Self-Consciousness Deficits in Alzheimer’s Disease and Frontotemporal Dementia

Abstract

Self-consciousness (SC) is multifaceted and considered to be the consciousness of one’s own mental states. The main aim of this paper is to compare SC in patients with Alzheimer’s disease (AD) and behavioral variant frontotemporal dementia (bvFTD). Three groups (control and patient groups) of 23 subjects each were assessed using an SC questionnaire. Both types of dementia clearly induce an alteration of SC. The bvFTD group showed a greater impairment in SC than the AD and control groups. The SC score was strongly associated with frontal functions. The most significantly impaired SC aspects in the bvFTD group were Anosognosia, Introspection, and Moral Judgments. For the AD group, the significantly impaired aspects of SC were Anosognosia and Prospective Memory. The differences in SC between the AD and bvFTD groups were essentially centered on the Anosognosia, Moral Judgments, and Introspection aspects, which were highly impaired in the bvFTD patients. This suggests that SC is related to orbito-frontal functioning and thus, to the default mode network.

Keywords

Alzheimer’s disease awareness consciousness dementia executive frontotemporal

INTRODUCTION

Self-consciousness (SC) is considered to be the consciousness of one’s own mental states. It allows individuals to be the object of their awareness [1, 2]. SC is multifaceted [3]; it includes the awareness of perception, of one’s own history [4], and of one’s body [1], as well as a moral consciousness [5, 6]. It is also inseparable from memory, thanks to the identity that all human beings forge for themselves [7].

Most studies addressing SC essentially focus on anosognosia in dementia [5 , 8–11]. The subtypes of dementias may display heterogeneous deficits in different aspects of SC. To our knowledge, only three previous studies from our laboratory have examined the different facets of SC in patients with dementia. These were two studies performed with patients with in Alzheimer’s disease (AD) [1, 12] and another one in patients with behavioral variant frontotemporal dementia (bvFTD) [13]. In particular, Gil et al. [1] studied SC in 45 AD patients by means of the Self-Consciousness Questionnaire (SCQ), which assesses seven aspects of SC: Personal Identity, Anosognosia, Affective State, Body Representation, Prospective Memory, Introspection, and Moral Judgments. We observed that the most disturbed aspects were Anosognosia, Moral Judgments, and Prospective Memory, while the least disturbed were Personal Identity and Body Representation. In addition, a similar SC profile was found in the study with AD patients. Furthermore, we found a very close correlation between SC and frontal test scores at the threshold of significance [12]. Concerning FTD, our research group has observed that the most disturbed ones in bvFTD patients were Anosognosia, Affective State, and Moral Judgments [13]. We suggested that SC deficits in bvFTD patients were related to behavioral SC aspects, which are more dependent on orbito-frontal functioning.

The medial prefrontal cortex may play a critical role in SC [13 –15]. bvFTD is a neurodegenerative disease that selectively affects the anterior portions of the brain and elicits behavioral and personality disturbances. By contrast, AD is a neurodegenerative disease essentially characterized by posterior cortex atrophy and cognitive perturbations.

To our knowledge there are no studies addressing the comparison between the SC of AD and bvFTD patients. Thus, the main aim of this paper is to compare SC in patients with AD and in patients with bvFTD in order to observe whether there are different profiles of SC as a function of the kind of dementia, and if so, which aspects of SC are affected by the different types of dementia.

MATERIAL AND METHODS

Participants

We studied 69 individuals, including 23 patients diagnosed with AD, 23 patients with bvFTD, and 23 normal healthy controls.

All patients fulfilled the research diagnostic criteria for bvFTD [16, 17] and for the AD diagnostic criteria of the “NINCDS-ADRDA Work Group” [18] and of the DSM III-R [16]. Other causes of dementia were excluded by clinical examination and blood and imaging tests. All patients had a score of less than 5 on the Hachinski Ischemic Scale [19]. All patients were taking anti-dementia medication during the study; in particular, the AD patients were receiving anti-acetylcholinesterase treatments and the bvFTD patients were taking serotonin reuptake inhibitors and benzodiazepines.

According to the Clinical Dementia Rating (CDR) scale [20] and Mini-Mental State Examination (MMSE) [21], the patients had mildly severe dementia. Only the patients whose verbal comprehension (assessed by the MMSE three-stage command) was equal to or above 2 were included in the study.

