International Psychogeriatrics, Vol. 12, No. 3, 2000, pp. 359-368 0 2000 International Psychogeriatric Association

Impairments of Social Cognition and Decision Making in Alzheimer’s Disease

TERESA TORRALVA, FLAVIA DORREGO, LILIANA SABE, ERAN CHEMERINSKI, AND SERGIO E. STARKSTEIN

ABSTRACT. Objective: To investigate the nature of deficits in social cognition and real-life decision making in a group of patients with Alzheimer’s disease (AD). Desigii: A comprehensive neuropsychological and psychiatric assessment, including the Moral Judgment Interview and the Bechara’s Card Test, was carried out in 25 patients with AD and 20 age- comparable normal controls. Setting: Outpatient clinic. Results: AD patients had significantly lower scores in the Moral Judgment Interview and obtained significantly less earnings in the card test when compared to the normal control group. The Moral Judgment Interview score correlated significantly with Raven’s Progressive Matrices and Block Design, whereas the card test correlated significantly with both the Benton Visual Retention Test and the Buschke Selective Reminding Test. No significant correlations were observed between the experimental tasks and the psychiatric variables. Conclusions: AD patients demonstrated significant deficits on tasks assessing social cognition and real-life decision making. These impairments correlated with deficits on specific neuropsychological tasks, but not with behavioral problems frequently found in AD patients.

Behavioral disturbances such as depres- sion, anxiety, and irritability are frequent findings among patients with Alzheimer’s disease (Burns et al., 1990). In a recent study that included a consecutive series of 196 patients with AD, we found aggressive behavior to be significantly associated with

From the Department of Neuropsychiatry, Raul Carrea Institute of Neurological Research - FLENI, Buenos Aires, Argentina (T. Torralva, PhD; F. Dorrego, PhD; L. Sabe, PhD; E. Chemerinski, MD; and S. E. Starkstein, MD, PhD).

Ojf/Jrints. Requests for offprints should be di- rected to Teresa Torralva, PhD, Raul Carrea In- stitute o f Neurological Research, Montafieses 2325, 1428 Buenos Aires, Argentina. e-mail: ses@fleni.org.ar

more frequent delusions and more severe irritability (Chemerinski et al., 1998). We also reported that AD patients with irrita- ble behaviors and aggressive outbursts had a significantly higher prevalence of patho- logical affect and anosognosia (i.e., lack of awareness of their intellectual and behav- ioral problems) (Starkstein et al., 1995). Based on findings in patients with disinhi- bition syndromes after brain damage or dementia, we speculated that specific cere- bral regions may modulate motor, intel- lectual, affective, and instinctive behaviors based on information from multimodal brain areas providing both biographical memories and relevant contextual cues (Starkstein et al., 1988).

Received October 5, 1999 Accepted February 10, 2000

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Whereas behavioral syndromes are classically diagnosed after a formal psy- chiatric assessment, cognitive "markers" of behavioral disorders have been as- sessed only recently. In an elegant study, Bechara and colleagues (1994) designed "an experimental neuropsychological task which simulates, in real time, per- sonal real-life decision-making relative to the way it factors uncertainty of pre- mises and outcomes, as well as rewards and punishment." This task requires patients to select cards from four differ- ent decks, and each card selection is as- sociated with gains or losses. The aim of the task is to maximize gains, which pa- tients may achieve by avoiding decks yielding high gains but higher losses and by selecting from more conservative decks.

A related issue is whether AD patients have the ability to understand the mean- ing of social situations, because deficits on this domain may underlie the pres- ence of behavioral problems such as para- noid thinking and aggressive outbursts. One method frequently used to measure social cognition is to present patients with a social dilemma, and based on their responses, calculate a stage of "mor- al development" (Price et al., 1990), but few studies using this instrument were carried out among patients with neuro- logical disorders (Kohlberg, 1976).

Our study had several aims. First, we wanted to determinewhether patients with AD had deficits in social knowledge and real-time risk-taking abilities. Secondly, we wanted to establish whether these abilities are significantly correlated with deficits in specific cognitive domains. Finally, we wanted to examine the corre- lation between social knowledge and risk-taking abilities and behavioral prob- lems frequently reported in AD.

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PATIENTS AND METHODS

Patients

AD Group. A consecutive series of 25 patients with AD who attended our in- stitute for regular follow-up visits par- ticipated in the study. The inclusion criteria were the following: (a) National Institute of Neurological and Communi- cative Disorders and Stroke-Alzheimer's Disease and Related Disorders Associa- tion (NINCDS-ADRDA) criteria (McKhann et al., 1984) for probable AD, (b) normal results on laboratory tests, (c) no history of closed head injury with loss of con- sciousness, strokes, or other neurologic disorder with central nervous system involvement, (d) no focal lesions on the magnetic resonance imaging scan, and (e) a Hachinski ischemic score (Hachin- ski et a]., 1975) 24 .

