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Human Brain Mapping 5:110–118(1997)
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Functional Anatomy of Verbal and Visuospatial
Span Tasks in Alzheimer’s Disease
Fabienne Collette,1,2 Eric Salmon,2,3* Martial Van der Linden,2
Christian Degueldre,2 and Georges Franck2,3
1Department
of Neuropsychology, University of Liege, 4000 Liege, Belgium
Research Centre, University of Liege, 4000 Liege, Belgium
3Department of Neurology, University of Liege, 4000 Liege, Belgium
2Cyclotron
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Abstract: The aim of the study was to emphasize cerebral regions which subserve the performance of
short-term memory tasks in patients with Alzheimer’s disease. We correlated scores obtained on span tasks
with cerebral metabolism measured at rest with positron emission tomography. Scores obtained on the
digit span task correlated with glucose metabolism in a brain area centered on the premotor cortex and
extending to the adjacent motor and parietal gyri. There exists some evidence suggesting that this area may
subserve the sequential organization of material stored in short-term memory. In a secondary analysis, we
also observed significant interregional correlations between left-sided brain areas which are part of the
neural network subserving verbal working memory processes in healthy controls. These data suggest that
individual performance on verbal span tasks in AD patients may essentially depend on the preservation of
their ordination processing capacity. The absence of correlation with prefrontal regions suggests that AD
patients might not spontaneously engage central executive resources to reach their maximal span score.
For simultaneous visuospatial span task, the performance of patients correlated with posterior brain
regions, and not with prefrontal cortices. Hum. Brain Mapping 5:110–118, 1997. r 1997 Wiley-Liss, Inc.
Key words: working memory; dementia; Alzheimer; emission tomography
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INTRODUCTION
Working memory refers to a limited capacity system, responsible for the temporary storage and processing of information. According to Baddeley’s model
[Baddeley, 1986], working memory comprises a modality-free attentional control system, the central execu-
Contract grant sponsor: Fonds National de la Recherche Scientifique
(FNRS); Contract grant number: 34551.95; Contract grant sponsor:
Fondation Medicale Reine Elisabeth.
*Correspondence to: Dr Eric Salmon, Cyclotron Research Centre,
University of Liege, B30 Sart Tilman, 4000 Liege, Belgium. E-mail
salmon@pet.crc.ulg.ac.be
Received for publication 4 October 1996; accepted 6 February 1997
r 1997 Wiley-Liss, Inc.
tive, and two main slave systems for temporary maintenance of information: the phonological loop and the
visual sketchpad. The phonological loop processes verbal
material, and is composed of two subsystems: a phonological store and an articulatory rehearsal system. The
visuospatial sketchpad system is assumed to hold and
to manipulate visuospatial images. According to Logie
[1995], the visuospatial system comprises a visual temporary store, which is subject to decay and to interference
from new incoming information, and a spatial temporary store which can be used to plan movement and
also to rehearse the content of the visual store.
A classic way to evaluate slave systems of the
working memory consists in a span procedure: sequences of items of increasing length are presented
and subjects have to recall the sequence immediately
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Span Tasks in AD r
in the same order. Memory span is taken as the
maximum number of items that can be recalled correctly [Miller, 1956]. With regard to the model of
working memory, deficits in span tasks may be related
to impaired functioning of one (or several) specific
subcomponents of the slave systems or to a dysfunction of the central executive [Baddeley, 1986]. Another
explanation of impaired span performance could be a
deficit in the transfer of information between shortand long-term memory [Hulme et al., 1991; 1995].
Positron emission tomographic (PET) studies in healthy
controls located the phonological store in the left supramarginal gyrus, and the articulatory rehearsal system in left
inferior frontal region [Paulesu et al., 1993; Salmon et
al., 1996]. Brain activation during verbal working memory
tasks was also observed in the temporal regions (involved in phonological processing), in the insula (possibly related to production of verbal automatic responses), in the premotor and in the supplementary
motor areas (tentatively related to motor aspects of
speech planning and execution) [Grasby et al., 1993;
Becker et al., 1994; Fiez et al., 1996; Awh et al., 1996].
