Increased Brain Activity in Frontal and Parietal Cortex
Underlies the Development of Visuospatial Working
Memory Capacity during Childhood
Torkel Klingberg, Hans Forssberg, and Helena Westerberg
Abstract
& The aim of this study was to identify changes in brain
activity associated with the increase in working memory (WM)
capacity that occurs during childhood and early adulthood.
Functional MRI (fMRI) was used to measure brain activity in
subjects between 9 and 18 years of age while they performed a
visuospatial WM task and a baseline task. During performance
of the WM task, the older children showed higher activation of
INTRODUCTION
The amount of information one can keep in working
memory (WM) increases throughout childhood and
early adulthood (Gathercole, 1999; Luciana & Nelson,
1998; Hale, Bronik, & Fry, 1997). This increase in WM
capacity is thought to be important for the development
of a wide range of cognitive skills, including reading and
logical reasoning (Engle, Kane, & Tuholski, 1999; Fry &
Hale, 1996; Hulme & Roodenrys, 1995). The changes in
WM capacity coincide in time with several neuronal
developmental processes, including a decrease in syn-
aptic density (Bourgeois & Rakic, 1993; Huttenlocher,
1979), axonal elimination (LaMantia & Rakic, 1990),
changes in global cerebral metabolism (Chugani &
Phelps, 1986; Kennedy & Sokoloff, 1957), myelination
(Klingberg, Vaidya, Gabrieli, Moseley, & Hedehus, 1999;
Paus et al., 1999; Yakovlev & Lecours, 1967; Flechsig,
1920), and changes in catecholamine receptor structure
and density (Lambe, Krimer, & Goldman-Rakic, 2000).
However, there have been no studies measuring any of
these maturational processes and correlating them with
WM capacity in the same individuals.
Functional neuroimaging studies show that children
activate similar areas as adults do during the perform-
ance of WM tasks (Nelson et al., 2000; Thomas et al.,
1999; Casey et al., 1995). Data from WM studies includ-
ing both adults and children is very limited (Thomas
et al., 1999), and none have made any direct voxel-by-
voxel comparisons of regional changes in brain activity
Karolinska Institute
D 2002 Massachusetts Institute of Technology
cortex in the superior frontal and intraparietal cortex than the
younger children did. A second analysis found that WM
capacity was significantly correlated with brain activity in the
same regions. These frontal and parietal areas are known to be
involved in the control of attention and spatial WM. The
development of the functionality in these areas may play an
important role in cognitive development during childhood. &
with age. Moreover, it has proven difficult to design the
tasks so that the different age groups perform at the
same level during scanning. When performance during
scanning varies between two groups, differences in
brain activity between the same groups are difficult to
interpret.
In the present study, we used a visuospatial WM task
(Figure 1) that is sensitive for measuring developmental
changes in WM capacity (Hale et al., 1997; Fry & Hale,
1996). Children between 9 and 18 years of age per-
formed the task while their brain activity was measured
with functional MRI (fMRI). By keeping the WM load low
in the scanner version of the task, we intentionally
created a ceiling effect in order to minimize interindi-
vidual differences in behavior during scanning. Differ-
ences in WM capacity was estimated outside the scanner.
The WM-related brain activity was then analyzed to find
correlations between brain activity and age, as well as
between brain activity and WM capacity.
RESULTS
Accuracy during scanning was generally high, except in
one subject where d0 = 0.03, which was >3 SD from
the mean of the other subject. This subject was there-
fore excluded from the analysis. After exclusion of this
subject, the mean d0 was 2.71 (SD = 0.29), with no
correlation between accuracy during scanning and age
(r = .31, p = .30). The mean reaction time during the
WM tasks was 718 (SD = 118) msec, with a non-
significant trend towards shorter reaction times in old-
er children (r = .50; p = .08).
Journal of Cognitive Neuroscience 14:1, pp. 1–10
 Areas activated as a main effect of WM, across all ages
and across both Load 3 and Load 5, are shown in Figure
2a–b and listed in Table 1. These areas covered parts of
the prefrontal cortex in the superior and middle frontal
gyri and inferior and superior frontal sulci, cingulate
cortex, and large parts of the parietal and occipital
cortices. The following analyses were restricted to those
areas in which a main effect of WM was seen.
Subtraction images first were created by subtracting
the brain activity during the baseline task from the mean
activity during the WM tasks. One subtraction image was
created for each subject. The subtraction images were
then used in a second-level analysis where age was used
as a covariate to find values in these subtraction images
that correlated with age. A positive correlation with age
was found bilaterally in the superior frontal sulcus, in the
intraparietal and superior parietal cortex, and in the left
occipital cortex (Table 1; Figure 2c–d and Figure 3). In
statistical terms, this correlation is an interaction be-
tween the effect of age and the effect of WM. All of these
areas were also significantly activated when accuracy
during scanning (d0 from each subject) was used as a
confound, that is, when variance in brain activity that
could be attributed to differences in performance during
scanning was removed prior to correlation with age. A
tendency towards a negative interaction was found in
the right inferior frontal sulcus (Table 1). As described
in the Introduction, such interaction could possibly
be explained by the trend of negative correlation
between reaction time and age. We therefore included
reaction times as a confound, that is, removed variance
due to differences in reaction times before analyzing the
effect of age. However, including reaction times as a
confound only marginally influenced this effect, decreas-
ing the overall significance of the cluster from p = .08 to
p = .11. In a different analysis, we investigated the
interaction between WM load and age (difference be-
tween Load 5 and Load 3 was correlated with age). No
such significant interaction was found.
Figure 1. Working memory
task performed during scan-
ning. The subjects were asked
to remember the location of red
circles that were presented se-
quentially in a 4  4 grid. After a
1500-msec delay, a circle ap-
peared and the subjects pressed
a button if the circle was in the
same location as any of the
dots. Two versions of this task
was given during scanning: one
with three circles to remember
and one with five. In the base-
line condition, subjects watched
as green circles were presented
sequentially in either of the four corner boxes (top-left, top-right, bottom-left, or bottom-right). After a 1500-msec delay, a green circle appeared in
the middle of the grid and the subjects pressed the button.
2 Journal of Cognitive Neuroscience
WM capacity was measured outside the scanner and
used as a covariate in the same way as the effect of age
was analyzed. Correlation between WM capacity and WM
activity was found in the left superior frontal sulcus and
in the left intraparietal cortex (Figure 2e–f; Table 1), thus
confirming that the correlation between age and WM
related activity was due to the age trends in WM
capacity.
To exclude that there was a lower signal-to-noise ratio
in the images from younger subjects, a ‘‘control-sub-
traction’’ was done. Because there were more visual
stimuli in the baseline task than in the Load 3 WM task
(five circles vs. three circles), subtraction of Load 3 from
baseline would presumably show an effect of this differ-
ence in visual stimulation. When brain activity during
Load 3 was subtracted from baseline task, a large,
significant activation of primary visual cortex and sur-
rounding early visual areas showed up. However, no
interaction was found between activity in this area and
age ( p = .98, using the same thresholds as in the
analysis of interaction between WM and age). This lack
of interaction between visually induced activity and age
confirmed that the interactions between WM-induced
activity and age were not due to a generally lower signal-
to-noise ratio in younger children.
To investigate if there was an age-related trend in the
amount of cortex activated, we performed a separate
statistical analysis of the main effect of WM in each single
subject. Significant clusters were identified (z > 3.09;
cluster size > 45), and the total number of voxels
in these clusters were counted for each subject and
correlated with age. However, there were no age-related
trends in the amount of cortex activated (r = .09,
p = .76).
DISCUSSION
A positive correlation between age and WM-related brain
activity was found in several areas, including the cortex
Volume 14, Number 1
Table 1. Areas Activated during WM Tasks and Correlation between Age and Activity

Coordinates

Area x y z t Value

Areas activated during performance of the WM tasks

Superior frontal sulcus
Right 22 8 60 8.67
20 10 64 6.29
Left 26 0 56 10.93
38 6 60 5.11
Middle frontal sulcus
Right 42 2 28 7.99
44 26 40 7.62
Left 50 4 32 9.97
52 30 32 6.42
Frontal operculum
Right 38 20 8 7.64
Left 46 18 8 7.13
Cingulate cortex 4 12 48 8.97
0 26 36 8.50
0 38 36 7.87
Caudate nucleus
Right 6 4 8 4.01
Inferior and intraparietal cortex
Right 22 72 56 11.32
42 42 44 8.85
Left 24 68 60 14.50
44 46 48 10.29

Correlation between WM-related activity and age

Positive correlations
Superior frontal sulcus
Right 30 0 52 4.72
Left 24 4 52 4.48
28 6 60 2.83
Superior and intraparietal cortex
Right 22 64 48 4.75
Left 26 60 60 4.65
Middle occipital gyrus
Left 32 72 16 3.55
Negative correlations
Inferior frontal sulcus
Right 42 4 40 2.90*

Klingberg, Forssberg, and Westerberg 3

Table 1. (continued )
Coordinates
Area x y
Correlation between WM-related activity and WM capacity
Positive correlations
Superior frontal sulcus
Left 26
Intraparietal cortex
Left 36
Inferior parietal cortex 50
For all clusters p < .05 corrected for multiple comparison, except *p = .08; **p = .13.
in the superior frontal sulcus and intraparietal sulcus,
bilaterally. In a second analysis, a positive correlation
between WM capacity and WM activity was found in the
left superior frontal and left intraparietal areas. This
second analysis suggests that the interaction between
brain activity and age in these areas was due to the
increases in WM capacity with age.
