Functional Role of the Basal Ganglia in the

Planning and Execution of Actions

Oury Monchi, PhD,1,2 Michael Petrides, PhD,3 Antonio P. Strafella, MD, PhD,3 Keith J. Worsley, PhD,3
and Julien Doyon, PhD1,3,4

Objective: Recent studies of functional brain imaging have shown the involvement of the basal ganglia in executive
processes such as planning and set-shifting. However, the specific contributions of the striatum in those processes remain
unknown. This study aimed to test the hypothesis that the caudate nucleus is primarily involved in the preparation of
a novel action and not in set-shifting per se. Methods: In the present event-related functional magnetic resonance imaging
(fMRI) study, a new task was developed that permitted, for the first time, to distinguish between shifts in classification
when the rule is implicitly given by the task from shifts that require cognitive comparison and planning. Results: Significantly increased activity in the caudate nucleus and the putamen was observed only in conditions in which cognitive
planning was required to perform a set-shift, whereas significant activation was seen in the subthalamic nucleus (another
region of the basal ganglia) in all shifting conditions whether or not planning was required. Interpretation: We suggest
that the caudate nucleus and the putamen are particularly important, respectively, in the planning and the execution of
a self-generated novel action, whereas the subthalamic nucleus may be required when a new motor program is solicited
independently of the choice of strategy.
Ann Neurol 2006;59:257264

Abnormalities of the basal ganglia (BG) have been described in many neurological disorders such as Parkinsons disease, and thus it is important to gain a greater
understanding of the functional role of the different
nuclei of the BG in the healthy brain in order to reveal
the neural origins of the cognitive and motor deficits
observed in those disorders. Traditionally thought to
be associated with the control of movement13 and
motor learning,4,5 BG has been shown by neuropsychological studies in patients with Parkinsons and
Huntingtons disease to contribute to a variety of executive functions, including planning and set-shifting
(ie, the ability to alter our mode of response in the face
of changing circumstances).6 9 Among the different
BG nuclei, the caudate nucleus has been shown to play
a greater role in executive processes,10 14 whereas other
structures such as the putamen and subthalamic nucleus have traditionally been associated with more
motor-related activities. However, there is evidence
that the role of the putamen may not be directly linked
to the movement itself, but rather to the condition under which it is made,15 whereas the subthalamic nucleus may exert a specific influence on the BG output
related to the control of movement.3,16,17 Hence,

whereas the evidence accumulated to date suggests that

the various nuclei of the BG may have different functional roles, their distinct contribution to the planning
and execution of action remains unknown.
Recently, functional magnetic resonance imaging
(fMRI) has been used routinely to investigate the neural substrates of various cognitive functions in normal
subjects as well as patients with neurological or psychiatric disorders. In the earlier fMRI studies, it was difficult to make fine distinctions in cognitive processing
and to distinguish between small neural structures, especially subcortical ones. However, recent methodological advances both in the type of acquisition sequences
and in data analysis has made it possible to study the
involvement of subcortical structures, such as the different parts of the BG, in specific cognitive conditions.
In a previous event-related fMRI study of the Wisconsin Card-Sorting Task in young healthy adults,12 we
observed significant activation in the caudate nucleus
specifically when subjects received negative feedback
(ie, when a set-shift was required). While the involvement of the caudate nucleus in set-shifting has also
been confirmed in other neuroimaging studies,11,13
there is still no evidence up to now of whether the

From the 1Functional Neuroimaging Unit, Institut Universitaire de

Geriatrie de Montreal; 2Department of Radiology, University of
Montreal; 3Montreal Neurological Institute, McGill University; and
4
Department of Psychology, University of Montreal, Montreal,
Quebec, Canada.

Published online Jan 23, 2006 in Wiley InterScience

(www.interscience.wiley.com). DOI: 10.1002/ana.20742

Received Jul 15, 2005, and in revised form Aug 30. Accepted for
publication Oct 7, 2005.

