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ABSTRACT
Background: Intra-individual variability (IIV) and the change of attentional functions have been reported to
be susceptible to both healthy ageing and pathological ageing. The current study aimed to evaluate the IIV of
attention and the age-related effect on alerting, orienting, and executive control in cognitively healthy older
adults.
Method: We evaluated 145 Chinese older adults (age range of 6580 years, mean age of 72.41 years) with
a comprehensive neuropsychological battery and the Attention network test (ANT). A two-step strategy of
analytical methods was used: Firstly, the IIV of older adults was evaluated by the intraindividual coefficient
of variation of reaction time (ICV-RT). The correlation between ICV-RT and age was used to evaluate
the necessity of subgrouping. Further, the comparisons of ANT performance among three age groups were
performed with processing speed adjusted.
Results: Persons correlation revealed significant positive correlations between age and IIV (r = 0.185, p =
0.032), age and executive control (r = 0.253, p = 0.003). Furthermore, one-way ANOVA comparisons among
three age groups revealed a significant age-related disturbance on executive control (F = 4.55, p = 0.01), in
which oldest group (group with age >75 years) showed less efficient executive control than young-old (group
with age 6570 years) (Conventional score, p = 0.012; Ratio score, p = 0.020).
Conclusion: Advancing age has an effect on both IIV and executive attention in cognitively healthy older
adults, suggesting that the disturbance of executive attention is a sensitive indicator to reflect healthy ageing.
Its significance to predict further deterioration should be carefully evaluated with prospective studies.
Key words: healthy ageing, attention network, intra-individual variability, executive control
Introduction
According to the latest World Alzheimer Report, 44
million adults now suffer from dementia worldwide,
and the projected number will double the current
brunt of disease by 2,030, even trebling the existing
number by 2,050 (Alzheimers Association, 2014).
Because there is no effective treatment to halt
the disease process and treatment outcomes are
unfavourable when the disease progresses to a later
stage, it is crucial to identify the specific cognitive
characteristics and markers that differentiate
cognitive ageing from conditions associated with
high risk of progressive neurodegeneration. The
potential clinical implications of these markers may
help to lay platforms for early intervention. Among
Correspondence should be addressed to: Linda C. W. Lam, MD, Department of
Psychiatry, The Chinese University of Hong Kong, G/F Multicenter, Tai Po
Hospital, Tai Po, Hong Kong. Phone: +(852) 2607-6027; Fax: +(852) 26675464. Email: cwlam@cuhk.edu.hk. Received 15 Apr 2015; revision requested
8 May 2015; revised version received 20 Aug 2015; accepted 26 Aug 2015.
H. Lu et al.
Methods
Study participants
A total of 145 right-handed Chinese older adults
aged from 65 to 80 years (mean age 72.41 years)
participated in this study. All participants were
recruited from another cohort study that aims to
establish a detailed characterization of cognitive
and healthy profiles of Chinese older adults and
to determine the diagnostic markers for preclinical
H. Lu et al.
Figure 1. (Colour online) The schematic diagram of attention network test (ANT).
MEASURE OF INTRA-INDIVIDUAL
VARIABILITY
RTcenter-cue )/RTcenter-cue
Orienting
ratio
=
(RTcenter-cue
RTspatial-cue )/RTspatial-cue
Executive control ratio = (RTincongruent
RTcongruent )/RTcongruent
Results
Quality control and ANT performance
According to the quality control standard
suggested by Fan Jin (Fan et al., 2002a), an accuracy
of ANT less than 70% indicates that the participate
does not well understand how to perform the
ANT. Thus, under this circumstances, the ANT
indices, including processing speed, and attentional
components calculated by subtractions of RTs,
are considered unqualified as well. To evaluate
the attention network functions with caution, eight
participants were excluded from the dataset. Thus,
a final sample of 137 healthy older adults was used
for further analysis. The group-level performance of
ANT was as follows: accuracy was higher than 99%;
the processing speed was 687.49 105.97 ms; the
ICV-RT was 19.99 4.57 ms; alerting score was
3.95 31.88; orienting score was 19.76 28.65;
executive control score was 59.86 45.86.
Age-related change of attention network
functions
Persons correlation analysis revealed that the
alerting score (r = 0.011, p = 0.895) and orienting
H. Lu et al.
6570 (N = 54)
AGE
7175 (N = 56)
AGE
>75 (N = 27)
P VALUE
............................................................................................................................................................................................................................................................................................................................