The controls were mainly volunteers from the French community or were members or visitors at the University Hospital in Poitiers whose results in a neurological examination were normal; they had a CDR score equal to zero; they scored 28/30 or higher on the MMSE, and displayed normal performance in neuropsychological testing.

Ethics

Written, informed consent was obtained from all the included patients. The study was approved by The Regional Committee for Research Ethics, CHU Poitiers.

Material

SC was evaluated using the SCQ [1] and composed of fourteen items, in order to obtain information from the patients about aspects of SC (Table 1). Four of these items concern identity (Nos. 1, 5, 6, and 7); three of them pursue knowledge about cognitive disturbances (Nos. 2, 3, and 4); one is a self-evaluation of the participant’s Affective State (No. 8); two concern knowledge about Body Representation (Nos. 9 and 10); one addresses anticipation or Prospective Memory (No. 11); one explores the participants’ capacities for Introspection (No.12), and two address Moral Judgments (Nos. 13 and 14). These are simple questions intended to study SC as ecologically as possible and in a manner as close as possible to the everyday life of the participants. Here, the examiners ensured that the answers were fully understood by the participants in order for them to be included in the study. The criteria for rating the answers were carefully determined by two of us as relevant (two points), incorrect (no points), or partly correct (one point). To contrast the total integrity and alteration of SC, the partlycorrect and incorrect answers were grouped together as poor/wrong answers with respect to “relevant” ones as good answers. We considered poor answers to be incorrect plus partly correct answers. The families helped us check the accuracy of the answers through autobiographical data and Affective State. Thus, the total maximum score for the seven aspects of SC was 28 points.

We also included a cognitive evaluation using the following general cognitive tests: MMSE [21] and the Frontal Assessment Short Test (FAST) [22].

Procedure

Clinical evaluations and neuropsychological testing were performed on all participants at around the time of the SC assessment (within 2 weeks). All were tested individually in a single session, underwent two cognitive tests, and took the SCQ 1. All assessments took between 35–60 min to complete.

Statistical analyses

Data were analyzed using the Statistical Package for the Social Sciences (SPSS) software (version 21). In this study, an α level of 0.05 was selected for statistical significance.

To check whether there were significant differences between the three groups as a function of age, we used analysis of variance (ANOVA); in the case of educational level and gender, we used χ² tests. We also implemented ANOVA to observe whether there were significant differences between the three groups in their general cognitive state as assessed by MMSE [21] and FAST [22].

In order to accomplish the main aim of this paper evaluating the differences in the performance on the SCQ between the three subject groups, we calculated the total score for the SCQ, the sum of scores obtained for the different items, and then used an analysis of covariance (ANCOVA), introducing severity of dementia and duration of disease as covariates, due to observe both variables were on the edge of significant difference between subjectgroups.

In addition, the scores obtained for each of these aspects of consciousness were divided by the number of questions corresponding to each aspect in order to obtain the proportion of correct answers. Following this, we calculated the proportion of poor answers in each aspect of SC, subtracting the proportion of correct answers from 1. Then, in order to see which patient group was most affected, we used ANCOVA with the corresponding a posteriori tests of the proportion of errors on the 7 factors conforming SC. In addition, we reported eta squared (η²) as our effect size measure; η² is the portion of the total variance that is attributed to a specific predictor.

Finally, we obtained the Pearson correlations between the total SC scores, age, the educational level, and the scores on the MMSE and FAST tests.

RESULTS

Demographic characteristics

The number of participants involved in the study was 69. The bvFTD, AD, and control groups did not differ significantly with respect to age [F(2,66) = 1.06; p = 0.37], gender ( $χ_{2}^{2}$ = 0.72; p = 0.69), or educational level ( $χ_{4}^{2}$ = 0.77; p = 0.95). The patient groups did not differ significantly with respect to the severity of the disease [t(44) = 2.05; p = 0.062] or the duration of the illness [t(44) = 2.11; p = 0.049], but both variables were on the threshold of signification. The demographic data for the three participant groups are shown in Table 2.

Regarding the AD group, the mean duration (±SD) of the disease was 40.93 (±21.54) months and mean disease severity (±SD) was 1.31 (±0.61). The AD group had a mean age (±SD) of 66.54 (±9.09) years. Regarding the bvFTD group, the mean duration (±SD) of the disease was 27.42 (±18.84) months and mean disease severity (±SD) was 1.95 (±0.69). The bvFTD group had a mean age (±SD) of 63.65 (±11.49) years. In the control group, the mean age (±SD) was 68.74 (±5.38) years. In addition, most patients and control participants had an educational level (EL) of 3-4, according to the classification of Barbizet and Duizabo [23]: illiterate (EL 1); can read, write, and count (EL 2); 6 years of education (EL 3); 9 years of education (EL 4); 11 or 12 years of education (EL 5); 13 years of education (EL 6); and more than 13 years of education (EL 7).