Normal Control Group. This group comprised 20 individuals who volunteered to participate in the study. All control subjects had a negative history of neuro- logical disorders or closed head injuries.

Psychiatric Examination

After informed consent was obtained, a psychiatrist unaware of the neuropsy- chological findings assessed patients and controls with the following instruments:

Structured Clinical I n t e r v i e w f o r DSM-lV(SCID) (Spitzer et al., 1992). The SCID is a semistructured diagnostic inter- view for making the major Axis I Diagnos- ticand Statistical Manual ofMental Disorders, fourth edition (DSM-IV; American Psychi- atric Association, 1994) diagnoses. The SCID was administered by a psychiatrist with the patient and at least one first- degree relative. Based on the SCID respons- es, DSM-IV Axis I diagnoses were made.

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Hamilton Depression Scale (HAM-D) (Hamilton, 1960). The HAM-D is a 17- item interviewer-rated scale that mea- sures psychological and autonomic symptoms of depression.

Hamilton Anxiety Scale (HAM-A) (Hamilton, 1959). The HAM-A is an 11- item interviewer-rated scale that mea- sures the severity of generalized or persistent anxiety.

Functional Independence Measure (Granger et al., 1986). This instrument as- sesses self-care, sphincter control, mobili- ty, locomotion, communication, and social cognition on a low-level scale. Higher scores indicate less impairment in activities of daily living.

Apathy Scale (Starkstein et al., 1995). This scale includes 14 items, which are scored by the patient’s relative or care- taker. Each question has four possible answers, which are scored from 0 to 3. Thus, the Apathy Scale scores range from 0 to 42 points, and higher scores indicate more severe apathy. We have demon- strated the reliability and validity of the Apathy Scale in AD (Starkstein et al., 1995).

Irritability Scale (Starkstein et al., 1995). This is a 14-item scale, which is rated by the patient’s relative or caretak- er. Scores range from 0 to 42, and higher scores indicate more severe irritability. We have demonstrated the validity and reliability of this scale in AD (Starkstein et al., 1995). The Spanish translation of both the Apathy Scale and the Irritabili- ty Scale was carried out by the same neuropsychiatrist (S.E.S.) that elaborat- ed the scales in the English version.

Dementia Psychosis Scale (Migliorel- li et al., 1995a). This is an 18-item scale, which quantifies the severity and types of delusions in demented patients at the time of the psychiatric evaluation. This

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inventory includes assessments of most types of delusions described in AD, such as paranoid delusions, the Capgras syn- drome, the phantom boarder syndrome, and hypochondriacal delusions. The psy- chiatrist rated this scale with the patient and at least one close relative or caretak- er. We have demonstrated the validity and reliability of this scale in AD (Migliorelli et al., 1995a).

Overt Aggression Scale (Yudofsky et al., 1995). This scale measures specific aspects of aggressive behavior based on observable criteria. Aggressive behav- ior is divided into four categories: verbal aggression, and physical aggression against objects, against self, and against others. Within each category, descrip- tive statements and numerical scores are provided to define and rate four levels of severity. Informants were asked about the presence and type of aggressive out- bursts during the 4 weeks preceding the psychiatric evaluation.

Social Ties Checklist (Starr et al., 1983). The Social Ties Checklist is a 10- item scale that measures the quantity and quality of social supports. Scores range from 0 to 10, and higher scores indicate better social supports. To as- certain duration of illness, both the pa- tient and at least one caregiver living with the patient were asked about the approximate date of onset of different cognitive deficits (e.g., memory defi- cits, orientation problems, anomia, dys- calculia).

Neuropsychological Examination

A neuropsychologist unaware of the psy- chiatric findings carried out a compre- hensive neurops ychological examination using the following instruments (only AD patients were assessed):

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Min i -Menta l S t a t e Examinat ion (MMSE) (Folstein et al., 1975). The MMSE is an 11-item examination found to be valid and reliable in assessing a limited range of cognitive functions in a global way.

Raven’s Progressive Matrices (Raven et al., 1986). This test measures visu- ospatial reasoning. Patients are present- ed with a pattern problem with one part removed and several pictured inserts, one of which contains the correct pat- tern. The patient has to select the miss- ing piece to complete the pattern. Performance is related to overall intel-. lectual functioning.

