Relationships Between Confabulations and Mental Time Travel in Alzheimer’s Disease

Confabulations can be defined as fictitious memories without the intent to deceive.^1,2 These memories can be entirely or substantially erroneous, or they can simply refer to real memories jumbled up and retrieved out of context.² Confabulations typically arise unintentionally, and the patient is usually unaware of their erroneous nature.² Experimental research and theoretical analyses have attempted to explain the underlying cognitive mechanisms involved in confabulations. However, there appears to be no consensus regarding the causes of confabulations or even their classifications and definition.^2–6 This lack of consensus about mechanisms that may underlie confabulations can also be extended to confabulations in Alzheimer’s disease.

Although research has succeeded in providing support for the occurrence of confabulations in the disease, it has not attained a consensus about their cognitive underpinnings. In a pioneering study, Kern et al.⁷ asked patients with Alzheimer’s disease to remember previously processed stories, and confabulations were observed that were defined as novel intrusions (i.e., elements that were not included in the original story). They observed a high level of confabulations in AD; however, the presence of confabulations was not significantly correlated with performances on tests of executive function. A similar observation was reported by Dalla Barba et al.,⁸ who assessed confabulations with the Confabulatory Interview,⁹ consisting of questions tapping general personal knowledge, specific personal memories, knowledge of famous facts and famous people, and personal future plans. In this study, confabulations were referred to answers that were inconsistent with the patients’ past, present, and future. Using this battery, they observed a high level of confabulations in Alzheimer’s disease. However, confabulations were not significantly correlated with tests of executive function. Similar findings were reported by Nedjam et al.,¹⁰ who did not observe significant correlations between performance on executive tasks and the tendency to produce confabulations in a group of patients with Alzheimer’s disease (see reference¹¹).

The above-mentioned research has mainly been concerned with the cognitive underpinnings of provoked confabulations (i.e., confabulations that are produced when the subject is directly questioned). El Haj and Larøi¹² assessed the cognitive underpinnings related to spontaneous confabulations (i.e., context-free, unprovoked confabulations). More specifically, provoked confabulations were assessed using an evaluation proposed by Dalla Barba and colleagues^9,13 and spontaneous confabulations were rated by nursing and medical staff. Results showed that both provoked and spontaneous confabulations were significantly correlated with general cognitive functioning as assessed with the Mini-Mental State Examination (MMSE).¹⁴ These findings mirror previous studies suggesting a relationship between provoked confabulations and general cognitive functioning.^15,16

Although research has succeeded at providing support for the occurrence of provoked and spontaneous confabulations in Alzheimer’s disease, there is no consensus regarding their cognitive underpinnings. One of the most often invoked hypotheses of confabulations in Alzheimer’s disease is the executive account, although this hypothesis has its origins specifically as an account of confabulations in patients with frontal lobe lesions.¹⁷ This hypothesis also stems from the observation that executive functions may recover in parallel with a decrease in confabulations in these patients.¹⁸ However, other studies suggest that amnesic patients with confabulations do not differ from nonconfabulating amnesic patients with regard to executive functions.^3,19,20 As for Alzheimer’s, studies suggest a lack of a relationship between confabulations and executive function.^8,11

Another cognitive account of confabulations in Alzheimer’s maintains that they are related to an impairment in general cognitive functioning. Although this account has been supported by research demonstrating significant correlations between confabulations and general cognitive functioning in AD,^14,21 it does not highlight specific cognitive mechanisms that may underlie confabulations. To address this issue, we investigated the specific cognitive mechanisms that may be related to confabulations in Alzheimer’s. Specifically, the aim was to examine whether confabulations would be related to patients’ difficulty to mentally project themselves back in time to retrieve the context in which confabulated memories were originally encoded.

