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Aging, Neuropsychology, and Cognition, 14: 370–393, 2007

http://www.psypress.com/anc
ISSN: 1382-5585/05 print; 1744-4128 online
DOI: 10.1080/13825580600678442

Differential Course of Executive Control


1744-4128
1382-5585/05
NANC
Aging, Neuropsychology, and Cognition
Cognition, Vol. 00, No. 0, June 2006: pp. 1–47

Changes During Normal Aging


Executive Control
Friederike H. TreitzChanges
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 exec-
utive control subcomponents. Four consecutive age groups (20–30 years, 31–45 years,
46–60 years, 61–75 years), matched on present state IQ and mood, were compared on
tasks of strategic memory processing, verbal fluency, reasoning, inhibition, task man-
agement, 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 unaf-
fected. Results suggest a sharp decline of executive function after age 60 and a differ-
ential 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 sys-
tems (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 hippoc-
ampal 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 vol-
ume 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
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 371

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 pre-
frontal 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 con-
sidered a model of diffuse mild prefrontal dysfunction and associated execu-
tive 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 con-
cept, 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 associ-
ated with the supervisory attentional system (SAS), which is responsible for
strategic control of mental processes, such as the use of strategies or rule-
guided retrieval from long-term memory. In novel and unfamiliar situations,
the SAS is responsible for strategy formation, planning, and problem-
solving 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 age-
related 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 orga-
nizational strategies in memory, such as self-generated use of semantic catego-
ries (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
372 FRIEDERIKE H. TREITZ ET AL.

& De Meersman, 1998a). Whether these inhibition deficits can be attributed to


a general slowing of information processing or whether they represent a spe-
cific 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 vari-
ables 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 elimi-
nated. 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, dif-
ferent 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 sug-
gested 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 20–30 year age range, the
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 373

TABLE 1. Group Size, Mean (SDs) Age, IQ Estimates, and Scores in the VAS (Visual Analogue
Scales) for the Consecutive Age Groups

20–30 yrs. 31–45 yrs. 46–60 yrs. 61–75 yrs. p

Mean age in yrs. 25.4 (3.3) 38.8 (4.3) 52.4 (3.9) 67.5 (4.4) –
N 16 16 13 17 –
IQ estimate 111.4 (4.8) 114.4 (4.6) 112.0 (5.7) 112.0 (7.4) 0.45
VAS 29.9 (11.9) 24.4 (9.3) 25.4 (11.4) 20.7 (13.3) 0.17

second group the 31–45 year range, the third group the 46–60 year range,
and the oldest group the 61–75 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, sub-
jects 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 consist-
ing of 16 items each were read to the subject at a one word per second pre-
sentation 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 sec-
ond list also contained four items of each of four categories (items of cloth-
ing, 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. Sub-
jects were asked to reproduce each list immediately after presentation.
Delayed free recall was assessed after a 30-min delay. The number of cor-
rectly reproduced items per list during both delays (immediate, delayed) as
well as retention rates (correct items delayed recall/immediate recall) were
analyzed.
374 FRIEDERIKE H. TREITZ ET AL.

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 cate-
gory condition (nouns beginning with “B”), and a switching condition (alter-
nate “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 subject’s knowledge and reasoning. Subjects were asked to give esti-
mates 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 person-
ality 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 (Bäumler,
1985) and a version of the AX-Continuous Performance Test (AX-CPT) pre-
viously 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
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 375

color and color names being incongruent (interference (INT)). To account for
reading speed and color-naming speed, reaction times (RTs) in the interfer-
ence 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 slow-
ing 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
376 FRIEDERIKE H. TREITZ ET AL.

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 sen-
sory 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 com-
puter 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 ver-
bally whether the letters were the same or different. Eighty trials were pre-
sented 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, Dual-
Task, 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 dif-
ferences 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
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 377

significance level was set to p < .05. In addition, eta2 effect sizes were calcu-
lated in case the demands for ANOVA were met.

RESULTS
Strategic Memory Processing
The results for word list recall are presented in Table 2. Repeated mea-
sures 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. inde-
pendent rating of dysexecutive behavior) as factors did not yield a signifi-
cant 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].
378 FRIEDERIKE H. TREITZ ET AL.

TABLE 2. Means (SDs) for Cognitive Performance in the Four Age Groups

20–30 Yrs. 31–45 Yrs. 46–60 Yrs. 61–75 Yrs.