Address correspondence to Dr Monchi, Centre de Recherhe, Institut Universitaire de Geriatrie de Montreal, 4565, Queen Mary
Road, Montreal (Quebec) H3W 1W5, Canada.
E-mail: oury.monchi@umontreal.ca or oury@bic.mni.mcgill.ca

2006 American Neurological Association

Published by Wiley-Liss, Inc., through Wiley Subscription Services

257

caudate nucleus is most important for the execution of

the shift per se or rather for its planning (ie, the cognitive decision to shift). Here, a new card-sorting task
was developed called the Montreal Card-Sorting Task
that allowed us to dissociate between these two aspects
of set-shifting. Using fMRI in young healthy adults, we
tested the hypothesis that the caudate nucleus is primarily involved in the preparation of a novel action
and not in the execution of set-shifting per se. A
mixed-design protocol was used in which trials occurred within blocks but were reconstructed and analyzed in an event-related manner.
Subjects and Methods
Subjects
Ten right-handed healthy subjects (mean age, 23.4 years;
range, 18 31; five males, five females) participated in this
study. Subjects had no previous personal or family history of
neurological or psychiatric disorders and were not taking any
prescribed medication at the time of scanning. Handedness
was assessed by the Edinburgh Handedness Inventory.18 All
subjects gave informed consent to the protocol, which was
reviewed and approved by the Research and Ethics Committees of the Montreal Neurological Institute.

Cognitive Task
Fig 1. The different conditions of the Montreal Card-Sorting
Task. (A) An example of the cue card that appears for 3.5 seconds at the beginning of a block of retrieval trials. In this example, the cue card contains two red circles. (B) An example of two
consecutive retrieval trials without shift. Because the color red is
the only attribute shared by the test card and the cue on both
trials, matching must be based on color. Note that the location of
the response on subsequent trials is the same, resulting in the same
finger being used to perform the matching response. In this and
the other examples (C, D, E), the orange line under one of the
reference cards indicates the selected response. (C) An example of
two consecutive retrieval trials with shift. Left: the test card contains four red stars and hence shares the color attribute with the
cue card (containing two red circles, shown in A). Right: on the
subsequent trial, the test card now shares a different attribute
with the cue card (in this example number). Thus, a shift in
classification category occurs requiring a novel response. Note also
that, in this condition, the location of the response necessarily
changes and a different finger has to be used. (D) An example of
two consecutive trials in the continuous shift condition. Left: the
only reference card that shares an attribute with the test card is
the second one, and therefore the second reference card has to be
selected according to color. Right: in the subsequent trial, a test
card containing one pink square is shown. The first reference card
must now be selected because it is the only one that shares an
attribute with the test card (number), and therefore a shift in
classification occurs. Thus, in this condition, a continuous shift
occurs guided implicitly by the only shared attribute between the
test card and one of the reference cards. Note that the location of
the response is always changing and therefore requires the use of a
different finger. (E) An example of a control trial. The test card
always matches exactly one of the reference cards and the subject
simply must select the twin reference card.

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In the Montreal Card-Sorting Task used here, four reference

cards were on display in a row at the top of a computer
screen in all trials. These reference cards displayed one red
triangle, two green stars, three yellow crosses, and four blue
circles, respectively (Fig 1). On each classification trial, a new
test card was presented in the middle of the screen below the
reference cards, and the subject had to match the test card to
one of the four reference cards. This was done by pressing
one of four buttons with the right hand, using one of four
fingers, each one corresponding to one of the reference cards.
The match of each test card to one of the reference cards was
determined by a classification rule that differed across experimental conditions. On each trial, as soon as the subject responded, a period of 2.3 seconds followed when the screen
became bright if the response was correct and dark if the
response was incorrect. This period only served as feedback
and was not useful for the correct execution of the subsequent trial. No incentives (financial reward or other) were
provided or suggested to the subjects for the accuracy of their
performance. The duration of each trial varied according to
the subjects reaction time during the matching, hence providing the asynchrony between stimulus presentation and
frame acquisition required for event-related acquisition.
There were four different experimental conditions in this experiment: (1) retrieval without shift; (2) retrieval with shift;
(3) continuous shift; and (4) control. Trials in the continuous
shift and the control conditions occurred in different blocks
presented in a random order. The retrieval without shift and
retrieval with shift trials were interleaved within the same
blocks.
In the retrieval blocks (see Fig 1AC), a series of classification trials were preceded by the brief presentation of a single cue card containing one to four objects that consisted of