Wisconsin Card Sorting Test (Nel- son, 1976). This test measures the abili- ty to develop new concepts, to shift sets, and to suppress a previously cor- rect response in order to learn a new correct one. Assessment of the overall proficiency of the test was judged by the number of categories achieved (max- imum 6).

Controlled Oral Word Association Test (Benton, 1968). This test examines access to semantic information with time constraint. Patients were instructed to name as many words beginning with the letter F as they could in 1 minute. Peo- ple’s names and proper nouns were not permitted. The letters A and S were then presented successively, 1 minute being allowed for each letter. The score was the number of words produced in 1 minute.

Busc h ke Se 1 ec t i ve Reminding Test (Buschke & Fuld, 1974). This test mea- sures verbal learning, recall, and recog- nition on a multiple-trial list learning task. The patient listens to a list of words, and has to recall as many words as pos- sible. Each subsequent learning trial in- volves the presentation of only those

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words that were not recalled on the immediately preceding trial. The score used was the total recall.

Benton Visual Retention Test (Ben- ton, 1974). This test assesses visual per- ception and nonverbal memory. Patients are exposed to geometric designs for 10 seconds, and are immediately presented with a card containing the correct design among three different foils. The patient has to select the correct one. The score was the total number of correct answers.

Digit Spun (Wechsler, 1955). This sub- test of the Wechsler’s Adult Intelligence Scale-Revised (WAIS-R) examines audi- tory attention, and includes two parts. In the first part (Digits Forward), the pa- tient is asked to repeat a string of num- bers as exactly as it is given, whereas in the second (Digits Backwards) the pa- tient must repeat the digit string in re- versed order.

Block Design (Wechsler, 1955). This WAIS-R subtest examines construction- al praxis.

Similarities (Wechsler, 1955). This test provides a measure of abstract reasoning.

A second neuropsychologist, who was unaware of the remaining clinical data, assessed the following tasks:

Moral Judgment Intemiew (Kohlberg & Colby, 1987). This measure provides a semi- standardized method for identifying the developmental level of moral judgments used by a subject to resolve hypothetical moral dilemmas. It consists of three paral- lel forms. Each form comprises three hy- pothetical moral dilemmas, and each dilemma is followed by 9 to 12 standard- ized probe questions designed to elicit jus- tifications, elaborations, and clarifications of the subject’s moral judgments. The scor- ing procedure involves classifying the pa- tient’s responses by issue, form, and element and finding matching criterion

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judgments in the Kohlberg and Colby (1987) scoring manual that specify their stage structure. After stage scores have been assigned, the scores are weighted and summed to produce both a global stage score and a weighted average score (WAS). These scores range from 100 (cor- responding to the lowest stage [Stage 11) to 600 (corresponding to the highest stage [Stage 61). Briefly, Stages 1 and 2 corre- spond to the preconventional level and their goal is to avoid breaking rules backed by punishment (Stage 1) and to follow rules only when it is to the person’s imme- diate personal interest (Stage 2). Stages 3 and 4 correspond to the conventional lev- el, and their goal is to live up to other people’s expectations (Stage 3) and to ful- fill duties agreed upon (Stage 4). Finally, Stages 5 and 6 correspond to the postcon- ventional level, and their goal is to behave according to social rules and values (Stage 5) and self-chosen ethical principles (Stage 6). Questions at specific intervals were also included to corroborate that patients had a correct comprehension of the story.

Bechum’s Curd Test (Bechara et al., 1994). This test simulates, in real time, personal real-life decision-making activ- ities that include rewards and punish- ments. Subjects have to sit in front of four decks of cards equal in appearance and size, and are given a $2,000 loan of play money. After turning each card, the patient receives some money. With some cards the patient is also asked to pay a penalty, which may vary upon the deck selected (i.e., some decks yield low gains and low losses, whereas others produce high yields but high losses). Net earn- ings can only be obtained by consistent- ly selecting from low-yield decks. The subjects are told that the goal of the game is to maximize profit, but they are free to switch from one deck to another.

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Statistical Analysis

Statistical analysis was carried out using means and SDs, analysis of variance (ANOVA) with repeated measures, and forward stepwise regression analysis. Frequency distributions were calculated using x2 tests with Yates’s correction for expected cell sizes less than 5. All p val- ues are two-tailed.

RESULTS

Demographic and Psychiatric Findings (Table 1)

No significant differences were found for age, gender, and years of education be- tween AD patients and normal controls.