The hypothesis that there is a relationship between confabulations and the ability to mentally travel in time to retrieve the context in which memories were encoded can be supported by the temporal consciousness model.¹³ According to this model, patients with confabulations have a disturbed sense of chronology, in that they are able to retrieve the content of events but not their order of occurrence. Consequently, they misattribute features of events that occurred at one time to other events that occurred at another time. In a similar vein, both the temporal confusion hypothesis²⁰ and the temporal context hypothesis^21,22 suggest that confabulators use information that may have been relevant in a previous event, but this information is interjected in a current event when it is no longer relevant or appropriate. These hypotheses can be supported by studies whereby patients with confabulations are asked to identify pictures to which they were previously exposed^4,19,23; patients are then presented with the same set of pictures arranged in a different order and are asked to forget what they had seen during the initial exposure and to indicate which of the pictures recurred in the second run. Results from these studies have demonstrated that patients fail to suppress the memory of what they had seen in the first set of pictures presented, resulting in high rates of false responses. Schnider et al.²⁴ found that recovery from confabulations was associated with recovery from temporal confusions in memory. Later research also found that temporal context confusion distinguishes amnesics with confabulations from those without confabulations.^3,25 A similar suggestion was made by Schnider et al.²⁰ who carried out two runs of a continuous recognition memory test in patients with confabulations. During the second run, previous distractors became targets and targets became distractors in order to provoke false recognition (i.e., confabulations). Results demonstrated false recognition in patients with confabulations in the second run of this test. Using similar procedures, Gilboa et al.²⁶ placed emphasis upon deficits in preconscious, postretrieval monitoring of responses, giving rise to confabulation. Together, the temporal consciousness model, the temporal confusion hypothesis, and the temporal context hypothesis relate confabulations to difficulties in remembering the context in which information was previously encountered. However, these accounts have never been previously tested in patients with Alzheimer’s disease. Furthermore, these accounts do not sufficiently emphasize the ability to mentally project oneself in time in order to retrieve the context of a memory.

In order to assess the relationship between confabulations in Alzheimer’s and the ability to mentally project oneself in time to retrieve the context of memories, our study used the remember/know paradigm. In this paradigm, participants are asked to provide a “remember” response if they are able to retrieve a specific event with its encoding context, or a “know” response if they just know that the event has occurred to them but cannot recall any contextual details.^27,28 In this paradigm, “remember” responses are considered to reflect autonoetic consciousness (i.e., the subjective experience when memories are consciously recalled through a process of mentally reliving them). By contrast, “know” responses are considered to reflect noetic consciousness (i.e., the general feeling of knowing or familiarity). Using this paradigm, several studies have shown that individuals with Alzheimer’s disease demonstrate a difficulty in projecting themselves mentally back in time to the context in which memories were encoded and in retrieving the relevant information accurately.^29–35

To summarize, the aim of the present study was to highlight specific cognitive mechanisms that may be related to confabulations in Alzheimer’s. In our view, confabulations in individuals with Alzheimer’s disease are related to difficulties in mentally projecting themselves back in time in order to retrieve the context in which memories were encoded, a difficulty that results in an activation of irrelevant memories at the expense of relevant ones during retrieval (i.e., confabulations). To test our hypothesis, we investigated the relationship between the performance of patients with Alzheimer’s disease on the remember/know paradigm and provoked and spontaneous confabulations.

Methods

Participants

The study included 27 participants (Table 1). An inclusion criterion was a clinical diagnosis of probable Alzheimer’s disease (moderate stage). All participants were living in retirement homes and were diagnosed with probable Alzheimer’s dementia (amnestic presentation) by an experienced neurologist or geriatrician based on the National Institute on Aging–Alzheimer’s Association diagnostic guidelines for Alzheimer’s disease.³⁶ More specifically, diagnosis was made based on biomarkers of brain amyloid-beta (Aβ) protein deposition. Diagnosis was also made based on neuropsychological evaluations of general cognitive functioning, episodic memory, and executive functions. Exclusion criteria were significant neurological/psychiatric illness, aphasia, and substance use disorders as defined in the DSM-5.³⁷ A history of neurological/psychiatric disorders was evaluated by examining the patients’ medical files, if available; in addition, the patients, family members, and caregivers were questioned about the presence of neurological/psychiatric symptoms during the patient’s lifetime (e.g., presence of hallucinations). As for aphasia, we excluded patients whose language impairment was severe enough so that they either could not understand the task instructions or could not perform the tasks. None of the participants presented any major visual or auditory acuity difficulties that would have prevented completion of the tasks. Based upon these exclusion criteria, two participants were excluded from the original sample due to major visual acuity difficulties, eight participants were excluded due to a history of neurological disorders, five participants were excluded due to a history of neurological disorders, and two participants were excluded due to linguistic difficulties. Thus, the final sample consisted of 27 participants. All participants provided written informed consent and were able to withdraw whenever they wished. The present study complied with the Declaration of Helsinki.

