Attention network functioning in patients with dementia with Lewy bodies and Alzheimer's disease.

Abstract

Attention deficits are at the core of the defects in neuropsychological performance which define both dementia with Lewy bodies (DLB) and Alzheimer's disease (AD). Most studies have used separate tasks to test different attention abilities in patients with these diagnoses, precluding the assessment of any interaction among the different attention components.
We used a version of the Attention Network Test in which the alerting, orienting and executive attention networks, along with their interactions, could be assessed with a single task. Three groups of participants were tested: DLB patients (n = 13), AD patients (n = 18) and healthy controls (n = 18).
The alerting signal improved orienting attention and increased the conflict effect in the healthy controls, but they had no effect on these networks in the AD patients. The DLB patients only showed preserved orienting and conflict effects when the alerting signal was present, indicating that there was regulation of the orienting and executive attention networks by the alerting signal.
The most important differences among the 3 groups were observed in the attention network interactions, where alerting played a more relevant role in the DLB than in the AD patients. Under alerting states, the DLB patients showed evidence of certain regulation in the orienting and executive attention networks.

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Fax +41 61 306 12 34
E-Mail karger@karger.ch
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Original Research Article
Dement Geriatr Cogn Disord 2010;29:139–145
DOI: 10.1159/000275672
Attention Network Functioning in
Patients with Dementia with Lewy
Bodies and Alzheimer’s Disease
Luis J. Fuentes a Pedro J. Fernández a Guillermo Campoy
Martirio M. Antequera b Julia García-Sevilla a Carmen Antúnez
a
b
a University of Murcia and b University Hospital Virgen de la Arrixaca, Murcia , Spain
actions, where alerting played a more relevant role in the
DLB than in the AD patients. Under alerting states, the DLB
patients showed evidence of certain regulation in the orient-
ing and executive attention networks.
Copyright © 2010 S. Karger AG, Basel
Introduction
It is now well accepted that dementia with Lewy bodies
(DLB) is a clinical entity distinct from Alzheimer’s dis-
ease (AD) [1, 2] . These patients’ brains are characterized
by the presence of Lewy bodies in the cerebral cortex,
substantia nigra, locus ceruleus and components of the
basal forebrain cholinergic system. Fluctuation in cogni-
tion, visual hallucinations and parkinsonism are the core
clinical manifestations of the disease. However, it re-
mains challenging to differentiate DLB from other de-
mentias, such as AD, given the overlapping neuropathol-
ogy that both clinical entities present. For instance, sev-
eral studies of hospital-based autopsies have suggested
that DLB accounts for 10–15% of the dementia cases [3] ,
but as many as 12–27% of the patients diagnosed as hav-
ing AD also meet the pathological criteria for a diagnosis
of DLB [2, 4] .
Key Words
Alzheimer’s disease ? Dementia with Lewy bodies ?
Cognitive neuropsychology, dementia
Abstract
Background: Attention deficits are at the core of the defects
in neuropsychological performance which define both de-
mentia with Lewy bodies (DLB) and Alzheimer’s disease (AD).
Most studies have used separate tasks to test different atten-
tion abilities in patients with these diagnoses, precluding the
assessment of any interaction among the different attention
components. Methods: We used a version of the Attention
Network Test in which the alerting, orienting and executive
attention networks, along with their interactions, could be
assessed with a single task. Three groups of participants
were tested: DLB patients (n = 13), AD patients (n = 18) and
healthy controls (n = 18). Results: The alerting signal im-
proved orienting attention and increased the conflict effect
in the healthy controls, but they had no effect on these net-
works in the AD patients. The DLB patients only showed pre-
served orienting and conflict effects when the alerting sig-
nal was present, indicating that there was regulation of the
orienting and executive attention networks by the alerting
signal. Conclusions: The most important differences among
the 3 groups were observed in the attention network inter-
Accepted: January 3, 2010
Published online: February 10, 2010
Luis J. Fuentes, PhD
Dpto. Psicología Básica y Metodología, Campus de Espinardo
Universidad de Murcia
ES–30100 Murcia (Spain)
Tel. +34 968 364 140, Fax +34 968 398 161, E-Mail lfuentes @ um.es
© 2010 S. Karger AG, Basel
1420–8008/10/0292–0139$26.00/0
Accessible online at:
www.karger.com/dem

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140
Recent studies have relied on neuropsychological and
cognitive testing as a way of finding a more reliable pro-
cedure to distinguish DLB from AD [5–9] . Some authors
have shown that attention fluctuations play a fundamen-
tal role in these pathologies [10, 11] , and both attentional
and perceptual processing might underlie the visual hal-
lucinations that are experienced by most DLB patients.