Neuropsychological and Psychiatric Findings (Table 1)

AD patients showed significantly low- er WAS scores (moral judgment) than the normal control group: F(1,43) = 120.3, p < .0001. Moreover, whereas all normal controls were classified in Mor- al Stages 4-6, no AD patient was classi- fied above Stage 3 (x’ = 45.0, df = 1 , p <

To examine specific neuropsycholog- ical correlates of moral judgment in AD, we calculated a forward stepwise re- gression analysis using the neuropsy- chological tests as independent variables and the WAS score as the dependent variable. The overall correlation was sig- nificant-R* = .55, F(7,15) = 4.88, p < .05-and the variables that accounted for a significant part of the variance were the Block Design ( R 2 = .22, p < .05) and the Raven’s Progressive Matrices (R2 = .16, p < .05).

.001).

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TABLE 1. Demographic, Psychiatric, and Neuropsychological Findings

Normal Controls AD Patients Range ~~~

Number 20 25 Age, mean years (SD) 68.2 (11.9) 70.2 (7.2) Gender, % female 70 56 Education, mean years ( S D ) 14.1 (2.3) 13.1 (5.1) Duration of illness, mean years (SD) - 4.6 (5.1)

WAS*, mean ( S D ) 410 (31) 277 (47) MMSE score, mean ( S D ) - 24.7 (4.1) 17-30

% Moral Stage IV-V* 100 0

Hamilton Depression Scale score, - 5.5 (5.7) 0-20 Card Task, mean earnings* ( S D ) 848 (505) -1,054 (1,047)

mean ( S D ) Hamilton Anxiety Scale score, mean (SD) - 3.8 (6.5) 0-24 Functional Independence Measure score, - 65.4 (7.0) 41-72

mean ( S D ) Apathy Scale score, mean (SD) - 13.8 (8.1) 0-25 Irritability Scale score, mean (SD) - 7.8 (6.9) 0-23 Dementia Psychosis Scale score, mean (SD) - 0.58 (1.2) 0-5 Overt Aggression Scale score, mean ( S D ) - 0.14 (0.65) 0-3 Social Ties score, mean ( S D ) - 3.3 (2.3) 0-8

Note. AD = Alzheimer’s disease; MMSE = Mini-Mental State Examination; WAS = weighted average score. ‘p < .01

To examine the psychiatric correlates of moral judgment, we calculated a re- gression analysis that included all the psychiatric variables as independent variables and the WAS score as the de- pendent variable. The overall correla- tion was not significant: R2 = .20, F(2,17) = 2.2, p = ns.

AD patients obtained significantly lower gains on the Bechara’s Card Test as compared to the normal control group, F (1,36) = 42 .6 ,~ < .0001 (Table 1). Further statistical analyses were carried out to determine the strategy used by AD pa- tients on this task. First, we examined the number of selections from “high risk- high gains” and ”low risk-low gains” decks. A two-way ANOVA with repeat- ed measures showed a significant Group x Deck interaction-F(3,108) = 13.3, p < .0001-and post-hoc analysis demon- strated that AD patients selected more

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cards from ”high risk” decks and less cards from ”low risk” decks as com- pared to the normal control group (Fig- ure 1).

To examine the pattern of earnings across time, we calculated a two-way ANOVA with repeated measures where the between-factor was group (AD vs. controls), and the repeated measure was the amount of gain or loss over each block of 10 cards. Whereas there was a significant group effect, F(1,36) = 26.9, p < .0001 (AD patients had a lower overall success score as compared to the control group), there was a nonsignificant Group x Trial interaction, F(9,324) = 0.89, p = ns (i.e., both groups had a similar pattern of earnings) (Figure 2).

A forward stepwise regression analysis for AD patients using earnings on the card test as the dependent variable and the neu- ropsychological variables as independent

Impaired Social Cognition in A D

35 1

600

v) En E

-200 * .- E w a -400

-600

-800 - /’ b

-1 000

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*- AD GROUP

j *

10 I DECK 1

T

T

+

- DECK 2 DECK 3 DECK 4

Disadvantage Advantage

I 0 AD Group Control group

Figure 1. Bar graph showing the percentage of card selection from disadvantageous (Decks 1 and 2) (i.e., high earnings but high losses) and advantageous decks (Decks 3 and 4) (i.e., low earnings but low losses) for AD patients and normal controls (*p < .05).

Trials

Figure 2. Line chart showing earnings obtained by either AD patients or normal controls every 10 card selections.

