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Aging, Neuropsychology, and Cognition

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Differential Course of Executive Control Changes During Normal Aging

Friederike H. Treitz a; Katrin Heyder a; Irene Daum a a Institute of Cognitive Neuroscience, Ruhr University of Bochum, Germany First Published on: 23 July 2006 To cite this Article: Treitz, Friederike H., Heyder, Katrin and Daum, Irene (2006) 'Differential Course of Executive Control Changes During Normal Aging', Aging, Neuropsychology, and Cognition, 14:4, 370 - 393 To link to this article: DOI: 10.1080/13825580600678442 URL: http://dx.doi.org/10.1080/13825580600678442

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Aging, Neuropsychology, and Cognition, 14: 370393, 2007 http://www.psypress.com/anc ISSN: 1382-5585/05 print; 1744-4128 online DOI: 10.1080/13825580600678442

Differential Course of Executive Control Changes During Normal Aging

1744-4128 1382-5585/05 NANC Aging, Neuropsychology, and Cognition Cognition, Vol. 00, No. 0, June 2006: pp. 147 Executive Control Friederike H. Treitz Changes et al. During Normal Aging

FRIEDERIKE H. TREITZ, KATRIN HEYDER AND IRENE DAUM

Institute of Cognitive Neuroscience, Ruhr University of Bochum, Germany

ABSTRACT
Normal aging has been associated with executive control deficits, but it is as yet unclear whether different executive subprocesses are differentially affected during the course of aging. The present study aimed to investigate age effects on a range of executive control subcomponents. Four consecutive age groups (2030 years, 3145 years, 4660 years, 6175 years), matched on present state IQ and mood, were compared on tasks of strategic memory processing, verbal fluency, reasoning, inhibition, task management, and self-rating of executive abilities. Deficits concerning the suppression of habitual and experimentally induced prepotent response tendencies and the ability to efficiently divide attention were observed in subjects over 60 years of age compared to the younger groups, while memory, verbal fluency, and reasoning were largely unaffected. Results suggest a sharp decline of executive function after age 60 and a differential course of different executive subcomponents across aging, adding further support to a multi-dimensional model of executive function.

The cognitive decline associated with normal aging is generally discussed in relation to mild neurodegenerative changes, including neuronal shrinkage, loss of dendritic and synaptic density, or alterations in neurotransmitter systems (Backman et al., 2000; Jernigan et al., 2001; Kaasinen et al., 2000; Resnick et al., 2003; Tisserand & Jolles, 2003; Wang et al., 1995, 1998). Disproportionate volume loss occurs within the frontal lobes and the hippocampal region, but changes in the thalamus and the mamillary bodies are also observed (Guttmann et al., 1998; Jernigan et al., 2001; Raz et al., 1992, 2004; Resnick et al., 2003; Salat et al., 2001; Van Der Werf et al., 2001; Woodruff-Pak, 1997). With respect to the prefrontal cortex, grey matter volume loss was reported to reach 8.9% per decade in subjects over 65 years of

Address correspondence to: Friederike H. Treitz, Institute of Cognitive Neuroscience, Department of Neuropsychology, Ruhr-University of Bochum, 44780 Bochum, Germany. E-mail: friederike.treitz@ ruhr-uni-bochum.de 2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business

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age (Van Petten et al., 2004). In addition, functional neuroimaging studies reported evidence of reduced activations within the prefrontal cortex in older compared to younger adults (Logan et al., 2002). Given the frequently reported neuropathological changes in the prefrontal cortex (PFC) relative to other cortical areas (Head et al., 2004; Jernigan et al., 2001; Raz et al., 2004; Resnick et al., 2003), older age has been considered a model of diffuse mild prefrontal dysfunction and associated executive control impairments (West, 1996). This view is supported by parallels in the cognitive profile of healthy elderly subjects and young individuals with acquired PFC lesions (Daum et al., 1996; Daum & Mayes, 2000; Daum & Schugens, 1999), characterized by deficits in source memory, memory for temporal order, or impaired use of cognitive strategies (Daum et al., 1995; Daum & Schugens, 1999; Glisky et al., 2001; Mayes & Daum, 1997). Executive control has recently been described as a heterogeneous concept, involving five major subcomponents (Smith & Jonides, 1999): a.focusing attention on relevant information and inhibiting irrelevant information; b.task management, including switching attention between tasks; c.planning a sequence of subtasks to accomplish a goal; d.updating working memory contents to determine the next step in a sequential task; e.coding context of representations in working memory. Following Shallice and Burgess (1991), the prefrontal cortex is associated with the supervisory attentional system (SAS), which is responsible for strategic control of mental processes, such as the use of strategies or ruleguided retrieval from long-term memory. In novel and unfamiliar situations, the SAS is responsible for strategy formation, planning, and problemsolving to achieve goals. Aging has been reported to adversely affect most of the executive control subcomponents defined by Smith and Jonides (1999), as well as executive processes describes by Shallice and Burgess (1991). Meta-analyses by Verhaeghen and Cerella (2002) yielded a consistent agerelated decline of task management abilities beyond the effect of general slowing. Set-shifting deficits in older adults have been related to mild frontal dysfunction (Keys & White, 2000; Kramer et al., 1999; Kray & Lindenberger, 2000; Meiran et al., 2001). Age effects have been reported for the use of organizational strategies in memory, such as self-generated use of semantic categories (Daum et al., 1996). Inhibition of habitual responses, as assessed by the Stroop Test (e.g., Wecker et al., 2000), as well as inhibition of newly learned prepotent responses, were also found to be affected by age (McDowd, 1997; Verhaeghen