one of four shapes in one of four possible colors for a period

of 3.5 seconds (see Fig 1A). This was then followed by a
blank period of 3.5 seconds. The cue card did not reappear
and had to be remembered throughout the series of classification trials. On every trial, a new test card that shared a
single attribute (color, shape, or number) with the cue card
held in memory was presented underneath the reference
cards (see Fig 1B, C). The subject had to select one of the
four reference cards based on this attribute. For instance, if
the test card and the cue card shared the color red (as in the
example shown in Fig 1B), a match to the reference card
that has red in it was required. There were two types of
classification trials in the retrieval blocks: trials without shift,
and trials with shift. Trials without shift (see Fig 1B) occurred when the test cards on two or more consecutive trials
shared the same attribute with the cue card. In the example
shown in Figure 1B, a different red test card is presented on
consecutive trials so that a match to the reference card that
has red in it was required on each of these trials. On the
other hand, trials with shift (see Fig 1C) occurred when the
test cards on two consecutive trials did not share the same
attribute with the cue card. In the example shown in Figure
1C, a trial where the only shared attribute between the cue
card and the test card is the color (both cards are red) was
followed by a trial in which the only shared attribute between the cue card and the test card is number (both cards
contain two objects). Hence a shift was required from classification according to color to classification according to
number. Three shift trials occurred within each retrieval
block of trials. Shifts in classification occurred randomly after
2, 3, 4, or 5 consecutive classifications in a row using the
same criterion, the total number of trials per block being
variable. In the retrieval with shift condition, an active comparison needed to be performed between the cue and the test
cards to execute the shift. Also, in this condition, the correct
reference card on subsequent trials was located at different
positions, requiring the use of a different finger on each trial.
In contrast, in the retrieval without shift condition, the correct reference card on subsequent trials was located in the
same position, hence requiring the same finger movement.
In the continuous shift condition (see Fig 1D), no cue card
was presented. Each test card contained only one attribute
shared with a single reference card, and thus there was only
one possible response based on this attribute. In this condition, test cards were presented so that shifts in classification
occurred on each new trial in a random order. In the example shown in Figure 1D, a trial was presented in which the
test card shared an attribute only with the second reference
card (the color green) followed by a trial in which the test
card shared an attribute only with the first reference card
(one object). Twelve trials occurred within each block of the
continuous shift condition. Unlike the retrieval with shift
condition, no active planning or comparison was needed to
execute the shift because the new rule for classification was
implicitly given by the task. Note also that, in this condition,
the correct reference card on subsequent trials was located at
different positions, requiring the use of a different finger on
each trial.
In the control condition, the test card on each trial was a
replica of one of the four reference cards (see Fig 1E), and
the subject was required only to match the test card to its

twin within the four reference cards. Twelve trials occurred

within each block of the control condition.
Subjects performed six retrieval blocks including both shift
and nonshift trials, as well as three blocks of the continuous
shift and control conditions per run. Before scanning, subjects were trained on the task using a personal computer.
During this training session, all subjects performed four series of six retrieval and three continuous shift and control
conditions.

Functional Magnetic Resonance Imaging Scanning

Subjects were scanned using a 1.5-Tesla Siemens Sonata
MRI scanner at the McConnell Brain Imaging Centre. Each
scanning session began with a T1-weighted threedimensional volume acquisition for anatomical localization,
followed by acquisitions of echo planar T2*-weighted images
with BOLD contrast. Functional images were acquired in six
runs containing 200 volumes each acquired every 2.5 seconds (TE, 50 milliseconds; FA, 90 degrees). Volumes contained 24 slices, voxel size 4.7 4.7 4.7mm3.

