Phenomenological Reliving and Visual Imagery During Autobiographical Recall in Alzheimer’s Disease

INTRODUCTION

There is a substantial body of literature documenting impaired autobiographical memory in Alzheimer’s disease (AD), an impairment that compromises social interactions [1], sense of identity [2], and phenomenological experience or the ability to relive past events [3–6] (for a review, see [7]). Previous studies evaluated autobiographical memory through several protocols. For instance, Addis and Tippett [2] assessed autobiographical memory in individuals with AD with the Autobiographical Fluency task [8], a task assessing their ability to retrieve general and specific autobiographical memories. For general autobiographical memories, participants had 90 s to produce as many names of people known to them as possible, whereas, for specific autobiographical memories, participants had 90 s to produce as many personally experienced events as possible. Besides the Autobiographical Fluency task, Addis and Tippett [2] administered the Autobiographical Memory Interview on which the participants had to recall general autobiographical facts (e.g., name of secondary school) and specific autobiographical facts [9]. Retrieval of specific autobiographical facts was evaluated with a scale ranging from zero to three points and high scores referred to specific events situated in time and space. Through this assessment process, Addis and Tippett [2] found decline of autobiographical recall in AD participants, especially, for retrieval of specific details. Mirroring these findings, reduced autobiographical specificity in AD was observed by other researchers who also administered the Autobiographical Memory Interview [10].

The decline of autobiographical specificity, as observed in individuals with AD, was reported by several studies using autobiographical assessment tools other than the Autobiographical Fluency task or the Autobiographical Memory Interview. For instance, Moses et al. [11] assessed autobiographical recall of individuals with AD with the Autobiographical Memory Test of Williams and Broadbent [12], in which as event is coded as specific if it occurs in less than a day. With this scoring system, Moses et al. [11] found fewer specific autobiographical memories in AD participants than in healthy older adults, indicating overgenerality of autobiographical recall in AD. In the same vein, reduced autobiographical specificity was reported by Irish et al. [13] who used the Autobiographical Interview [14]. On this task, individuals with AD had to retrieve detailed autobiographical events and each event was analyzed according to its spatiotemporal specificity and phenomenological relevance, a concept referring to details describing emotion and thoughts. With this scale, Irish et al. [13] observed significant disruption of autobiographical specificity and phenomenological reliving in AD. The present study expands upon this finding by investigating the nature of phenomenological decline in AD.

Phenomenological reliving, as triggered by retrieval of specific details, refers to re-experiencing past events and mentally travelling back in subjective time, a state that is termed autonoetic consciousness [15]. This subjective experience is critically involved in episodic recall and can be contrasted with noetic consciousness, or awareness of general information in the absence of any recollection, which is involved in semantic recall [15]. The distinction can be evaluated with the Remember–Know paradigm in which a “Remember” response can be provided when subjects succeed in recalling a specific event with the presence of phenomenological details (e.g., feelings, emotion, perceptions); by contrast, a “Know” response can be provided when subjects relive a feeling of familiarity without specific details [16]. Using this paradigm, several investigations found alterations of phenomenological experience in individuals with AD [3–6]. A similar conclusion is drawn by a series of studies employing assessments other than the Remember/Know paradigm. In these studies [5, 17–19], phenomenological experience was assessed with the TEMPau scale (Test épisodique de mémoire du passé [20]). This scales attributes zero points to an absence of memory or only general information, two points to a repeated/extended event if it was situated in time and space or one point if it was not, three points for a specific event with spatiotemporal details and four points if the latter event triggers phenomenological details (e.g., feelings, emotion, perceptions). Taken together, a substantial body of literature supports the hypothesis that the phenomenological experience is disrupted in AD.

Overall, previous studies convincingly demonstrated that autobiographical memory declines in AD but failed to identify specific phenomenological elements and subjective features (e.g., reliving, back in time, remembering, emotion, or spatiotemporal specificity) that are selectively vulnerable in the disease. This shortcoming can be partially addressed with the Autobiographical Memory Interview on which the maximum score (i.e., three points) refers to specific events situated in time and space. Unfortunately, besides providing a comprehensive index of specificity, this scale does not allow assessing specificity characteristics (e.g., special or temporal information) that may be prone to forgetting in AD. The same thing can be said for the TEMPau scale, which offers general evaluation of phenomenological experience without assessing specific phenomenological elements (e.g., back in time, emotion, or perceptions). Finally, in a study by Moses et al. [11] showing overgenerality of autobiographical recall in AD, specificity was based only on event duration and no further phenomenological details were assessed.

In addition, a core phenomenological concept, visual imagery, was barely assessed by these studies. According to Conway [21], autobiographical memories are predominantly represented in the form of visual images. Visual imagery is also considered to be a defining element of the sense of recollection and phenomenological experience of autobiographical recall [22]. In line with this assumption, phenomenological experience was found to be fairly correlated with ratings of visual imagery [23]. Further evidence about the link between visual imagery and autobiographical memory can be found in neurophysiological studies, showing activation in occipital lobes during autobiographical retrieval [24, 25], as well as lesion studies, showing that damage to visual cortex leads to autobiographical decline [23]. Therefore, in this study, we decided to evaluate visual imagery in the setting of phenomenological experience of autobiographical recall in AD.