The positive correlation between WM capacity and
brain activity is contrary to the results of some prior
imaging studies that have associated improved perform-
ance as a result of training with lower activity in pre-
frontal areas (Klingberg & Roland, 1998; Jenkins, Brooks,
Nixon, Frackowiak, & Passingham, 1994; Raichle et al.,
1994). The tasks where frontal activity decreased, how-
ever, can presumably become automatic with training,
which is not the case with WM tasks. In general, lower
prefrontal activity associated with superior performance
(Haier et al., 1988) could be due to shorter reaction
times, and thus less time on task (Poldrack, 2000;
D’Esposito et al., 1997). Higher accuracy can also be
associated with less prefrontal activity related to error
detection and error correction. In the present study,
however, interindividual differences in behavior during
scanning were minimized. The increased activity with
higher age therefore represents a developmental trend
in the relationship between behavior and brain activity.
The anatomy and functionality of the frontal and
parietal areas will first be commented on, before discus-
sing the possible mechanism underlying the interaction
between age and WM activity.
Functions of the Superior Frontal Sulcus
Correlation between age and WM activity was found in
the cortex lining the superior frontal sulcus, extending
anteriorly from the intersection of the superior frontal
sulcus and precentral sulcus. Several previous studies of
visuospatial WM have also reported activation at this
location (Rowe, Toni, Josephs, Frackowiak, & Passing-
ham, 2000; Postle & D’Esposito, 1999; Courtney, Petit,
4 Journal of Cognitive Neuroscience
z t Value
4 60 3.59
76 44 5.83
46 56 2.90**
Maisog, Ungerleider, & Haxby, 1998; Sweeney et al.,
1996; Smith et al., 1995; Jonides et al., 1993). In addition
to spatial WM tasks, visual but nonspatial WM tasks
activate this region (Postle & D’Esposito, 1999; Kling-
berg, 1998; Cohen et al., 1997). Several studies have
further characterized the temporal dynamics of activity
in this area and found that it exhibits sustained activity
during the delay period when information is held in WM
(Rowe et al., 2000; Cohen et al., 1997; Courtney, Un-
gerleider, Keil, & Haxby, 1997). The activity thus resem-
bles the delay-specific activity, which is generally
considered to be the hallmark of WM activity in electro-
physiological studies of WM in macaques (Funahashi,
Bruce, & Goldman-Rakic, 1989; Fuster & Alexander,
1971).
The region where we observed a significant correla-
tion was located close, although slightly superior and
anterior, to previously reported activations associated
with voluntary eye movements. Eye-movement-related
activity is generally found along the anterior wall of the
precentral sulcus (Corbetta et al., 1998; Luna et al., 1998;
Paus, 1996; Fox, Fox, Raichle, & Burde, 1985). Further-
more, in the present study, the number of stimuli per
trial, and thus presumably the number of saccades, was,
on average, higher during the baseline condition (five
dots) than in the WM conditions (three and five dots,
respectively); therefore, the activation in the WM tasks
in this study was presumably not due to saccadic eye
movements. Courtney et al. (1998) suggested that activ-
ity underlying visuospatial WM is topographically sepa-
rate from that produced by voluntary saccades. In their
study, eye-movement-related and WM-related activities
overlapped in the intersection of the superior frontal
sulcus and the precentral sulcus. However, the eye
movement–related activity extended inferiorly along
the precentral sulcus, while the WM-related activity
extended anteriorly along the superior frontal sulcus,
consistent with the location of the WM-related activity in
the present study and with eye-movement-related activ-
ity in other studies (Corbetta et al., 1998; Paus, 1996; Fox
Volume 14, Number 1
Figure 2. BOLD responses during the WM tasks. (a, b) Main effect of WM in the right (a) and left (b) hemisphere. (c, d) Areas showing a correlation
between WM activity and age: (c) horizontal section showing activity bilaterally in the superior frontal sulcus and intraparietal sulcus; (d) coronal
section showing activity in the left superior frontal sulcus. (e, f ) Areas showing a correlation between WM capacity and WM-related activity: (e)
horizontal section showing the left superior frontal sulcus and left inferior- and intraparietal cortex; (f ) coronal section showing activity in the left
superior frontal sulcus.

Klingberg, Forssberg, and Westerberg 5


Figure 3. BOLD responses in the superior frontal cortex. (A) Relative
signal change plotted against age. A = boys; 6 = girls. (B) Activation
in the two versions of the WM tasks; Load 3 and Load 5, for younger
and older children.
et al., 1985). Nonetheless, a later study could not
reproduce the topographical separation of activity re-
lated to eye movements from that related to WM (Postle,
Berger, Taich, & D’Esposito, 2000). If the same area is
activated by both WM and eye movement, it would be
analogous to the results suggesting that top-down at-
tention and eye movements activate the same anatom-
ical area (Corbetta et al., 1998).
Several tasks involving ‘‘top-down’’ or ‘‘voluntary
control’’ of attention have found activation at an almost
identical superior frontal site as in visuospatial WM tasks
(Hopfinger, Buonocore, & Mangun, 2000; Kastner,
Pinsk, De Weerd, Desimone, & Ungerleider, 1999; Cor-
betta et al., 1998). In these tasks, the subject is cued
about the location of a future target or searches for a
particular known target. The subject thus needs to keep
a representation of the target or its location in WM in a
similar way as information is kept on-line in WM tasks.
Top-down attention and WM could thus be overlapping
concepts, with overlaps in the underlying brain activity,
as have also been suggested previously (Kastner &
Ungerleider, 2000; Desimone & Duncan, 1995).
Functions of the Intraparietal Cortex
The inferior and intraparietal cortex shares many func-
tional characteristics with the superior frontal cortex: It
is active during visuospatial WM tasks (Rowe et al., 2000;
Postle & D’Esposito, 1999; Courtney et al., 1998; Swee-
ney et al., 1996; Smith et al., 1995; Jonides et al., 1993)
and shows sustained activity during the delays in the WM
tasks (Rowe et al., 2000; Cohen et al., 1997). The intra-
parietal cortex is also active in tasks demanding volun-
tary control of visual attention (Corbetta, Kincade,
Ollinger, McAvoy, & Shulman, 2000; Hopfinger et al.,
2000; Kastner et al., 1999) and has sustained activity
during the cue period in such tasks (Corbetta et al.,
2000; Hopfinger et al., 2000; Kastner et al., 1999).
Although the functional parcellation of the intra-
and inferior parietal cortex is unclear at this point, this
intra/inferior parietal region can be separated from an
area in the temporo-parietal junction (about 15 mm
above the AC–PC line), which is not involved in top-
6 Journal of Cognitive Neuroscience
down control but is involved in orienting (Corbetta
et al., 2000; Downar, Crawley, Mikulis, & Davis, 2000)
and arousal (Coull, Nobre, & Frith, 2001). Intraparietal
and inferior parietal cortex is active in a wide range of
tasks demanding WM and control of attention. Several
studies comparing different types of stimuli within the
same session have found evidence of activity in the
inferior and intraparietal cortex that is independent of
the modality of the stimuli (Bushara et al., 1999; Coull &
Frith, 1998; Klingberg, 1998; Klingberg, Roland, & Kawa-
shima, 1996). A possible supramodal function would be
especially interesting in light of the present results, since
development of functionality in a supramodal area could
explain the increase in WM capacity and the improve-
ment in control of attention, which both occur across
different sensory modalities.
Fronto-parietal networks have been suggested to
underlie WM in macaques (Friedman & Goldman-Rakic,
1994; Quintana & Fuster, 1993). In humans, the inferior
and intraparietal cortex is often co-activated, as well as
correlated, with areas in the superior and middle
frontal gyri during tasks demanding WM and top-down
attention (Klingberg, O’Sullivan, & Roland, 1997). Re-
cordings of electrical activity also show that frontal and
posterior association cortices increase coherence dur-
ing the delay period in WM tasks (Sarnthein, Petsche,
Rappelsberger, Shaw, & von Stein, 1998). Taken to-
gether, this suggests that performance of visuospatial
WM tasks will not only depend on local computations
within these areas, but will also depend on the com-
munication between them.
Possible Mechanisms Underlying the Age-Related
Changes
There are several maturational processes that coincide
in time with the increase in WM capacity. Myelination is
of particular interest because the inferior parietal cortex,
where we found an interaction between activity and age,
is among the last brain regions to myelinate (Yakovlev &
Lecours, 1967; Flechsig, 1920). This late myelination
includes intracortical neuropil, as well as radial fibers
and tangential fibers entering the supragranular layer.
Myelination of the parietal fibers would presumably
increase transmission speed locally within the parietal
cortex, as well as effect the communication between the
parietal and frontal cortices. Myelination could thus
enhance cortico-cortical excitation and metabolism in a
fronto-parietal network. The functional relevance of this
would be a fronto-parietal activity that is more stable
during WM delays and cue periods and thus is more
resistant to interference. The superior frontal sulcus is
not among the last regions to myelinate, but the corre-
lation of activity and age could possibly be secondary to
the development of the intraparietal cortex, which, in
this particular task, forms a network with cortex in the
superior frontal sulcus.