Cognitive Measures

Participants were administered tests of general cognitive functioning, episodic memory, and working memory. General cognitive functioning was assessed with the MMSE, with a maximum total score of 30 points. Episodic memory was assessed with the episodic task of Grober and Buschke³⁸ in which participants were presented with the names of 16 items, each belonging to a different semantic category. After immediate cued recall, participants underwent a distraction phase in which they had to count backward by one from 374 for 20 seconds. This phase was immediately followed by a free recall phase lasting 2 minutes. The score on the latter phase was retained as a measure of episodic recall.¹⁶ Executive control of working memory was assessed with a task that is quick and easy to administer (i.e., digit spans), during which participants had to repeat a string of single digits in the same order (forward span) or in the inverse order (backward span). The number of correctly repeated digits was calculated.

Procedures

Provoked confabulations.

Provoked confabulations were assessed with the Confabulation Battery.³⁹ This interview includes 10 questions concerning personal semantic memory, 10 questions on episodic memory, 10 general semantic memory questions (e.g., “What is the capital of the United Kingdom?”) and 10 distractor questions. Questions on personal semantic memory assessed general personal facts, such as the participant’s name and date and place of birth. Episodic memory questions assessed previously experienced autobiographical events. Distractors were questions that were logically coherent but referred to concepts or situations not based in reality (e.g., “Who is the Italian king?” [NB: Italy is a republic, not a monarchy]). Thus, the appropriate response to these questions would be “I don’t know” or “There is no monarchy in Italy.” Participants were reassured prior to the interview that no person is able to remember all aspects of her/his life; thus, they should only answer the questions if they were completely convinced that their answers were right. Otherwise they should answer “I don’t know.” Whenever participants provided wrong answers on the distractor questions, they were asked once again whether they were certain about their response. If they were uncertain, they were encouraged to retract their response. Answers were scored as “correct,” “wrong,” or “confabulation,” with reference to information collected from relatives and caregivers. Minor distortions between responses provided by participants and those provided by informants were considered errors, whereas major discrepancies were considered confabulations. All confabulations were summed up to constitute a total confabulation score. The maximum confabulation score was 40 points.

Spontaneous confabulations.

Unlike provoked confabulations, spontaneous confabulations are difficult to assess in an interview because an interviewer can never be sure whether he or she provoked a confabulation in some way. Thus, spontaneous confabulations were evaluated based on observations by physicians and the nursing staff in the retirement homes where the Alzheimer’s participants were recruited. Procedures were based on previous studies on spontaneous confabulations in patients with Korsakoff’s syndrome or severe amnesia.^19,40 More specifically, the nursing and medical staff were provided with the following definition of spontaneous confabulation behavior, a definition provided by Kessels et al.⁴⁰:

Remember/know.

This task was based on procedures described by Rauchs et al.³¹ Participants were asked to “recount a family event in detail,” “recount a professional event in detail,” and “recount a holiday event in detail.” These three cues (i.e., family, profession, and holiday), counterbalanced across participants, were chosen because they tend to elicit autobiographical memories in participants with Alzheimer’s.⁴¹ Participants were instructed to be precise and specific, so that events had to have lasted no more than a day and spatiotemporal details, such as the time and place at which the events had occurred, had to be provided. Participants were allowed 3 minutes to describe their memories, and the duration was made clear to them so that they could structure their memories accordingly. These instructions and the time limit were adopted to avoid redundancy or distractibility and has previously been found to be sufficient for autobiographical recollection in individuals with Alzheimer’s.^33,42,43 Following each memory, participants were asked to indicate whether or not they could consciously recollect its prior occurrence by making separate remember/know judgments. More specifically, and after each memory, participants were provided with the following instructions:²⁸ “If the event implies a specific place and time, as well as specific feelings, thoughts, or emotions, then you must provide a remember answer. If the event is retrieved without involving such specific information, then you must provide a know answer.” In accordance with the procedures described in Rauchs et al.,³¹ we counted the number of “remember” and “know” responses, with the maximum score being 3.

