Executive function deficits in patients with dementia of the Alzheimer's type A study with a Tower of London task

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Executive function deficits in patients with dementia of the Alzheimer's type A study with a Tower of London task
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  Archives of Clinical Neuropsychology17 (2002) 513–530 Executive function deficits in patients with dementiaof the Alzheimer’s typeA study with a Tower of London task  Constant Rainville a , b , ∗ , Hélène Amieva b , Sylviane Lafont b ,Jean-François Dartigues b , c , Jean-Marc Orgogozo b , c , Colette Fabrigoule b a Centre de Recherche, Institut Universitaire de Gériatrie de Montréal, 4565 chemin de la Reine-Marie, Montreal, Canada H3W 1W5 b Unité Inserm U. 330, Université de Bordeaux II, Bordeaux, France c Service de Neurologie, Hˆ opital Pellegrin, Bordeaux, France Accepted 20 April 2001 Abstract A growing number of studies report a deterioration of the executive function (EF) in dementia of the Alzheimer type (DAT). To evaluate EFs in DAT, a new version of the Tower of London (TOL)task, srcinally developed by Shallice (1982), was adapted. The new version of the test was built upin its easiest possible feature in order to be administrable to early- or middle-stage demented patients.Seventeen DAT patients, and 17 controls matched for age and sex, were administered the TOL. Theprotocol followed a “hierarchical paradigm,” that is, simpler problems were embedded in more com-plex, subsequent problems. Results showed that DAT patients were impaired compared to controls.Both control and DAT groups showed a decrease in percentage of success rate in relation to the numberof movements required by the task. On the more complex problems, the performance of DAT subjectswas proportionally more impaired. Qualitative analysis revealed that rule breaking was a salient per-formance feature of the DAT group. These findings are consistent with the presence of an EF deficitin DAT.©2002NationalAcademyofNeuropsychology.PublishedbyElsevierScienceLtd.Allrightsreserved. Keywords:  Executive function; Dementia of the Alzheimer’s type; Tower of London task  ∗ Corresponding author. Tel.: + 1-514-340-3440, ext. 4767; fax: + 1-514-340-3530.  E-mail address : rainvilc@magellan.umontreal.ca (C. Rainville).0887-6177/02/$ – see front matter © 2002 National Academy of Neuropsychology.PII: S0887-6177(01)00132-9  514  C. Rainville et al. / Archives of Clinical Neuropsychology 17 (2002) 513–530 1. Introduction In dementia of the Alzheimer type (DAT), deterioration of cognitive abilities collectivelyknown as executive function (EF) are increasingly reported (Cummings & Benson, 1992;Grady et al., 1988; Jolles & Hijman, 1983; Passini, Rainville, Marchand, & Joanette, 1995;Patterson, Mack, Gelmacher, & Whitehouse, 1996). Many studies are consistent with thepossibility that an impairment in EF occurs early in DAT (see Perry & Hodges, 1999). Forinstance, Janowsky and Thomas-Thrapp (1993) and Strub and Black (1981) suggested that deficiencies in organizational and executive abilities may signal the early stages of DAT. Theyreportedthattasksdependingonfamiliarinformationandroutineoperationsaremostresistantto disruption. Conversely, new and complex tasks deteriorate most evidently. The presence of early EF dysfunction has been reported by Almkvist (1996), Binetti et al. (1996) and Collette, Andres, and Van der Linden (1999). Laflèche and Albert (1995) administered seven tests to assess EF in DAT patients. They observed that DAT differed significantly from controls onfour tests. According to these researchers, performance on these tests was impaired becausethey require concurrent manipulation of information (e.g., set shifting, self-monitoring, or se-quencing) and cue-directed attention (e.g., the ability to use cues to direct attention). Bhutani,Montaldi, Brooks, and McCulloch (1992) used four neuropsychological tests (verbal fluency,delayed alternation, subject-ordered pointing, and the Wisconsin Card Sorting Test) to de-termine frontal lobe involvement in DAT. They showed that DAT subjects were impaired inthe first three tasks. Impairments were present at all stages of the disease and were relatedto disease severity. In a longitudinal study, Sahakian et al. (1990) observed also the presenceof executive dysfunction in the early stage of DAT. In a prospective study, Fabrigoule et al.