Volume 14, Number 1
 Synaptic and axonal pruning is another possible con-
tributor to the interaction between brain activity and
age. There is an overproduction of connections and
synapses early in life, with a pruning of the connections
that are not used (Bourgeois & Rakic, 1993; LaMantia &
Rakic, 1990; Huttenlocher, 1979). Less competition with
input from other areas could leave the fronto-parietal
communications more stable. Therefore, although the
total number of synapses decreases, the connections
related to WM would be more active during perform-
ance of WM tasks. Yet, another possibility is that the
activities in the frontal and parietal areas were effected
by developmental changes outside the superior frontal
and parietal areas. One example would be increased
input to the fronto-parietal network from a more ante-
rior prefrontal area that was inconsistently located be-
tween individuals and therefore did not show up in the
group analysis.
Conclusions
This study found a positive correlation between age-
related increases in WM capacity and brain activity in the
superior frontal and intraparietal cortex. Future studies,
using verbal tasks or more complex problem-solving
tasks, might show other or additional areas where
activity changes with age. The present study suggests
that the relationship between WM capacity and brain
activity is positive, that is, with higher activity in older
children, presumably because this is associated with a
more stable and interference-resistant delay activity.
The areas where we observed a developmental trend
are known to be involved in a wide range of functions
that demand visuospatial WM and control of attention.
The parietal area is, furthermore, one of the last in the
brain to myelinate and is involved in a wide range of
tasks requiring attention and WM. The development of
functionality in these areas may therefore be an impor-
tant contributor to the development of cognitive abil-
ities during childhood.
METHODS
Subjects
Fourteen healthy volunteers participated in the study.
After exclusion of one subject (see Results), the 13
remaining participants (4 girls, 9 boys) were aged 9.4–
18.5 years (mean 13.4). The study was approved by the
local ethics committee.
Tasks
WM Tasks During Scanning
This task is illustrated and described in Figure 1. Two
versions of the WM tasks were used: one with three
targets and one with five targets. In order to have the
same overall time for the target presentation period,
there were longer delays between the stimuli during the
presentation period in the three-target version than in
the five-target version and the baseline task.
Baseline Task
Five green, filled circles were presented sequentially.
After a 1500-msec delay, a green unfilled circle appeared
in the middle of the grid. The subjects were instructed
to look at each of the green filled circles as they
appeared and always press the button when the unfilled
green circle appeared. The control condition was thus
designed to control for visual stimulation, eye move-
ments, and motor output.
WM Task Outside the Scanner
The task was similar to the scanning task in that circles
were presented sequentially in a 4  4 grid. However,
after the delay, the subject indicated, by using a com-
puter mouse, each of the locations where targets had
appeared. The number of targets varied from three to
nine, with two trials on each level. The total number of
correctly indicated locations in all trials on all levels was
taken as our measurement of the individuals WM ca-
pacity. The WM capacity was later used as a covariate in
the analysis of fMRI data.
Procedure
The WM capacity of each subject was tested before
scanning. Subjects received additional training on the
scanner version of the WM task before entering the
scanner. All stimuli were presented on a computer using
E-prime software (Psychology Software Tools). During
scanning, the subjects watched the stimuli on a screen
via a mirror mounted on the head coil. The subjects
responded by pressing a button with their right index
finger. Responses were collected using a button-
response unit connected to the computer controlling
the stimuli. Head movements were restricted by wedge-
formed pillows on both sides of the head and an addi-
tional adhesive tape over their forehead. During scan-
ning, 30-sec epochs of baseline task and WM tasks were
alternated, with the order counterbalanced between the
two runs. Each run lasted 5 min.
MR Scanning
Images were acquired using a 1.5-T GE Signa scanner.
T2*-weighted, gradient echo, spiral echo-planar images
were acquired with TR = 2500 msec, TE = 70, flip angle
= 858, 18 axial slices, 5.0 mm slice thickness, 220  220
mm FOV, 64  64 grid, resulting in voxels that were
3.4  3.4  5.0 mm. For each subject, 240 volumes were
acquired during two 5-min sessions. T1-weighted spin–
Klingberg, Forssberg, and Westerberg 7
echo images, FOV=220  220 mm, 256  256 grid, were
acquired in the same position as the functional images
and used for anatomical normalization of the functional
images. Total time in the scanner was less than 35 min
for most subjects.
Data Analysis
The data were analyzed with SPM99 (Welcome Depart-
ment of Cognitive Neurology, London, UK) (Friston
et al., 1995). Motion during scanning was estimated by
six parameters (three translations, three rotations),
which were used to realign the functional images to
the first image in the series, and later used as confounds
in the statistical analysis. The T1-weighted images were
normalized to Talairach space using a template from the
Montreal Neurological Institute. The parameters from
this normalization were then used to normalize the
functional images, which were subsampled to a voxel
size of 2  2  4 mm and then smoothed with an
isotropic Gaussian kernel of 6.0 mm.
There were two different version of the WM task, one
with three and one with five stimuli. However, in the
present analysis, these two conditions were analyzed
together relative to the baseline task. To identify areas
involved in the WM tasks, a fixed-effects model was used,
including all images from all subjects. The main effect of
WM was estimated by a general linear model. Low
frequency (<1/120 Hz) drifts in the signal were removed
by including cosine basis functions as confounds in the
model. The six parameters describing head movement
during scanning were also included as confounds, as was
the effect of scanning session.
To identify age-related changes in activity, a so called
‘‘random-effects’’ model was used. For each subject, the
main effect of WM was estimated with a general linear
model removing low-frequency drifts, motion-corre-
lated signals, and session effects as described above.
An image was then formed for each subject, describing
the estimated mean activity during WM tasks, as com-
pared to the baseline task. A correlation was then made
between age (or WM capacity) and voxel values in these
images describing estimated mean activity during the
WM tasks.
Estimating the Effect of Removing Motion-Related
Signals
Removal of signal correlated with head motion, as
described above, could potentially in itself introduce
age-related differences in signal detection (Josephs &
Henson, 1999). To evaluate the effect of removing
motion-correlated signals, we first formed a vector Y,
with ones and zeros describing the on–off pattern of WM
and control condition. Motion-correlated variance was
then removed from Y using multiple regression analysis.
The residuals from Y were then bandpassed using the
8 Journal of Cognitive Neuroscience
same bandpass filter that was applied to the functional
data. The bandpassed data was then Fourier-trans-
formed, and the energy was calculated as the sum of
the power spectrum. This energy is a measurement of
the signal-to-noise of the image (Josephs & Henson,
1999) and was calculated for each individual and then
correlated with age. There was no significant correlation
between age and energy (r = .18; p = .55), demon-
strating that the removal of signals correlated with head
motion did not introduce any age-related bias.
Estimating Age-Related Differences in Brain Size
From the 4  4 matrix containing the normalization
parameters, the linear scaling factor in the x, y, and z
directions, were identified from each subject and then
correlated with age. No significant correlation between
age and brain size was found: (X: r = .05; p = .87;
Y: r = .34; p = .26; Z: r = .09; p = .76). This is consistent
with previous investigations showing that the total brain
size does not increase during the time between ages 9
and 18 (Reiss, Abrams, Singer, Ross, & Denckla, 1996).
Reprint requests should be sent to Torkel Klingberg, Kar-
olinska Institute, Department of Neuropediatrics, Astrid
Lindgrens Children’s Hospital Q2:07, 171 76 Stockholm,
Sweden, or via e-mail: torkel.klingberg@neuro.ki.se.
The data reported in this experiment have been deposited in
the fMRI Data Center (http://www.fmridc.org). The accession
number is 2-2001-1123Y.
REFERENCES
Bourgeois, J. P., & Rakic, P. (1993). Changes of synaptic density
in the primary visual cortex of the macaque monkey from
fetal to adult stage. Journal of Neuroscience, 13, 2801–2820.
Bushara, K. O., Weeks, R. A., Ishii, K., Catalan, M. J., Tian, B.,
Rauschecker, J. P., & Hallett, M. (1999). Modality-specific
frontal and parietal areas for auditory and visual spatial
localization in humans. Nature Neuroscience, 2, 759–766.
Casey, B. J., Cohen, J. D., Jezzard, P., Turner, R., Noll, D. C.,
Trainor, R. J., Giedd, J., Kaysen, D., Hertz-Pannier, L., &
Rapoport, J. L. (1995). Activation of prefrontal cortex in
children during a nonspatial working memory task with
functional MRI. Neuroimage, 2, 221–229.
Chugani, H. T., & Phelps, M. E. (1986). Maturational changes in
cerebral function in infants determined by 18FDG positron
emission tomography. Science, 231, 840–843.
Cohen, J. D., Pearstein, W. M., Braver, T. S., Nystrom, L. E.,
Noll, D. C., Jonides, J., & Smith, E. E. (1997). Temporal
dynamics of brain activation during a working memory task.
Nature, 386, 604–608.
Corbetta, M., Akbudak, E., Conturo, T. E., Snyder, A. Z., Ollin-
ger, J. M., Drury, H. A., Linenweber, M. R., Petersen, S. E.,
Raichle, M. E., Van Essen, D. C., & Shulman, G. L. (1998). A
common network of functional areas for attention and eye
movements. Neuron, 21, 761–773.
Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P., &
Shulman, G. L. (2000). Voluntary orienting is dissociated
from target detection in human posterior parietal cortex.
Nature Neuroscience, 3, 292–297.
Volume 14, Number 1
Coull, J. T., & Frith, C. D. (1998). Differential activation of right
superior parietal cortex and intraparietal sulcus by spatial
and nonspatial attention. Neuroimage, 8, 176–187.
Coull, J. T., Nobre, A. C., & Frith, C. D. (2001). The noradre-
nergic a2 agonist clinidine modulates behavioural and neu-
roanatomical correlates of human attentional orienting and
alerting. Cerebral Cortex, 11, 73–84.
Courtney, S. M., Petit, L., Maisog, J. M., Ungerleider, L. G., &
Haxby, J. V. (1998). An area specialized for spatial working
memory in human frontal cortex. Science, 279, 1347–1351.
Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. V.
(1997). Transient and sustained activity in a distributed
neural system for human working memory. Nature, 386,
608–611.
Desimone, R., & Duncan, J. (1995). Neural mechanisms of se-
lective visual attention. Annual Reviews of Neuroscience,
18, 193–222.
D’Esposito, M., Zarahn, E., Aguirre, G. K., Shin, R. K., Auerbach,
P., & Detre, J. A. (1997). The effect of pacing of experimental
stimuli on observed functional MRI activity. Neuroimage, 6,
113–121.
Downar, J., Crawley, A. P., Mikulis, D. J., & Davis, K. D. (2000).
A multimodal cortical network for the detection of changes
in the sensory environment. Nature Neuroscience, 3, 277–
283.
Engle, W. R., Kane, J. M., & Tuholski, S. W. (1999). Individual
differences in working memory capacity and what they tell
us about controlled attention, general fluid intelligence, and
functions of the prefrontal cortex. In A. Myake & P. Shah
(Eds.), Models of working memory (pp. 102–134). Cam-
bridge: Cambridge University Press.
Flechsig, P. (1920). Anatomie des Menschlichen Gehirns und
Rückenmarks auf Myelogenetischer Grundlage. Leipzig,
Germany: Thieme.
Fox, P. E., Fox, J. M., Raichle, M. E., & Burde, R. M. (1985). The
role of cerebral cortex in the generation of voluntary sac-
cades: A positron emission tomographic study. Journal of
Neurophysiology, 54, 348–369.
Friedman, H. R., & Goldman-Rakic, P. S. (1994). Coactiva-
tion of prefrontal cortex and inferior parietal cortex in
working memory tasks revealed by 2DG functional map-
ping in the rhesus monkey. Journal of Neuroscience, 14,
2775–2788.
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C.
D., & Frackowiak, R. S. J. (1995). Statistical parametric maps
in functional imaging: A general linear approach. Human
Brain Mapping, 2, 189–210.
Fry, A. F. & Hale, S. (1996). Processing speed, working mem-
ory, and fluid intelligence. Psychological Science, 7, 237–
241.
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989).
Mnemonic coding of visual space in the monkey’s dorsola-
teral prefrontal cortex. Journal of Neurophysiology, 61, 331–
349.
Fuster, J. M. & Alexander, G. E. (1971). Neuron activity related
to short-term memory. Science, 173, 652–654.
Gathercole, S. E. (1999). Cognitive approaches to the develop-
ment of short-term memory. Trends in Cognitive Sciences,
3, 410–419.
Haier, R. J., Siegel, B. V., Nuechterlein, K. H., Hazlett, E., Wu, J.
C., Paek, J., Browning, H. L., & Buchsbaum, M. S. (1988).
Cortical glucose metabolic-rate correlates of abstract rea-
soning and attention studied with positron emission
tomography. Intelligence, 12, 199–217.
Hale, S., Bronik, M. D., & Fry, A. F. (1997). Verbal and spatial
working memory in school-age children: Developmental
differences in susceptibility to interference. Developmental
Psychology, 33, 364–371.
Hopfinger, J. B., Buonocore, M. H., & Mangun, G. R. (2000).
The neural mechanisms of top-down attentional control.
Nature Neuroscience, 3, 284–291.
Hulme, C. & Roodenrys, S. (1995). Practitioners review: Verbal
working memory development and its disorders. Journal of
Child Psychology and Psychiatry, 36, 373–398.
Huttenlocher, P. (1979). Synaptic density in human frontal
cortex — developmental changes and effects of aging. Brain
Research, 163, 195–205.
Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S. J., &
Passingham, R. E. (1994). Motor sequence learning: A study
with positron emission tomography. Journal of Neu-
roscience, 14, 3775–3790.
Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S.,
& Mintun, M. A. (1993). Spatial working memory in humans
as revealed by PET. Nature, 363, 623–625.
Josephs, O. & Henson, R. N. (1999). Event-related functional
magnetic resonance imaging: Modelling, inference and op-
timization. Philosophical Transactions of the Royal Society
of London, Series B: Biological Sciences, 354, 1215–1228.
Kastner, S., Pinsk, M. A., De Weerd, P., Desimone, R., &
Ungerleider, L. G. (1999). Increased activity in human visual
cortex during directed attention in the absence of visual
stimulation. Neuron, 22, 751–761.
Kastner, S. & Ungerleider, L. G. (2000). Mechanisms of visual
attention in the human cortex. Annual Reviews of Neu-
roscience, 23, 315–341.
Kennedy, C. & Sokoloff, L. (1957). An adaptation of the nitrous
oxide method to the study of the cerebral circulation in
children; normal values for cerebral blood flow and cerebral
metabolic rate in childhood. Journal of Clinical Investiga-
tions, 36, 1130–1137.
Klingberg, T. (1998). Concurrent performance of two working
memory tasks: Potential mechanisms of interference. Cere-
bral Cortex, 8, 593–601.
Klingberg, T., O’Sullivan, B. T., & Roland, P. E. (1997). Bilateral
activation of fronto-parietal networks by incrementing
demand in a working memory task. Cerebral Cortex, 7,
465–471.
Klingberg, T. & Roland, P. E. (1998). Right prefrontal activation
during encoding, but not during retrieval, in a non-verbal
paired associates task. Cerebral Cortex, 8, 73–79.
Klingberg, T., Roland, P. E., & Kawashima, R. (1996). Activation
of multi-modal cortical areas underlies short-term memory.
European Journal of Neuroscience, 8, 1965–1971.
Klingberg, T., Vaidya, C. J., Gabrieli, J. D. E., Moseley, M. E., &
Hedehus, M. (1999). Myelination and organization of the
frontal white matter in children: A diffusion tensor MRI
study. NeuroReport, 10, 2817–2821.
LaMantia, A. S. & Rakic, P. (1990). Axon overproduction and
elimination in the corpus callosum of the developing rhesus
monkey. Journal of Neuroscience, 10, 2156–2175.
Lambe, E. K., Krimer, L. S., & Goldman-Rakic, P. S. (2000).
Differential postnatal development of catecholamine and
serotonin inputs to identified neurons in prefrontal
cortex of rhesus monkey. Journal of Neuroscience, 20,
8780–8787.
Luciana, M. & Nelson, C. A. (1998). The functional emergence
of prefrontally-guided working memory systems in four- to
eight-year-old children. Neuropsychologia, 36, 273–293.
Luna, B., Thulborn, K. R., Strojwas, M. H., McCurtain, B. J.,
Berman, R. A., Genovese, C. R., & Sweeney, J. A. (1998).
Dorsal cortical regions subserving visually guided saccades in
humans: An fMRI study. Cerebral Cortex, 8, 40–47.
Nelson, C. A., Monk, C. S., Lin, J., Carver, L. J., Thomas, K. M., &
Truwit, C. L. (2000). Functional neuroanatomy of spatial
working memory in children. Developmental Psychology,
36, 109–116.
Klingberg, Forssberg, and Westerberg 9
Paus, T. (1996). Location and function of the frontal eye field.
Neuropsychologia, 34, 47–483.
Paus, T., Zijdenbos, A., Worsley, K., Collins, D. L., Blumenthal,
J., Giedd, J. N., Rapoport, J. L., & Evans, A. C. (1999).
Structural maturation of neural pathways in children and
adolescents: In vivo study. Science, 283, 1908–1911.
Poldrack, R. A. (2000). Imaging brain plasticity: Conceptual and
methodological issues — a theoretical review. Neuroimage,
12, 1–13.
Postle, B. R., Berger, J. S., Taich, A. M., & D’Esposito, M. (2000).
Activity in human frontal cortex associated with spatial
working memory and saccadic behavior. Journal of Cogni-
tive Neuroscience, 12, 2–14.
Postle, B. R. & D’Esposito, M. (1999). ‘‘What-Then-Where’’ in
visual working memory: An event-related fMRI study. Jour-
nal of Cognitive Neuroscience, 11, 585–597.
Quintana, J. & Fuster, J. M. (1993). Spatial and temporal factors
in the role of prefrontal and parietal cortex in visuomotor
integration. Cerebral Cortex, 3, 122–132.
Raichle, M. E., Fiez, J. A., Videen, T. O., MacLeod, A.-M., Pardo,
J. V., Fox, P. T., & Al, E. (1994). Practice-related changes in
human brain functional anatomy during nonmotor learning.
Cerebral Cortex, 4, 8–26.
Reiss, A. L., Abrams, M. T., Singer, H. S., Ross, J. L., & Denckla,
M. B. (1996). Brain development, gender and IQ in children
— a volumetric imaging study. Brain, 119, 1763–1774.