During visuospatial working memory tasks, brain activation was observed in occipital, parietal, and premotor
cortices [Jonides et al., 1993; Owen et al., 1996]. Parietal
and occipital activations were related to the generation
and short-term storage of visuospatial images [Smith
et al., 1995; Salmon et al., 1996]. There was no explanation for premotor involvement. Finally, prefrontal activation was observed in both verbal and non-verbal
working memory tasks [Smith and Jonides, 1995; Salmon
et al., 1996; Fiez et al., 1996; Owen et al., 1996], and was also
reported in PET or functional magnetic resonance imaging
(fMRI) studies using random generation, concurrent performance of tasks, or updating tasks, which are considered to tap specifically central executive resources
[Petrides et al., 1993; d’Esposito et al., 1995; Salmon et
al., 1996]. In this context, prefrontal activation observed in span tasks could be related to the specific
storage function of the central executive [Baddeley,
1986] or to its coordination function between shortand long-term memory [Hulme et al., 1991, 1995].
Working memory deficits in Alzheimer’s disease
(AD) can be demonstrated using a variety of procedures. AD patients show poor performance on verbal
memory span tasks. However, behavioural factors
such as phonological similarity or articulatory suppression exert normal effects on performance, so that the
phonological loop appears intact in AD [Morris et al.,
1984, 1987]. Short-term memory deficits should then
arise from central executive impairment [Morris, 1986;
Baddeley et al., 1986, 1991]. AD patients also show a
decrease of visuospatial span capacity [Spinnler et al.,
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1986; Grossi et al., 1993; Ergis et al., 1995], but the
nature of the deficit has not been precisely identified.
A previous study based on regions-of-interest showed
that the best predictive metabolic model for verbal shortterm memory performance in Alzheimer’s disease included left superior temporal, parietal, frontal associative, and frontal basal areas [Perani and al., 1993]. The
best predictive model for spatial short-term memory
included metabolic values in the right parietal and
frontal associative areas [Perani et al., 1993].
We used statistical parametric mapping (SPM) [Friston et al., 1995] to look for correlations between scores
at span tasks and cerebral glucose metabolism during
quiet wakefulness in AD, avoiding the a priori hypotheses inherent in ROI analysis. Our first aim was to
show which cerebral regions are correlated to span
tasks memory performance in AD patients. In a second
analysis we searched for correlations between those
cerebral regions and other brain areas, to confirm that
they were included in networks of functionally connected areas already observed in healthy subjects and
AD’s short-term memory activation studies.
METHODS AND PROCEDURES
Subjects
Sixteen subjects (five males and 11 females) with
probable AD [McKhann et al., 1984] were selected for
the study (Table I). They all suffered from dementia
with progressive memory disorder (DSM-III-R, 1987),
and mean duration was 3.4 6 2.3 years. The diagnosis
was based on general medical, neurological, and neuropsychological examination. CT scans showed at
most mild atrophy. Mean age was 71.9 6 5.2 years
(range 64–83) and the mean score at the mini mental
state exam (MMSE) [Folstein et al., 1975] was 19.5 6 4.4
(range 12–29). All patients underwent (18F)fluorodeoxyglucose positron emission tomography (18FDGPET). Patients and relatives gave informed consent to
take part in the study, which was approved by the
University of Liege Ethics Committee.
Neuropsychological scores were compared to those
obtained in a group of 12 volunteers (10 males and two
females) with a mean age of 67.4 6 9.9 years (range:
58–83) which did not differ significantly from that of
AD patients (t 5 1.80, P 5 0.09).