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& De Meersman, 1998a). Whether these inhibition deficits can be attributed to a general slowing of information processing or whether they represent a specific age-related executive impairment, is a matter of an ongoing debate (Gamboz et al., 2002; Grant & Dagenbach, 2000; Schelstraete & Hupet, 2002; Shilling et al., 2002; Uttl & Graf, 1997; Van der Linden, 2000; Verhaeghen & De Meersman, 1998b; Wecker et al., 2000; West & Alain, 2000). In spite of the wealth of empirical data, the pattern and course of age effects on executive function is as yet inconclusive. The available studies were mainly based on extreme group comparisons where a number of variables other than age may influence group differences (e.g., Brink & McDowd, 1999; Grant & Dagenbach, 2000; Shilling et al., 2002; Van der Linden, 2000). Longitudinal studies often reported an accelerated decline in later life (e.g. Schaie, 1996), while cross-sectional studies suggest a gradual linear decline across adulthood (Park et al., 1996; Salthouse, 2003). By using a cross-sectional design with four consecutive age groups, the present study aimed to assess the course of executive function changes during adulthood. The investigation of consecutive age groups is useful to economically assess linear vs. critical threshold changes with respect to different subprocesses of executive control, even though cohort effects cannot be completely eliminated. The data should contribute to the issue of whether age-related changes manifest themselves gradually or whether deficits occur once a critical threshold has been reached, leading to a nonlinear change. In addition, different executive control subprocesses may be associated with independent neuronal substrates (see Heyder et al., 2004; Smith & Jonides, 1999), and may therefore follow a differential course during aging. It has been suggested that processes related to the dorsolateral PFC are particularly affected by aging (MacPherson et al., 2002), given that there is evidence of relative sparing of the orbitofrontal region (Salat et al., 2001), although comparable effects on dorsolateral and orbital PFC regions have also been reported (Raz et al., 1997; Tisserand et al., 2002). These conflicting results may relate to the methods of volume measurement (Tisserand et al., 2002). In summary, the present study aimed to further elucidate the effect of normal aging on the course of executive control changes, focusing on task management and inhibition as the most elementary executive processes (see Smith & Jonides, 1999).

METHODS Subjects Sixty-two healthy subjects (34 men and 28 women) were selected from a large subject pool to form four consecutive age groups matched on general intellectual abilities. The first group comprised the 2030 year age range, the

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TABLE 1. Group Size, Mean (SDs) Age, IQ Estimates, and Scores in the VAS (Visual Analogue Scales) for the Consecutive Age Groups 2030 yrs. Mean age in yrs. N IQ estimate VAS 25.4 (3.3) 16 111.4 (4.8) 29.9 (11.9) 3145 yrs. 38.8 (4.3) 16 114.4 (4.6) 24.4 (9.3) 4660 yrs. 52.4 (3.9) 13 112.0 (5.7) 25.4 (11.4) 6175 yrs. 67.5 (4.4) 17 112.0 (7.4) 20.7 (13.3) p 0.45 0.17

second group the 3145 year range, the third group the 4660 year range, and the oldest group the 6175 year range. The four groups were closely matched on present state IQ, as assessed by the Similarities and Picture Completion subtests of the short German version from the Wechsler Adult Intelligence Scale (Dahl, 1972). The groups were also matched on sex ratio and present-state mood (Visual Analogue Scales; Bond & Lader, 1974). For an overview of background data see Table 1. Subjects were recruited by advertisements in the local press. They were screened in an interview for health problems. Based on the interview, subjects were excluded from participation if they had suffered from psychiatric or neurological disease in the past or present or from diseases potentially effecting the central nervous system. Subjects gave written informed consent and received a 20 euro reimbursement. Neuropsychological Assessment Strategic Memory Processing To assess the self-generated use of memory strategies, verbal memory was assessed by word list recall (Daum & Mayes, 2000). Three lists consisting of 16 items each were read to the subject at a one word per second presentation rate. The first list consisted of four items of each of four categories (metals, animals, landscape formations, vegetables), which were presented in order of category membership (consecutive categories list; CC). The second list also contained four items of each of four categories (items of clothing, fruit, furniture, and weather conditions), which were presented in randomized order (randomized categories list; RC). Encoding and retrieval of the RC list can be improved by self-generated categorization of the list according to semantic categories. The third list was uncategorized (RR), i.e., the 16 items were unrelated. List order was randomized across subjects. Subjects were asked to reproduce each list immediately after presentation. Delayed free recall was assessed after a 30-min delay. The number of correctly reproduced items per list during both delays (immediate, delayed) as well as retention rates (correct items delayed recall/immediate recall) were analyzed.