10 Journal of Cognitive Neuroscience
Rowe, J. B., Toni, I., Josephs, O., Frackowiak, R. S., & Passing-
ham, R. E. (2000). The prefrontal cortex: Response selection
or maintenance within working memory? Science, 288,
1656–1660.
Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., & von
Stein, A. (1998). Synchronization between prefrontal and
posterior association cortex during human working memory.
Proceedings of the National Academy of Sciences, U.S.A., 95,
7092–7096.
Smith, E. E., Jonides, J., Koeppe, R. A., Awh, E., Schumacher, E.
H., & Minoshima, S. (1995). Spatial versus object working
memory: PET investigations. Journal of Cognitive Neu-
roscience, 7, 337–356.
Sweeney, J. A., Mintun, M. A., Kwee, S., Wiseman, M. B., Brown,
D. L., Rosenberg, D. R., & Carl, J. R. (1996). Positron emis-
sion tomography study of voluntary saccadic eye movements
and spatial working memory. Journal of Neurophysiology,
75, 454–468.
Thomas, K. M., King, S. W., Franzen, P. L., Welsh, T. F., Ber-
kowitz, A. L., Noll, D. C., Birmaher, V., & Casey, B. J. (1999).
A developmental functional MRI study of spatial working
memory. Neuroimage, 10, 327–338.
Yakovlev, P. I. & Lecours, A.-R. (1967). The myelogenetic cycles
of regional maturation of the brain. In A. Minkowski (Ed.),
Regional development of the brain in early life (pp. 3–65).
Oxford: Blackwell.
Volume 14, Number 1
This article has been cited by:

1. Virve Vuontela, Ping Jiang, Maksym Tokariev, Petri Savolainen, YuanYe Ma, Eeva T. Aronen, Tuija Fontell, Tiina Liiri, Matti
Ahlström, Oili Salonen, Synnöve Carlson. 2013. Regulation of brain activity in the fusiform face and parahippocampal place areas
in 7–11-year-old children. Brain and Cognition 81:2, 203-214. [CrossRef]
2. Eliane C. Miotto, Cary R. Savage, Jonathan J. Evans, Barbara A. Wilson, Maria G.M. Martin, Joana B. Balardin, Fabio G. Barros,
Griselda Garrido, Manoel J. Teixeira, Edson Amaro Junior. 2013. Semantic strategy training increases memory performance and
brain activity in patients with prefrontal cortex lesions. Clinical Neurology and Neurosurgery 115:3, 309-316. [CrossRef]
3. Dietsje D. Jolles, Mark A. van Buchem, Eveline A. Crone, Serge A.R.B. Rombouts. 2013. Functional brain connectivity at rest
changes after working memory training. Human Brain Mapping 34:2, 396-406. [CrossRef]
4. Sarah J. Short, Jed T. Elison, Barbara Davis Goldman, Martin Styner, Hongbin Gu, Mark Connelly, Eric Maltbie, Sandra
Woolson, Weili Lin, Guido Gerig, J. Steven Reznick, John H. Gilmore. 2013. Associations between white matter microstructure
and infants' working memory. NeuroImage 64, 156-166. [CrossRef]
5. Ivan Myatchin, Lieven Lagae. 2012. Developmental changes in visuo-spatial working memory in normally developing children:
Event-related potentials study. Brain and Development . [CrossRef]
6. Myriam C. Sander, Ulman Lindenberger, Markus Werkle-Bergner. 2012. Lifespan age differences in working memory: A two-
component framework. Neuroscience & Biobehavioral Reviews 36:9, 2007-2033. [CrossRef]
7. Russell M. Bauer, Callie Beck DunnResearch Methods in Neuropsychology . [CrossRef]
8. Marinos Kyriakopoulos, Danai Dima, Jonathan P. Roiser, Richard Corrigall, Gareth J. Barker, Sophia Frangou. 2012. Abnormal
Functional Activation and Connectivity in the Working Memory Network in Early-Onset Schizophrenia. Journal of the American
Academy of Child & Adolescent Psychiatry 51:9, 911-920.e2. [CrossRef]
9. Bronwyn Glaser, Amelie Lothe, Mélanie Chabloz, Daniel Dukes, Catherine Pasca, Jérôme Redoute, Stephan Eliez. 2012.
Candidate Socioemotional Remediation Program for Individuals with Intellectual Disability. American Journal on Intellectual and
Developmental Disabilities 117:5, 368-383. [CrossRef]
10. Eveline A. Crone, Ronald E. Dahl. 2012. Understanding adolescence as a period of social–affective engagement and goal flexibility.
Nature Reviews Neuroscience 13:9, 636-650. [CrossRef]
11. Lubin Wang, Hui Shen, Feng Tang, Yufeng Zang, Dewen Hu. 2012. Combined structural and resting-state functional MRI
analysis of sexual dimorphism in the young adult human brain: An MVPA approach. NeuroImage 61:4, 931-940. [CrossRef]
12. T Ziermans, I Dumontheil, C Roggeman, M Peyrard-Janvid, H Matsson, J Kere, T Klingberg. 2012. Working memory brain
activity and capacity link MAOA polymorphism to aggressive behavior during development. Translational Psychiatry 2:2, e85.
[CrossRef]
13. Jacob A. Burack, Tamara Dawkins, Jillian Stewart, Heidi Flores, Grace Iarocci, Natalie Russo“The Mysterious Myth of Attention
Deficit…” Revisited 42, 147-177. [CrossRef]
14. Gerbrich E. van den Bosch, Hanan El Marroun, Marcus N. Schmidt, Dick Tibboel, Dara S. Manoach, Vince D. Calhoun, Tonya
J.H. White. 2012. Brain connectivity during verbal working memory in children and adolescents. Human Brain Mapping n/a-
n/a. [CrossRef]
15. Verena D. Schmittmann, Han L.J. van der Maas, Maartje E.J. Raijmakers. 2011. Distinct discrimination learning strategies
and their relation with spatial memory and attentional control in 4- to 14-year-olds. Journal of Experimental Child Psychology
. [CrossRef]
16. Hikaru Takeuchi, Yasuyuki Taki, Yuko Sassa, Hiroshi Hashizume, Atsushi Sekiguchi, Ai Fukushima, Ryuta Kawashima.
2011. Verbal working memory performance correlates with regional white matter structures in the frontoparietal regions.
Neuropsychologia 49:12, 3466-3473. [CrossRef]
17. Marjolein Spronk, Lisa M. Jonkman. 2011. Electrophysiological evidence for different effects of working memory load on
interference control in adolescents than adults. International Journal of Psychophysiology . [CrossRef]
18. Martin Vestergaard, Kathrine Skak Madsen, William F. C. Baaré, Arnold Skimminge, Lisser Rye Ejersbo, Thomas Z. Ramsøy,
Christian Gerlach, Per Åkeson, Olaf B. Paulson, Terry L. Jernigan. 2011. White Matter Microstructure in Superior Longitudinal
Fasciculus Associated with Spatial Working Memory Performance in Children. Journal of Cognitive Neuroscience 23:9, 2135-2146.
[Abstract] [Full Text] [PDF] [PDF Plus]
19. Leah H. Somerville, Todd Hare, B. J. Casey. 2011. Frontostriatal Maturation Predicts Cognitive Control Failure to Appetitive
Cues in Adolescents. Journal of Cognitive Neuroscience 23:9, 2123-2134. [Abstract] [Full Text] [PDF] [PDF Plus]
20. M.J. Taylor, E.J. Donner, E.W. Pang. 2011. fMRI and MEG in the study of typical and atypical cognitive development.
Neurophysiologie Clinique/Clinical Neurophysiology . [CrossRef]
21. Dražen Domijan. 2011. A computational model of fMRI activity in the intraparietal sulcus that supports visual working memory.
Cognitive, Affective, & Behavioral Neuroscience . [CrossRef]
22. Tessa Dekker, Denis Mareschal, Martin I. Sereno, Mark H. Johnson. 2011. Dorsal and ventral stream activation and object
recognition performance in school-age children. NeuroImage 57:3, 659-670. [CrossRef]
23. I. Dumontheil, T. Klingberg. 2011. Brain Activity during a Visuospatial Working Memory Task Predicts Arithmetical Performance
2 Years Later. Cerebral Cortex . [CrossRef]
24. Yvonne Brehmer, Anna Rieckmann, Martin Bellander, Helena Westerberg, Håkan Fischer, Lars Bäckman. 2011. Neural correlates
of training-related working-memory gains in old age. NeuroImage . [CrossRef]
25. Thomas E. Gladwin, Bernd Figner, Eveline A. Crone, Reinout W. Wiers. 2011. Addiction, adolescence, and the integration of
control and motivation. Developmental Cognitive Neuroscience . [CrossRef]
26. Joshua Carp, Kate Dimond Fitzgerald, Stephan F. Taylor, Daniel H. Weissman. 2011. Removing the effect of response time
on brain activity reveals developmental differences in conflict processing in the posterior medial prefrontal cortex. NeuroImage
. [CrossRef]
27. Maree J. Webster, Michael Elashoff, Cynthia Shannon Weickert. 2011. Molecular evidence that cortical synaptic growth
predominates during the first decade of life in humans. International Journal of Developmental Neuroscience 29:3, 225-236.