Gender (F/M)
Education (years)
Systolic BP
Diastolic BP
CSDD
PSQI
ADL
CDR-SOB
CMMSE
HK MoCA
ADAS
Delayed recall
Digit span backward (DSB)
Trail making test B (time)
Trail making test A
Digit span forward (DSF)
21/33
8.59 4.26
138.51 20.98
79.85 10.99
0.63 2.12
5.98 3.16
0.990 0.025
0.47 0.63
28.54 1.13
27.46 2.02
4.69 2.19
7.91 1.46
3.65 1.28
57.35 30.94
12.57 5.96
7.78 1.13
27/29
10.05 4.10
140.39 18.90
77.14 10.89
0.11 0.41
6.57 3.83
0.996 0.015
0.44 0.59
28.70 1.21
27.18 1.72
5.17 2.06
7.45 1.31
3.98 1.46
69.40 35.73
12.37 6.03
7.54 1.11
13/14
9.30 4.55
136.67 17.50
76.96 9.64
0.33 0.96
5.30 2.60
0.989 0.036
0.54 0.10
28.74 1.63
27.00 1.73
4.79 1.94
7.56 1.72
3.48 1.09
81.34 61.72
14.64 7.67
7.52 1.16
0.516
0.177
0.704
0.332
0.161
0.261
0.321
0.668
0.605
0.634
0.489
0.265
0.199
0.041
0.283
0.550
Note. Data are raw scores and presented as meanSD. CSDD = The Cornell Scale for Depression in Dementia; PSQI = Pittsburgh Sleep
Quality Index; CDR-SOB = Clinical dementia rating-sum of box; ADL = Activity of daily living scale.
Table 2. Accuracy under different cue/anker conditions among three age groups
AGE
6570 (N = 54)
AGE
7175 (N = 56)
AGE
>75 (N = 27)
P VALUE
............................................................................................................................................................................................................................................................................................................................
NoCue_Neutral
NoCue_Congruent
NoCue_Incongruent
CenterCue_Neutral
CenterCue_Congruent
CenterCue_Incongruent
DoubleCue_Neutral
DoubleCue_Congruent
DoubleCue_Incongruent
SpatialCue_Neutral
SpatialCue_Congruent
SpatialCue_Incongruent
0.9891 0.0194
0.9908 0.0132
0.9887 0.0160
0.9893 0.0170
0.9910 0.0118
0.9889 0.0162
0.9896 0.0185
0.9914 0.0122
0.9894 0.0168
0.9889 0.0190
0.9906 0.0132
0.9886 0.0178
0.9879 0.0225
0.9907 0.0193
0.9871 0.0176
0.9853 0.0261
0.9881 0.0227
0.9845 0.0209
0.9884 0.0214
0.9913 0.0178
0.9876 0.0180
0.9858 0.0216
0.9886 0.0179
0.9849 0.0171
0.9879 0.0154
0.9887 0.0150
0.9844 0.0190
0.9876 0.0131
0.9883 0.0129
0.9841 0.0169
0.9885 0.0154
0.9893 0.0156
0.9850 0.0210
0.9873 0.0144
0.9880 0.0144
0.9838 0.0199
0.057
0.176
0.573
0.515
0.438
1.041
0.064
0.195
0.520
0.359
0.346
0.865
0.945
0.839
0.565
0.598
0.646
0.356
0.938
0.823
0.596
0.699
0.708
0.424
Note. Data are raw scores and presented as meansSD. NoCue_Neutral represents the ANT trial with no cue as cue type and neutral as
flanker type.
6570 (N = 54)
AGE
7175 (N = 56)
AGE
>75 (N = 27)
VALUE
............................................................................................................................................................................................................................................................................................................................
ICV-RT
NoCue_Neutral
NoCue_Congruent
NoCue_Incongruent
CenterCue_Neutral
CenterCue_Congruent
CenterCue_Incongruent
DoubleCue_Neutral
DoubleCue_Congruent
DoubleCue_Incongruent
SpatialCue_Neutral
SpatialCue_Congruent
SpatialCue_Incongruent
20.72 7.75
657.36 101.05
664.66 102.07
688.14 103.97
656.49 104.33
663.78 105.33
687.26 107.39
658.67 102.64
665.96 104.08
689.44 106.04
666.46 105.50
673.75 106.86
697.23 109.19
20.55 7.03
665.22 108.91
673.86 113.93
705.66 107.17
662.31 108.27
670.94 113.59
702.74 107.72
667.29 112.93
675.93 118.18
707.73 111.72
671.68 109.64
680.32 115.02
712.12 109.06
22.44 8.23
698.97 102.12
701.24 98.58
740.19 99.09
696.76 96.84
699.03 93.41
737.98 95.27
698.64 102.14
700.91 100.04
739.86 101.07
707.49 97.94
709.76 95.28
748.72 95.99
0.626
1.480
1.076
3.238
1.422
1.014
2.092
1.291
0.923
1.984
1.459
1.039
2.103
0.536
0.231
0.344
0.111
0.245
0.366
0.127
0.279
0.400
0.142
0.236
0.357
0.126
Note. Data are raw scores and presented as meansSD. NoCue_Neutral represents the ANT trial with no cue as cue type and neutral as
flanker type.
