntary autobiographical memory was measured in 24 AD patients and 24 matched control participants using self-report measures. Participants were asked to report the frequency with which involuntary autobiographical memories were experienced in their daily life and to describe and self-assess one example of an involuntary memory.
Results:
We showed that AD patients and control participants did not differ in terms of the frequency or subjective characteristics of their involuntary autobiographical memories in daily life, except for feelings of intrusiveness. Compared to control participants, AD patients reported their involuntary autobiographical memories as being more intrusive. In addition, more negative and vague involuntary autobiographical memories were associated with greater depressive symptoms.
Conclusions:
These findings open up a new avenue for research to better understand the extent to which involuntary autobiographical memory might be preserved in AD patients and why these memories may in turn become intrusive to patients.
INTRODUCTION
The loss of autobiographical memory (i.e., the memory of personal experiences and facts) 1 is the hallmark of Alzheimer’s disease (AD). 2 Until now, autobiographical memory impairments have been characterized using formal memory assessments, in which patients are asked to remember past events in response to tests or probing questions. 2 This corresponds to a strategic and highly cognitively demanding mode of memory recall resulting from a consciously and deliberately initiated retrieval process. 3 Evidence suggests that executive deficits in AD patients may impair the ability to access memories voluntarily, affecting controlled search processes. 4
In contrast to this voluntary mode of recall, involuntary retrieval of past personal events is at least as frequent in everyday life. 5 Involuntary autobiographical memories are mental representations of personally experienced past events that come to mind unexpectedly, that is, with no preceding attempt to recall them.5,6, 5,6 Involuntary retrieval is based on associative processes that connect the current (inner and outer) situation with features of personal memories. 6 These processes are automatic and beyond cognitive control. 7 As it is relatively effortless and based on associative processes, involuntary recall represents a possibly preserved way for AD patients to remember past events, bypassing the cognitive alterations that characterize these patients. It implies that persons with AD may experience more memories than they have the ability to effectively convey to caregivers and family members or during formal memory testing. Involuntary autobiographical memories have been overlooked, if not ignored, in AD patients, while the literature strongly suggests interest in investigating involuntary recall in these patients.
First, research on mind-wandering (i.e., the tendency to withdraw from the immediate external environment to intentionally or unintentionally generate internally driven thoughts, including memories 8 ) in AD patients showed mixed results concerning its occurrence, probably resulting from different measurement methods (e.g., self-reports or experimental elicitation). While AD patients self-reported higher frequencies of intentional and unintentional mind-wandering than did control participants, 9 persons with amnestic mild cognitive impairment reported fewer spontaneous thoughts than did control participants during a vigilance task (an experimental elicitation of mind-wandering), particularly past-oriented thoughts. 10 Mind-wandering was also self-reported as more negative and more oriented toward the past but less vivid and specific by AD patients than control participants. 11 These results suggest the involuntary emergence of memories in AD patients, which has not been investigated thus far.
Second, previous research on autobiographical memory suggested that providing AD patients with situational and sensory cues (during a memory task) may facilitate autobiographical recall, probably enhancing associative processes. When AD patients are asked to remember personal events, cueing them with music— in particular, music of personal significance to the rememberer— or odor improved the voluntary recall of autobiographical events.12–14 Interestingly, the music- or odor-cued memories were retrieved faster, suggesting that specific sensory cues may have engaged less effortful (or more spontaneous) retrieval. Recently, Rasmussen and colleagues 15 showed that after viewing nostalgia-inducing videos, AD patients expressed more involuntary autobiographical memories and emotional reactions— with greater physiological reactivity— than control participants. These results provide the first evidence that AD patients frequently engage in involuntary remembering when viewing movie content dated from their youth.