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Verbal Fluency/Cognitive Flexibility To assess efficiency of rule-guided retrieval from long-term memory, a verbal fluency task with three conditions was administered (see Daum et al., 1994). This procedure involved rule-guided search strategies, strategic retrieval from semantic long-term memory, as well as cognitive flexibility. The number of correctly produced exemplars was assessed in three fluency conditions: a semantic category condition (countries), a phonemic category condition (nouns beginning with B), and a switching condition (alternate vegetables and male first names). The switching condition was added as a measure of task management, which requires the switching of attention between tasks. Subjects were asked to produce as many exemplars as possible within 1 minute for each condition. Reasoning A German adaptation of the Cognitive Estimates Test (CET; see Shallice & Evans (1978) and Daum & Mayes (2000) was administered to assess the ability to draw plausible conclusions and to give realistic estimates based on the subjects knowledge and reasoning. Subjects were asked to give estimates for 10 problems such as How tall is the Cologne Cathedral? Based on criteria described by Hodges (1996), the scoring ranged from 0 (response within the normal range) to 3 (large deviation from the normal range). Everyday Behavioral Correlates of Executive Impairment To evaluate the everyday consequences of reduced executive control, the Dysexecutive Questionnaire (DEX) from the Behavioral Assessment of the Dysexecutive Syndrome (BADS) Test battery (Wilson et al., 1996) was administered. The 20-item questionnaire addresses a range of problems associated with the Dysexecutive Syndrome including emotional or personality changes, motivational changes, or behavioral problems. Each item was scored on a 5-point scale ranging from never to very often. Sum scores were obtained for the self-rating and the independent rating, respectively. In the independent rating, the DEX was also completed by a close relative or friend. Inhibition To assess the ability to focus attention on relevant information and to inhibit irrelevant responses, an adaptation of the Stroop Test (Bumler, 1985) and a version of the AX-Continuous Performance Test (AX-CPT) previously described by Braver et al. (1999) were administered. In the Stroop Test, subjects had to read out the names of colors printed in black (reading color words (RCW)), name the color of colored patches (NCP), and they also had to name the print color of color words, with print

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color and color names being incongruent (interference (INT)). To account for reading speed and color-naming speed, reaction times (RTs) in the interference condition were analyzed using RTs in the RCW and NCP conditions as covariates. The number of errors in the interference condition was also recorded. In the AX-CPT task, letters were presented sequentially on a computer screen. Letter size was 3.8 3.8 visual angle at a distance of 40 cm. In 70% of the trials, the letter X followed the letter A and subjects had to press a target key to the A-X sequence. The remaining trial types were A followed by the letter Y (the inhibition trial type), B-X and B-Y trial types (Y represents all letters except X, and B represents all letters except A) with a frequency of 10% each. To these combinations, subjects had to press a nontarget key on the keyboard. Subjects used the index and middle finger of their dominant hand. The high frequency of the A-X combination induced a prepotent response tendency to the target key after presentation of the letter, A which had to be suppressed for the rare A-Y sequence (which requires the nontarget key). The task was administered in a short- and a long-delay condition (100 trials each), with order being randomized across subjects. Each trial started with a hyphen presented for 200 ms in the center of the screen for fixation, followed by the first letter (200 ms). The interstimulus interval (ISI) was 1000 ms (short-delay condition) or 4000 ms (long-delay condition), thereby varying working memory load. Then the second letter appeared for 200 ms, to which the subject had to respond. Median RTs and errors were recorded for each trial type. Based on the procedure used by Braver et al. (1999) and Carter et al. (1998), difference scores representing inhibition and use of context entered analysis: 1. Context cost: RTs A-Y minus RTs B-Y: Degree of response slowing in nontarget trials where the prepotent response tendency has to be suppressed. 2. Inhibition cost: RTs A-Y minus RTs A-X. Index of inhibition, where the prepotent response to the target key induced by A needs to be inhibited if Y occurs. 3. Context use: RTs B-X minus RTs B-Y. Degree of response slowing in nontarget trials on the ambiguous X stimulus. Small differences between both trial types indicate benefit from use of context. Task Management Task management in stimulus processing was assessed by two tasks, the Divided Attention subtest of a German Attention Test Battery (Zimmermann & Fimm, 1993) and by a dual-task paradigm described by Stablum et al. (2000). In the Divided Attention task, subjects had to