(1998) showed that preclinical cognitive deficits in Alzheimer’s disease may be interpreted asthe disturbance of controlled processes.Royal, Mahurin, and Cornell (1994) found that a measure of EF was better correlated thanminimentalstatusexamination(MMSE)scoreswithfunctionalstatus.Accordingtothem,thisobservation suggests that executive dysfunction has a substantial role in determining patient’slevel of functioning that is perhaps more important than global cognitive impairment. Exec-utive dysfunctions have been associated with greater neuropsychiatric symptomalogy (Chen,Sultzer, Hinkin, Mahler, & Cummings, 1998). Moreover, a number of studies associated im-pairments in EF with inability to perform daily activities in AD (Chen et al., 1998; Grigsby, Kaye, Baxter, Shetterly, & Hamman, 1998; Willis et al., 1998). For Royal (1994) and Royal et al. (1994), DAT might be better understood as a syndrome of executive dyscontrol. Romanand Royall (1999) have suggested that impairments in EF were a robust determinant of func-tional status, disability, and dementia.In sum, the evaluation of EF in DAT is recognized as an important aspect in clinic and maybeusefulfortheearlydetectionofDAT.However,classicalEFtasksarenotalwaysadaptedforDATpopulation.Forinstance,Chenetal.(1998)observedthatsevenoftheproposedexecutive skillstestscouldnotbeperformedby32–55%ofamoderatelyimpairedDATgroup.Therefore,an effort needs to be provided to adapt these tests to that population.The EF includes a broad range of abilities whose number and nature vary according todifferent authors. In the literature, a number of interrelated skills have been distinguished, in-cludingrecognitionandselectionofappropriategoals,manipulationofconcurrentinformation  C. Rainville et al./Archives of Clinical Neuropsychology 17 (2002) 513–530  515 (e.g., set shifting, sequencing, and monitoring), cue-directed attention, concept formation(e.g., abstraction) (Anderson, 1980; Denkla, 1996; Glosser & Goodglass, 1990; McCarthy & Warrington,1990).ForWelsh,Pennington,andGroisser(1991),itinvolvesstrategicplanning, impulse control, and organized search, as well as flexibility of thought and action. Thus, in-hibitory mechanisms play a central role in EF (Luria, 1966, 1973; Shallice, 1982). Subjects must maintain a smooth flow of planning and control behavior in the face of potential distrac-tions. At each step of the task, they have to obtain relevant information in light of their goal(or subgoals), on one hand, and they have to inhibit irrelevant information, on the other hand.Moreover, the immediate attainment of one subgoal may conflict with the attainment of moreappropriate subgoals that lead to the final goal.Within this broadly conceived framework, our study will focus on a central feature of theEF: planning abilities which imply the attainment of a goal through a series of intermediatestepswhichdonotnecessarilyleaddirectlytothatgoal.Inordertostudythistypeofprocessesin EF, Shallice (1982) elaborated the Tower of London (TOL) test. This test was designed as ameansofidentifyingimpairmentsofsuchsuperveningplanningprocesses.Itwasderivedfromthe Tower of Hanoi Disk-Transfer task, which consists of well-defined start and goal states, aswell as a constrained set of legal operators (i.e., behavioral responses) for movements throughthe problem solving space. The TOL requires planning such as means—ends analysis in orderto solve a series of successively more difficult problems and to avoid incorrect moves. SolvingTOL problems requires the rearrangement of colored balls on three pegs to match a goalarrangement (i.e., duplication of the experimenter’s ball configuration) of balls presented onanadjacentmodel(startposition).Thesimplerproblemscanbesolvedbydirectlytransferringballs from a start to a goal position, whereas complex problems involve planning the correctsequence of moves. In these cases, the goal is achieved by being broken down into subgoals.The TOL is a non-verbal task. It is also a novel task for all people, so that subjects did not havethe opportunity to previously develop subroutines. This test is well recognized to measureEF (Anderson, Anderson, & Lajoie, 1996). It has been administered to many populations,including traumatic head injury cases (Azouvi et al., 1995; LeThiec et al., 1999; Levin et al.,1996), and patients with focal frontal lesions (Glosser & Goodglass, 1990; Goel & Grafman,1995; Shallice, 1982; Shallice & Burgess, 1991). Thus, it follows that the TOL test appears to be appropriate for the assessment of EF,which is an important clinical aspect in DAT. However, concerning this population, it maybe necessary to use a simplified version of the task. For the elderly population, Allamano,Della Sala, Laicona, Pasetti, and Spinnler (1987) developed a version of the TOL which