Third, while involuntary autobiographical memory corresponds to a basic and adaptive mode of remembering, intrusive involuntary memories are described in clinical populations and are a central characteristic of posttraumatic stress disorder (PTSD). 16 Intrusive memories are described as a dysfunctional side-effect of the normally functional involuntary memory mechanisms when applied to stressful events in vulnerable populations. 17 Several single-case reports described AD patients who experienced intrusions of past— often traumatic— events, possibly leading to the emergence of anxiety symptoms and late-onset PTSD. 18 In a series of cases, Johnston 19 reported that each episode of aggressive behavior in AD patients was precipitated by the presence of an environmental trigger, possibly eliciting intrusive memories. These triggers include reminders of past traumatic experiences, such as television coverage, flowers, loud noises, seeing others in distress, being in an institutional environment, and interpersonal behaviors with caregivers who exert authority or control.19–22 Involuntary memories are associated with greater emotional impact23–25 and greater emotion regulation (e.g., suppression of emotion expression) than autobiographical memories retrieved in a controlled and voluntary manner. 26 Although normally adaptive, or at least benign, involuntary autobiographical remembering can be a source of distress, as observed in relation to PTSD. In PTSD, the traumatic event is “persistently re-experienced” in terms of, among other things, “recurrent and intrusive distressing recollections of the event”. 27
Taken together, the literature suggests that involuntary recall of personal past events occurs in AD patients and might persist longer than voluntary recall. However, along with the hypothetical spared involuntary memories in AD, intrusive memories may be experienced, as reported in multiple case studies of AD patients.
For the first time, the present study aimed to investigate the extent to which AD patients experience involuntary autobiographical memories in their daily lives and the nature of these involuntary memories using self-report measures. Investigating involuntary memories in AD patients consists of examining what these patients still remember from their personal lives, despite the neurodegenerative disorder. This approach represents a shift in the investigation of memory in AD patients, moving from a strong focus on what is lost, impaired or dysfunctional toward an exploration of a preserved way to remember past events.
Based on the above presented findings, we hypothesized that involuntary autobiographical memories would be more frequent in AD patients’ and control participants’ daily lives and that AD patients’ involuntary memories would be more intrusive and associated with more emotional impact at retrieval than would those of control participants.
METHODS
Participants
Twenty-four patients with mild AD (17 women and seven men) and 24 control participants (18 women and six men) were included in the present study. AD participants were recruited from local retirement homes and had received a probable AD diagnosis by a neurologist or a geriatrician based on the National Institute of Aging-Alzheimer Association criteria. 28 Control participants were recruited from the same retirement home and were matched on living place, sex and education level (Table 1). None of the control participants presented a history of psychiatric or neurological diagnosis. All participants were native French speakers. Participants with auditory or visual correction were included in the present study. All participants provided written informed consent, were free to participate and could stop the study whenever they wanted. The study was approved by the Research Ethics Committee of the University of Lille (reference number 2021-545-S99) and was done in accord with the Helsinki Declaration of 1975.
AD patients and control participants demographic information, clinical and cognitive measures
GDS, Geriatric Depression Scale; MMSE, Mini-Mental State Examination. #p < 0.10; *p < 0.05; **p < 0.01; ***p < 0.01.
The number of participants included in the present study was based on previous studies showing autobiographical memory alterations in AD patients.12,15,29–31, 12,15,29–31
Clinical and neuropsychological measures
General cognitive functioning was measured using the Mini-Mental State Examination (MMSE). 32 In addition, a short battery of neuropsychological tests was conducted to assess inhibition using the Victoria Stroop test, 33 for which we considered the interference time; mental flexibility using the Trail-Making Test (TMT), 34 for which we considered the shifting time (TMT B-A); short-term memory and working memory using the digit span subtest of the WAIS-IV, 35 for which we considered the number of correct answers. Participants were also assessed for phonemic (letter P) and semantic (animal category) verbal fluency. 36 For both fluency tasks, the score was the number of correctly generated words.
Participants were also screened for depressive symptoms using the Geriatric Depression Scale. 37 The self-report scale consists of 15 items that can be answered with a yes or no response in reference to how a respondent felt over the past week. Higher scores are indicative of depression, with scores less than 5 considered to be within the normal range.
Involuntary autobiographical memory measures
Involuntary autobiographical memory inventory (IAMI). 38 An adapted version of the IAMI was used to measure the frequency of involuntary autobiographical memories experienced in daily life. The IAMI consists of two subscales— one for measuring involuntary memories and one aimed at evaluating the frequency of involuntary future thoughts. In the present study, only the past-directed subscale was used (i.e., 10 questions). After explaining what an involuntary autobiographical memory is, presenting several examples and ensuring that the participants understood, they were presented with the subscale describing various daily life situations to evaluate the occurrence of involuntary autobiographical memories (e.g., “Listening to some music or songs bring memories of past events to mind— without me consciously trying to remember them”; “When I am bored, memories of past events come to my mind by themselves— without me consciously trying to remember them”).