ICV-RT = Intra-individual coefficient of variation (ICV) of Reaction Time.
6570 (N = 54)
AGE
7175 (N = 56)
AGE
>75 (N = 27)
P VALUE
............................................................................................................................................................................................................................................................................................................................
1.76 27.28
19.94 26.64
46.96 38.41
0.0048 0.0425
0.0283 0.0374
0.07 0.06
Alerting
Orienting
Executive control
Alerting ratio
Orienting ratio
Executive control ratio
5.83 34.71
18.75 27.23
63.59 48.54
0.0101 0.0517
0.03 0.04
0.10 0.08
4.43 35.12
21.47 35.69
77.91 47.94
0.0060 0.5009
0.03 0.05
0.12 0.78
0.799
0.922
0.011
0.837
0.964
0.020
ALERTING
ORIENTING
CONTROL
............................................................................................................................................................................................................................................................................................................................
CDR-SOB
CMMSE
HK MoCA
ADAS
Delayed Recall
DSB
TMT-B
TMT-A
DSF
0.007
0.039
0.288
0.078
0.062
0.093
0.191
0.139
0.081
0.937
0.654
0.001
0.373
0.479
0.287
0.028
0.112
0.358
0.022
0.059
0.060
0.055
0.007
0.076
0.018
0.066
0.143
0.804
0.498
0.492
0.530
0.936
0.385
0.838
0.451
0.102
0.167
0.131
0.092
0.058
0.028
0.024
0.016
0.046
0.125
0.055
0.134
0.295
0.505
0.747
0.784
0.858
0.601
0.154
0.068
0.043
0.033
0.025
0.020
0.027
0.122
0.000
0.127
0.437
0.621
0.709
0.780
0.816
0.760
0.164
0.997
0.147
H. Lu et al.
positive correlation between ICV-RT and TMTB (r = 0.191, p = 0.028, 95% CI [0.021,
0.359]). Within ANT indices, no relationship was
found between ICV-RT and ANT scores. The
results indicated that attention network functions
measured by ANT were relatively independent from
other cognitive functions. However, the declined
cognitive functions might have an effect on the
within-person variability, or vice versa.
Discussion
To the best of our knowledge, this is the first
work to detect both IIV and attention network
functions in community-dwelling Chinese healthy
older adults. With advancing age, increased withinperson variability and declined executive control
function have been found in current study.
Meanwhile, the oldest group (age > 75 years)
showed less efficient executive control function than
the group with age 6570 years. These findings
suggest that executive control measured by ANT,
rather than processing speed, alerting and orienting,
is a sensitive marker of healthy ageing, even in the
context of relatively normal cognition.
Age and intra-individual variability (IIV)
Until recently, variability has been considered
as an important individual difference measure
relevant to understanding age differences in brain
function (Garrett et al., 2013). Indeed, inspired
by previous attempts (MacDonald et al., 2003;
Bunce et al., 2004; Salthouse et al., 2006; Kennedy
et al., 2013), our observations demonstrate that the
within-person variability increased in old age, and
appeared to highlight the necessity of subgrouping
in a sample of older adults (Rabbitt et al., 2001;
Tractenberg and Pietrzak, 2011; Phillips et al.,
2013). The increased within-person variability in
old age suggests that older adults have more
difficulty on keeping the consistency of performance
across the experimental trials.
Given the declined brain functions in late
adulthood, it is applaudable to assume that withinperson variability maybe affected by the declined
executive functions (Bellgrove et al., 2004). As
outlined nicely by MacDonald et al. (2009), greater
IIV is associated with the reduced functional MRI
(fMRI) activities in the regions related to executive
functions (MacDonald et al., 2009). A further
question emerges from this work is whether poorer
executive control and decision-making function
in older adults are reflected by within-person
variability of neuropsychological measure as well?
Interestingly, the positive correlations between
age, ICV-RT, and TMT-B supported that the
Conict of interest
None.
Acknowledgments
This research was supported by Lui Che Woo
Institute of Innovation Medicine grant at The
Chinese University of Hong Kong. The authors
would like to thank all the participants and their
relatives that kindly agreed to participate in the
study. And we also want to thank the reviewers
for their valuable comments and suggestions to
improve the quality of the paper.
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