Archives of Clinical Neuropsychology 21 (2006) 1521

Executive function decits in early Alzheimers disease and their relations with episodic memory
Sophie Baudic a, , Gianfranco Dalla Barba b , Marie Claude Thibaudet c , Alain Smagghe c , Philippe Remy d,e , Latchezar Traykov e,f
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INSERM/UPVM Unite 421, Facult de M decine, 8 rue du G n ral Sarrail, 94010 Cr teil Cedex, France e e e e e b INSERM U 610, H pital de la Piti -Salp tri` re, Paris, France o e e e c Service de R adaptation G rontologique, H pital Notre Dame de Bon Secours, Paris, France e e o d URA CEA-CNRS 2210, H pital Frederic Joliot, Orsay, France o e Service de Neurologie, H pital Henri Mondor, Universit Paris XII, Cr teil, France o e e f Department of Neurology, University Hospital Alexandrovska, Soa, Bulgaria Accepted 7 July 2005

Abstract Previous research suggests that patients with Alzheimers disease (AD) are impaired on executive function early in the course of disease, but negative ndings were reported. To evaluate the performance on executive tasks in early AD and to determine the involvement of memory on the outcome of executive tasks. Thirty-six AD patients were divided into two subgroups on the basis of the MMSE: very mild and mild. The comparison with 17 normal controls shows that very mild AD patients had decits on visuospatial short-term memory, episodic memory, exibility and self-monitoring abilities, concept formation and reasoning. The mild AD patients showed additional decits on the Similarities test. Episodic memory and executive decits occur in the very early stage of AD and precede impairment in constructional praxis, language and sustained attention. With the progression of the disease, additional decit is observed in abstract thinking. In mild AD, memory failure is also related to executive impairment. 2005 National Academy of Neuropsychology. Published by Elsevier Ltd. All rights reserved.
Keywords: Alzheimers disease; Early stage; Executive function; Episodic memory

1. Introduction In recent years, the literature has reported that Alzheimers disease (AD) patients are impaired on a variety of tasks that have commonly been considered a measure of executive function (Collette, Delrue, Van Der Linden, & Salmon, 2001; Lambon, Patterson, Graham, Dawson, & Hodges, 2003; Logie, Cocchini, Della Sala, & Baddeley, 2004). According to some authors (Anderson & Tranel, 2002), executive function encompasses a number of cognitive abilities which are generally conceived of controlling or guiding behavior in a topdown fashion such as decisionmaking, planning, self-monitoring, and behavior initiation, organization and inhibition. Baddeley, Bressi, Della Sala, Logie, and Spinnler (1991) showed that AD patients were particularly impaired on dual-tasks even when the difculty of the tasks, performed separately, was equated across the groups and when the subjects did not have to store presented

Corresponding author. Tel.: +33 1 49 81 36 82; fax: +33 1 49 81 37 09. E-mail address: baudic@im3.inserm.fr (S. Baudic).

0887-6177/$ see front matter 2005 National Academy of Neuropsychology. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.acn.2005.07.002