Positron emission tomography
Scans were acquired during quiet wakefulness with
eyes closed, on a Siemens 951/31R tomograph (CTI,
Knoxville, TN) with collimated septa extended, using
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Collette et al. r
TABLE I. Characteristics of the Alzheimer population*
Subjects
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
Mean
Std deviation
Controls
Mean
Std deviation
DiagDuraSimV
Age nostic Sex tion MMSE DS SS
65
74
70
66
68
75
71
64
78
70
83
71
69
73
75
79
71.9
5.2
AD
SAD
SAD
AD
AD
SAD
SAD
AD
SAD
AD
SAD
SAD
SAD
SAD
SAD
SAD
F
F
F
M
F
F
F
F
M
F
M
F
M
F
F
M
4
3
1
2
3
1
3
5
3
8
1
4
3
9
2
2
3.4
2.3
67.4
9.9
21
23
22
29
12
17
15
15
12
21
20
20
22
19
21
23
19.5
4.4
5
4
4
6
4
5
6
3
4
5
3
6
5
3
4
6
4.5
1.1
6
2
5
7
2
5
4
2
8
6
6
5
4
4
6
5
4.8
1.8
5.6
1.0
6.0
0.7
Statistical analysis
* (S)AD 5 (senile) Alzheimer’s disease; MMSE 5 mini mental state
exam. Age and duration are expressed in years. DS 5 digit span;
SimVSS 5 simultaneous visuospatial span.
the 18FDG autoradiographic technique [Phelps et al.,
1979]. A transmission scan was acquired for attenuation correction using three rotating sources of 69Ge.
Emission scans were reconstructed using a Hanning
filter cut-off frequency of 0.5 Hz, giving a transaxial
resolution of 8.7 mm full width at half maximum
(FWHM), and an axial resolution of 5 mm FWHM for
each of 31 planes, with a total field of view of 10.8 cm in
the axial direction.
Span memory tasks
For the digit span task, the examiner read aloud
sequences of digits of increasing length, and subjects
were required to repeat the sequence in the same order.
Three trials were presented per length, and the procedure continued until the subject failed on two sequences of a particular length.
For the simultaneous visuospatial span [Wilson et
al., 1989], subjects looked during three seconds at grids
of increasing size, in which half the squares were black.
Subjects were required to reproduce the pattern. Four
trials were presented per size, and the procedure
continued until the subject failed on three grids of the
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same size. Contrary to the block tapping test [devised
By Corsi, see Milner, 1971] and digit span, this test
does not involve sequencing, but rather consists in
memorizing spatial positions (filled cells in matrix
patterns) which are presented simultaneously. This
task also limits the possibilities of verbal encoding.
Performances on short-term memory tasks were
compared between patients and controls using the
Student t-test.
Parametric images of glucose consumption in Alzheimer’s disease were analysed using SPM [Friston et al.,
1995]. Statistical parametric maps are spatially extended statistical processess which are used to characterize regionally specific effects on imaging data. For
each scan, the 31 transverse planes were interpolated
to 43 planes to render the voxels approximately cubic.
Images were subsequently normalized into a standard
stereotactic anatomical space [Talairach and Tournoux,
1988], and were smoothed using a Gaussian filter (12
mm FWHM) to accommodate intersubject differences
in gyral and functional anatomy, and to increase the
signal to noise ratio in the data set. Correlational studies
between clinical features and resting cerebral metabolism
have frequently been performed in control populations
and mainly in Alzheimer’s disease using region-ofinterest analysis [Riege et al., 1985; Haxby et al., 1985;
Foster et al., 1986; Nybäck et al., 1991; Parasuraman
and Haxby, 1993], but SPM enables to consider the
entire brain metabolic volume for correlations [Friston
et al., 1991, 1992, 1995; Martin et al., 1991]. In order to
identify region-dependent correlations, a pixel by pixel
linear regression of regional out of global metabolism
was performed to remove the confounding effect of
differences in global metabolism [Friston et al., 1990].
