Impaired Decision Making in Alzheimer’s Disease

Abstract

To assess whether the decline of decision-making processes in people diagnosed with Alzheimer’s disease (AD) is explained by the use of an inappropriate analytic strategy induced by their high level of uncertainty about their ability, we used happiness induction to activate an appropriate heuristic processing of information. Healthy older adults and AD patients performed the Iowa Gambling Task either in a standard condition or after viewing a funny film clip. Although AD patients had impaired performances in the standard condition, the happiness condition significantly increased AD patient performance level compared with that of the control subgroups. Additional analyses showed that uncertainty levels were reduced in happy AD patients and that performances in the Iowa Gambling Task were not due to impairment in executive or memory functions. We suggest that higher uncertainty levels in patients with mild AD, which induce an inappropriate analytic strategy, can be reduced through emotional remediation techniques.

Keywords

Alzheimer’s disease decision making Iowa Gambling Task (IGT)analytical processing heuristic processing

Few studies have focused on decision making (DM) in Alzheimer’s disease (AD), but these few studies have reported converging findings (see Gleichgerrcht, Ibanez, Roca, Torralva, & Manes, 2010, for a review). Studies have shown that AD patients are deficient in both risky (Delazer, Sinz, Zamarian, & Benke, 2007; Sinz, Zamarian, Benke, Wenning, & Delazer, 2008) and ambiguous decision tasks (Sinz et al., 2008; Torralva, Dorrego, Sabe, Chemerinski, & Starkstein, 2000). They have difficulty finding the more advantageous strategy and maintaining a consistent pattern of choices. Patients’ performance at a prodromal stage of AD suggests that DM processes could be early and deeply affected (Zamarian, Weiss, & Delazer, 2007) and could be a behavioral marker of the conversion to AD during the following year (Triebel et al., 2009).

In previous studies, researchers have correlated a decline in patient performance with memory deficits (Torralva et al., 2000; Zamarian et al., 2007) or executive function impairment (Delazer et al., 2007; Sinz et al., 2008); these researchers have proposed that patients are unable to maintain their strategy because of executive function impairment. However, in a recent and well-documented review, Toplak, Sorge, Benoit, West, and Stanovich (2010) found that most of the variability in performance in DM could not be explained by deliberative cognition. Their analysis confirmed that performance in DM tasks is not strictly dependent on high cognitive ability in the global population or, more specifically, in individuals diagnosed with AD. Another explanation for the deficits in AD patients could be related to the critical role of emotion in guiding DM (Damasio, 1994; Wagar & Dixon, 2006). The processing of emotional information would allow individuals to make correct choices without having an explicit awareness of the most effective strategy (Bechara, Damasio, Tranel, & Damasio, 1997). Affective disturbances have been consistently reported in individuals diagnosed with AD (Bungener, Jouvent, & Derouesne, 1996; Hargrave, Geck, Reed, & Mungas, 2000) and may reflect a more global emotional processing deficit (Rosen et al., 2006). From the early stage of AD, neural loss is observed in the emotional part of the prefrontal cortex (Chu, Tranel, Damasio, & Van Hoesen, 1997) and the amygdala (Poulin, Dautoff, Morris, Barrett, & Dickerson, 2011).

Taken together, these results suggest that the informative value of emotion for DM may work less efficiently in AD patients. However, the profile of emotional deficits in AD does not clearly support this hypothesis. In fact, although emotional facial expression recognition is noticeably impaired (for a meta-analysis, see Klein-Koerkamp, Beaudoin, Baciu, & Hot, 2012), emotional feeling seems to be relatively preserved (Burton & Kaszniak, 2006; Henry, Rendell, Scicluna, Jackson, & Phillips, 2009). Findings from Blessing, Keil, Linden, Heim, and Ray (2006) demonstrated in particular that in a task of new emotional learning, AD patients had no explicit recognition of affective situations 3 hr after the test, whereas their affective disposition toward cues associated with negative and positive information remained preserved.