Data Analysis
The methods for data analysis were the same as in our previous studies12,19 and made use of the fmristat software developed by Worsley and colleagues.20 The first three frames
in each run were discarded because the BOLD signal does
not reliably reach steady state during those frames. Images
from each run then were realigned to the fourth frame for
motion correction and smoothed using a 6mm full-width
half-maximum (FWHM) isotropic Gaussian kernel. The statistical analysis of the fMRI data was based on a linear model
with correlated errors. The design matrix of the linear model
was first convolved with a difference of two gamma hemodynamic response functions timed to coincide with the acquisition of each slice. The correlation structure was modeled
as an autoregressive process. At each voxel, the autocorrelation parameter was estimated from the least squares residuals,
after a bias correction for correlation induced by the linear
model. The autocorrelation parameter was first regularized
by spatial smoothing and then was used to whiten the data
and the design matrix. The linear model was reestimated using least squares on the whitened data to produce estimates
of effects and their standard errors. The resulting effects and
standard effect files then were spatially normalized by nonlinear transformation into the standard proportional stereotaxic space of Talairach and Tournoux21 using the algorithm
of Collins and colleagues.22 Anatomical images were also
normalized to the Talairach space using the same transformation. In a second step, runs, sessions, and subjects were
combined using a mixed-effects linear model for the data
taken from the previous analysis. A random-effects analysis
was performed by first estimating the ratio of the randomeffects variance to the fixed-effects variance, and then regularizing this ratio by spatial smoothing with a Gaussian filter.
The amount of smoothing was chosen to achieve 110 effective degrees of freedom.20,23 Statistical maps were thresholded at p value less than 0.05 corrected for multiple comparisons for all peaks and at p value less than 0.001
uncorrected for predicted peaks within the BG.
Error trials were not considered in the fMRI analysis be-

Monchi et al: Basal Ganglia and Action

259

Table. The Coordinates (x, y, z) in Standard Stereotaxic Space and the t Values of Significant Peaks in Subcortical Regions
in All Contrasts
Caudate
Nucleus
Right

Subthalamic
Nucleus
Left

Subthalamic
Nucleus
Right

Putamen
Left

Globus
Pallidum
Right

Thalamus
Left

14, 4, 22
t: 3.66
10, 4, 10
t: 3.29

10, 0, 10
t: 4.29

12, 24,
2 t: 4.79

12, 20,
4 t: 3.26

20,
2, 12
t: 4.33
28,
6, 4
t: 3.85

10
28 12
t: 4.97
10 8
14 t:
3.88

14 20
12 t:
3.71

Retrieval
with shift
vs continuous shift

10, 4, 12
t: 3.53

Continuous
shift vs
retrieval
without
shift

10, 22,
10 t: 4.58

20 32
4 t: 4.12

Retrieval
Retrieval
without
shift vs
control
Retrieval
with shift
vs control
Continuous
shift vs
control
Retrieval
with shift
vs retrieval
without
shift

cause the error rate was very low during scanning (below 3%
across all conditions for all subjects). Furthermore, the trial
following an error trial in the retrieval condition was also
removed because it cannot be classified into any of the two
categories (with shift, without shift). Activity during the
matching period (from the moment a new test card is presented to the moment a response is made) on each trial of
the four conditions (retrieval without shift, retrieval with
shift, continuous shift, and control) was combined to generate the following six contrasts for statistical analysis: (1) retrieval without shift minus control; (2) retrieval with shift
minus control; (3) continuous shift minus control; (4) retrieval with shift minus retrieval without shift; (5) retrieval
with shift minus continuous shift; (6) continuous shift versus
retrieval without shift.
We predicted that the caudate nucleus would be particularly involved in the retrieval with shift, that is, the condition
requiring active planning to perform a shift in classification,
but not in the continuous shift nor the retrieval without shift
conditions in which no such planning is required.