Each item is rated as 0 (never), 1 (once a month or more), 2 (once a week or more), 3 (once a day or more), or 4 (once an hour or more). In addition to these initial ratings, two more alternative answers were added: “I experience involuntary memories in this situation but I don’t know how often” and “I don’t know if I experience involuntary memories in this situation”. Considering the difficulties in self-assessing these mental events in patients with AD, possibly suffering from anosognosia,39,40, 39,40 these response options prevented participants from randomly answering the inventory and instead allowed them to report their difficulties in self-assessing involuntary memories. The number of alternative answers was considered for each participant, and the mean frequency scores were calculated based on the remaining self-assessed items.
Involuntary autobiographical memory characteristics. To assess the subjective characteristics of involuntary memories, participants were asked to identify and describe one example of an involuntary autobiographical memory they had experienced in their life.41,42, 41,42 Participants answered a series of questions to characterize the qualities (e.g., temporal distance, vividness, emotion, mood impact, intrusiveness, etc.) of this memory. These questions were derived or modified from previous work.43–45 Table 2 shows the question and the rating scale for each item.
Variable labels, questions and ratings composing the questionnaires for the example of involuntary autobiographical memories
Data analysis
All the statistical analyses were performed using SPSS software (version 26). We first compared demographic information and clinical and cognitive data between the two groups (patients with AD and control participants) using t tests and chi-square tests.
Because the two groups of participants significantly differed in age, a one-way ANCOVA was conducted to determine the statistically significant difference between groups (patients with AD versus control participants) in involuntary autobiographical memory measures controlling for age. Pearson correlations of demographic information, clinical and cognitive measures, and involuntary autobiographical memory measures were performed for all participants.
RESULTS
Clinical and cognitive measures
Descriptive measures and statistics are reported in Table 1. AD patients were significantly older than control participants were t(46)=–3.95, p < 0.001, but did not differ from control participants in terms of gender or education level. Compared with control participants, AD patients had lower general cognitive functioning than control participants, t(46)=6.78, p < 0.001, lower cognitive inhibition, t(46)=–1.91, p = 0.03, lower working memory, t(46)=3.71, p < 0.001, and lower semantic and phonemic verbal fluencies, ts(46)>4.05, p < 0.001. AD patients also tended to report higher scores for depressive symptoms than did control participants, t(46) = –1.42, p = 0.08.
Involuntary autobiographical memory measures
Involuntary autobiographical memory inventory (see Table 3). The mean frequency of involuntary autobiographical memories did not differ between groups after controlling for age F(2,45)=0.06, p = .81. The number of patients with answers of “I experience involuntary memories in this situation but I don’t know how often” and “I don’t know if I experience involuntary memories in this situation” did not differ between AD patients and control participants after controlling for age, Fs(2,45)<1.42, ps > 0.24.
Between-group comparisons using analyses of covariance with age as a covariable
IAMI, Involuntary Autobiographical Memory Inventory. *p<0.05.
Correlations between demographic information, clinical & cognitive measures and involuntary autobiographical memory measures, for all participants grouped together
N = 48. GDS, Geriatric Depression Scale; IAMI, Involuntary Autobiographical Memory Inventory; MMSE, Mini-Mental State Examination. *p < 0.05; **p < 0.01.
Involuntary autobiographical memory characteristics (see Table 3). Seventeen AD patients and 22 control participants were able to report an example of an involuntary memory they experienced. Most of the reported involuntary memories concerned past events that had happened years ago (17 out of 17 participants in the AD group and 21 out of 22 participants in the control group; χ2 = 0.79, p = 0.37). The subjective characteristics of the involuntary autobiographical memories reported and described by participants did not significantly differ between AD patients and control participants, except for intrusiveness, after controlling for age. AD patients reported their involuntary autobiographical memory to be significantly more intrusive than control participants did, F(2,36)=4.96, p = 0.03. The impact of involuntary memories on mood did not differ between groups.