wasgiven to 131 normal subjects. They found a decline of performance in normals. There wasno significant influence of education and sex on the test performance. There is, however, anumberofdifficultieswiththeirtestingprocedure.First,therewasatimelimitintheexecutionoftheproblemsandthisisapotentialproblemforapopulationwhocouldhaveasensorimotorslowness. Second, in presence of rule breaking, the examiner stopped the test to remind thesubject that a rule has been broken and the scoring system is complex and used global score.However, the “microanalysis” of individual performances (e.g., types of error) often providesa good clinical insight on patient’s cognitive disturbances.ThegoalofthisresearchwastostudyEFdeficitsinDATbymeansofanew,adaptedversionoftheShallice(1982)TOLtest.Thisversionfollowsa“hierarchicalparadigm,”thatis,simpler  516  C. Rainville et al. / Archives of Clinical Neuropsychology 17 (2002) 513–530 problems are embedded in more complex, subsequent problems. Moreover, it should allowassessmentofthesetypesofdeficitsinDATpatients,andcontrolthebasicabilitiesinvolvedinthis task, with the subject beginning with very simple problems and then going through moreand more complex problems (the complexity is defined by the minimum number of movesneeded to match the model). This task also allows a qualitative analysis of patient’s errors,providing further knowledge of the underlying deficits. 2. Method 2.1. Subjects Theexperimentalgroupwascomposedof17DATpatients(10women,7men)whosemeanage was 72.0 (S . D .  =  5 . 1). Ages of patients ranged from 62 to 79. All DAT patients weregiven a diagnosis of DAT by a senior staff neurologist according to the criteria developed byNINCDS-ADRDAgroup(McKahnetal.,1984).Laboratorytestingwasperformedtoruleoutsome other possible causes of dementia. Patients with a history of severe head injury (loss of consciousnessformorethan48h),alcoholism,anddepressivesymptomatologywereexcluded.To reduce the possibility of including multi-infarct dementias, patients with a score of 5 orgreater on the Hachinski scale were excluded. The dementia severity measured by the MMSE(Folstein, Folstein, & McHurgh, 1975) was mild to moderate (mean MMSE score  =  21 . 5;S . D . = 2 . 4).The normal control group was composed of 17 healthy seniors with a mean age of 72.9(S . D . = 4 . 7).Agesofsubjectsrangedfrom63to79.ThemeanMMSEwas27.6(S . D . = 1 . 7).They were matched with the experimental group for age and sex. There was no significantdifference in the number of years of schooling between the groups. Control subjects wererandomly selected from a list of beneficiaries of a pension fund. None of them showed anysign of dementia according to the DSM-IIIR criteria (Diagnostic and Statistical Manual of Mental Disorders, 1987). Exclusion criteria included cerebrovascular disease, Parkinson’sdisease,severetrauma(lossofconsciousnessformorethan48h),depressivesymptomatology,or chronic alcoholism. 2.2. Material and procedure The TOL materials included two kits, one for goal arrangement (examiner’s kit) and onefor start position (subject’s kit) (Fig. 1), each made of a wooden base 22cm × 6cm × 2cm.Three wooden pegs of different lengths (12, 8, and 4.5cm) were mounted on the base. Foreach kit, there were three colored balls (yellow, red, and blue), 3cm in diameter, with holescut through the core so that they can easily be placed on the pegs.The protocol included 15 problems organized in the following way. First, three problems of fivemovementswereselected.Twoofthemwereselectedaccordingtothepresenceorabsenceofa“trigger.”Atriggerisanincitationtothesubject,atthebeginningofthetask,tomoveaballto its final position according to the model (Collette & Van der Linden, 1993). For instance, Problem13(Fig.1)containsa“positivetrigger,”whichhelpstoreproducethemodel.Problem  C. Rainville et al./Archives of Clinical Neuropsychology 17 (2002) 513–530  517Fig. 1. Schematic representation of the adaptation of the Tower of London stimuli. R, Y, and B designate positionsfor the red, yellow, and blues balls on the pegs. There is one start position for each series. Three problems weregiven at each level (L) of complexity. 15 contains a “negative trigger,” which is an obstruction to the following moves. Hence, it is apotential distracter that could lead to a failure in appropriate goal-directed behavior. Problem14 is “neutral,” that is, it contains no trigger.Each of the three srcinal problems was segmented into five steps (Fig. 1). Each step was usedtodefineadifferentproblem.Hence,eachofthethreeoriginalproblemsmadeupaseries
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