Correlations between neuropsychological scores and
cerebral metabolism were then computed on a pixel by
pixel basis by covariance analysis, using age as the
covariate, and scores at span tasks as the variable of
interest. Since we have no time series of images, but
only images of individual brain metabolic distribution,
we tried to explore functional connectivity by using
covariance analysis. Effectively, previous AD studies suggested that correlation coefficients between regional metabolic values could provide a measure of their functional association [Metter et al., 1984; Riege, 1985;
Horwitz et al., 1987; Nybäck et al., 1991]. In a second
stage, after partialling out the effect of global metabolism, we then computed an interregional covariance
analysis for the most significant brain region found in
the first analysis, using age as the covariate, and
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Span Tasks in AD r
individual glucose metabolism in this precise region as the
variable of interest. By doing so, we obtained networks of
functionally related brain regions in AD patients.
For both correlation analyses, we used SPM with a
Z-score threshold of 2.58, corresponding to a significance level of P , 0.005 (uncorrected for multiple
comparisons). We retained cerebral areas where the
probability to obtain the observed number of pixels by
chance over the entire brain volume analysed was
lower than 0.05 (Bonferonni correction). The tables
display the location of pixels with the maximal
Z-values comprised in those brain areas.
RESULTS
Verbal span task
Global cerebral metabolism values did not correlate
with span score in AD (r 5 20.43, P 5 0.095).
Mean verbal span for AD patients was 4.5 6 1.1. This
performance was significantly lower than that of the
controls (5.6 6 1.0, t 5 2.54, P , 0.05), and this
remained true when age was introduced as covariable
[F(1,25) 5 4.40, P , 0.05]. An analysis of occurrence
frequencies of different repetition error types revealed
an important variability between subjects, but omissions and transposition errors were the most frequent
(percentage of omission errors: 36.25 6 27.09; percentage of intervertion errors: 34.16 63 8.45).
A positive correlation was observed between digit
span scores and regional cerebral metabolism in a
brain area centred on the left premotor and precentral
gyrus (Brodmann’s area or BA 6/4), extending to the
left inferior parietal gyrus, in BA 2/40 (Figs. 1 and 2,
and Table II).
When metabolic values in the premotor region were
correlated to whole brain metabolism, significant interregional correlations were observed with a set of left-sided
regions known to subserve verbal short-term memory
in controls: supplementary motor area, medial frontal,
and supramarginal gyrus (BA 40) (Table III).
Simultaneous visuospatial task
Global cerebral metabolism values did not correlate
with span score in AD (r 5 20.37, P 5 0.17).
Mean simultaneous visuospatial span for AD patients was 4.8 6 1.8. This performance was significantly
lower than that obtained by the controls (6.0 6 0.7, t 5
22.14, P , 0.05), and this remained true when age was
introduced as covariable [F(1,25) 5 4.46, P , 0.05].
The brain regions which significantly related to
visuospatial short-term memory performance (Figs. 2
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and 3, and Table IV) were the right superior parietal
and precuneus (BA 7), inferior parietal (BA 40), and
occipital gyrus (BA 18/19).
Metabolic values in parietal area 7 were then correlated to whole brain metabolism. Parietal and occipital
regions were strongly correlated, and correlations were
also observed with the right superior temporal region
(Table V).
DISCUSSION
We first confirmed that our patients with Alzheimer’s disease had a lower digit span than control
subjects. We then observed a positive correlation between digit span performances and metabolism in a
brain area centered on the left ‘‘premotor’’ cortex, and
extending to parietal regions. We further obtained a
positive functional correlation between this brain area
and several left cortical structures such as the supplementary motor area and the supramarginal gyrus,
previously described as subserving the phonological
loop [Paulesu et al., 1993; Salmon et al., 1996]. These
results are consistent with those obtained by Becker et
al. [1996], who showed in an activation study that the
network subserving verbal short-term memory processes was activated to the same extent in Alzheimer’s
disease patients as in controls performing subspan
tasks. Moreover, in a subsequent analysis of the same
data, the left precentral gyrus was activated in the AD
population during the verbal short-term memory task
[Herbster et al., 1996].