For instance, Calderon et al. [6] showed that DLB patients
performed poorly and below AD patients in most vi-
suoperceptual tasks that required both the ventral and
the dorsal processing pathways, and in all attentional
tasks that needed sustained, selective and divided atten-
tion. In contrast, AD patients were impaired in tasks that
required the ventral processing pathway, but showed un-
compromised sustained attention compared with the
matched control group. Ballard et al. [10] assessed atten-
tion performance through the use of a standardized bat-
tery of computerized tasks that required both rapid and
accurate responses. DLB patients were impaired in both
cognitive reaction time (RT) and the vigilance tasks com-
pared with AD patients, and likewise exhibited greater
variability in RTs. These results support the hypothesis
that fluctuation in attention is a critical feature of DLB.
These attention deficits in DLB patients might reflect an
important deficiency in the cholinergic system, which
plays a relevant role in the orientation of visual attention
[12] . However, as Ballard et al. [10] point out, deficits in
attention become more pronounced in both DLB and AD
patients as the severity of dementia increases, and hence
a more detailed evaluation of attention functioning would
be useful to aid in the diagnostic assessment.
Many attention studies in dementia, however, lack a
theoretical framework that takes into consideration both
how the different components of attention might work
independently and how they might interact. The cogni-
tive neuroscience model of attention by Posner and Pe-
tersen [13] might constitute such a theoretical back-
ground. The model distinguishes 3 attention-related
neural networks. The alerting network is involved in
achieving and maintaining an alert state, which is de-
fined as an internal condition that prepares the individ-
ual to perceive or respond to a target. Pharmacological
studies have revealed a relationship between this network
and the norepinephrine system rooted in the locus ceru-
leus [12] , and it has been shown that the right parietal and
frontal areas are activated when people maintain an alert
state [14] . The orienting network is involved in aligning
attention with a source of sensory input. Pharmacologi-
cal studies conducted with animals have shown that cho-
linergic systems arising in the basal forebrain seem to
modulate covert orienting responses [12] . The parietal
lobe, pulvinar, superior colliculus and frontal eye fields
form part of the anatomical framework of the orienting
network. Finally, the executive network is required for
activities that involve planning, novelty, target detection,
error detection, monitoring and resolving conflict, and
the inhibition of automatic responses. The anterior cin-
gulate and lateral prefrontal areas comprise part of the
neural circuitry involved in different forms of conflict
tasks [15] , and some portions of the basal ganglia supply
dopamine to the network.
The Attention Network Test (ANT) has been designed
to assess the function of the 3 attention networks in a
single experiment [1, 16, 17] . Response to conflict, a func-
tion of the executive network, is assessed by means of a
flanker task. In this paradigm, a central arrow (the target)
points to the left or the right. The target is flanked by 4
distracting arrows that can be either congruent (pointing
in the same direction as the target) or incongruent (point-
ing in the opposite direction to the target). Subjects are
told to respond to the direction of the target arrow and
ignore the distracters. The orienting network is assessed
by using peripheral cues (asterisks) to summon attention
to a location. In cued trials, the target is presented at the
location of the previous peripheral cue, while in uncued
trials, it is presented at the opposite location of the pe-
ripheral cue. The alerting network is assessed observing
the effects of playing a tone prior to the cue presentation.
The ANT has proved to be a useful approach in decom-
posing the attention system into the 3 different attention
networks proposed by Posner and Petersen [13] .