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information. Bhutani, Montaldi, Brooks, and McCulloch (1992) showed decits on a series of executive tasks (verbal uency test, delayed alternation, Self Ordering Pointing Test and Wisconsin Card Sorting test) administered to very mild, mild and moderate AD patients. Laeche & Albert (1995) found that their very mild AD patients differed signicantly from controls on executive tasks (Self-Ordering task, Hukok Logical Matrices, Trail Making Test and verbal uency test) that required concurrent manipulation of information, i.e., set shifting, self-monitoring, or sequencing tasks. Some reports, however, are in contradiction with executive dysfunction in the early stage of the disease. For Broks et al. (1996), executive function is relatively spared in the early stage of the disease. Executive impairment was related to the severity and duration of AD. Similarly, Pillon, Dubois, Lhermitte, and Agid (1986) claimed that executive decits simply reect a moderate or severe cognitive deterioration. Another controversy lies in the implication of memory failure in the outcome of executive decits in AD. Broks et al. (1996) clearly attributed executive decits in their AD patients to memory impairment. The authors suggest that failure in executive function reects a selective vulnerability within limbiccortical networks secondary to a temporal lobe dysfunction. In contrast, Laeche and Albert (1995) failed to show a relation between memory and executive decits in their very mild AD patients, despite a variety of statistical analyses. Moreover, it must be pointed out that variability across studies in both tasks used to examine aspects of executive function, and in the disease severity, makes it difcult to determine which aspects of attention are affected earliest in AD, and how executive impairment is related to other cognitive modules. Consequently, we selected executive tasks which are more universally accepted like those mentioned in following studies (Grady et al., 1988; Laeche and Albert, 1995; Bhutani et al., 1992). The objective was to avoid to further clouding the issue by introducing additional measures. These conicting results lead us to conduct the current study. The aim of our study was to provide a more detailed analysis of the cognitive effects of AD in the earliest stages and, therefore to throw light on the relationships between the executive function and episodic memory. 2. Methods 2.1. Subjects Between January 1997 and December 1998, patients were referred for diagnostic investigation of dementia to the Notre Dame de Bon Secours Hospital, Paris, France. The evaluation procedure consisted in detailed medical history, physical and neurological examinations, cognitive evaluations, appropriate laboratory tests and neuroimaging. All patients underwent brain computed tomography (CT) or magnetic resonance imaging (MRI). History of medical, neurological and psychiatric troubles were obtained from the patient and family members (usually the patients spouse or children) or other caregivers. The Mini Mental State Examination (MMSE) (Folstein, Folstein, & Mc Hugh, 1975) was used to characterize global cognitive level. Signorets Battery of Cognitive Efcacy (B.E.C. 96; Signoret et al., 1989) was employed to diagnose AD using DSM IV and NINCDS-ADRDA criteria. None of these tests were used in the total battery. In order to allow for inclusion of mildly impaired patients, inclusion criteria were set arbitrarily to an MMSE score equal to or higher than 20/30. Among the 216 patients fullling the DSM-IV criteria for Dementia (Diagnostic and Statistical Manual of Mental Disorders, 1994), patients were excluded because of the following: (1) probable AD (McKhann et al., 1984) MMSE < 20 (n = 56); (2) possible AD (McKhann et al., 1984), or possible vascular dementia (VaD, Roman et al., 1993) (n = 49), or AD with cerebrovascular disease (CVD) (n = 38); (3) probable VaD (Roman et al., 1993) (n = 14); (4) other forms of dementia (n = 30) and (5) coexisting dementia and major depression (Diagnostic and Statistical Manual of Mental Disorders, 1994) (n = 42). The reminding 36 consecutive patients met DSM-IV criteria for Dementia of the Alzheimers Type (Diagnostic and Statistical Manual of Mental Disorders, 1994) and the NINCDS-ADRDA criteria (McKhann et al., 1984) for probable AD. At inclusion, the patients were divided into two subgroups on the basis on their scores on the MMSE. An upper cut-off of 24 was chosen to divide the two groups: very mild (corresponding to minimal cognitive impairment, very mild or possible AD in other classications; 2430 of MMSE) and mild (2023 of MMSE) (Perry, Watson, & Hodges, 2000). Eighteen patients presented mild AD and 18 minimal AD. The choice of the score of 24 as the split point is based on relevant theoretical grounds (Morris et al., 2001; Salmon et al., 2002). None of the AD patients demonstrated focal neurological signs or radiological evidence of stroke. In order to exclude, as much as we could, mixed (i.e., AD with CVD) (Roman et al., 1993) cases, patients who fullled NINCDS-ADRDA