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process two sensory channels in parallel, while motor output did not differ. In the Dual Task, subjects had to coordinate between information from two sensory channels and two motor responses. In the Divided Attention task, subjects were asked to press a key as fast as possible to particular stimulus configurations presented in two sensory domains. In the visual domain, subjects had to respond if crosses appearing randomly on a computer screen formed a square. Subjects had to simultaneously attend to a sequence of high and low pitched tones. If two consecutive tones were of the same pitch, the response key had to be pressed. Reaction times and errors were recorded. The Dual Task procedure comprised a single- and a dual-task part and assessed the ability to process two stimulus features and to coordinate two motor responses. During both subtests, two letters (3.8 9.5 visual angle at a distance of 40 cm) appeared in a vertical arrangement on a computer screen (17), either to the right or to the left of a central fixation point. The letters were either the same or different (50% each) and were presented for 150 msec. In the initial single task part, subjects were instructed to press a left or a right key, depending on the location relative to the central fixation point. In the dual task part, subjects also had to make the location decision by pressing the respective keys, but they additionally had to indicate verbally whether the letters were the same or different. Eighty trials were presented in each condition; RTs and errors were recorded. In addition, dual task costs were assessed by calculating a dual task variable (DTC: (RTs dual task RTs single task)/RTs single task). General Procedure All subjects completed the test battery in one session. Each session lasted 1.5 to 2 hours. Tasks were administered in the following order: Verbal Fluency, Cognitive Estimation Test, Word List Recall (immediately), Divided Attention, AX-CPT, Word List Recall (delayed), Stroop-Test, DualTask, DEX. AX-CPT test administration was followed by a rest interval. The list order for word list recall was randomized between subjects. Data Analysis Statistical analysis was performed using SPSS version 11.0 (SPSS Inc.). Group differences were evaluated by nonparametric Kruskal-Wallis-H or Analysis of Variance (ANOVA), where appropriate. If significant group differences were found, pairwise comparisons were performed (Mann-Whitney-U and Bonferroni, respectively). For nonparametric post-hoc comparisons, the significance level was set to p < .008. Repeated measure ANOVAs were performed with Bonferroni adjusted post-hoc testing. When Analysis of Covariance (ANCOVA) was performed, the significance level for post-hoc pairwise ANCOVAS was set to p < .008. For Pearson correlations, the

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significance level was set to p < .05. In addition, eta2 effect sizes were calculated in case the demands for ANOVA were met. RESULTS Strategic Memory Processing The results for word list recall are presented in Table 2. Repeated measures ANOVA with Group, List (CC, RC, RR) and Delay (immediate vs. delayed free recall) as factors did not yield a significant group effect (p = .19) or significant interactions involving the group factor (all p > .59). Effect size was eta2 = 0.3. A significant delay effect [F1,58 = 450.808; p < .001] indicated better recall at immediate relative to delayed recall. A significant list effect [F2,116 = 51.146; p < .001], followed by a paired t-test indicated best recall of the consecutive categories and randomized categories list and poorest recall of the uncategorized list (all p < .001). Analysis of retention rates with group and list as factors indicated a significant main effect for List [F2,116 = .511; p < .001], but no significant effects involving the group factor (all p > .79). For the CC-list, effect size was eta2 = 0.04, for the RC list it was eta2 = 0.01 and eta2 = 0.06 for the RR-list. Verbal Fluency/Cognitive Flexibility The results for the three fluency subtests are presented in Table 2. The four age groups did not differ significantly with respect to the number of correctly produced items in the semantic (p = .18; eta2 = 0.08), phonemic (p = .60; eta2 = 0.03), or switching condition (p = .25; eta2 = 0.07). Reasoning The results for the Cognitive Estimation Test are presented in Table 2. Nonparametric group comparisons did not reveal significant age group differences (Hdf = 3.58 = 2.265; p = .52). Everyday Consequences of Executive Impairment The results for the DEX questionnaire are presented in Table 2. Repeated measure ANOVA with group and condition (self-rating vs. independent rating of dysexecutive behavior) as factors did not yield a significant group effect (p = .56, eta2 = 0.04) or a significant interaction (p = .12, eta2 = 0.11). Separate group comparisons of subjects DEX self-rating and relatives independent rating of dysexecutive behavior did not reveal significant group differences [(F3,58 = .241; p = .87; eta2 = 0.01) and (F5,50 = 1.392; p = .26; eta2 = 0.07), respectively].