In this study, we assessed attention functioning in
people diagnosed as having either DLB or AD, as well as
a group of healthy matched controls (HC). The ANT ver-
sion used here allowed us to assess dementia-related def-
icits not only in the function of the individual attention
networks but also in the interactions among them [1,
17] .
Methods
Participants
Eighteen HC, 13 patients diagnosed as having DLB and 18 pa-
tients with AD participated in the experiment. The HC partici-
pants were recruited from the community and were free from
serious medical conditions (i.e. heart disease, cancer, stroke, de-
mentia, or drug and alcohol abuse). The AD and DLB participants
were patients from the Dementia Unit at the University Hospital
Virgen de la Arrixaca (Murcia, Spain). The probable AD and DLB
diagnoses were made by a neurologist according to NINCDS-
ADRDA criteria and the 3rd report of the DLB consortium [18] .

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Dement Geriatr Cogn Disord 2010;29:139–145
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MRI, CT or SPECT were used in the patients’ diagnosis. The 3
groups were equated in age and education. We obtained written
informed consent to participate in the study from the participants
and patients’ caregivers. The ethics committees of both the Vir-
gen de la Arrixaca Hospital and the University of Murcia ap-
proved this study.
The ANT
A computer controlled the task, with stimuli being displayed
on a 17?? monitor set to a screen resolution of 640 ! 480 pixels.
Responses were collected through a PST Serial Response Box
(Psychology Software Tools, Inc.) connected to the computer. Ex-
ternal speakers were used to present the alerting tones. The basic
display, which was visible throughout the experiment, consisted
of a black fixation cross between 2 rows of 5 horizontally arranged
rectangular boxes ( fig. 1 ). The boxes were 40 pixels wide and 30
pixels high, while the fixation cross was 18 pixels wide and 18 pix-
els high. The distance between the fixation cross and the central
box of each row was 60 pixels from center to center. For the vi-
sual cue, the outline around the central box of the relevant row
was briefly increased from 1 to 4 pixels wide. In each trial, 5 black
arrows were presented inside each of the 5 boxes in the row.
The arrow presented in the central box was the target, whereas
the arrows in the other 4 boxes were the flankers. The arrows
were 36 pixels in length. The alerting tone was a 50-ms beep of
2,000 Hz.
Each trial began with the basic configuration being presented
for a variable duration between 1,200 and 2,600 ms (the duration
was determined randomly with the constraint that the entire
range was homogeneously represented within every block of tri-
als). The alerting tone was presented for 50 ms in half of the trials
(tone condition), whereas an equivalent empty audio file was run
in the other half of the trials (no-tone condition). The orienting
visual cue appeared 350 ms after the tone and was presented for
50 ms in the central box of either the upper or the lower box row.
The cue could appear in the same box as the target (cued condi-
tion) or in the other row (uncued condition). In trials without a
visual cue, the basic configuration remained unchanged during
the corresponding interval (no-cue condition). Finally, after an
interval of 50 ms (stimulus onset asynchrony, SOA = 100) or 450
ms (SOA = 500), the target and flankers were presented until the
participants indicated the direction of the target arrow by press-
ing the right or left key of the response box. The target arrows
pointed to the right in half of the trials and to the left in the other
half. The flanker arrows pointed in the same direction as the tar-
get (congruent condition) in half of the trials or in the opposite
direction (incongruent condition) in the other half. The partici-
pants were instructed to respond as quickly and accurately as pos-
sible.
The test comprised 288 trials divided into 3 blocks of 96 trials
that combined alerting (tone, no-tone), cueing (cued, uncued, no-
cue), cue-target SOA (100 and 500 ms), flanker congruency (con-
gruent, incongruent), target locus (upper row, lower row) and tar-
get orientation (right, left). Target locus and orientation were not
experimental factors. There were a total of 12 trials per experi-
mental condition. The participants ran 10 practice trials, with
additional blocks of 10 new trials until there were at least 9 correct
responses with no RTs 1 2.5 s in the last practice block. Rest peri-
ods were established every 48 trials.