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(McKhann et al., 1984) criteria for probable AD and had a single silent lacunae or a small cortical infarct found after brain imaging, were excluded from analysis in the study. We believe that this group clinically represents the possible AD with CVD category according to NINDS-AIREN criteria (Roman et al., 1993). Furthermore, AD patients with extensive white matter changes (i.e., extending periventricular and diffuse deep white matter changes) were excluded from the study. That means that patients with mild periventricular white matter changes were not excluded from this study. Seventeen normal controls (NC) without history or symptoms of psychiatric or neurological disease and with intact cognitive functions were recruited among patients relatives. They were matched to AD groups according to age and education level. 2.2. Material and procedure Global cognitive efciency was assessed with the MMSE. Short-term memory was evaluated by the Corsi Block Tapping Test (Milner, 1971). Episodic memory was examined by the Story Recall test from the Wechsler Memory Scale (WMS, Wechsler, 1987) and Buschkes Free and Cued Selective Reminding Test (FCSRT, Buschke, 1984), assessing free recall (number of items retrieved over three learning trials), total recall (number of words recalled with free and cued procedures over three learning trials), recognition and delayed recall (number of items recall with free and cued procedures over a delay of 20 min). Attention/Executive function were assessed by the Mental Control subtest (months backward) of the WMS; the Trail-Making Test (TMT), part A and part B (Reitan, 1958), assessing the number of correctly relayed items to avoid the ceiling effect on time measurement (4 min were allowed for each of the trials); and the Modied Card Sorting Test (MCST; Nelson, 1976) assessing the number of criteria achieved and perseverative errors. Language abilities were measured by an abbreviated formthe Similarities subtest of the WAIS Similarities (Boller & Hecaen, 1979), the 15-items subset of the Boston Naming Test (Kaplan, Goodglass, & Weintraub, 1983), the Token test (De Renzi & Faglioni, 1978) and the verbal uency test (names of animals produced in 1 min). Visuospatial abilities were evaluated by the Ravens Colored Progressive Matrices (RCPM; Raven, 1965) and constructional praxis (the copy of ve complex designs). 2.3. Statistical analyses We performed a multivariate analysis of variance (MANOVA) on the dependent variables of each test with the group factor to eliminate variations that cannot be attributed to the cognitive items under study. One-way analysis of variance (ANOVA) on each test variable was performed separately. If signicant main effects were found, pairwise difference was sought using post hoc analysis by Scheffes t-tests. All p-values are two-tailed. Statistical signicance was accepted at p < 0.05 level. Pearsons correlation coefcients were realized between the performances of episodic memory and executive tasks both in the very mild and mild AD patients. 3. Results Demographic characteristics of the patients and controls are presented in Table 1. There were no signicant differences between the groups of patients and controls according to age and education. The neuropsychological performances of the three groups included in this study are shown in Table 2. MANOVA revealed a signicant difference between groups on neuropsychological tests, Wilks lambda = 0.07, F (34, 68) = 5.553,
Table 1 Demographics and clinical characteristics NC (n = 17) Gender (M/F) Age (years) Education MMSE 3/14 81.6 (5.0) 9.5 (3.7) 29.1 (0.6) vmAD (n = 18) 3/15 81.4 (6.8) 8.4 (3.1) 25.6 (1.0) mAD (n = 18) 6/12 83.7 (6.7) 8.7 (4.4) 21.2 (1.2)
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NC: normal controls; vmAD: very mild Alzheimers disease; mAD: mild Alzheimers disease; values are means (S.D.).

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NC Memory Corsi Test Story Recall FCSRT free recall FCSRT total recall FCSRT recognition FCSRT delayed recall Attention/Executive function Mental Control Trail Making Test A Trail Making Test B MCST criteria MCST (PE) Language Similarities Boston Naming Test Verbal uency (score) Token test Visuospatial abilities Constructional praxis RCPM 5.1 (0.7)a,b 11.4 (2.7)a,b 31.7 (4.4)a,b 47.2 (1.1)a,b 15.7 (0.8)b 16.0 (0.0)a,b 12.9 (0.3)b 25.0 (0.0) 23.9 (2.5)a,b 5.8 (0.4)a,b 1.7 (2.1)a,b 10.7 (1.4)b 14.3 (0.9)b 19.2 (4.4)a,b 33.3 (2.2) 8.1 (0.8) 30.9 (3.0)a,b

vmAD 4.2 (0.9) 4.8 (2.4) 10.2 (6.3) 33.5 (9.0)c 14.4 (1.8) 12.4 (3.6)c 12.5 (0.9) 24.4 (1.7) 17.5 (7.2) 3.2 (1.6)c 7.3 (4.8)c 8.4 (3.5) 13.5 (1.6) 13.1 (4.9) 32.3 (2.6) 6.9 (2.0) 22.9 (6.0)

mAD 4.1 (0.7) 4.3 (4.1) 8.7 (8.9) 24.4 (13.2) 13.4 (3.1) 8.3 (5.0) 11.3 (2.6) 24.9 (2.9) 13.2 (6.3) 2.1 (1.0) 12.1 (6.3) 6.8 (3.3) 12.4 (2.5) 11.9 (5.0) 31.4 (3.5) 6.7 (2.1) 19.9 (5.3)

F 9.2 27.1 61.2 26.2 5.0 20.4 4.8 0.4 15.3 49.1 21.0 8.0 5.1 11.9 2.0 3.4 22.6

p <.0004 <.0001 <.0001 <.0001 <.0103 <.0001 <.013 <.647 <.0001 <.0001 <.0001 <.001 <.0098 <.0001 <.148 <.0424 <.0001