Correlation analyses
We conducted correlation analyses for all participants grouped together. We observed that age was negatively correlated with the mean score of involuntary autobiographical memory frequency, the feeling of reliving, the feeling of intrusiveness and the feeling of control associated with involuntary memories, rs< –0.30, ps < 0.04, and was positively correlated with the emotional intensity of the memories, r = 0.45, p = 0.004.
The presence of depressive symptoms was associated with more negative, r = 0.37, p = 0.02, and less vivid, r=–0.42, p = 0.01, involuntary autobiographical memories.
With regard to cognitive functioning, we observed a few sporadic significant correlations. Higher mental flexibility was associated with more answers of “I experience involuntary memories in this situation but I don’t know how often” in the IAMI and with lower emotional intensity of involuntary memories, rs > 0.43, ps < 0.02. Higher short-term memory performance was associated with greater feelings of reliving, r = 0.43, p = 0.007. The better a participant’s working memory was, the fewer “I don’t know if I experience involuntary memories in this situation” answers they provided on the IAMI, and the more positive their involuntary memories were, rs< –0.31, ps < 0.04. A higher semantic verbal fluency was related to a greater frequency of involuntary memories, a greater feeling of reliving, rs > 0.35, ps < 0.02, a lower emotional intensity and fewer “I do not know if I experience involuntary memories in this situation” answers on the IAMI, rs< –0.34, ps < 0.03. Higher phonemic verbal fluency was associated with greater emotional intensity, r=–0.33, p = 0.04, and greater feelings of reliving, r = 0.32, p = 0.05.
DISCUSSION
The present study assessed for the first time how AD patients involuntarily remember personal past events in their daily lives using self-report measures. In the present sample of participants, AD patients and control participants did not differ in terms of the frequency or subjective characteristics of their involuntary autobiographical memories in daily life, except for the feeling of intrusiveness. AD patients reported their involuntary autobiographical memories as being more intrusive than did control participants. In addition, in the whole sample of participants, we observed that more negative and vague involuntary autobiographical memories were associated with greater depressive symptoms. The characteristics of involuntary remembering were not related to general cognitive functioning but were sporadically associated with specific cognitive measures.
Loss of memory is the hallmark of AD. Loss of memory is a required symptom for diagnosis 27 and severely affects the autobiographical memory system. 2 Despite the cognitive impairments characterizing the present sample, the AD patients and control participants did not differ regarding reports of experiencing involuntary autobiographical memories in their daily lives. In contrast to former studies, which have similar or smaller sample sizes and focus on the voluntary and strategic recall of past events,29,30,46–48, 29,30,46–48 the present study was one of the first to investigate what AD patients spontaneously or involuntarily remember from their past and showed that they did not report experiencing significantly fewer involuntary autobiographical memories than control participants did. In addition, the subjective characteristics of involuntary autobiographical memories were not rated differently between the AD and control groups. These results contrast with those of former studies highlighting alterations in the subjective recollection— in terms of vividness and reliving— of voluntary autobiographical memories in AD patients, also using self-reports.30,31,47, 30,31,47 These results are particularly interesting because they allow us to envisage that involuntary autobiographical memories are preserved longer in AD patients. These findings align with those of Rasmussen and colleagues, 15 who showed that AD patients expressed more spontaneous autobiographical memories after watching a nostalgic movie than did control participants. Together, these recent findings open a new avenue for research on the involuntary retrieval of past events in AD patients, which has been ignored until recently. As mentioned in the introduction, involuntary autobiographical memory represents a direct route toward memories of one’s past, beyond one’s control or will, and might therefore represent a way for AD patients to bypass cognitive alterations and to continue mentally traveling back in time.