[CrossRef]
28. Duncan E. Astle, Gaia Scerif. 2011. Interactions between attention and visual short-term memory (VSTM): What can be learnt
from individual and developmental differences?. Neuropsychologia 49:6, 1435-1445. [CrossRef]
29. Soohyun Cho, Srikanth Ryali, David C. Geary, Vinod Menon. 2011. How does a child solve 7 + 8? Decoding brain activity
patterns associated with counting and retrieval strategies. Developmental Science no-no. [CrossRef]
30. B. J. Casey, Rebecca M. Jones, Leah H. Somerville. 2011. Braking and Accelerating of the Adolescent Brain. Journal of Research
on Adolescence 21:1, 21-33. [CrossRef]
31. Tonya White, Donaya Hongwanishkul, Marcus Schmidt. 2011. Increased anterior cingulate and temporal lobe activity during
visuospatial working memory in children and adolescents with schizophrenia. Schizophrenia Research 125:2-3, 118-128. [CrossRef]
32. Paul Bangirana, Peter Allebeck, Michael J Boivin, Chandy C John, Connie Page, Anna Ehnvall, Seggane Musisi. 2011. Cognition,
behaviour and academic skills after cognitive rehabilitation in Ugandan children surviving severe malaria: a randomised trial. BMC
Neurology 11:1, 96. [CrossRef]
33. Nadia Gaoua, Sebastein Racinais, Justin Grantham, Farid El Massioui. 2010. Alterations in cognitive performance during passive
hyperthermia are task dependent. International Journal of Hyperthermia 1-9. [CrossRef]
34. Ian D. Holloway, Daniel Ansari. 2010. Developmental Specialization in the Right Intraparietal Sulcus for the Abstract
Representation of Numerical Magnitude. Journal of Cognitive Neuroscience 22:11, 2627-2637. [Abstract] [Full Text] [PDF] [PDF
Plus]
35. John R. Best, Patricia H. Miller. 2010. A Developmental Perspective on Executive Function. Child Development 81:6, 1641-1660.
[CrossRef]
36. Melanie Stollstorff, Jennifer Foss-Feig, Edwin H. Cook, Mark A. Stein, William D. Gaillard, Chandan J. Vaidya. 2010. Neural
response to working memory load varies by dopamine transporter genotype in children. NeuroImage 53:3, 970-977. [CrossRef]
37. Dietsje D. Jolles, Sietske W. Kleibeuker, Serge A.R.B. Rombouts, Eveline A. Crone. 2010. Developmental differences in prefrontal
activation during working memory maintenance and manipulation for different memory loads. Developmental Science no-no.
[CrossRef]
38. Martin Mrazik, Stefan Dombrowski. 2010. The Neurobiological Foundations of Giftedness. Roeper Review 32:4, 224-234.
[CrossRef]
39. Shefali B. Brahmbhatt, Desirée A. White, Deanna M. Barch. 2010. Developmental differences in sustained and transient activity
underlying working memory. Brain Research 1354, 140-151. [CrossRef]
40. Philip David Zelazo, Wendy S. C. LeeBrain Development . [CrossRef]
41. Tom A. de Graaf, Alard Roebroeck, Rainer Goebel, Alexander T. Sack. 2010. Brain Network Dynamics Underlying Visuospatial
Judgment: An fMRI Connectivity Study. Journal of Cognitive Neuroscience 22:9, 2012-2026. [Abstract] [Full Text] [PDF] [PDF
Plus]
42. Alecia Dager Schweinsburg, Brian C. Schweinsburg, Krista Lisdahl Medina, Tim McQueeny, Sandra A. Brown, Susan F. Tapert.
2010. The Influence of Recency of Use on fMRI Response During Spatial Working Memory in Adolescent Marijuana Users.
Journal of Psychoactive Drugs 42:3, 401-412. [CrossRef]
43. Wolfgang SchneiderMemory Development in Childhood 347-376. [CrossRef]
44. Torkel Klingberg. 2010. Training and plasticity of working memory. Trends in Cognitive Sciences 14:7, 317-324. [CrossRef]
45. Adriana Galván. 2010. Neural plasticity of development and learning. Human Brain Mapping 31:6, 879-890. [CrossRef]
46. Katya Rubia, Zoe Hyde, Rozmin Halari, Vincent Giampietro, Anna Smith. 2010. Effects of age and sex on developmental neural
networks of visual–spatial attention allocation. NeuroImage 51:2, 817-827. [CrossRef]
47. Prasanna Karunanayaka, Vincent J. Schmithorst, Jennifer Vannest, Jerzy P. Szaflarski, Elena Plante, Scott K. Holland. 2010. A
group independent component analysis of covert verb generation in children: A functional magnetic resonance imaging study.
NeuroImage 51:1, 472-487. [CrossRef]
48. Kirsten O’Hearn, James E. Hoffman, Barbara Landau. 2010. Developmental profiles for multiple object tracking and spatial
memory: typically developing preschoolers and people with Williams syndrome. Developmental Science 13:3, 430-440. [CrossRef]
49. A. Jucaite, H. Forssberg, P. Karlsson, C. Halldin, L. Farde. 2010. Age-related reduction in dopamine D1 receptors in the human
brain: from late childhood to adulthood, a positron emission tomography study. Neuroscience 167:1, 104-110. [CrossRef]
50. Iroise Dumontheil, Sam J. Gilbert, Paul W. Burgess, Leun J. Otten. 2010. Neural correlates of task and source switching: Similar
or different?. Biological Psychology 83:3, 239-249. [CrossRef]
51. Beatriz Luna, Aarthi Padmanabhan, Kirsten O’Hearn. 2010. What has fMRI told us about the Development of Cognitive Control
through Adolescence?. Brain and Cognition 72:1, 101-113. [CrossRef]
52. Sunita Bava, Rebecca J. Theilmann, Miriam Sach, Susanne J. May, Lawrence R. Frank, John R. Hesselink, Duc Vu, Doris A.
Trauner. 2010. Developmental changes in cerebral white matter microstructure in a disorder of lysosomal storage. Cortex 46:2,
206-216. [CrossRef]
53. Gregory Z Tau, Bradley S Peterson. 2010. Normal Development of Brain Circuits. Neuropsychopharmacology 35:1, 147-168.
[CrossRef]
54. Joni Holmes, Susan E. Gathercole, Darren L. DunningPoor working memory 39, 1-43. [CrossRef]
55. Andrea D. Spadoni, Alissa D. Bazinet, Susanna L. Fryer, Susan F. Tapert, Sarah N. Mattson, Edward P. Riley. 2009.
BOLD Response During Spatial Working Memory in Youth With Heavy Prenatal Alcohol Exposure. Alcoholism: Clinical and
Experimental Research 33:12, 2067-2076. [CrossRef]
56. Lars Bäckman, Sari Karlsson, Håkan Fischer, Per Karlsson, Yvonne Brehmer, Anna Rieckmann, Stuart W.S. MacDonald, Lars
Farde, Lars Nyberg. 2009. Dopamine D1 receptors and age differences in brain activation during working memory. Neurobiology
of Aging . [CrossRef]
57. T. G. Beteleva, S. V. Sinitsyn, D. A. Farber. 2009. Age-related specificity of the processing of visual information in the system
of working memory. Human Physiology 35:6, 672-683. [CrossRef]
58. S. Rotzer, T. Loenneker, K. Kucian, E. Martin, P. Klaver, M. von Aster. 2009. Dysfunctional neural network of spatial working
memory contributes to developmental dyscalculia. Neuropsychologia 47:13, 2859-2865. [CrossRef]
59. John R. Best, Patricia H. Miller, Lara L. Jones. 2009. Executive functions after age 5: Changes and correlates. Developmental
Review 29:3, 180-200. [CrossRef]
60. Paul Bangirana, Bruno Giordani, Chandy C. John, Connie Page, Robert O. Opoka, Michael J. Boivin. 2009. Immediate
Neuropsychological and Behavioral Benefits of Computerized Cognitive Rehabilitation in Ugandan Pediatric Cerebral Malaria
Survivors. Journal of Developmental & Behavioral Pediatrics 30:4, 310-318. [CrossRef]
61. Michael C. Stevens. 2009. The developmental cognitive neuroscience of functional connectivity. Brain and Cognition 70:1, 1-12.
[CrossRef]
62. L. Mandolesi, F. Addona, F. Foti, D. Menghini, L. Petrosini, S. Vicari. 2009. Spatial competences in Williams syndrome: a radial
arm maze study. International Journal of Developmental Neuroscience 27:3, 205-213. [CrossRef]
63. Rayna Azuma, Eileen M. Daly, Linda E. Campbell, Angela F. Stevens, Quinton Deeley, Vincent Giampietro, Michael J. Brammer,
Beate Glaser, Fiona Z. Ambery, Robin G. Morris, Steven C. R. Williams, Michael J. Owen, Declan G. M. Murphy, Kieran
C. Murphy. 2009. Visuospatial working memory in children and adolescents with 22q11.2 deletion syndrome; an fMRI study.
Journal of Neurodevelopmental Disorders 1:1, 46-60. [CrossRef]
64. Moriah E. Thomason, Elizabeth Race, Brittany Burrows, Susan Whitfield-Gabrieli, Gary H. Glover, John D. E. Gabrieli. 2009.