Strategic Memory Processing


Word list recall immediately (no. correct)
consecutive categories 10.6 (2.0) 10.9 (2.6) 9.5 (3.6) 9.7 (2.1)
randomized categories 9.1 (2.3) 8.4 (3.5) 7.5 (2.3) 8.2 (2.3)
uncategorized 7.6 (2.2) 7.7 (2.6) 6.3 (1.8) 6.4 (1.7)
Word list recall delayed (no. correct)
consecutive categories 6.8 (2.2) 6.4 (2.8) 5.7 (2.9) 5.1 (2.4)
randomized categories 6.1 (3.2) 5.3 (3.8) 4.9 (2.6) 5.3 (2.5)
uncategorized 2.6 (1.6) 3.4 (2.8) 2.6 (2.0) 1.8 (1.5)
Verbal Fluency/Cognitive Flexibility (no. correct)
semantic 29.9 (9.5) 28.1 (6.5) 25.7 (7.4) 24.5 (5.9)
phonemic 13.1 (3.8) 12.9 (2.6) 13.2 (3.2) 11.8 (3.8)
switching 16.3 (4.0) 17.1 (2.5) 14.7 (2.7) 15.9 (3.0)
Reasoning
Cognitive Estimation Test 4.5 (2.5) 3.7 (3.1) 3.4 (2.5) 3.5 (2.4)
Subjective Rating
DEX self-rating 22.1 (6.0) 22.7 (11.7) 22.3 (7.6) 20.4 (7.0)
DEX independent rating 14.9 (8.0) 17.4 (9.7) 21.7 (10.7) 23.7 (17.8)
Inhibition
Stroop Test
RTs RCW 25.9 (2.1) 28.6 (5.0) 30.0 (5.8) 33.8 (3.8)
RTs NCP 44.1 (6.9) 45.0 (8.4) 43.2 (9.5) 48.7 (6.7)
RTs INT 67.4 (10.2) 70.9 (14.6) 80.2 (18.8) 91.5 (14.6)
INT no. corrected errors 2.9 (2.3) 3.0 (2.7) 2.5 (2.9) 4.0 (4.1)
INT no. uncorrected errors 0.8 (0.7) 0.6 (1.0) 2.6 (2.8) 2.5 (2.4)
AX-CPT
context use −10.8 (35.7) −6.4 (34.8) 16.4 (60.3) 13.5 (38.7)
context costs 220 (53) 189 (85) 200 (57) 341 (117)
inhibition costs 145 (43) 147 (59) 137 (64) 211 (93)
Multi-tasking
Divided Attention
RTs in msec 597 (67) 641 (55) 694 (51) 707 (74)
no. errors 2.4 (2.5) 2.4 (2.2) 5.2 (3.4) 4.4 (3.4)
Dual task
RTs single condition 298 (33) 345 (45) 364 (65) 397 (44)
single condition no. errors 0.7 (0.9) 0.4 (0.6) 0.4 (0.7) 0.4 (0.7)
RTs dual condition 386 (48) 431 (116) 454 (66) 675 (138)
dual condition no. errors 2.2 (2.0) 1.3 (1.5) 2.1 (3.2) 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).
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 379

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 cor-
rected errors (Hdf = 3 = 1.344; p = .72), but there was a significant group dif-
ference 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 sig-
nificant 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
380 FRIEDERIKE H. TREITZ ET AL.

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
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 381

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 compari-
sons 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 compari-
sons 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.
382 FRIEDERIKE H. TREITZ ET AL.

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.
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 383

Comparable results emerged for the dual task costs variable (DTC:
(RTs dual task – RTs single task)/RTs single task). The groups differed sig-
nificantly on DTC [F3,57 = 18.112; p < .001, eta2 = 0.49]. Post-hoc compari-
sons 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). Post-
hoc analyses yielded significant Group × Task interactions (all p < .003)
when the oldest group was compared to the two youngest groups. Compari-
sons 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 differ-
ence 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). Intercorrela-
tions 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. Fol-
lowing Smith and Jonides’ (1999) subdivision of executive control, the inhi-
bition 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 tenden-
cies as well as weaker, experimentally induced predominant responses. Abil-
ities to coordinate information from two sensory channels and to coordinate
384 FRIEDERIKE H. TREITZ ET AL.

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). Cross-
sectional 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 inter-
ference condition of Stroop-type tasks appears to be a particular sensitive
test (Woodruff-Pak, 1997), with elderly subjects needing to recruit addi-
tional PFC resources for adequate performance (Langenecker et al., 2004). It
is, however, as yet unclear whether older subjects suffer from a genuine inhi-
bition 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 pat-
tern, it is unlikely that the findings in subjects over 60 years old are attribut-
able 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 para-
digm, where the distractor of one trial serves as the target in the following
trial, inducing a response delay. Age effects on negative priming are incon-
sistent (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
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 385

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 infor-
mation 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 there-
fore 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-associ-
ated 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 genu-
ine impairment than response-slowing alone.
As to the course or development of executive impairment, it is of inter-
est 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 sug-
gests an early onset of executive problems, which manifest themselves dur-
ing the more difficult tasks, and extend to a wider range with increasing age.
The interindividual variability of inhibition and task management perfor-
mances 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 func-
tion 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 stimu-
lating activities during middle age (Hartman-Stein & Potkanowicz, 2003),
emotional support (Seeman et al., 2001), or depression (Fischer, 1996) needs
to be clarified.
386 FRIEDERIKE H. TREITZ ET AL.

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 strate-
gies 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 strate-
gies, 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 cate-
gorize 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 perfor-
mance 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 sub-
tests 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 ques-
tionnaire 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 sec-
ond, that also self-awareness for behavior is intact in the older group.
Even though statistical analysis did not yield significant differences between
EXECUTIVE CONTROL CHANGES DURING NORMAL AGING 387

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 multi-
plying younger subjects’ RTs with a constant (Verhaeghen et al., 2003). This
procedure implies a disproportional RT increase of older subjects in com-
plex compared to simple conditions, which poses a problem for the interpre-
tation 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, how-
ever, 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-to-
learn 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 conclu-
sions 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.
388 FRIEDERIKE H. TREITZ ET AL.

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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