However, the mechanism of lower digit span in Alzheimer’s disease must be discussed. Indeed, it has been
suggested that normal verbal span performance not
only involves the phonological loop system but also
requires a contribution of central executive resources
[Baddeley, 1986] and long-term memory [Hulme et al.,
1991, 1995; Salmon et al., 1996]. In this perspective, it
could be argued that while Alzheimer patients rely
exclusively on the automatic process of the phonological
loop to realize the span task, healthy controls’ performance depends on both the phonological loop and the
central executive or long-term memory [Morris, 1987].
A premotor activation, in left or right BA 6, was
reported in most studies of verbal or non-verbal
short-term memory in controls [Petrides et al., 1993;
Jonides et al., 1993; Awh et al., 1996; Owen et al., 1996;
Courtney et al., 1996]. There is an important amount of
literature on single-cell recording of premotor activity
in monkeys planning arm movement [Mitz et al., 1991;
Kurata, 1993; Crammond and Kalaska, 1996], but most
PET studies are controlled for arm movement and
speech, and our correlation study argues for the
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Collette et al. r
Figure 1.
SPM for the positive correlations between verbal working memory performance (verbal span task)
and cerebral metabolism in Alzheimer’s patients.
cognitive nature of premotor activation. Which cognitive process may then be subserved by the premotor
cortex? Fiez et al. [1996] suggested that premotor
activation in verbal short-term memory tasks was
related to maintenance of a ‘‘motor set’’ across a delay
interval, but they also involved prefrontal cortex in
short-term maintenance of information. In a PET study
of movement selection, the premotor cortex was activated for random movements of a joystick or for
learned sequences, but not when a single movement
was performed, be it fixed or conditional (Debeir et al.,
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1991]. There exists some evidence in the literature that
premotor activation might be related to sequential
organization of information stored in working memory.
Owen et al. [1996] recently proposed that the midventrolateral frontal cortex (BA 47) is activated when
the experimental task requires the organization of
remembered series of responses. This remains consistent with our hypothesis that BA 6 is required to
organize series of informations, while BA 47 would be
recruited to remember actively sequences of responses.
In visuospatial working memory tasks, for example,
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Collette et al. r
Figure 2.
Plot of individual span scores and adjusted regional cerebral metabolic activity in Alzheimer’s patients
for the most significant area found in the first analyses.
both BA 6 and BA 47 are activated when subjects have
to organize information about spatial location to subsequently compare stored information with a probe
location [Jonides et al., 1993]. On the contrary, BA 47 is
not required if subjects keep in front of them a pattern
where they just have to organize (using BA6) sequential locations to be remembered [Owen et al., 1996;
Courtney et al., 1996]. Vice versa, BA 47, but not BA 6,
is required when subjects have to remember a well
learned, fixed spatial sequence, that does not need to
be reorganized [Owen et al., 1996]. Although serial
recall was not required in a verbal short-term memory
task which produced left precentral activation in AD
[Herbster et al., 1996], ordinated organization of information might be a simple process already engaged for
three-word recall in AD. The inclusion of pre- and
post-central regions in an area possibly subserving the
organization of information in verbal short-term
memory is not a surprise, for these regions are functionally interconnected. With regard to langage processes,
this ordination function would fit in with a more
general translation process of a phonological diagram
TABLE III. Correlations between metabolic value of the
most significant area presented in Table II (BA 6, 240,
28, 40) and whole brain metabolism*
TABLE II. Correlations between brain metabolism
and digit span in AD*
Brain area
(Brodmann’s area)
L. precentral gyrus (BA 6/4)
L. inferior parietal (BA 2/40)
x
y
z
Z
score
240
232
238
28
222
226
40
48
44
3.49
3.10
3.01
L. medial frontal (BA 8/6)
L. SMA (BA 6)
L. precentral (BA 4)
L. supramarginal gyrus (BA 40)
* AD 5 Alzheimer’s disease; L 5 left; x, y, and z, expressed in mm,
are coordinates in the stereotactical space of Talairach and Tournoux
[1988].