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variables showed a significant overall ef- fect-R2 = .61, F(5,15) = 4.75, p < .Ol-and the variables that accounted for a signifi- cant part of the variance were the Benton Visual Retention Test (R2 = .43, p c .05) and the Buschke-delayed recall (R2 = .32,p < .01). On the other hand, a forward stepwise regression analysis using earnings on the card test as the dependent variable and the psychiatric variables as independent vari- ables showed no significant overall effect: R2 = .59, F(10,7) = 1.04, p = HS.

DISCUSSION

This study examined impairments of social judgment and decision making in , AD and there were several important findings. First, AD patients with mild dementia performed significantly worse on a measure of social judgment than age-comparable normal controls. This deficit correlated with more severe im- pairments on tasks of abstract reasoning and constructional praxis. Second, AD patients also showed significantly worse performance than the control group on a risk-based decision-making task. This def- icit correlated with more severe impair- ments on tasks of visual and verbal anterograde memory. Third, no signifi- cant correlations were found between def- icits on the social judgment measure and the card test and psychiatric scales assess- ing frequent behavioral problems in AD.

In recent assessments of behavioral prob- lems in AD patients, we found a high prev- alence of abnormal behaviors, which tended to cluster in definite syndromes. Thus, we found a significant association between depression, anxiety, and apathy, which we considered a ”depressive behavioral syn- drome” (Starksteinet al., 1995), and asignif- icant association between irritability,

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aggressive episodes, delusions, and anosog- nosia, which we considered a ”disinhibited behavioral syndrome’’ (Migliorelli et al., 1995b). However, the mechanisms for these syndromes still remain poorly understood.

Several studies examined clinical cor- relates and potential mechanisms of dis- inhibition in demented patients. We found that demented patients with dis- inhibition had significantly lower cere- bral blood flow in orbitofrontal and basotemporal cortices as compared to demented patients without disinhibition but a similar severity of dementia (Stark- stein et al., 1994). On the other hand, there were no significant between-group differences on specific cognitive tasks. Hence, this current study included two cognitive tasks that were designed to measure complex cognitive domains and have been previously used in patients with behavioral disturbances. To deter- mine whether behavioral problems may be related to impairments in social knowledge, Price and colleagues (1990) assessed with the Moral Judgment Inter- view two adult patients who developed severely disinhibited behaviors after bi- lateral prefrontal damage during child- hood. Both patients achieved only low stages of moral development. Saver and Damasio (1991) assessed a patient with ventromedial frontal damage and social conduct disorder with tasks that tag the evaluation of social situations and moral reasoning. Based on their patient’s normal performance, Saver and Damasio suggest- ed that disinhibited behaviors could occur in the context of preserved ability to gener- ate adequate social judgments.

Our study demonstrated a significant deficit on a measure of social judgment in AD patients with mild dementia as com- pared to age-comparable normal controls. Because we have no longitudinal data,

Impaired Social Cognition in A D

whether the low scores on moral judg- ment resulted from the dementing pro- cess or froma low social functioningcould not be determined. However, the latter is unlikely because there were no signifi- cant correlations between moral judgment and social functioning scale scores.

Impairments in moral judgment could also be secondary to generalized cogni- tive dysfunction, and our present find- ings provide partial support for this hypothesis, because cognitive tasks ex- plained 44% of the variance in moral judgment scores. The cognitive tasks that explained most of the variance were those tapping visuospatial reasoning. None of the psychiatric variables were signifi- cantly correlated with moral judgment scores, suggesting a dissociation between social reasoning and the behavioral dis- orders of AD patients. Alternatively, this lack of significant correlations may re- sult from a narrow range of psychiatric scores in our group with mild dementia.

Bechara and colleagues (1994) found that patients with prefrontal lesions had significant deficits on a card test that mimics real-life decision making. Our study demonstrated similar deficits in AD patients on the same task. These patients obtained significantly lower net gains and made significantly more selec- tions from the disadvantageous decks as compared to the control group. Cogni- tive functioning (primarily verbal and visual memory tasks) explained a signif- icant proportion of the variance on the card test (61%). On the other hand, be- havioral symptoms did not explain a significant part of the variance on this test, leading to the conclusion that defi- cits in moral judgment and real-life deci- sion making do not relate to behavioral disorders, and seem to depend on defi- cits of more basic intellectual functions.

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Future studies should assess moral judg- ment and real-life decision making in patients with more severe dementia and potentially greater behavioral problems.

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Acknowledgments. This study was partially supported by grants from the Raul Carrea Institute of Neurological Research and the Fundacidn Perez Companc. We thank Fred Bylsma, PhD, for his helpful suggestions, a n d Antoine Bechara, PhD, for providing advice and neuropsychological material.

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