Development of Spatial and Verbal Working Memory Capacity in the Human Brain. Journal of Cognitive Neuroscience 21:2,
316-332. [Abstract] [Full Text] [PDF] [PDF Plus]
65. LARS NYBERG, ERIKA DAHLIN, ANNA STIGSDOTTER NEELY, LARS BÄCKMAN. 2009. Neural correlates of variable
working memory load across adult age and skill: Dissociative patterns within the fronto-parietal network. Scandinavian Journal
of Psychology 50:1, 41-46. [CrossRef]
66. Virve Vuontela, Maija-Riikka Steenari, Eeva T. Aronen, Antti Korvenoja, Hannu J. Aronen, Synnöve Carlson. 2009. Brain
activation and deactivation during location and color working memory tasks in 11–13-year-old children. Brain and Cognition
69:1, 56-64. [CrossRef]
67. Paul J. Eslinger, Clancy Blair, JianLi Wang, Bryn Lipovsky, Jennifer Realmuto, David Baker, Steven Thorne, David Gamson,
Erin Zimmerman, Lisa Rohrer. 2009. Developmental shifts in fMRI activations during visuospatial relational reasoning. Brain
and Cognition 69:1, 1-10. [CrossRef]
68. Andria L. Norman, Nicole Crocker, Sarah N. Mattson, Edward P. Riley. 2009. Neuroimaging and fetal alcohol spectrum disorders.
Developmental Disabilities Research Reviews 15:3, 209-217. [CrossRef]
69. Timo Mantyla, Martin Karlsson, Markus Marklund. 2009. Executive Control Functions in Simulated Driving. Applied
Neuropsychology 16:1, 11-18. [CrossRef]
70. Eveline A. Crone, Carter Wendelken, Linda van Leijenhorst, Ryan D. Honomichl, Kalina Christoff, Silvia A. Bunge. 2009.
Neurocognitive development of relational reasoning. Developmental Science 12:1, 55-66. [CrossRef]
71. Beatriz LunaDevelopmental Changes in Cognitive Control through Adolescence 37, 233-278. [CrossRef]
72. B LUNA, K VELANOVA, C GEIER. 2008. Development of eye-movement control. Brain and Cognition 68:3, 293-308.
[CrossRef]
73. Elizabeth D. O'Hare, Lisa H. Lu, Suzanne M. Houston, Susan Y. Bookheimer, Elizabeth R. Sowell. 2008. Neurodevelopmental
changes in verbal working memory load-dependency: An fMRI investigation. NeuroImage 42:4, 1678-1685. [CrossRef]
74. Kirsten O'Hearn, Miya Asato, Sarah Ordaz, Beatriz Luna. 2008. Neurodevelopment and executive function in autism. Development
and Psychopathology 20:04, 1103. [CrossRef]
75. Karin Kucian, Michael von Aster, Thomas Loenneker, Thomas Dietrich, Ernst Martin. 2008. Development of Neural Networks
for Exact and Approximate Calculation: A fMRI Study. Developmental Neuropsychology 33:4, 447-473. [CrossRef]
76. Moriah E. Thomason, Catherine E. Chang, Gary H. Glover, John D.E. Gabrieli, Michael D. Greicius, Ian H. Gotlib. 2008.
Default-mode function and task-induced deactivation have overlapping brain substrates in children. NeuroImage 41:4, 1493-1503.
[CrossRef]
77. Monica Rosselli, Alfredo Ardila, Esmeralda Matute, Olga Inozemtseva. 2008. Gender Differences and Cognitive Correlates of
Mathematical Skills in School-Aged Children. Child Neuropsychology 15:3, 216-231. [CrossRef]
78. E. A. CRONE, K. ZANOLIE, L. VAN LEIJENHORST, M. P. WESTENBERG, S. A. R. B. ROMBOUTS. 2008. Neural
mechanisms supporting flexible performance adjustment during development. Cognitive, Affective, & Behavioral Neuroscience 8:2,
165-177. [CrossRef]
79. Monique Ernst, Sven C. Mueller. 2008. The adolescent brain: Insights from functional neuroimaging research. Developmental
Neurobiology 68:6, 729-743. [CrossRef]
80. Iroise Dumontheil, Paul W Burgess, Sarah-Jayne Blakemore. 2008. Development of rostral prefrontal cortex and cognitive and
behavioural disorders. Developmental Medicine & Child Neurology 50:3, 168-181. [CrossRef]
81. Daniela PeraniChapter 4 Functional neuroimaging of cognition 88, 61-111. [CrossRef]
82. Kevin M. Antshel, Wanda Fremont, Wendy R. Kates. 2008. The neurocognitive phenotype in velo-cardio-facial syndrome: A
developmental perspective. Developmental Disabilities Research Reviews 14:1, 43-51. [CrossRef]
83. Shefali B. Brahmbhatt, Tara McAuley, Deanna M. Barch. 2008. Functional developmental similarities and differences in the neural
correlates of verbal and nonverbal working memory tasks. Neuropsychologia 46:4, 1020-1031. [CrossRef]
84. Hannah A.D. Keage, Christopher R. Clark, Daniel F. Hermens, Leanne M. Williams, Michael R. Kohn, Simon Clarke,
Christopher Lamb, David Crewther, Evian Gordon. 2008. Putative biomarker of working memory systems development during
childhood and adolescence. NeuroReport 19:2, 197-201. [CrossRef]
85. FREDRIK EDIN, TORKEL KLINGBERG, TOMMY STÖDBERG, JESPER TEGNÉR. 2007. FRONTO-PARIETAL
CONNECTION ASYMMETRY REGULATES WORKING MEMORY DISTRACTIBILITY. Journal of Integrative
Neuroscience 06:04, 567-596. [CrossRef]
86. L. Visu-Petra, O. Benga, I. Ţincaş, M. Miclea. 2007. Visual-spatial processing in children and adolescents with Down's syndrome:
a computerized assessment of memory skills. Journal of Intellectual Disability Research 51:12, 942-952. [CrossRef]
 87. Philip S. Lee, Jennifer Foss-Feig, Joshua G. Henderson, Lauren E. Kenworthy, Lisa Gilotty, William D. Gaillard, Chandan J.
Vaidya. 2007. Atypical neural substrates of Embedded Figures Task performance in children with Autism Spectrum Disorder.
NeuroImage 38:1, 184-193. [CrossRef]
88. H WESTERBERG, T KLINGBERG. 2007. Changes in cortical activity after training of working memory — a single-subject
analysis. Physiology & Behavior 92:1-2, 186-192. [CrossRef]
89. Kimberly G. Noble, Bruce D. McCandliss, Martha J. Farah. 2007. Socioeconomic gradients predict individual differences in
neurocognitive abilities. Developmental Science 10:4, 464-480. [CrossRef]
90. Charles A. Nelson, Kathleen M. Thomas, Michelle de HaanNeural Bases of Cognitive Development . [CrossRef]
91. K. Kucian, M. von Aster, T. Loenneker, T. Dietrich, F. W. Mast, E. Martin. 2007. Brain activation during mental rotation in
school children and adults. Journal of Neural Transmission 114:5, 675-686. [CrossRef]
92. Fredrik Edin, Julian Macoveanu, Pernille Olesen, Jesper Tegnér, Torkel Klingberg. 2007. Stronger Synaptic Connectivity as a
Mechanism behind Development of Working Memory-related Brain Activity during Childhood. Journal of Cognitive Neuroscience
19:5, 750-760. [Abstract] [PDF] [PDF Plus]
93. Greg S. Harrington, Dana Farias, Christine H. Davis, Michael H. Buonocore. 2007. Comparison of the neural basis for imagined
writing and drawing. Human Brain Mapping 28:5, 450-459. [CrossRef]
94. Pasl A. Jalil. 2007. Working Memory, Cerebellum, and Creativity. Creativity Research Journal 19:1, 39-45. [CrossRef]
95. D YURGELUNTODD. 2007. Emotional and cognitive changes during adolescence. Current Opinion in Neurobiology 17:2,
251-257. [CrossRef]
96. S BUNGE, S WRIGHT. 2007. Neurodevelopmental changes in working memory and cognitive control. Current Opinion in
Neurobiology 17:2, 243-250. [CrossRef]
97. Mariëtte Huizinga, Maurits W. van der Molen. 2007. Age-Group Differences in Set-Switching and Set-Maintenance on the
Wisconsin Card Sorting Task. Developmental Neuropsychology 31:2, 193-215. [CrossRef]
98. A.M. Passarotti, J. Smith, M. DeLano, J. Huang. 2007. Developmental differences in the neural bases of the face inversion effect
show progressive tuning of face-selective regions to the upright orientation. NeuroImage 34:4, 1708-1722. [CrossRef]
99. Tara McAuley, Shefali Brahmbhatt, Deanna M. Barch. 2007. Performance on an episodic encoding task yields further insight
into functional brain development. NeuroImage 34:2, 815-826. [CrossRef]
100. Martha Ann Bell, Christy D. Wolfe. 2007. Changes in Brain Functioning From Infancy to Early Childhood: Evidence From EEG
Power and Coherence Working Memory Tasks. Developmental Neuropsychology 31:1, 21-38. [CrossRef]
101. R EENSHUISTRA, K RICHARDRIDDERINKHOF, M WEIDEMA, M VANDERMOLEN. 2007. Developmental changes
in oculomotor control and working-memory efficiency. Acta Psychologica 124:1, 139-158. [CrossRef]
102. Wendy R. Kates, Beth R. Krauss, Nuria AbdulSabur, Deirdre Colgan, Kevin M. Antshel, Anne Marie Higgins, Robert J.
Shprintzen. 2007. The neural correlates of non-spatial working memory in velocardiofacial syndrome (22q11.2 deletion syndrome).