Statistical Analysis
Sociodemographic data and participants’ performance in
neuropsychological tests were analyzed by simple analysis of vari-
ance (ANOVA) with group (HC, AD, DLB) serving as the be-
tween-subjects factor. Post hoc t tests were performed when ap-
propriate to compare mean scores across groups.
Two main analyses were conducted regarding the ANT.
(1) Mean RTs for correct responses were submitted to a mixed
ANOVA with alerting (tone, no-tone), cueing (cued, uncued),
cue-target SOA (100, 500 ms) and congruency (congruent, in-
congruent) as the within-subject factors and group (HC, AD,
DLB) as the between-subjects factor. We did not include no-
cue trials in this first analysis to appreciate better the possible
interactions between alerting and orienting and between ori-
enting and congruency (note that no-cue trials were irrelevant
to those purposes). When necessary, interactions were ana-
lyzed by additional F tests.
(2) A mixed ANOVA was preformed on no-cue trials only. This
allowed us to study the potential interaction between alerting
and congruency without the additional alerting effect gener-
ated by the visual cue [1, 12] . Again, interactions were analyzed
by additional F tests.
Equivalent analyses in terms of number of errors were also
performed. They did not reveal additional effects and did not
show evidence of trade-off between speed and accuracy, so they
are not reported . All statistical analyses were conducted with
SPSS 14 for Windows (SPSS Inc., USA). The criterion for statistical
significance was set at 5%. RTs above or below 3 standard devia-
tions from the participant’s mean were not included in the analy-
ses.
+
1,200/2,600 ms
+
50 ms
+
350 ms
+
50 ms
+
50/450 ms
+
cue-target SOA:
100 ms/500 ms
Fig. 1. Outlined representation of the experimental procedure.

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Dement Geriatr Cogn Disord 2010;29:139–145
142
Results
Demographic information, cognitive functioning
scores and statistical differences among the 3 groups are
presented in table 1 .
The first analysis of participants’ performance in the
ANT revealed the main effects of alerting, cueing, SOA
and congruency (all p ! 0.05), demonstrating that correct
responses were given faster in the alerting-tone than in
the no-tone trials (alerting effect = 39 ms), in cued than
in uncued trials (cueing effect = 121 ms), for long-SOA
than for short-SOA trials (SOA effect = 45 ms) and for
congruent than for incongruent trials (congruency ef -
fect = 141 ms). The difference among the groups was also
significant (p ! 0.01). The DLB patients were slower than
both the AD patients (p ! 0.05) and HC participants (p !
0.05), with the DLB group tending to be slower than the
AD patients (p = 0.07). The RT means for the HC, AD and
DLB groups were 728, 1,082 and 1,581 ms, respectively.
There was an alerting ! cueing interaction (p ! 0.05),
but it was qualified by the 3-way interaction involving
alerting, cueing and group (p ! 0.05; fig. 2 ). Further anal-
yses showed an alerting ! cueing interaction for HC
(p ! 0.01) and DLB (p = 0.03) but not for AD (F ! 1). The
interaction in the HC group was due to a larger cueing
effect in the alerting-tone condition than in the no-tone
condition, although the cueing effect was observed in
both alerting conditions (p values ! 0.01). For the AD pa-
tients, the cueing effect was also observed in both alerting
conditions (p values ! 0.01), but contrary to the HC group,
the size of such an effect did not differ between the 2
alerting conditions (F ! 1). The DLB patients, however,
showed a cueing effect only in the alerting-tone (p ! 0.01)
but not in the no-tone condition (F ! 1).