In the present study, we examined a third explanation for the decline in DM performance on the basis of the fact that the main difference between patients and control participants in all previous studies (Delazer et al., 2007; Sinz et al., 2008; Torralva et al., 2000; Zamarian et al., 2007) was that patients alternated more frequently between risky and safe choices. This pattern of response is surprisingly similar to the pattern reported in healthy young participants in whom an uncertainty state has been induced (Bagneux, Bollon, & Dantzer, 2012; Bollon & Bagneux, 2013; Tiedens & Linton, 2001). Researchers have explained differences between individuals in highly certain and uncertain states by the fact that uncertainty levels introduce a differentiated type of information processing (Han, Lerner, & Keltner, 2007; Lerner & Keltner, 2000; Lerner & Tiedens, 2006; Tiedens & Linton, 2001), namely, systematic versus heuristic styles of information processing. When people process information systematically, they do so slowly and analytically; they take into account available information in a detailed manner and seek to integrate it into decision formulation. When processing information heuristically, people think faster and use simple or general inference rules, which induces less effort. Findings with healthy participants have suggested that people with a high level of uncertainty choose systematic processing to find clues in the environment that could reduce this state (Tiedens & Linton, 2001).

Influences of heuristic and analytic processing have been well described for one of the most classic tasks of DM, the Iowa Gambling Task (IGT; Bechara, Damasio, Damasio, & Anderson, 1994). The IGT is a sequential task during which participants have to find which decks of cards among four are overall more advantageous for winning money. Each choice is followed by a positive (gain) or negative (loss) outcome. The wide range of rewards and punishments makes it impossible to find advantageous decks by calculating the net gains or losses for each option. In other words, systematic processing is an inappropriate strategy to succeed in the IGT, whereas heuristic processing would be successful. Applied to AD patients, our hypothesis is that they mainly use systematic processing, which is especially inappropriate because of their impaired declarative and working memory. At an early stage of AD, patients are often aware of a memory decline (Mimura, 2008), which places them in a perpetual situation of doubt. According to the predictions of Tiedens and Linton (2001), uncertain AD patients tend to engage in more systematic processing of information, including massive memory processing recruitment, when they have to perform IGT.

In summary, we agree with the dominant explanation (Delazer et al., 2007; Sinz et al., 2008; Torralva et al., 2000) that bad choices in decision tasks are sustained by the (disadvantageous) strategy chosen by people diagnosed with AD. We assume, however, that this choice is induced by their affective state at the beginning of the task rather than the impairment of cognitive processing. Thus, we predict that performance in AD patients could be improved if they are pushed toward an appropriate strategy. The theoretical assumptions of the appraisal-tendency framework (Han et al., 2007; Lerner & Keltner, 2000; Lerner & Tiedens, 2006) provide a useful approach for modulating the strategy of processing information in people diagnosed with AD without giving explicit rules that they may quickly forget. Studies have shown that positive emotions encourage heuristic processing of subsequent tasks, whereas negative emotions encourage systematic processing (for a theoretical review, see Martin & Clore, 2001). Indeed, positive affect may reduce uncertainty levels and, by consequence, initiate more heuristic processing of information. We predict that performances observed in the classic IGT will be better for happy AD patients compared with control AD patients with no emotional induction. In addition, if poor performance results mainly from an induced unsuitable strategy, we predict that performance of the AD patients should not significantly differ from that of healthy older adults (HOAs).

Method

Participants

Seventy-eight participants were included in the study. Because of inefficient emotional induction of the pleasant film clip or positive feeling associated with the neutral film clip, 17 participants were removed from the study, which left 32 HOA participants (mean age ± SD: 75.65 ± 5.63 years; 19 females, 13 males) and 29 patients with probable mild AD (79.17 ± 6.35 years; 20 females, 9 males) in the analysis. All participants were Caucasians and native French speakers.

AD patients were recruited in the Neuropsychology Unit at the Department of Neurology of Saint Etienne Hospital and the Geriatric Unit of Grenoble Hospital. The AD patients were selected after neurological examination, structural MRI, and neuropsychological assessment for probable AD using the criteria of the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer’s Disease and Related Disorders Association (McKhann et al., 1984). HOAs were members of the Université Savoisienne du Temps Libre, a French association dedicated to the diffusion of academic knowledge toward older adults. There were no age, gender, or educational differences between the two groups (see Table 1 for participant demographics). Exclusion criteria included use of antipsychotic medication, history of severe medical or surgical illness, and other neurological or visual disorders. The regional ethics committee approved the study, and all participants gave their informed consent before participating.

Table 1.