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Values are means (S.D.); FCSRT: Free and Cued Selective Reminding Test; MCST: Modied Card Sorting Test; PE: persevarative errors; RCPM: Raven Colored Progressive Matrices. a Scheff test of means: compared with vmAD. e b Scheff test of means: compared with mAD. e c Scheff test of means: compared with mAD. e

p < 0.05. ANOVA showed a signicant group effect for the majority of the tests (Table 2). Post hoc analysis showed a clear decit between the very mild AD patients and the controls on Corsi Block-tapping Test (p = 0.004), Story Recall (p = 0.0001), FCSRT (free recall p = 0.0001, total recall p = 0.0003, and delayed recall p = 0.018), TMT-B (p = 0.007), MCST (criteria p = 0.0001 and perseverative errors p = 0.004), verbal uency (animals, p = 0.002) and RCPM (p = 0.0001). Post hoc analysis also revealed a signicant difference between controls and mild AD. They were found to provide decits on Corsi Block-tapping Test (p = 0.001), Story Recall (p = 0.0001), FCSRT (free recall p = 0.0001, total recall p = 0.0001, recognition p = 0.011 and delayed recall p = 0.0001), Mental Control (p = 0.018), TMT-B (p = 0.0001), MCST (criteria p = 0.0001 and perseverative errors p = 0.0001), WAIS Similarities (p = 0.001), Boston Naming Test (p = 0.01), verbal uency (p = 0.0002) and RCPM (p = 0.0001). Post hoc analysis also indicated that the mild AD group was impaired relative to the very mild on FCSRT (total recall p = 0.02 and delayed recall p = 0.005), MCST criteria and perseverative errors (p = 0.03 and p = 0.02). Correlation analysis between the scores of executive function tasks and FCSRT were performed. No signicant correlation was observed in very mild AD patients. In contrast, correlations were noted in mild AD, the rst ones between recognition and MCST criteria number (r = 0.59, p < 0.01) and perseverative errors (r = 0.47; p = 0.05) and the second ones between WAIS Similarities and FCSRT (free recall (r = 0.49, p < 0.05) and delayed recall (r = 0.48, p < 0.05). 4. Discussion The results of our study support the presence of executive impairment in AD patients, early in the course of the disease. Furthermore, the results show that impairment of executive function in very mild AD patients precedes the disturbance of sustained attention, language (oral comprehension, verbal abstraction and naming)