Table 1. Demographic information, means of neuropsychological
testing and GDS scores for each group
Sociodemographic data and testsMaxi-
mum
HCDLB AD
N
Sex (F/M)
Age, years
Education, years
MMSEa, b
GDSa, b
CERAD battery
Semantic fluencya, b
Boston Naming Testb
Word list memorya, b
Word list recalla, b
Word list recognitiona, b
Constructional praxis
Recall of constructional praxisa–c11
Trail Making Test (part A)a, b
Trail Making Test (errors)
Barcelona Test (subtests)
Imitation of postures (praxis)a, c
Forward digit span
Backward digit spana
Abstractiona, b
Random Letters Test (errors)
Phonological fluency (P)b
18 1318
10/8
72 (9)
5 (3)
20 (3)
4 (0)
9/9
70 (9)
6 (3)
29 (1)
1 (0)
4/9
76 (9)
6 (5)
22 (3)
4 (0)
30
7
16 (2)
13 (1)
7 (1)
5 (2)
19 (1)
10 (1)
8 (2)
78 (34) 257 (120) 186 (76)
1 (2)2 (2)
9 (2)
12 (2)
5 (1)
2 (2)
16 (3)
9 (2)
4 (3)
11 (4)
11 (2)
4 (2)
1 (2)
14 (3)
9 (2)
2 (3)
15
10
10
20
11
2 (3)
8
9
8
8 (0)
4 (1)
3 (0)
7 (2)
1 (1)
8 (4)
6 (2)
4 (1)
2 (1)
5 (3)
4 (4)
5 (3)
7 (1)
4 (1)
3 (1)
4 (2)
2 (5)
5 (4)
12
Figures in parentheses are SD. Trail Making Test part B was not
included due to the small number of records in this condition as a
consequence of the low academic level of the patients and controls.
The MMSE was corrected by age and education [19]. MMSE = Mini-
Mental State Examination; GDS = Global Deterioration Scale;
CERAD = the Consortium to Establish a Registry for Alzheimer’s
Disease.
a Significant difference between HC and DLB.
b Significant difference between HC and AD.
c Significant difference between DLB and AD.
400
600
800
1,000
1,200
1,400
1,600
1,800
2,000
2,200
Mean RT (ms)
Cued
Uncued
Tone
No-tone
HC
Tone ToneNo-toneNo-tone
AD DLB
Fig. 2. Mean RTs as a function of cueing
(cued, uncued), alerting (tone, no-tone)
and group. Only cued and uncued trials
are considered. Errors bars represent mean
standard errors.

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Dement Geriatr Cogn Disord 2010;29:139–145
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There was an alerting ! SOA interaction (p ! 0.03)
that was modulated by the marginally significant 3-way
interaction among alerting, SOA and group (p = 0.067).
The alerting effect did not differ between SOAs for HC
and AD (F ! 1), whereas alerting had an effect in the DLB
patients with the long SOA (p ! 0.01) but not with the
short SOA (F ! 1).
There was a cueing ! congruency interaction (p !
0.01) that showed a larger congruency effect in uncued
(congruency effect = 167 ms) than in cued trials (congru-
ency effect = 117 ms).
The second main analysis revealed a 3-way interaction
between group, alerting and congruency (p = 0.02; fig. 3 ).
The alerting ! congruency interaction was observed for
HC (p = 0.015) and DLB (p = 0.05) but not for AD (F ! 1).
The alerting ! congruency interaction in the HC group
indicated a larger congruency effect with the alerting
tone than without it. The DLB patients, however, showed
a congruency effect with the alerting tone (p = 0.02) but
not in no-tone trials (F ! 1).
Discussion
First, the data generated by the HC group showed
some interesting results and confirmed the utility of the
ANT as a means by which to test interactions among the
attention networks. The interaction between cueing and
congruency revealed that the visual cue helped focus at-
tention on the target location by filtering out distracting
flankers, an operation that has been attributed to the pul-
vinar nucleus of the thalamus [20] . The interaction be-
tween cueing and alerting showed that orienting was
more effective with the alerting tone than without it in
both cue-target SOAs, supporting the hypothesis that
phasic alerting enhances the functioning of the orienting
network [1] . Finally, the interaction between alerting and
congruency demonstrated that the tone increased the
conflict score, a result that has been interpreted as a re-
duction in the effectiveness of the executive network to
resolve conflict due to the alerting signal [14, 17] . These
results obtained with HC participants replicate previous
findings and therefore constitute an adequate baseline to
assess dementia-related changes in attention network
functioning.
The primary attention deficits observed in both AD
and DLB patients are found in the network interactions.