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Brain area
(Brodmann’s area)
x
y
z
Z
score
214
216
230
244
16
22
224
222
48
48
48
16
2.92
3.24
4.42
3.51
* L 5 left; x, y, and z, expressed in mm, are coordinates in the
stereotactical space of Talairach and Tournoux [1988]; SMA 5
supplementary motor area.
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Span Tasks in AD r
Figure 3.
SPM for the positive correlations between visual working memory performance (simultaneous span
task) and cerebral metabolism in Alzheimer’s patients.
into a verbal production by means of an innervatory
pattern [see also Rothi et al., 1991, for praxis model].
Visuospatial spans in our AD patients were essentially correlated with brain metabolism in the dorsal
occipito-parietal stream, involved in visuospatial processing [Mishkin et al., 1983]. Brain activation in these
regions was related to visuospatial working memory
processes and to visual imagery [Jonides et al., 1993;
Kosslyn et al., 1993; Courtney et al., 1996; Goldberg et
al., 1996; Salmon et al., 1996]. There was also a
correlation with the occipito-temporal ventral stream,
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more precisely with the lingal gyrus. On the contrary,
we did not observe any correlation between visuospatial span and metabolic activity in the prefrontal
regions of our AD patients. This is in agreement with
the results of a previous activation study, showing that
occipital (BA 19/7) and parietal (BA 7), but not frontal
regions were activated when a visuospatial short-term
memory task was compared to a control somatomotor
task [Courtney et al., 1996]. By comparison with verbal
span tasks, we could postulate that AD patients do not
spontaneously engage central executive resources to
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Collette et al. r
TABLE IV. Correlations between brain metabolism
and simultaneous visuospatial span in AD*
Brain area
(Brodmann’s area)
R. superior parietal (BA 7)
R. inferior parietal (BA 40)
R. middle occipital (BA 18/19)
R. lingual gyrus (BA 19)
ACKNOWLEDGMENTS
x
y
z
Z
score
12
28
16
40
28
24
24
264
262
278
230
272
282
254
48
48
40
32
20
8
24
3.93
3.75
3.29
3.62
2.96
3.33
3.4
REFERENCES
* AD 5 Alzheimer’s disease; R 5 right; x, y and z, expressed in mm,
are coordinates in the stereotactical space of Talairach and Tournoux
(1988).
reach their plateauing performance in visuospatial
span tasks, but rely essentially on posterior associative
cortices. AD patients’ individual levels of performance
would then depend on the degree of metabolic impairment in posterior associative cortices.
The putative hypothetical function of BA 6 and BA 7
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increasing word list length from 2 to 13 correlated with
increasing rCBF in left and right lateral premotor
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superior and middle frontal gyrus. Our next step is to
design parametric activation studies using subspan
tasks to confirm the role of the regions emphasized in
this report, and to question the relative contribution of
frontal regions to short-term memory processes.
TABLE V. Correlations between metabolic value of the
most significant area presented in table IV (BA 7, 12,
264, 48) and whole brain metabolism*
Brain area
(Brodmann’s area)
R. insula
R. precuneus (BA 7)
R. inf. parietal (BA 40)
Mid./sup. occipital (BA 18/19)
R. sup. temporal (BA 42/22)
x
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Z
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34
16
24
40
52
28
24
42
240
278
248
232
232
272
282
234
24
40
36
32
28
20
12
8
3.91
3.29
3.70
3.46
3.49
3.12
3.61
3.26
*R 5 right; inf 5 inferior; sup 5 superior; mid 5 middle; x, y, and z,
expressed in mm, are coordinates in the stereotactical space of
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The study was supported by a grant (34551.95) from
the Fonds National de la Recherche Scientifique (FNRS)
and by the Fondation Medicale Reine Elisabeth. E.S. is
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