Results
Significantly increased cortical activity was found in all
subtractions described above and these were in agreement with our results previously reported using fMRI
during the performance of the Wisconsin Card-Sorting
Task.12 Because the present fMRI protocol was specif-

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Thalamus
Right

ically designed to study BG involvement in executive

processes, only the subcortical peaks are reported and
discussed here.
As predicted, there was a significant increase in activity in the right caudate nucleus (1) when the retrieval with shift was compared with the control condition, (2) when the retrieval with shift was compared
with the retrieval without shift condition, and (3) when
the retrieval with shift was compared with the continuous shift condition (Table, Fig 2AC).
Significant activation was also observed in the left
putamen when retrieval with shift was compared with
retrieval without shift (Figs 2B and 3A) and also in the
globus pallidus when the continuous shift was compared with the retrieval without shift condition (see
Table).
In addition, there was significant activity in the region of the brain that encompasses the subthalamic nucleus. Although with the fMRI resolution used here it
may be difficult to determine with certainty whether
the observed increases in activity in this region are actually focused in the subthalamic nucleus, the coordinates of the activity clusters observed coincided well
with the delimitation of this nucleus in the Talairach
and Tournoux atlas. In the subthalamic nucleus, sig-

Fig 2. Location of the striatal peaks in the various subtractions. The anatomical magnetic resonance images shown are the average
of the T1 acquisitions of the 10 subjects transformed into stereotaxic space. (A) Location of the right caudate activation in the retrieval with shift versus the control condition. Coronal sections are shown every 2mm from Talairach coordinate Y 6 to Y
6. (B) Location of the right caudate activation and the left putamen activation in the retrieval with shift versus the retrieval
without shift condition. Coronal sections are shown every 2mm from Talairach coordinate Y 6 to Y 4. (C) Location of
the right caudate activation in the retrieval with shift versus the continuous shift condition. Axial sections are shown every 2mm
from Talairach coordinate Z 8 to Z 14.

nificant increase in activity was observed, bilaterally

when the retrieval with shift was compared with the
retrieval without shift condition, and, in the left side
only, when the continuous shift was compared with the

retrieval without shift condition (see Table). For the retrieval with shift minus the retrieval without shift subtraction, the cluster of significant voxels for this region
lay in the left side of the brain between X 16 to

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Fig 3. Location of the subthalamic nucleus peaks in the various subtractions. The anatomical MRI images shown are the average of
the T1 acquisitions of the 10 subjects transformed into stereotaxic space. (A) Location of the bilateral subthalamic nucleus activation in the retrieval with shift versus the retrieval without shift condition. Note also the presence of a peak in the left putamen.
Axial sections are shown every 2mm from Talairach coordinate Z 8 to Z 2. (B) Location of left subthalamic activation
in the continuous shift versus the retrieval without shift condition. Axial sections are shown every 2mm from Talairach coordinate
Z 12 to Z 6.

7, Y 30 to 20, and Z 14 to 0 (Fig 3A),

and in the right side of the brain between X 11 to
15, Y 23 to 18, and Z 8 to 2 (see Fig
3A). For the continuous shift minus the retrieval without shift subtraction, the cluster of significant voxels for
this region lay in the left side of the brain between
X 19 to 7, Y 26 to 18, and Z 14 to
6 (see Fig 3B).
Finally, significantly increased activity was observed
in the thalamus, bilaterally, when the retrieval with
shift was compared with the retrieval without shift condition, and in the right thalamus when the continuous
shift was compared with the retrieval without shift condition (see Table). Note that no other subcortical region reached significance, even at a low level of significance of p value less than 0.01 uncorrected in any of
the subtractions.
Discussion
These results show that the caudate nucleus is specifically involved in the active planning of a novel action.
Increased activity in the caudate nucleus in this experiment cannot be attributed to the short-term retention
in memory of the cue card because significant activation in this structure was observed when comparing the
retrieval with shift to the retrieval without shift conditions (both conditions having identical short-term

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memory requirements) and not when comparing the

retrieval without shift to the control condition (even
though the retrieval condition had a short-term memory requirement and the control did not). This finding
is consistent with the fMRI study of Lewis and colleagues14 who suggest that the caudate nucleus is particularly involved in cognitive manipulation, but not in
maintenance or retrieval of information within working
memory.
In earlier neuroimaging studies that showed the involvement of the caudate nucleus in set-shifting,1113
the experimental design could not determine whether
the caudate nucleus is important in the shift per se or
its planning (ie, the cognitive decision to shift). Here,
the experimental design was such that it enabled us to
distinguish between these possibilities. Indeed, the continuous shift condition, in which the rule is provided
implicitly to the subject, permitted us to examine
whether the caudate nucleus is involved in the shift per
se, or rather in the active planning of the novel action
solicited by the task. Importantly, there was no increase
in activity during the continuous shift versus the control
condition in the caudate nucleus, showing that shifting
per se is not the cause of the increase in neostriatal
activity in shifting tasks. This conclusion is further
supported by the fact that activity in the caudate nucleus was significantly increased both during the re-