With respect to cognitive aspects (Table 2), the patient and control groups differed significantly in the general cognitive state, as assessed by the MMSE, and in frontal functions as assessed by the FAST [F(2,66) = 16.75; p < 0.001, η² = 0.44; F (2, 66) = 31.7, p < 0.001, η² = 0.74, respectively]. The AD subjects performed most poorly on the MMSE, while the bvFTD patients’ performance was between that of the AD and control individuals. However, the AD and bvFTD groups did not differ significantly in the MMSE scores (p = 0.642). Concerning the FAST test, the bvFTD subjects performed most poorly, while the AD patients’ performance was between that of the bvFTD and control individuals. However, the AD and bvFTD groups differed significantly in the FAST scores (p = 0.032).

The self-consciousness questionnaire

Our main analyses involved evaluating the differences in the performance of SC aspects between the bvFTD, AD patients, and control groups (Table 3).

There was a significant difference in the SC total score between the patient and control groups [F (2,64) = 6.76; p = 0.002; η² = 0.17]. The total score on the SC questionnaire of the patients groups were significantly lower than that of control group (p < 0.001). In addition, the total score on the SC questionnaire of the bvFTD group was significantly lower than that of the AD group (p < 0.001) (Table 3 and Fig. 1).

Considering the percentages of errors in each aspect of SC, the control group produced 13% pertaining to the aspect of Moral Judgments, 4.4% to Affective State, 4.2% to Prospective Memory, 2.9% to Anosognosia, 0.5% to Personal Identity, and no errors regarding the Introspection and Body Representation aspects. The AD group produced 42% of errors pertaining to the aspect of Anosognosia; 26.1% to Prospective Memory; 19.6% to Introspection; 17.4% to Affective State; 13% to Moral Judgments; 5.4% to Personal Identity, and 1% to Body Representation. The bvFTD patients produced 71% of errors pertaining to the aspect of Anosognosia, 61% to Introspection, 46.7% to Moral Judgments, 45.7% to Affective State, 34.1% to Prospective Memory, 4.9% to Personal Identity, and no errors to Body Representation. The means and standard deviations of the error percentages for each SC aspect produced by all groups are shown in Table 3 and Fig. 2.

We next compared the error proportions in each of the aspects of SC between the three participant groups. The bvFTD group showed significant differences in Anosognosia (p < 0.001), Affective State (p < 0.001), Introspection (p < 0.001), and Moral Judgments (p < 0.001) in comparison with the control group. However, the AD group only showed significant differences in the Anosognosia (p < 0.001) and Prospective memory (p = 0.009) aspects of SC with respect to the control group. Moreover, our analyses revealed a significant difference in the Anosognosia (p = 0.004), Affective state (p = 0.001), Introspection (p < 0.001), and Moral Judgments (p < 0.001) aspects of SC between the AD and bvFTD groups. We also failed to observe any significant differences in the aspects of Personal Identity and Body Representation among the three participant groups (p > 0.05).

Besides, there was no significant correlation between the score for the SC questionnaire and age or educational level in all participants together (r = 0.7; p = 0.55, and r = 0.16; p = 0.18, respectively). Moreover, we found a non-significant correlation between the SC score and the duration of the disease (r = –0.03; p = 0.83) in both patient groups together, but asignificant correlation between the SC score and the severity of the disease (r = –0.56; p < 0.01). Furthermore, we observed a significant correlation between the SC score and cognitive state as evaluated by the MMSE (r = 0.37; p = 0.01), as well as a significant correlation between the SC score and frontal score as evaluated by the FAST test (r = 0.55; p < 0.001) in both patient groups together.

DISCUSSION

The aim of the present study was to compare the effects of bvFTD with those of AD on SC and in the analyses we controlled for variance in severity and duration of disease. The two types of dementia clearly induce an alteration of SC, but not an abolition of the participants’ SC. In general, bvFTD exhibited a greater impairment in SC than AD. In addition, these deficits in SC could not be accounted for in terms of gender, age, and educational level. The SC score was associated with severity of diseases, as well as with cognitive and frontal dysfunctions, but we found a stronger association with frontal functions.