In the AD patients, for instance, the alerting tone did
not improve orienting with either the short or the long
SOA, in contrast to what was seen with the HC partici-
pants. Phasic alerting triggered by the tone is thought to
be a transient alert state that depends on ascending tha-
lamic projections to the right parietal and frontal lobes;
this network is modulated by the neurotransmitter nor-
epinephrine coming from the locus ceruleus. It has been
shown that phasic alerting can be used to ameliorate
right-hemisphere-based orienting deficits in brain-
damaged patients [21–23] . Thus, the alerting network
seems to coactivate the orienting network, mainly via
the region of the parietal cortex involved in spatial ori-
entation of attention [24] . The lack of improvement in
orienting in the tone-cued tests in AD participants
might be caused by the significant loss of locus ceruleus
noradrenergic neurons that is associated with the dis-
ease [25] . Such a loss might not have a dramatic impact
on the alerting effect, possibly due to top-down modula-
tion of the noradrenergic alerting system coming from
the frontal cortex [26] , but might still have detrimental
400
600
800
1,000
1,200
1,400
1,600
1,800
2,000
2,200
Mean RT (ms)
Congruent
Incongruent
Tone
No-tone
HC
Tone Tone No-toneNo-tone
ADDLB
Fig. 3. Mean RTs as a function of flanker
congruency (congruent, incongruent),
alerting (tone, no-tone) and group. Only
no-cue trials are considered. Errors bars
represent mean standard errors.

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Dement Geriatr Cogn Disord 2010;29:139–145
144
consequences to produce the coactivation of the orient-
ing network. AD patients also seem to have difficulty in
maintaining an optimal level of response readiness,
which is needed to deal with tasks that require rapid re-
sponses. This reduction in sustained alertness might be
responsible for the longer RTs of these patients com-
pared with HC.
DBL shared with AD the reduction in sustained
alertness and was associated with even longer RTs. How-
ever, the DBL patients showed a completely different
pattern of attention deficits compared with the AD pa-
tients. Alerting effects appeared later in the DLB pa-
tients than in AD (the effect was observed only with the
long SOA in the former group). Importantly, without the
alerting tone, the DLB patients showed neither cueing
(orienting) nor congruency (conflict) effects. It seems as
if the patients, on their own, were not capable of attain-
ing the minimal activation of alertness needed for both
attention and information processing to operate. The
observed deficit in alerting is compatible with an im-
portant role for the deterioration that occurs in the locus
ceruleus noradrenergic system. Also, the DLB patients
had serious difficulties in drawing their attention to the
cue location, resulting in a lack of orienting effects. Such
a deficit is consistent with deterioration in the choliner-
gic system of the basal forebrain. Finally, these patients
had problems processing the target display in both con-
gruent and incongruent trials, resulting in long RTs in
both conditions. Interestingly, when an alerting tone
was provided before both the cue and the target, the
DLB patients successfully regulated their orienting and
conflict effects. These results agree with previous stud-
ies that showed that alerting is a basic prerequisite for
normal functioning of the other 2 attention networks
[27] . The threshold of intensity to recruit the attention
system seems to be seriously compromised in DLB pa-
tients.
The present study has revealed that the ANT, a task
that allows us to assess the different components of atten-
tion and their interactions in a single experiment, proved
to be useful in comparing and differentiating attention-
related deficits in both DLB and AD patients. Concerning
cognitive training, previous trials have shown that pa-
tients with left-side neglect improve their orienting defi-
cits after an alerting training program [23] . Given that in
the present study, the orienting and executive network
functioning of the DLB patients was improved by simply
providing an auditory warning, it is a matter of future
research to assess the usefulness of such training with
these patients. With training, an extrinsic alerting condi-
tion might lead to a change in intrinsic alertness, similar
to what is observed in patients with brain damage under-
going such programs.
Acknowledgments
We wish to thank all participants, particularly the patients and
their relatives who kindly agreed to participate in the study.
This study was supported by the Spanish Ministry of Science
and Innovation grants PSI2008-00464/PSIC and DSD2008-
00048 and Fundación Séneca grant 03066/PHCS/05.
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