trieval with shift versus the continuous shift condition

and during the retrieval with shift versus the control
condition. Thus, the significant increase in activity observed in this nucleus in set-shifting must be caused by
the active planning of a novel action, and not to the
shift per se. This hypothesis is consistent with a previous positron emission tomography study10 in which
significantly increased activity in the caudate nucleus
was observed only in conditions in which multiple
moves had to be planned in advance during the performance of a planning task (ie, the Tower of London).
The significant increase in activity in the putamen in
this study when retrieval with shift was compared with
retrieval without shift is in agreement with our previous
fMRI study of the Wisconsin Card-Sorting task in
which significant activity in the putamen was only observed during matching after negative feedback (ie,
during the execution of a set-shift), but not during
matching following positive feedback (ie, matching using the same rule as previously).12 This study provides
further evidence that the putamen is involved in the
execution of nonroutine actions. Cunnington and colleagues24 had reported significant activity of the putamen during self-initiated movements, but not during
externally triggered alternating movements. Interestingly, in the present study, significant putamen activity
was not observed during the continuous shift condition
in which the movement to be performed is implicitly
given by the task (via the only possible choice of card)
and therefore externally triggered. Altogether these
results indicate that the putamen may play an important role in the execution of an action that is based on
a self-determined novel strategy.
The fact that a significant increase in activity was
observed only in the left putamen is consistent with
the required contralateral motor response.12,25 Furthermore, significantly increased activity was only found in
the right caudate nucleus and not the left. This seems
in agreement with previous positron emission tomography studies reporting that, in Parkinsons disease, significant decreased dopamine release in the right caudate nucleus only correlated with performance on
frontal executive tasks,26,27 and fMRI experiments
showing significant increased activity in the right caudate nucleus only during the performance of a cognitive task in healthy adults.25,28 However, other fMRI
studies of cognitive functions have also reported bilateral activation of the caudate nucleus,12,14 and bilateral
activation of the putamen has also been reported in an
fMRI study of finger movements where movements
were performed only with the right hand.24
In sharp contrast with the striatum, increased activity in the subthalamic nucleus was observed when
comparing conditions in which the finger used to respond changed on each trial with conditions in which

the finger used to respond remained the same (ie, retrieval with shift versus retrieval without shift and continuous shift versus retrieval without shift). These findings indicate that activity in the subthalamic nucleus is
not linked to the active planning of an action, but
rather to the execution of a new movement (ie, finger
movement in this particular study). This finding receives support from previous neurophysiological studies
in monkeys and humans showing that a large proportion of neurons in the subthalamic nucleus respond
during active and passive limb movements.3,16,17 Indeed, it has been suggested that the subthalamic nucleus exerts a specific influence on the BG output related to the control of movement parameters.3,16,17
Along with this hypothesis, we suggest that activity in
the subthalamic nucleus is less context dependent than
in the caudate nucleus and putamen because subthalamic activity was not dependent on the planning of a
set-shift, but rather on the execution of a different limb
movement.
In conclusion, the present fMRI study enabled us to
dissociate between the activity of different BG structures and allowed us to determine the specific functional contribution of the caudate nucleus in planning
and set-shifting. We were able to separate the functional roles of the caudate nucleus, the putamen, and
the subthalamic nucleus in the preparation and execution of actions. Such functional imaging studies may
allow for a better understanding of the pathophysiology of the cognitive and motor deficits in illnesses
linked to BG dysfunction, such as Parkinsons disease.19
This work was funded by grants from the Fond de la Recherche en
Sante du Quebec (2816, O.M.) and the Canadian Institutes for
Health Research (MOP-37753, M.P.).
We thank the staff at the McConnell Brain Imaging Unit for their
assistance.

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