Neuropsychologia 45:12, 2863-2873. [CrossRef]
103. Rodney M.J. CotterillAn Inside-Out Paradigm for Consciousness and Intelligence 177-191. [CrossRef]
104. Katya Rubia, Anna B. Smith, James Woolley, Chiara Nosarti, Isobel Heyman, Eric Taylor, Mick Brammer. 2006. Progressive
increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human
Brain Mapping 27:12, 973-993. [CrossRef]
105. K CIESIELSKI, P LESNIK, R SAVOY, E GRANT, S AHLFORS. 2006. Developmental neural networks in children performing
a Categorical N-Back Task. NeuroImage 33:3, 980-990. [CrossRef]
106. E CRONE, R SOMSEN, K ZANOLIE, M VANDERMOLEN. 2006. A heart rate analysis of developmental change in feedback
processing and rule shifting from childhood to early adulthood. Journal of Experimental Child Psychology 95:2, 99-116. [CrossRef]
107. A DOWKER. 2006. What can functional brain imaging studies tell us about typical and atypical cognitive development in
children?. Journal of Physiology-Paris 99:4-6, 333-341. [CrossRef]
108. Eleni Kotsoni, Dana Byrd, B.J. Casey. 2006. Special considerations for functional magnetic resonance imaging of pediatric
populations. Journal of Magnetic Resonance Imaging 23:6, 877-886. [CrossRef]
109. Robert V. Mulkern, Peter E. Davis, Steven J. Haker, Raul San Jose Estepar, Lawrence P. Panych, Stephan E. Maier, Michael
J. Rivkin. 2006. Complementary aspects of diffusion imaging and fMRI; I: structure and function. Magnetic Resonance Imaging
24:4, 463-474. [CrossRef]
110. Jerzy P. Szaflarski, Vincent J. Schmithorst, Mekibib Altaye, Anna W. Byars, Jennifer Ret, Elena Plante, Scott K. Holland. 2006.
A longitudinal functional magnetic resonance imaging study of language development in children 5 to 11 years old. Annals of
Neurology 59:5, 796-807. [CrossRef]
111. Madison M. Berl, Chandan J. Vaidya, William Davis Gaillard. 2006. Functional imaging of developmental and adaptive changes
in neurocognition☆. NeuroImage 30:3, 679-691. [CrossRef]
112. Rudi Črnčec, Sarah J. Wilson, Margot Prior. 2006. No Evidence for the Mozart Effect in Children. Music Perception 23:4, 305-318.
[CrossRef]
113. W. John Curtis, Jiancheng Zhuang, Elise Townsend, Xiaoping Hu, Charles Nelson. 2006. Memory in Early Adolescents Born
Prematurely: A Functional Magnetic Resonance Imaging Investigation. Developmental Neuropsychology 29:2, 341-377. [CrossRef]
114. Eliane C. Miotto, Cary R. Savage, Jonathan J. Evans, Barbara A. Wilson, M.G.M. Martins, Suzan Iaki, Edson Amaro. 2006.
Bilateral activation of the prefrontal cortex after strategic semantic cognitive training. Human Brain Mapping 27:4, 288-295.
[CrossRef]
115. Dennis P. Carmody, Margaret Bendersky, Stanley M. Dunn, J. Kevin DeMarco, Thomas Hegyi, Mark Hiatt, Michael Lewis.
2006. Early Risk, Attention, and Brain Activation in Adolescents Born Preterm. Child Development 77:2, 384-394. [CrossRef]
116. A SMITH, P FRIED, M HOGAN, I CAMERON. 2006. Effects of prenatal marijuana on visuospatial working memory: An
fMRI study in young adults. Neurotoxicology and Teratology 28:2, 286-295. [CrossRef]
117. E. Darcy Burgund, Heather M. Lugar, Francis M. Miezin, Bradley L. Schlaggar, Steven E. Petersen. 2006. The development of
sustained and transient neural activity. NeuroImage 29:3, 812-821. [CrossRef]
118. Kun Ho Lee, Yu Yong Choi, Jeremy R. Gray, Sun Hee Cho, Jeong-Ho Chae, Seungheun Lee, Kyungjin Kim. 2006. Neural
correlates of superior intelligence: Stronger recruitment of posterior parietal cortex. NeuroImage 29:2, 578-586. [CrossRef]
119. J. Macoveanu, T. Klingberg, J. Tegnér. 2006. A biophysical model of multiple-item working memory: A computational and
neuroimaging study. Neuroscience 141:3, 1611-1618. [CrossRef]
120. John Colombo, Carol L. CheathamThe emergence and basis of endogenous attention in infancy and early childhood 34, 283-322.
[CrossRef]
121. Bonnie Nagel, Valerie Barlett, Alecia Schweinsburg, Susan Tapert. 2005. Neuropsychological Predictors of BOLD Response
During a Spatial Working Memory Task in Adolescents: What Can Performance Tell Us About fMRI Response Patterns?. Journal
of Clinical and Experimental Neuropsychology 27:7, 823-839. [CrossRef]
122. Scott Slotnick. 2005. Spatial working memory specific activity in dorsal prefrontal cortex? Disparate answers from fMRI beta-
weight and timecourse analysis. Cognitive Neuropsychology 22:7, 905-920. [CrossRef]
123. ALECIA D. SCHWEINSBURG, BONNIE J. NAGEL, SUSAN F. TAPERT. 2005. fMRI reveals alteration of spatial working
memory networks across adolescence. Journal of the International Neuropsychological Society 11:05. . [CrossRef]
124. Monica Luciana, Heather M. Conklin, Catalina J. Hooper, Rebecca S. Yarger. 2005. The Development of Nonverbal Working
Memory and Executive Control Processes in Adolescents. Child Development 76:3, 697-712. [CrossRef]
125. M THOMASON, B BURROWS, J GABRIELI, G GLOVER. 2005. Breath holding reveals differences in fMRI BOLD signal
in children and adults. NeuroImage 25:3, 824-837. [CrossRef]
126. BJ Casey, Adriana Galvan, Todd A Hare. 2005. Changes in cerebral functional organization during cognitive development. Current
Opinion in Neurobiology 15:2, 239-244. [CrossRef]
127. E BIRMINGHAM, J PRATT. 2005. Examining inhibition of return with onset and offset cues in the multiple-cuing paradigm.
Acta Psychologica 118:1-2, 101-121. [CrossRef]
128. Torkel Klingberg, Elisabeth Fernell, Pernille J. Olesen, Mats Johnson, Per Gustafsson, Kerstin Dahlström, Christopher G.
Gillberg, Hans Forssberg, Helena Westerberg. 2005. Computerized Training of Working Memory in Children With ADHD-A
Randomized, Controlled Trial. Journal of the American Academy of Child & Adolescent Psychiatry 44:2, 177-186. [CrossRef]
129. M SCHROETER, S ZYSSET, M WAHL, D VONCRAMON. 2004. Prefrontal activation due to Stroop interference increases
during development?an event-related fNIRS study. NeuroImage 23:4, 1317-1325. [CrossRef]
130. James R. Booth, Douglas D. Burman, Joel R. Meyer, Barbara L. Trommer, Nicholas D. Davenport, Todd B. Parrish, Darren
R. Gitelman, M. Marsel Mesulam. 2004. Brain-behavior correlation in children depends on the neurocognitive network. Human
Brain Mapping 23:2, 99-108. [CrossRef]
131. Victor A. F. Lamme. 2004. Weg met de psychologie!. Netherlands journal of psychology 59:4, 90-100. [CrossRef]
132. Eveline Crone, Maurits van der Molen. 2004. Developmental Changes in Real Life Decision Making: Performance on a
Gambling Task Previously Shown to Depend on the Ventromedial Prefrontal Cortex. Developmental Neuropsychology 25:3, 251-279.
[CrossRef]
133. Kevin A Pelphrey, J Steven ReznickWorking Memory in Infancy 31, 173-227. [CrossRef]
134. Christopher Gillberg. 2003. ADHD and DAMP: A General Health Perspective. Child and Adolescent Mental Health 8:3, 106-113.
[CrossRef]
135. H Kang. 2003. Comparison of functional activation foci in children and adults using a common stereotactic space. NeuroImage
. [CrossRef]
136. Alessandra M. Passarotti, Brianna M. Paul, Joseph R. Bussiere, Richard B. Buxton, Eric C. Wong, Joan Stiles. 2003. The
development of face and location processing: an fMRI study. Developmental Science 6:1, 100-117. [CrossRef]
137. Sarah Durston, Kathleen M. Thomas, Yihong Yang, Aziz M. Ulug, Robert D. Zimmerman, B.J. Casey. 2002. A neural basis for
the development of inhibitory control. Developmental Science 5:4, F9-F16. [CrossRef]
138. B.J. Casey, Matthew Davidson, Bruce Rosen. 2002. Functional magnetic resonance imaging: basic principles of and application
to developmental science. Developmental Science 5:3, 301-309. [CrossRef]