The phenomenological experience, and also visual imagery, during autobiographical recall in AD was evaluated by Irish and colleagues [26] who asked AD participants to rate their subjective autobiographical experience along the following dimensions: vividness (i.e., when you recall this event how would you describe it in terms of vividness?), viewer perspective (i.e., “are you viewing the scene through your own eyes or can you see yourself in the memory from a third-person perspective?), continuity of accompanying imagery (i.e., do you visualize the event as a continuous video that plays with no breaks or like a set of snapshots with no movement?), rehearsal (i.e., how often would you estimate you have thought/spoken about this memory since it first occurred?), emotional re-experience (i.e., do you re-experience any of the emotion you originally felt at the time?), mental time travel (i.e., Would you say you are reliving this memory or looking back on it?”), and overall re-experience (i.e., To what extent are you re-experiencing this memory as a percentage?). Results showed a compromised capacity to mentally relive past memories as well as an impoverished visual imagery in AD.

The study of Irish and colleague [26] is of crucial interest. It, however, misses some crucial phenomenological features such as realness, auditory imagery, importance, and sense of remembering. The aim of the present study was to test these phenomenological features, as well as those tested by Irish and colleague [26] in a cohort of participants with mild AD compared to controls. Based on the reviewed literature, we hypothesized that individuals with AD would show poorer phenomenological experience, with especially poor visual imagery.

METHODS

RESULTS

We first compared differences on general autobiographical performance as assessed with the TEMPau scale. We then compared differences on phenomenological characteristics between AD participants and older adults and within each population. Due to the scale nature of variables and their abnormal distribution, non-parametrical tests were conducted. Between groups comparisons were performed using Mann-Whitney’s U test and within groups comparisons were performed using Wilcoxon signed rank test.

DISCUSSION

Our study aimed to assess the nature of phenomenological impairment that underlies the autobiographical decline in AD. When asked to retrieve autobiographical events, AD participants showed poorer autobiographical recall than controls. The phenomenological experience of AD participants was characterized by poorer reliving, travel in time, remembering, realness, visual imagery, auditory imagery, language, rehearsal, spatial details, and temporal details than controls, a decline that was especially pronounced for visual imagery. Yet, in a contradictory manner, AD participants showed higher ratings for emotion and importance.

Reduced autobiographical memory in AD has been the subject of considerable study (for a review, see [7]). However, beyond documenting declines in general autobiographical recall and autobiographical specificity, this body of literature has provided a comprehensive rather than piecemeal attempt to investigate phenomenological reliving in individuals with AD. Our work fills this gap by assessing specific features of phenomenological experience, thanks to the Autobiographical Memory Questionnaire. Using this instrument, we were able to observe low reliving for some phenomenological features and, interestingly, high reliving for other phenomenological features in AD.

Regarding phenomenological features, our AD participants showed low rating for visual imagery, a defining element of the sense of recollection and phenomenological experience. Indeed, it has been widely suggested that autobiographical memories are dominated by visual imagery and that the retrieval of visual images is the core feature of autobiographical reliving [22, 37]. In line with this idea, a study has shown poor autobiographical recall in healthy young participants with low ability to generate pictorial mental images of objects [38]. Neuropsychological studies have also shown that lesions resulting in a loss of the ability to generate visual images also result in retrograde amnesia [39–41]. For instance, Greenberg et al. [40] reported the case of a patient with damage in the right occipital lobe along with the occipitotemporal junction who demonstrated difficulty generating visual images, as well as retrograde amnesia. In addition, neuroimaging studies have shown activation of visual brain areas during autobiographical recall (for a review, see [42]). Moreover, there is evidence of low autobiographical recall in blind individuals [43]. These findings suggest visual processing as a core component of phenomenological reliving during autobiographical recall. As for AD, Irish and colleague [26] found that whereas younger adults reported viewing their autobiographical memories as a continuous video, the AD group reported imagery resembling static snapshots akin to photographs or hazy imagery and lacking a real-life three-dimensional quality. In our view, any decrease in the ability to generate visual images, as in the case of its poor rating in our AD participants, may compromise autobiographical recall and its phenomenological experience. A limited ability to generate and manipulate visual images may deprive individuals with AD of the function is most needed in integrating the components of autobiographical experience into a whole coherent event.