Participant Demographics and Results of Neuropsychological Background Tests

Demographic/Test	Group		F value	Effect size (η2)
Demographic/Test	HOA (n = 32)	AD (n = 29)	F value	Effect size (η2)
Age (years)	75.65 ± 5.63	79.17 ± 6.35	1.94	.08
Education (%)			0.55	.001
Level 1	14	19
Level 2	49	46
Level 3	37	35
MMSE	29.2 ± 0.83	23.34 ± 1.42	387.19**	.87
Cued + Free Recall (/48 ± SD)^a	29.68 ± 6.44	47.40 ± 0.91	229.84**	.8
Executive function (s)^b	81 ± 52.04	119 ± 43	14.69**	.19
Semantic memory^c	79.31 ± 1	71.06 ± 6.75	61.58**	.52

Note: Data are mean ± standard deviation unless noted otherwise. HOA = healthy older adult; AD = Alzheimer’s disease; Education: Level 1 = basic school-leaving qualification and vocational-training qualification, Level 2 = from secondary school certificate until high school diploma and higher education, Level 3 = high school diploma and higher education; MMSE = Mini-Mental State Examination.

Subtest of the Grober and Buschke (1987) test; “/48” indicates the maximum score for this test. ^bWe investigated executive functions by employing the Trail Making Test (TMT); the score we used was TMT B – TMT A (Reitan & Wolfson, 1995). ^cSemantic memory was assessed with a picture-naming test: DO 80 (Metz-Lutz, Kremin, & Deloche, 1991).

p < .001.

Materials and protocol

Emotion induction

Participants watched randomly one of two film clips that were pretested as inducing happiness or neutral cognitive states in older adults. The happiness clip was a famous scene from a classical French comedy, Les aventures de Rabbi Jacob (57th min; length: 5 min 12 s). The neutral clip was an extract on tuna fishing from the French television show Thalassa (length: 5 min 7 s). A manipulation check was conducted to ensure that the clips induced the target emotions and that the induced emotions were associated with the expected certainty-uncertainty and pleasantness appraisal tendencies. First, the participants reported the intensity of their emotional state by responding to the following: “When I watched the film, I felt: no emotions at all (1)/intense emotions (7).” We then asked the participants to respond to five items adapted from the Dimensional Ratings Questionnaire (Smith & Ellsworth, 1985) to ascertain their degree of certainty (three items) and pleasantness (two items).

IGT

Participants performed a computer version of the IGT (see Bechara et al., 1994, for details) presented with Eprime 2.0 on a 17-in. screen. Participants responded verbally and the examiner validated their response on Eprime; this technique was used to reduce participants’ anxiety and the cognitive costs often associated with the use of a computer in older adults. Participants had to try to maximize an initial $2,000 of virtual money by avoiding bad decks and selecting good decks among four presented on the screen. Each deck was associated with the variables gain or loss; the first two decks (A and B) were associated with a net loss for every 10 choices, whereas the last two decks (C and D) yielded a net gain. Participants made 100 sequential choices. An IGT score was calculated for each group of 20 choices by adding the number of cards picked from the good decks and then subtracting the number of cards picked from the bad decks [(C + D) – (A + B)].

Results

Neuropsychological assessments

AD patients showed cognitive deficits typical for mild AD and scored significantly lower than did control participants in both memory and executive functions. For example, the Mini-Mental State Examination (Folstein, Folstein, & McHugh, 1975; French version: Hugonot-Diener, Barbeau, Michel, Thomas-Antérion, & Robert, 2008) mean score of AD patients was 23.34 (SD = 1.42, range: 22–28) and the mean score of HOAs was 29.2 (SD = 1.2, range: 28–30; see Table 1 for neuropsychological background test results).

Differences between the emotional states

Two analyses of variance (ANOVAs) were conducted on the happiness and certainty scores of the Dimensional Ratings Questionnaire with group (HOA, AD) and emotional induction (happy, neutral) as between-subjects factors. Participants who saw the pleasant film clip felt happier than did participants who saw the neutral clip, F(1, 57) = 5.73, p < .01, η² = .49, with no impact of dementia, F(1, 57) = 0.141, n.s., η² = .001. The ANOVA showed a significant main effect of emotional induction for the certainty scores, F(1, 57) = 15.44, p < .001, η² = .21, which stemmed from a higher level of certainty associated with happiness induction. The interaction Emotional Induction × Group was not significant, F(1, 57) = 0.51, n.s., η² = .006, which suggests that a similar certainty state was induced in the two groups.