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and constructional abilities. In the group of mild AD patients, that is, with the progression of the disease, we observed a correlation between the performance on MCST (criteria and perseverative errors) and episodic memory. Our results of executive function impairment in the earliest stage of AD are in agreement with those of Laeche and Albert (1995). In addition to this study, our very mild AD patients also presented signicantly lower performance on RCPM and on verbal uency test. These additional results are not in contradiction with the suggestion of executive dysfunction in the very mild AD. Concerning the RCPM, we suggest that this early appearance of decit is rather the result of early impairment of processes such as non-verbal reasoning and decision-making, than of visuospatial abilities. Accordingly, Le Carret et al. (2003) studying the performance on RCPM in patients with early AD, found signicant impairment independently of the educational level and concluded that the cognitive processes that make it possible to discover complex rules are particularly vulnerable in AD. According to Carpenter, Just, and Shell (1990), RCPM depends heavily upon internal representation of previous sets and the current conceptual set. It is itself a working memory function involving the prefrontal cortex (Prabhakaran, Smith, Desmond, Glover, & Gabrieli, 1997). With regard to the early verbal uency impairment, our ndings are in agreement with previous studies showing a high sensitivity of verbal uency test for detecting dementia. It must be pointed out that verbal uency relates to multiple cognitive abilities. This task appears to involve lexical access to words belonging to a given semantic category, storage decit for a specic semantic category, decit of retrieval reecting an executive dysfunction, or merely a decit in processing speed, since this task is a timed task (Ruff, Light, Parker, & Levin, 1997). Therefore, it is difcult to know whether a decit of verbal uency can be traced back to a linguistic, a semantic, or an executive dysfunction. Our results also agree with the suggestion that some subcomponents of executive control, such as the capacity to divide attention and to shift between two concurrent tasks, may be particularly susceptible to the effect of AD, while other attentional/executive processes may be relatively preserved (Baddeley, Baddeley, Bucks, & Wilcock, 2001). In fact, we obtained normal performance on the task of sustained attention (Mental Control and TMT-A), whereas we observed marked impairment in the capacity of AD patients to combine performance on two simultaneous tasks. Our results also concur with the conclusion of Perry et al. (2000) that appears to indicate differential impairment of different aspects of attention. According to these authors, sustained attention is the least affected among the three potentially separable subsystems of attention (sustained, selective and divided attention). It might be reasonable to interpret the ndings in terms of topographical distribution of neuropathology in early AD. While it is generally agreed that early memory impairment in AD is associated with medial temporal lesions early in the course of the disease, it is very difcult to explain the early impairment of executive function in terms of direct early involvement of frontal regions. It must be stressed, however, that the precise anatomical correlates of executive function are still a matter of debate. Several authors (Kessler, Mielke, Grond, Herholz, & Heiss, 2000; Collette et al., 2001) have proposed that early disconnection of the cortico-cortical tracts is the cause of the executive impairment in AD. The disruption of connections between the posterior and anterior association areas hinders the integration of information that comes from the different cerebral areas. Executive function is sustained by a distributed cortical neural network rather than by a unique frontal region and is very sensitive to disruption. Moreover, a fairly large number of tasks have been used to measure frontal functions, but their specicity has not always been clearly established. These tests may sometimes be affected by lesions of non-frontal areas (Anderson, Bigler, & Blatter, 1995; Van der Werf, Witter, Uylings, & Jolles, 2000) and in diffuse pathology (Boller et al., 1995) or, paradoxically, may be spared by lesions that clearly affect the frontal lobes (Andres & Van der Linden, 2002). With regard to correlation analysis, our results revealed that episodic memory is implicated in the outcome of executive function decits on MCST as the disease progresses. Compatible with the results of Laeche and Albert (1995), we failed to show any interaction between memory and executive function decits in the group of very mild AD patients. However, in the group of patients with mild AD, we observed signicant correlations between recognition memory and Modied Wisconsin on one hand, and free recall and WAIS Similarities on the other. In this more advanced stage, the additional decit that appeared in comparison to the very mild group was the verbal concept formation ability, as was shown by the lower performance of mild AD patients on WAIS Similarities. This impairment is probably implicated in the interactions shown in mild AD between the performance of executive tasks and episodic memory on certain tasks. Recognition and free recall involve verbal concept formation for active search mechanisms to locate and verify a unique item. This process may share elements of processing with the strategies needed in the Modied Wisconsin and Similarities performances. Existence of correlations between MMSE score and individual

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tests of the battery (Raven, Similarities, FCST total and delayed recall, TMT-B and MCST criteria and perseverative errors, all p < 0.05) in the total group of AD strengthens this hypothesis. There are some limitations to the current study. We cannot be certain about our rate of diagnostic misclassication because of the lack of neuropathological conrmation of our clinical diagnoses. However, to avoid misdiagnosis, especially with fronto-temporal dementia (FTD), we have carefully examined the presence of behavioral abnormalities in our patients. Behaviors were assessed during caregiver interviews using the dysfunctional frontal scale (Lebert, Pasquier, Souliez, & Petit, 1998). The cognitive prole of patients was examined in detail. None received a clinical diagnosis of FTD based on criteria developed by the Lund and Manchester Groups (Brun et al., 1994). However, the detailed clinical and neuropsychological assessments, neuro-imaging to clarify cerebral abnormalities, and nally, the use of a trained research team consisting of a neuropsychologist, geriatrician, and neurologist (also trained in brain imaging) reasonably limited the chance for diagnostic misclassication. We paid special attention not to include patients with subcortical vascular lesions or depression in our study. In conclusion, our results show that executive function is impaired in early AD patients, even in the very early stage of disease. Moreover, episodic memory and executive function decits precede impairment in constructional praxis, language and sustained attention. Executive function decits appear predominantly in tasks requiring resolution of competing response tendencies, cognitive exibility and self-monitoring. Furthermore, our results lead to the conclusion that episodic memory seems to be implicated in the outcome of executive function decits as the disease progresses. As preventive strategies are developed and new cognitive enhancing therapies emerge, these results may also help us to anticipate which cognitive domains are expected to improve in populations with very mild Alzheimers disease. Acknowledgement We wish to express our appreciation to Dr Anne Petrov for her helpful assistance in reviewing the English version of the manuscript. References
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