Statistical Analysis

Means and standard deviations of participants on the assessments of provoked and spontaneous confabulations are summarized in Table 2, in addition to the number of “remember” and “know” responses. Because we expected a relationship between the performance of Alzheimer’s patients on the remember/know paradigm and provoked and spontaneous confabulations, we carried out correlations between both types of confabulations and remember/know responses. Correlations were conducted after controlling for age and educational level.

Results

As presented in Table 3, analyses showed significant negative correlations between provoked confabulations and “remember” responses, whereas significant positive correlations were observed between provoked confabulations and “know” responses. Analyses also showed significant negative correlations between spontaneous confabulations and “remember” responses, whereas significant positive correlations were observed between spontaneous confabulations and “know” responses.

Additional Analyses

For convenience, we assessed correlations between confabulations and episodic memory and the central executive of working memory. No significant correlations were observed between provoked/spontaneous confabulations and these cognitive abilities. However, significant negative correlations were observed between provoked confabulations and MMSE score (r=–0.41, p<0.05) and spontaneous confabulations and MMSE score (r=–0.57, p<0.01).

Discussion

This study examined the relationship between confabulations in patients with Alzheimer’s disease and their ability to project themselves in time to retrieve the context in which memories were encoded. Using the remember/know paradigm, significant negative correlations between provoked and spontaneous confabulations and “remember” responses were observed, as well as significant positive correlations between provoked and spontaneous confabulations and “know” responses. In other words, the more the Alzheimer’s patients produced confabulations, the less they were able to project themselves in time in order to reexperience past events.

Research has succeeded in providing support for the occurrence of confabulations in Alzheimer’s disease. Research has also demonstrated a relationship between confabulations and general functioning in Alzheimer’s.^12,15 However, little is known about the specific cognitive underpinnings of confabulations in the disease. Our study addressed this issue by highlighting the relationships between occurrence of confabulations and difficulties in autonoetic consciousness in Alzheimer’s. More specifically, our Alzheimer’s participants showed significant correlations between provoked and spontaneous confabulations and remember/know responses.

The remember/know paradigm has been widely used to evaluate the subjective experience of memory, with “remember” responses assumed to index conscious recollection and “know” responses assumed to index familiarity.²⁸ By this account, unlike “know” responses, “remember” responses have been considered to reflect the recollection of information about the encoding context of an event, such its spatiotemporal characteristics, the vividness of its visual imagery, or its elicited emotions.²⁸ Using the remember/know paradigm, studies have demonstrated an impaired ability in Alzheimer’s disease to consciously recollect information about the context in which a unique episode took place.^29–34,44 Furthermore, studies have demonstrated a substantial shift from autonoetic to noetic experience of autobiographical memories in Alzheimer’s.^{33,42,45–56} A shift that implies a difficulty to mentally relive past events and a general sense of familiarity may be expressed by Alzheimer’s patients as a sense of “having experienced this before.”

Thus, the correlations between remember/know responses and confabulations in our Alzheimer’s participants may be interpreted as reflecting a relationship between confabulations and difficulties in the ability to mentally travel in time to reexperience memories during retrieval. In our view, the diminished subjective experience of memories may lead to a difficulty to control their encoding context and probably to a sense of familiarity for irrelevant memories (for further details, see references^1,57,58). This difficulty results in an activation of these memories at the expense of relevant ones and consequently to the occurrence of confabulations.

The relationship between confabulations and diminished autonoetic consciousness in Alzheimer’s disease, as suggested by our findings, can be compared with the temporal consciousness model.^5,13,59 According to this model, patients with confabulations have a disturbed sense of temporal consciousness; they are able to access stable traces concerning habits and factual information but cannot retrieve relevant detailed traces from long-term memory. Similarly, the temporal confusion hypothesis²⁰ and the temporal context hypothesis^20,22 suggest that patients with confabulations use previous memories that may have been relevant in a previous situation, but these memories are interjected in a current situation when it is no longer relevant or appropriate. On a clinical level, the temporal consciousness model, the temporal confusion hypothesis, and the temporal context hypothesis, as well as our own findings, can be supported by the consideration that patients with severe confabulations, when directly probed on what they have done previously, usually retrieve routine activities prior to hospitalization. For instance, they may claim that they spent the weekend at home with family even though they were hospitalized during the weekend. In other words, they replace inaccessible specific memories by repeated events. Together, our findings may be considered as providing empirical support for the temporal consciousness model, the temporal confusion hypothesis and the temporal context hypothesis.