Net scores for the IGT

IGT performances were assessed with a repeated measures ANOVA with blocks (1–5) as a within-subjects factor and subgroups (happy AD, control AD, happy HOA, control HOA) as a between-subjects factor. For all ANOVAs, we used the Greenhouse-Geisser epsilon correction to adjust the degrees of freedom of F ratios when appropriate. The analysis showed a main effect for block, F(4, 228) = 23.82, p < .001, η² = .25, which stemmed from increasing performances throughout the task—linear trend: F(1, 57) = 50.88, p < .001, η² = .21. Block effects also entered into a highly significant interaction with subgroup, F(12, 228) = 10.23, p < .001, η² = .15. The upper portion of Figure 1 shows that the control HOA subgroup progressively learned to make advantageous choices, linear trend: F(1, 57) = 27.24, p < .001, η² = .32, whereas the control AD subgroup in a similar condition did not, linear trend: F(1, 57) = 0.38, n.s., η² = .01.

Fig. 1.

Net scores for each block of 20 decisions as a function of the subgroup (upper panel) and correlation between executive functions and Iowa Gambling Task (IGT) performances in AD patient subgroups under the standard condition (TMT A; middle panel) and under the happy condition (TMT B; lower panel). AD = Alzheimer’s disease; HOA = healthy older adult; TMT = Trail Making Test.

In addition, comparisons between subgroups in each block showed that AD patients in the standard condition of the IGT more frequently chose disadvantageous decks than did other subgroups for the last three blocks—Block 3: F(1, 57) = 2.74, p < .10, η² = .04; Block 4: F(1, 57) = 13.97, p < .005, η² = .20; Block 5: F(1, 57) = 25.18, p < .001, η² = .30; however, this was not the case for the first two blocks—Block 1: F(1, 57) = 2.63, n.s., η² = .04; Block 2: F(1, 57) = 0.3, n.s., η² = .06. Most important, happy AD patients were also able to increase the frequency of good choices throughout the task—linear trend: F(1, 57) = 11.42, p < .001, η² = .17. In contrast, our analysis did not detect differences between happy AD and HOA subgroups except for in Block 2, F(1, 57) = 4.18, p < .05, η² = .11, which suggests that their performances were globally similar.

Correlations between DM and memory and executive tasks

Correlative analyses (Pearson’s rs) between global performance score on the IGT {[(C + D) – (A + B)]^{block 5} – [(C + D) – (A + B)]^{block 1}} and neuropsychological tests were performed only for the AD patient subgroups because of ceiling effects in the HOA subgroups. No correlation was found between episodic memory scores or semantic memory scores and performances on the IGT for either AD patient subgroup. As the middle and lower portions of Figure 1 show, when patients completed the IGT in the standard condition, their performance was significantly correlated to executive scores (r = .717, p = .003), whereas no significant correlation was found between these two scores in the happy condition (r = .2, n.s.).

Discussion

In this study, we examined the assumption that metacognition regarding early stage AD patients’ memory capacity induced an uncertainty state, which initiated an inappropriate analytic strategy for information when they had to perform a classic DM task (the IGT). We attempted to induce a more relevant (i.e., heuristic) strategy for making good choices during the IGT (De Vries, Holland, & Witteman, 2008; Wilson, 2002) by inducing a happy state in a portion of the patients by having them watch a funny movie prior to the DM task. Our results showed that AD patients who viewed the funny clip (a) had a reduced feeling of uncertainty compared with AD patients who viewed the neutral clip and (b) developed a tendency to make advantageous decisions that were similar to those reported in HOAs.

At a theoretical level, our findings provide indirect evidence supporting the valence of emotions as the source that triggers the type of processing that guides DM. Consequently, failing to adopt an advantageous strategy in complex DM situations could be explained in part by the global affective state of the individual, including individuals diagnosed with neurodegenerative disorders. According to current models of emotional influences on cognition (De Vries et al., 2008; Tiedens & Linton, 2001), AD patients performing the IGT in the happy condition should tend to make their decisions according to their gut feeling and to rely more strongly on emotional cues toward different options as a result of intuitive processing. Conversely, AD patients performing the IGT in the standard condition might adopt more deliberative processing. Because of the complexity of the IGT in terms of amount of information and limited cognitive capacities of working memory, AD patients with massively impaired declarative memory are engaged in an analysis that will be fatally flawed. In other words, we suggest that AD patients who performed unsuccessfully on the DM tasks did so because they thought that they would not be able to succeed.