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TABLE 2. Means (SDs) for Cognitive Performance in the Four Age Groups 2030 Yrs. Strategic Memory Processing Word list recall immediately (no. correct) consecutive categories 10.6 (2.0) randomized categories 9.1 (2.3) uncategorized 7.6 (2.2) Word list recall delayed (no. correct) consecutive categories 6.8 (2.2) randomized categories 6.1 (3.2) uncategorized 2.6 (1.6) Verbal Fluency/Cognitive Flexibility (no. correct) semantic 29.9 (9.5) phonemic 13.1 (3.8) switching 16.3 (4.0) Reasoning Cognitive Estimation Test 4.5 (2.5) Subjective Rating DEX self-rating 22.1 (6.0) DEX independent rating 14.9 (8.0) Inhibition Stroop Test RTs RCW 25.9 (2.1) RTs NCP 44.1 (6.9) RTs INT 67.4 (10.2) INT no. corrected errors 2.9 (2.3) INT no. uncorrected errors 0.8 (0.7) AX-CPT context use 10.8 (35.7) context costs 220 (53) inhibition costs 145 (43) Multi-tasking Divided Attention RTs in msec 597 (67) no. errors 2.4 (2.5) Dual task RTs single condition 298 (33) single condition no. errors 0.7 (0.9) RTs dual condition 386 (48) dual condition no. errors 2.2 (2.0) 3145 Yrs. 4660 Yrs. 6175 Yrs.

10.9 (2.6) 8.4 (3.5) 7.7 (2.6) 6.4 (2.8) 5.3 (3.8) 3.4 (2.8) 28.1 (6.5) 12.9 (2.6) 17.1 (2.5) 3.7 (3.1) 22.7 (11.7) 17.4 (9.7)

9.5 (3.6) 7.5 (2.3) 6.3 (1.8) 5.7 (2.9) 4.9 (2.6) 2.6 (2.0) 25.7 (7.4) 13.2 (3.2) 14.7 (2.7) 3.4 (2.5) 22.3 (7.6) 21.7 (10.7)

9.7 (2.1) 8.2 (2.3) 6.4 (1.7) 5.1 (2.4) 5.3 (2.5) 1.8 (1.5) 24.5 (5.9) 11.8 (3.8) 15.9 (3.0) 3.5 (2.4) 20.4 (7.0) 23.7 (17.8)

28.6 (5.0) 45.0 (8.4) 70.9 (14.6) 3.0 (2.7) 0.6 (1.0) 6.4 (34.8) 189 (85) 147 (59)

30.0 (5.8) 43.2 (9.5) 80.2 (18.8) 2.5 (2.9) 2.6 (2.8) 16.4 (60.3) 200 (57) 137 (64)

33.8 (3.8) 48.7 (6.7) 91.5 (14.6) 4.0 (4.1) 2.5 (2.4) 13.5 (38.7) 341 (117) 211 (93)

641 (55) 2.4 (2.2) 345 (45) 0.4 (0.6) 431 (116) 1.3 (1.5)

694 (51) 5.2 (3.4) 364 (65) 0.4 (0.7) 454 (66) 2.1 (3.2)

707 (74) 4.4 (3.4) 397 (44) 0.4 (0.7) 675 (138) 5.6 (4.2)

DEX-Dysexecutive Questionnaire; AX-CPT-AX-Continuos Performance Test.

Inhibition Stroop Test Results for the Stroop Test are presented in Figure 1. ANCOVA with RTs in the RCW and NCP conditions as covariates indicated a significant group effect for RTs in the INT condition (F3,56 = 6.302; p = .001, eta2 = 0.25).

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FIGURE 1. Mean interference scores and SDs of the four age groups in the Stroop Test. INT-interference; RCW-read color words; NCP-name color pictures.

After Bonferroni correction, subsequent paired group ANCOVAs revealed significant group effects for comparisons of the oldest and the two youngest groups (all p < .008), indicating a significant slowing of the 61+ group in the interference condition. The results for errors in the interference condition are presented in Table 2. The four age groups did not differ with respect to corrected errors (Hdf = 3 = 1.344; p = .72), but there was a significant group difference for uncorrected errors (Hdf = 3 = 12.092; p < .01), with the oldest group making more errors than the youngest group (p = .001). Continuous Performance Task Because repeated measures ANOVA of RTs with Group, Condition, and Delay as factors did not yield any significant interactions involving the delay factor (all p > .38), further analyses were performed with RTs pooled for the two delays. Analysis of inhibition costs (RTs A-Y minus A-X, see Figure 2) and context costs (RTs A-Y minus B-Y, see Figure 3) yielded significant age group differences [(F3.58 = 4.159, p < .01, eta2 = 0.18) and (F3,58 = 11.418, p < .001, eta2 = 0.37), respectively], with higher inhibition cost for the oldest compared to the youngest and second oldest group (all p < .05) and higher context cost (all p .001) for the oldest group compared to all

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FIGURE 2. Means and SDs of inhibition costs (RTs A-Y minus A-X) in the AX-CPT task for the four age groups.