Although AD patients did not report experiencing more involuntary autobiographical memories in their daily life than control participants in the present study, the feeling of intrusiveness associated with their memories was significantly higher. AD patients reported their involuntary autobiographical memories as being more intrusive than did control participants. However, contrary to our hypothesis, involuntary memories did not impact mood in AD patients differently than in controls. The greater feeling of intrusiveness in AD patients might be explained by impaired cognitive control and, in particular, a failure of cognitive inhibition, preventing patients from regulating their memories.49,50, 49,50 However, in the present study, no correlations were observed between feelings of intrusiveness and cognitive functioning. In line with this result, El Haj and colleagues showed that difficulty in suppressing memory in AD patients was correlated with the presence of hallucinations. 51 If involuntary autobiographical memory represents an enhanced way for AD patients to recall past events, contrast with voluntary autobiographical memory alterations might also foster the feeling of intrusiveness associated with the spontaneous recollection of past events.
This study has several limitations. The main weakness of the study is the difference in age between the AD patients and control participants. However, it is noteworthy that the age difference was controlled for in the statistical analyses. This difference is partly explained by the other control participants recruitment criteria and strengths of the study. More precisely, control participants were matched with AD patients on the living conditions and were then recruited from the same nursing home as AD patients were. Also, any control participants with psychiatric or neurological disorders were excluded. These recruitment criteria represent important strengths of the present study. The use of self-report measures might also be considered a weakness of the present study. Although AD patients presented mild cognitive impairments and possibly metacognition dysfunction, as described in the literature, 40 they did not report more alternative answers on the IAMI— reflecting difficulties in assessing involuntary memories— than did control participants. We also believe that grasping the subjective experience of AD patients using self-report measures is crucial in the investigation of preserved memories. Finally, we used a retrospective method to assess the characteristics of involuntary autobiographical memory. This method requires participants to voluntarily retrieve experiences of having involuntary memories, which might be more challenging for AD patients than control participants. Future investigations of involuntary autobiographical memory in AD should include other methods, such as external observations and assessments, to replicate and extend the present findings.
Building upon recent findings on involuntary autobiographical memories in AD patients, further research is needed. First, involuntary autobiographical memories should be compared to voluntarily retrieved memories to understand the extent to which the former are preserved in AD patients. Second, this investigation should be conducted at different stages of the disease to highlight the course of involuntary memories in AD patients. Third, given the strong link between autobiographical memory alterations and identity impairments in AD, 48 the preservation of involuntary retrieval of past events might help maintain a sense of identity for a longer period in AD patients. Although involuntary autobiographical memories are generally described as more mundane and less central to the self, compared to their voluntary counterparts, 5 they still enable individuals to mentally travel back in time, reexperiencing personal events and thus reconnecting with their past selves. The relationship between involuntary autobiographical memories and the sense of personal continuity in AD patients remains to be explored.
In conclusion, the present study showed for the first time that AD patients, who present inherent memory alterations, experience involuntary autobiographical memories no differently than control participants in their daily lives. The involuntary memories reported by AD patients did not differ from those reported by control participants except for the feeling of intrusiveness. These findings open up a new avenue for research to better understand the extent to which involuntary autobiographical memory might be preserved in AD patients and why these memories may in turn become intrusive to patients. The outcome of this investigation will have clinical implications. First, it will enable the development of new psychological interventions that support the elicitation of involuntary autobiographical memories, using sensory cues, for instance, and facilitate their maintenance and elaboration into consciousness. Second, it will also enhance the understanding and management of psychological and behavioral reactions associated with the involuntary occurrence of memories, particularly when they are intrusive. Identifying profiles of patients who are more at risk for experiencing intrusive memories can help professionals anticipate their occurrence and assist patients in coping with these memories, such as through emotion regulation strategies.
AUTHOR CONTRIBUTIONS
Mélissa C. Allé (Conceptualization; Formal analysis; Methodology; Project administration; Writing – original draft; Writing – review & editing); Christelle Joseph (Resources; Writing – review & editing); Pascal Antoine (Methodology; Resources; Writing – review & editing).
Footnotes
ACKNOWLEDGMENTS
We extend our sincere gratitude to all the nursing homes from the GCMS Grand Lille that participated in the present research project. In particular, we would like to express our appreciation to Dr. Cédric Barbe, Hervé Titeca, Caroline Ruget, and Aurélie Daniel for their invaluable contributions, which made this study possible.
FUNDING
The authors have no funding to report.
CONFLICT OF INTEREST
The authors have no conflict of interest to report.
DATA AVAILABILITY
The data supporting the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