A comparison of the learning curves in our subgroups supports our hypothesis. In fact, AD patients in the happy condition had better performances mainly for the last few blocks of the IGT. Performance in the first half of this sequential task tended to be lower for AD patients than for HOAs. This result is consistent with the different processing requirements of the two distinctive parts of the IGT. At the beginning of the task, systematic processing is useful for accumulating knowledge on the task. Consequently, heuristic processing induced in happy participants is less relevant at this stage and can even disrupt learning. However, the second part of the IGT is associated mainly with heuristic processing, which explains why our emotional induction is related to greater differences between AD patients who performed in the happy condition versus those who performed in the standard condition.

An important issue raised by our data concerns the level of impairment of complex cognitive functions in AD. Our findings suggest that DM processes could be relatively preserved in the early stage of AD. This result is in accordance with the assessment of DM in more ecological conditions, such as medical DM. For instance, patients diagnosed with mild cognitive impairment (Okonkwo et al., 2008) and patients diagnosed with mild AD (Marson, Ingram, Cody, & Harrell, 1995) were able to make good choices concerning their medical treatment. Marson et al. (1995) also reported, however, that this capacity was preserved when criteria were obvious but fell dramatically with increasing cognitive change and the spread of AD. These and other results from correlative analyses performed in prior studies run counter to a strong version of our hypothesis that DM capacity is solely a spurious effect induced by the constraints of the DM task. It is clear that DM processes are highly complex and require efficient cognitive abilities that are impaired early on in AD patients. Our correlative analysis results suggest that executive functions and DM performance decline at the same time rather than that declines in executive functions reduce DM performance in AD.

In fact, we reproduced previous significant correlations between executive functions and DM performance in the standard condition, but these performances were not correlated in AD patients in whom a happy state had been induced. At a clinical level, an interesting consideration suggested by our data is the possible improvement of the DM deficit in early stage AD. For individuals diagnosed with AD, the weight of metacognition of their own cognitive decline is probably underestimated. Our results showed that part of the deficits reported in a wide range of cognitive tasks that are indirectly related to brain atrophy could be examined in a different way.

The present study provides additional information to further the understanding of impairments in DM tasks under ambiguous conditions. These tasks are sequential, and the outcomes of a decision influence subsequent decisions. However, impairments in people diagnosed with AD have also been reported in studies focused on DM under risky conditions. In these studies, decisions are limited in number and independent of one another. Because there is a major distinction between these descriptive tasks and more complex tasks, such as sequential and experiential tasks (Camilleri & Newell, 2010), future research involving individuals with AD should focus on providing further insights into the influence of uncertainty on DM performance under risky conditions.

On a more general level, our work was based on the assumption that individuals with early stage AD have a continuously high level of uncertainty, in which they systematically orient toward analytic processing of their environment. If this hypothesis is correct, its implications should concern more than just the decision process because all tasks that are advantageously performed with a heuristic strategy should be impaired in AD patients, independently of the cognitive abilities involved in these tasks. Future studies might reassess declines in AD when tasks mainly involve heuristic processing by measuring the link between performance and uncertainty levels of patients. A second, counterintuitive, hypothesis, based on the same main assumption and awaiting further investigation, is that this cognitive state could confer an advantage on individuals with AD when they perform tasks requiring analytic processing of information. One main issue regarding the empirical verification of this hypothesis is to find experimental designs that require analytic processing that must be relatively preserved in people with AD.

Another question related to this work is how to involve individuals diagnosed with AD in more durable heuristic processing of their environment. Among other possibilities, we assume that the influence of incidental emotion (i.e., emotions elicited from nonrelevant factors for the current situation) on subsequent cognition provides a useful method to modulate the cognitive strategy. However, although the duration of this influence has not been clearly elucidated, it cannot exceed a few minutes. A promising method of investigation is to instead attempt to induce a more tonic state by mood induction or emotional disposition. The appraisal-tendency framework theory predicts that a more stable affective state should have effects similar to transitory emotional induction. In addition, previous studies have confirmed that mood and affective states modify performances in DM tasks (Buelow & Suhr, 2009; Miu, Heilman, & Houser, 2008). By the same token, because clinical reports have suggested the existence of massive emotional disturbances (Derouesne, Piquard, Thibault, Baudouin-Madec, & Lacomblez, 2001), future research is also needed to elucidate the influence of such disturbances on cognitive impairments, in particular with regard to DM.

Footnotes

Acknowledgements

Editing was provided by Barbara Every of BioMedical Editor.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with respect to their authorship or the publication of this article.

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