FIGURE 3. Means and SDs of context costs (RTs A-Y minus B-Y) in the AX-CPT task for the four age groups.

other groups. Analysis of context use (RTs B-X minus B-Y, see Table 2) did not yield significant group differences (F3,58 = 1.594, p = .20, eta2 = 0.08). In further analyses, group differences were explored using RTs in the B-Y condition as covariate. ANCOVA yielded highly significant age group

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differences for inhibition cost (p < .01) and context cost (p < .001), and the respective paired age group comparisons also remained significant for context costs (all p .001). For inhibition costs, paired group comparisons revealed significant differences between the oldest and youngest group (p < .004). Task Management Divided Attention Results for the Divided Attention task are presented in Figure 4. There was a significant age group difference for RTs (F3,58 = 10.193; p < .001, eta2 = 0.35), with the oldest group showing longer RTs than the youngest (p < .001) and the second youngest group (p < .02). The second oldest group was also slower than the youngest group (p = .001). There was a significant age group difference for errors (Hdf = 3 = 10.655; p < .01). Post-hoc comparisons did not yield significant differences for error rates (all p > .008). Dual Task The results for the dual task are illustrated in Table 2 and Figures 5 and 6. RT analysis with Group and Task as factors yielded a significant interaction (F3,57 = 24.482; p < .001, eta2 = 0.55). Post-hoc paired group comparisons revealed significant Group Task interactions (all p < .001) in all comparisons involving the oldest group, suggesting that the oldest group showed larger dual task costs than any of the other groups.
FIGURE 4. Means and SDs of RTs and number of errors in the divided attention task for the four age groups.

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FIGURE 5. Scattergram of mean RTs in the single and dual condition of the dual task.

FIGURE 6. Mean RTs and SDs in the single and dual condition of the dual task for the four age groups.

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Comparable results emerged for the dual task costs variable (DTC: (RTs dual task RTs single task)/RTs single task). The groups differed significantly on DTC [F3,57 = 18.112; p < .001, eta2 = 0.49]. Post-hoc comparisons revealed significant differences between the oldest group and all other groups (all p < .001). Repeated measures ANOVA of errors with Group and Task as factors yielded a significant interaction (F3,57 = 7.205; p < .001, eta2 = 0.28). Posthoc analyses yielded significant Group Task interactions (all p < .003) when the oldest group was compared to the two youngest groups. Comparisons including the oldest group, indicating a disproportional increase in errors from the single to the dual task condition in the oldest group. After statistical control of response speed by using RTs of the single task as covariate, ANCOVA yielded a highly significant age group difference for RTs in the dual task (F3,56 = 14.823; p < .001, eta2 = 0.44), which was due to slower RTs in the oldest compared to the second youngest and second oldest group (all p .001). Correlations To supplement the group comparisons, cognitive test performance was correlated with age. Significant correlations were found for found for a range of executive function variables of the Stroop Test (INT-RCW, r = .50, p < .001; INT-NCP, r = .63, p < .001; uncorrected errors, r = .45, p < .001), the AX-CPT (inhibition cost, r = .34, p < .01; context cost, r = .32, p = .01; context benefit, r = .26, p = .05), divided attention (RTs, r = .58, p < .001; errors, r = .36, p = .004) and the dual task (RTs: single condition, r = .65, p < .001; dual condition, r = .73, p < .001; errors, r = .39, p < .01). Intercorrelations between tests yielded correlations between AX-CPT context costs and Stroop INT-RCW (r = .28, p = .03) as well as INT-NCP (r = .35, p < .01). DISCUSSION The present study aimed to investigate the effect of normal aging on the course of executive function subcomponents in four consecutive age groups covering age ranges from 20 to 75 years. The groups were well matched for present state IQ and mood. Taken together, the results show a differential effect of normal aging on different subcomponents of executive control. Following Smith and Jonides (1999) subdivision of executive control, the inhibition and task management subcomponents were both significantly affected by age. Combined inhibition and task management deficits were observed in subjects over 60 years of age on all tests, which addressed such abilities. Impairments involved both the inhibition of strong habitual response tendencies as well as weaker, experimentally induced predominant responses. Abilities to coordinate information from two sensory channels and to coordinate