Regarding the bvFTD group, the four most significant impaired SC aspects were Anosognosia, Introspection, Moral Judgments, and Affective State Self-Assessment. For the AD group, the most impaired aspects were Anosognosia, Prospective Memory, Introspection, and Affective State Self-Assessment, but the two latter aspects were not significantly poorer than in the control participants. Personal Identity and Body Representation aspects of SC were the least altered in all of the participants. Moreover, the pattern of SC in our AD group was fairly similar to those reported in previous studies [1, 12] and the profile of SC in our bvFTD was similar to that of another study carried out by our research group [13].

The bvFTD patients were more profoundly anosognosic than the AD patients. In this sense, Affective State Self-Assessment in the bvFTD group was also poorer than that of the AD group. These findings are to be expected, since many previous studies have found reduced self-awareness in AD [8–11 , 24] and in bvFTD [25 –27]. In FTD, impaired self-awareness occurs early in the illness and was included as one of five core diagnostic features in the Neary criteria [10]. Such patients are less aware of their general health state and of specific affective, behavioral, and cognitive deficits than AD patients [25 –27]. In AD, an alteration of one’s awareness of one’sdifficulties is common, and increases in severity as the disease progresses [8, 24]. Nevertheless, some studies attempting to measure insight without the aid of an informant have not consistently revealed differences in insight between FTD and AD, which is at odds with the clinical characterization of FTD [28, 29].

Furthermore, bvFTD affects the orbito-frontal cortex and elicits substantial deficits in self-awareness before cognitive alterations become manifest. Thus, our bvFTD group had a mild-severity disease with minor cognitive deficits and they showed a marked anosognosia. In contrast, AD is associated with posterior cortical atrophy and our AD patients showed a less patent alteration of SC than the bvFTD group. This suggests that these atrophied posterior areas cannot send an adequate quality, quantity, or sequential order of information to the associative frontal cortex in order to control and produce adequate SC. Thus, Gil and his research group [1, 5] suggested that perturbations in SC could be more associated with the orbito-frontal cortex and particularly, with the default (or automatic) mode network involving posterior cingulate cortex, medial and orbital prefrontal cortex as well as angular gyrus [30].

Concerning the Introspection aspect, we observed that the bvFTD group showed a more important impairment than the other two participant groups. However, the AD and control groups had a similar capacity for introspection. These findings are in keeping with those reported by James and Ricouer [31, 32] regarding the “maintenance of Self”, or ipseity, which is considered to be the experiential sense of being a vital and self-identical subject of experience, allowing people to make coherent choices regarding social, material, and spiritual aspects during their lives and hence no transformations of the Self. Frontal patients have many difficulties in choosing among options and in maintaining their Self, as seen from the transformations of their usual behavior (e.g., aggressiveness, lack of respect for social norms, etc.). In addition, functional neuroimaging studies have suggested that the non-dominant frontal lobe is a neural region that is essential to ipseity [33, 34].

Another very important impaired SC aspect in bvFTD as compared with the AD and control groups was Moral Judgment. In this sense, most studies addressing frontal dementias using mind theory tasks have found deficits in social cognition [35, 36].

We found a poorer Prospective Memory capacity in the bvFTD and AD groups than in the control group. In addition, the Prospective Memory aspect was the second most impaired aspect of SC in the AD group. This could be due to the fact that this aspect is more dependent on executive functions.

In conclusion, it seems that the first altered aspect of SC that appears in both dementias is Anosognosia, although this is significantly more perturbed in the bvFTD group. The differences in SC between the AD and bvFTD groups are essentially centered on the Moral Judgment and Introspection aspects, which are markedly impaired in bvFTD patients. These altered aspects of SC in the bvFTD group reflect the classical clinical characteristics of FTD, such as changes in personal and social conduct, as well as early and emotional blunting [37, 38].

Finally, impaired SC in dementia influences patients’ willingness to seek and comply with treatment, thereby increasing the burden of caregiver [39]. Clinical assessments in dementia should include a social cognition protocol in order to help the early diagnosis of dementia, the optimum treatments, and juridical-social protection. Furthermore, accurate quantitative measurements are necessary to further study the cognitive and neural mechanisms mediating SC. Although many studies have indicated an important role for the frontal lobes, particularly on the right side [14, 15], little is known about the specific frontal functions involved in SC.

DISCLOSURE STATEMENT

Authors’ disclosures available online (http://j-alz.com/manuscript-disclosures/16-0770r1).

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