As we tend to suggest, confabulations in Alzheimer’s disease can be associated with difficulties in the ability to mentally travel in time in order to reexperience memories during retrieval. This assumption can be supported by research considering confabulations as a deficit in retrieval.²⁶ More specifically, Gilboa et al.²⁶ suggested that impairment or failure of strategic retrieval is involved in confabulations. The monitoring system, which is involved in strategic retrieval,²⁶ encompasses two components: one is an early, rapid, and preconscious component, and the other is conscious and elaborate. According to Gilboa et al.,²⁶ failure of at least the former component is both necessary and sufficient for confabulations. Interestingly, Gilboa et al.²⁶ suggested that other deficits, including those that affect temporal context and content confusions, may be required for confabulations to arise.

Our findings did not support the executive account, as no significant correlations were observed between confabulations in our participants and performance on the span tasks. This lack of relationship mirrors studies of Alzheimer’s,^8,10,11,12 as well as studies suggesting that amnesic patients with confabulations do not differ from nonconfabulating amnesic patients with regards to executive functions.^3,19,20 Besides the lack of a relationship between confabulations and executive function, our findings demonstrated no significant correlations between confabulations and episodic memory. This outcome can be attributed to the fact that the episodic memory task by Grober and Buschke³⁸ assesses simple item memory rather than autobiographical memory.

Besides demonstrating the absence of significant correlations between confabulations and executive function/episodic memory, our findings also demonstrated the lack of significant correlations between provoked and spontaneous confabulations. These findings mirror the results reported in Kessels et al.,⁴⁰ which showed no significant correlations between spontaneous and provoked confabulations in patients with Korsakoff’s syndrome, in agreement with the notion that both types of confabulations are dissociated.⁶⁰

Although our study considered the distinction between provoked and spontaneous confabulations, different forms have been proposed by Schnider,⁶¹ who distinguished between four categories of confabulation: 1) intrusions in memory tests; 2) momentary confabulations, which are false statements in a discussion or other situation inciting patients to make comments; 3) fantastic confabulations, which have no basis in reality and are nonsensical and logically inconceivable; and 4) behaviorally spontaneous confabulations, which occur in severe amnesia and disorientations. Different forms of confabulation therefore have been proposed, but they have noteworthy similarities. For instance, except for certain cases, their content is usually plausible and therefore indistinguishable from true memories, unless one is very familiar with the patient’s past. Furthermore, as our findings suggest, confabulations reflect a difficulty of patients to project themselves in the past to retrieve the appropriate information.

One limitation of the present study is the lack of a control group, especially in light of the fact that that confabulations may be observed in normal aging.^6,62–64 Another limitation is the lack of a structured assessment of behavioral and psychiatric symptoms and concurrent medications (especially cholinesterase inhibitors, memantine, and antipsychotics) in our Alzheimer’s participants. This assessment is important because cognitive function in Alzheimer’s has been associated with behavioral and psychiatric symptoms and medication.^65–67 Additionally, we used the MMSE to assign stage of disease, whereas staging of Alzheimer’s disease requires combined assessment of both cognitive impairment and functional status. Future replications could use the Clinical Dementia Rating,⁶⁸ a rating system to assess cognitive and functional decline across the spectrum of Alzheimer’s disease. Considering the remember/know paradigm, our participants showed high levels of “remember” responses. This outcome may be attributed to the fact that participants had to retrieve only three events. The cue words used in our study have also been found to trigger relatively high autobiographical recall in Alzheimer’s,^41,43 probably due to their emotional valence. Future replications could assess more autobiographical cues. Future research may also consider assessing autonoetic experience with a scale assessing a variety of phenomenological features (e.g., reliving, back in time, remembering, realness, visual imagery, auditory imagery, etc.). These features can be evaluated with a scale that was conceived to evaluate these features in dementia.³⁵

To summarize, although confabulations have important consequences on cognitive assessment and in the everyday life of patients with Alzheimer’s, little is known about their cognitive underpinnings. Although our study addresses the latter issue, clinical studies are needed to offer strategies to alleviate confabulations in Alzheimer’s disease.