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two motor responses were also significantly affected. A milder problem in task management, which manifested itself only if two sensory channels had to be processed in parallel was also present in subjects in the 46 to 60 year age range. Strategic memory processing, cognitive flexibility, reasoning, or self-report and awareness of executive problems in everyday life, on the other hand, did not yield age differences. Taken together, this pattern suggests an accelerated cognitive decline after the age of 60. In middle-aged subjects of comparable general abilities, executive control problems are weak, affecting the ability to divide attention only, or even absent. These findings are consistent with longitudinal aging studies, which suggested that cognitive changes tend to be minor before age 60 and show a sharp decline after the age of 80 (Schaie, 1996). Crosssectional studies on the other hand, have so far suggested a gradual decline across the adult life span (Park et al., 1996; Salthouse, 2003). The results of the present study are generally consistent with the idea of age-associated executive dysfunction. Although PFC lesions in younger subjects appear to differentially affect inhibition of habitual and short-term weaker response tendencies (see Heyder et al., 2004), both inhibition types are consistently found to be affected by nonpathological aging (McDowd, 1997; Verhaeghen & De Meersman, 1998a; Wecker et al., 2000). The interference condition of Stroop-type tasks appears to be a particular sensitive test (Woodruff-Pak, 1997), with elderly subjects needing to recruit additional PFC resources for adequate performance (Langenecker et al., 2004). It is, however, as yet unclear whether older subjects suffer from a genuine inhibition problem, as suggested, e.g., by electrophysiological studies (West, 2004; West & Alain, 2000) or whether large interference effects are secondary to general slowing with age (Shilling et al., 2002; Verhaeghen & De Meersman, 1998b; Wecker et al., 2000). In the present study, long RTs in the oldest group were accompanied by high error rates (maximum of nine uncorrected errors compared to two in the youngest group). Given this pattern, it is unlikely that the findings in subjects over 60 years old are attributable to response-slowing only, but rather seem to present a genuine inhibition problem. As the age groups differed only on uncorrected, but not on corrected errors, the oldest group may have an additional problem in error processing (Nieuwenhuis et al., 2002). The inhibition of short-term, experimentally induced prepotent response tendencies has been studied mainly with the negative priming paradigm, where the distractor of one trial serves as the target in the following trial, inducing a response delay. Age effects on negative priming are inconsistent (Gamboz et al., 2000, 2002; Grant & Dagenbach, 2000; Kramer et al., 1994; Verhaeghen & De Meersman, 1998a). In the AX-CPT task used in the present study, a prepotent response tendency towards the target key to the presentation of the letter A was induced by the high probability of A-X

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combinations (70%). This tendency had to be suppressed for the rare A-Y sequence (requiring the nontarget key). Subjects over 60 needed more time than younger subjects to inhibit the inappropriate response towards the target key, which was indicated by an increase of both context and inhibition cost. Inhibition took longer, even if general age-associated response slowing was statistically accounted for. Use of context, on the other hand, was unaffected by age, indicating a preserved ability to benefit from the unambiguous information for response preparation. Unlike the Stroop Test, where inhibition can be prepared and needs to be upheld throughout the task, the need to inhibit a prepotent response emerges phasically and unpredictably and therefore requires a high degree of flexibility. These more demanding tasks might be of particular use to study mild executive impairments in healthy older subjects. Task management was consistently found to be impaired in subjects over 60, irrespective of whether or not stimulus input was within the same modality. Deficits in divided attention tasks or tasks requiring the coordination of two responses have been frequently reported in the elderly (Verhaeghen et al., 2003), although it is unclear whether these effects are due to age-associated response slowing (Salthouse et al., 1995). The task management deficit of older subjects observed in our study was significant even when simple RT differences were taken into account. In younger subjects, the dual task cost (relative to single task RT) was 30%, while it was 70% in the oldest group who also committed more errors. This pattern is more consistent with genuine impairment than response-slowing alone. As to the course or development of executive impairment, it is of interest that middle-aged subjects (age range 46 to 60 years) had only difficulties in dividing attention between two input modalities, while inhibition and the coordination of two motor responses was still unimpaired. This pattern suggests an early onset of executive problems, which manifest themselves during the more difficult tasks, and extend to a wider range with increasing age. The interindividual variability of inhibition and task management performances also appeared to increase with age, which is consistent with previous reports (Glisky et al., 2001; Rosen et al., 2002). While some older adults are able to maintain their cognitive performance at a level comparable to young individuals (successful aging; Rowe & Kahn, 1997, 2000), others suffer from significant cognitive decline. Whether preservation of executive function relates to factors such as activation of additional brain resources (Cabeza et al., 2002; Grady, 2000; Langenecker & Nielson, 2003; Reuter-Lorenz et al., 2000; Rosen et al., 2002), level of education (Albert et al., 1995; Chou & Chi, 2002), low blood pressure (Kilander et al., 2000), cognitively stimulating activities during middle age (Hartman-Stein & Potkanowicz, 2003), emotional support (Seeman et al., 2001), or depression (Fischer, 1996) needs to be clarified.