The compromise of ability to generate visual image, as reported by our AD participants, can be understood by considering previous research on “visual” and “spatial” mental imagery. Although both processes allow generating mental images, visual imagery deals with the representation of visual appearance of objects (e.g., color), whereas spatial imagery deals with manipulating of objects in the space (e.g., rotating objects in the space). A study by Hussey and colleagues [44] assessed visual imagery with the Taller/Wider task [45] and spatial imagery with the Clock Angles test [46]. In the Taller/Wider task, participants had to generate a mental image of an object (e.g., pen) presented as a word and determine whether the object is taller than it is wide. In the Clock Angles test the participants had to imagine the angle created by the hands on a clock, as set to a certain time, and determine whether that angle was <90 degrees. Relatively to controls, AD participants showed similar performance on the Taller/Wider task but lower performance on the Clock Angles test. According to Hussey and colleagues [44], basic visual imagery seems to be spared by AD, unlike spatial imagery that requires heavy executive demand. By this view, the compromise of ability to generate visual image during autobiographical retrieval, as reported by our AD participants, may be attributed to compromise in spatial imagery as the latter ability allows effortful manipulation and integration of visual images into a coherent (autobiographical) scene.

Besides low visual imagery, our AD participants showed low reliving, travel in time, remembering, and realness. These outcomes reflect poor autonoetic consciousness or the ability to experience past events and mentally travel back in subjective time [15]. In line with our findings, several studies have shown decreased autonoetic consciousness in individuals with AD, supporting the idea of a disruption of recollection in AD [3–6]. Another poor-rated phenomenological element in AD participants was auditory imagery. Imagery in modalities other than visual (e.g., auditory) may be present but less common in autobiographical remembering [47]. Poor auditory reliving may also be responsible for the low score for the statement “I or other people are talking”. Another phenomenological feature that was rated low by AD participants was rehearsal. According to Conway [37], repeated retrieval, or rehearsal, serves to shape autobiographical knowledge into patterns of accessibility, improving retrieval and availability of this knowledge. Rehearsal decline, as reported by our AD participants may hence limit the accessibility of autobiographical memories and consequently, their phenomenological relieving. This rehearsal decline may be due to reduction in social contacts, which limits opportunities for memories transmitting and memories telling. Rehearsal decline, as reported by our AD participants, may also be related with linguistic difficulties that limit autobiographical narration. Research demonstrates impoverished linguistic ability in AD, including reliance on conversational fillers (e.g., “well”, “so”, “basically”, “actually”, “um”, “ah”) as well as on non-specific indefinite nouns (e.g., something, anything) and high frequency low-imageability verbs (e.g., get, give, go, have) [48–50]. This linguistic compromise may limit description of autobiographical memories in AD, and consequently, rehearsal of these memories.

Similar to poor ratings for the above-mentioned phenomenological features (i.e., reliving, travel in time, remembering, realness, visual imagery, auditory imagery, language, and rehearsal), our AD participants showed decrease in spatiotemporal details. This is not surprising, since several reports demonstrated poor spatiotemporal recall in AD [10, 52]. Due to their difficulty in retrieving specific spatiotemporal details of the encoding context, individuals with AD may retrieve events based on a feeling of familiarity rather than recollection, which may explain the decrease in autobiographical recall and its phenomenological experience in the disease.

Although showing low experience of many phenomenological features, AD participants demonstrated high ratings for emotion and importance. In a broad manner, studies suggest better recall for emotional information in AD, especially if self-related. In this body of research, Sundstrøm [53] asked AD participants to retain neutral items and emotional self-related items (i.e., gifts to the participants). Better recall was detected for emotional items than for neutral items. Also, Kalenzaga et al. [54] asked AD patients to rate neutral and emotional adjectives describing themselves. Better recall was observed for emotional adjectives than for neutral adjective. Another study reported that AD patients can experience prolonged states of emotion that persist well beyond the patients’ memory for the events that originally caused the emotion [55]. A neuroimaging study in AD has found that whereas general memory performance correlated with the hippocampus, precuneus and posterior cingulate, regions, emotional enhancement of memory was associated exclusively with the integrity of the right orbitofrontal and subcallosal cortex. Together, these outcomes suggest high recall for self-related emotional information in AD, which may explain the high emotional rating for autobiographical, or self-related, events in our participants.

High emotional rating was not only observed in AD participants, but also in control older adults. This finding fits with studies showing high recall for emotional information in normal aging (e.g., [56, 57]). It is noteworthy that the age gap in episodic memory performance can be, somehow, narrowed by emotion [58]. However, and unlike AD participants, older adults showed high visual imagery ratings. This is not surprising, since, unlike AD participants, older adults demonstrated substantial autobiographical specificity, as assessed with the TEMPau scale.

Although our interpretation of the findings draws heavily on visual imagery, we caution the reader that this phenomenological aspect was only assessed with one item. Future studies should further investigate its involvement with a variety of tasks assessing visual imagery, as well as spatial ability, an ability that could be evaluated with the spatial subscale of the Survey of Autobiographical Memory [59]. The absence of spatial ability assessment may be considered as a crucial shortcoming for our visual imagery hypothesis. It is of note, however, that we controlled for visual acuity by including only participants with reported corrected-to-normal vision and excluding those with major visual impairments.

To summarize, individuals with AD have been found to show difficulties on both specificity and phenomenological reliving. The present study contributes to these findings by highlighting decreases in many phenomenological features, but also preservation of some other features.