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Strategic memory processing, reasoning, verbal fluency, cognitive flexibility, or executive problems in everyday life were not affected by age in the present study, which is partly inconsistent with previous findings. For example, age effects have been reported for the use of organizational strategies in memory, such as self-generated use of semantic categories (Daum et al., 1996; Glisky et al., 2001). With respect to the use of encoding strategies, age effects have been reported for both list learning (Wegesin et al., 2000) and single-trial list recall (Daum et al., 1996). Even though we found a large list effect, indicating differential performance depending on the nature of the list (i.e. better performance if words from different categories were presented), this effect was not significantly affected by age. Older and younger subjects seemed to benefit in a similar way from the ability to categorize the material. The lack of significant findings may relate to the small sample size. For effect sizes, we found a moderate effect of age on performance for learning of the uncategorized list, where other than the apparent strategy to categorize the material must be used. Preservation of cognitive estimation or reasoning (Della-Maggiore et al., 2002; Della Sala et al., 2004; Gillespie et al., 2002) may be related to the use of semantic knowledge which is generally unaffected by age (Burke & Mackay, 1997). Whether or not reductions of verbal fluency occur until the late 70s is still debated (Brady et al., 2001; Bryan et al., 1997; Dursun et al., 2002; Isingrini & Vazou, 1997; Kempler et al., 1998; Mathuranath et al., 2003; Mejia et al., 1998; Rodriguez-Aranda, 2003). It has been argued, that age-related deficits in verbal fluency may exclusively be due to general cogntive slowing (Bryan et al., 1997; Rodriguez-Aranda, 2003). The preservation of verbal fluency in the three subtests of the present study may relate to well-preserved semantic knowledge, which may at least partly compensate for reduced access speed. As the IQ estimate used for matching the age groups relied on semantic knowledge, the verbal fluency tasks used here, including the switching condition assessing cognitive flexibility, might be too insensitive to detect executive control problems in relatively high-functioning older adults. Preserved fluency in our sample may be due to the relative small sample size. Effect sizes ranged from small in the phonemic category to moderate in the semantic and switching category. In a recent study, Amieva and colleagues (2003) used the DEX questionnaire to elucidate the nature of dysexecutive behavioral problems in older adults and their relation to cognitive changes. The authors derived five factors from the DEX, which also correlated with cognitive performance. The third factor, for example, which was called inhibition, correlated with RTs and errors in the Stroop Test. Our results suggest first, that in spite of cognitive executive deficits, older adults show preserved behavior, and second, that also self-awareness for behavior is intact in the older group. Even though statistical analysis did not yield significant differences between

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independent ratings of executive behavior, the data indicate an increase of dysexecutive behavior as well as an increase of interindividual variability of dysexecutive behavior. This is in accordance with the findings of increased between-subject variability in cognitive performance in older age groups (Hultsch et al., 2002; Shammi et al., 1998). A major problem in the study of age effects on executive function is that performance is mainly assessed via speed measures, and global slowing contributes significantly to cognitive deficits in normal aging (Lowe & Rabbitt, 1997; Uttl & Graf, 1997; Verhaeghen & De Meersman, 1998b). It has been suggested that RTs of older subjects can be represented by multiplying younger subjects RTs with a constant (Verhaeghen et al., 2003). This procedure implies a disproportional RT increase of older subjects in complex compared to simple conditions, which poses a problem for the interpretation of significant group condition interactions. An age-related decline in performance is only considered valid if the constant, i.e., the age-related slowing factor, changes from the simple to the complex task. There is, however, disagreement as to whether cognitive decline in aging can simply be attributed to RT slowing (Van der Linden, 2000; West & Alain, 2000). In a meta-analysis of 33 aging studies of task management, Verhaeghen et al. (2003) concluded that the larger dual-task costs in older subjects go beyond the effect of general slowing. As the present study involved simple, easy-tolearn tasks (Hartley, 2001) with an emphasis on both speed and accuracy and as age changes were observed for both RTs and errors, the task management deficits in the oldest group most likely reflect genuine executive control impairments. Of course, fatigue effects cannot totally be excluded for the Stroop Test or the Dual Task which were administered towards the end of the session. But older subjects were also impaired on the Divided Attention task and the AX-CPT which were administered early in the test session. Several attempts have been made to relate age-associated impairments to specific PFC regions. MacPherson (2002) suggested that the dorsolateral PFC undergoes more extensive changes than the ventromedial PFC, although there is little direct evidence from neuroimaging studies for this distinction (Raz et al., 1997; Salat et al., 2001; Tisserand et al., 2002). Although the conclusions about brain location on the basis of behavioral data alone are limited and speculative, the combined age-related inhibition and task management changes observed in the present study would be consistent with dorsolateral PFC mechanisms, but would also be consistent with a possible involvement of the anterior cingulate cortex (Cummings, 1993; Dreher & Grafman, 2003; Loose et al., 2003; Sturm & Zimmermann, 2000; Suchan et al., 2003, 2005). This is also supported by neuroimaging results of decreased rCBF within the frontal cingular gyri in older subjects (Larsson et al., 2001). Taken together, our results suggest a differential effect of normal aging on the inhibition and task management subcomponents of executive control.

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The pattern suggests an accelerated cognitive decline after the age of 60, which is consistent with longitudinal aging studies.
Original manuscript received March 30, 2005 Revised manuscript accepted October 18, 2005 First published online July 23, 2006

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