Neuroscience 179 (2011) 94 103

FUNCTIONAL NEUROANATOMY ASSOCIATED WITH THE

EXPRESSION OF DISTINCT MOVEMENT KINEMATICS IN MOTOR
SEQUENCE LEARNING
P. ORBAN,a,b* P. PEIGNEUX,b,c O. LUNGU,a K. DEBAS,a
M. BARAKAT,a P. BELLEC,a H. BENALI,d P. MAQUETb,e
AND J. DOYONa,d

Key words: fMRI, humans, motor control, sequence learning,

putamen, cerebellum.

a
Functional Neuroimaging Unit, Geriatric Institute Research Center,
Universit de Montreal, Queen Mary 4565, Montreal, Canada H3W
1W5

From early childhood, the human brain builds and retains a

broad repertoire of complex motor behaviors. Many of
them may be conceived as single movements, for instance
when reaching tools and throwing objects, or may consist
of even simpler ballistic actions, for example when performing pinch finger presses. Numerous motor actions
additionally require the capacity to combine and articulate
elementary movements into a well-coordinated sequence
like when speaking or writing. Due to brain plasticity, our
innate, limited motor repertoire expands over life in order to
adapt to novel environmental demands and to carry out
more complex actions. Thus, adjustments with practice
may occur through motor adaptation at the level of single
movements, and through learning of novel motor sequences whereby complex chains of movements eventually come to be performed as fast and automatic action
units. Although most often treated as separate abilities in
laboratory settings, it should be stressed that motor adaptation of single movements and motor sequence learning
may actually coexist in real-life behaviors, suggesting that
the motor system can acquire them simultaneously (Overduin et al., 2008; Moisello et al., 2009). In fact, in many
cases, learning a novel motor sequence involves the concomitant motor adaptation of the sequences elementary
components.
Brain imaging research has used a variety of experimental paradigms to identify the brain areas associated
with the acquisition of motor sequences in humans (Hikosaka et al., 1999, 2002; Doyon and Benali, 2005; Ashe et
al., 2006; Orban et al., 2008; Doyon et al., 2009). In the
serial reaction time task, subjects are asked to learn, incidentally or intentionally, a new motor sequence by pressing spatially compatible key presses corresponding to specific series of stimuli (Peigneux et al., 2000; Doyon et al.,
2002; Seidler et al., 2002; Destrebecqz et al., 2005). Other
paradigms require to discover a repeating pattern of motor
responses by trial-and-error (Jueptner et al., 1997a,b), to
execute an explicitly known motor sequence paced via
visual or auditory cues (Karni et al., 1995; Lehricy et al.,
2005), or to learn to draw simple Chinese word characters
forming a graphomotor sequence in order to study handwriting in a more naturalistic context (Swett et al., 2010).
Together, such studies have provided valuable insights
into the brain structures mediating this form of learning,
highlighting the role of the cortico-striatal and cortico-cer-

Cyclotron Research Center, Universit de Lige, Belgium

Neuropsychology and Functional Neuroimaging Research Unit, Universit Libre de Bruxelles, Belgium
d
Unit Mixte de Recherche-S 678, Institut National de la Sant et de la
Recherche Mdicale/University of Paris 6, Centre Hospitalier Universitaire Piti-Salptrire, Paris, France
e

Department of Neurology, CHU, Universit de Lige, Belgium

AbstractA broad range of motor skills, such as speech and

writing, evolves with the ability to articulate elementary motor
movements into novel sequences that come to be performed
smoothly through practice. Neuroimaging studies in humans
have demonstrated the involvement of the cerebello-cortical
and striato-cortical motor loops in the course of motor sequence learning. Nonetheless, the nature of the improvement
and brain mechanisms underlying different parameters of
movement kinematics are not yet fully ascertained. We aimed
at dissociating the cerebral substrates related to the increase
in performance on two kinematic indices: velocity, that is the
speed with which each single movement in the sequence is
produced, and transitions, that is the duration of the gap
between these individual movements. In this event-related
fMRI experiment, participants practiced an eight-element sequence of finger presses on a keypad which allowed to record those kinematic movement parameters. Velocity was
associated with activations in the ipsilateral spinocerebellum
(lobules 4-5, 8 and medial lobule 6) and in the contralateral
primary motor cortex. Transitions were associated with increased activity in the neocerebellum (lobules 6 bilaterally
and lobule 4-5 ipsilaterally), as well as with activations within
the right and left putamen and a broader bilateral network of
motor cortical areas. These findings indicate that, rather than
being the product of a single mechanism, the general improvement in motor performance associated with early motor
sequence learning arises from at least two distinct kinematic
processes, whose behavioral expressions are supported by
partially overlapping and segregated brain networks. 2011
IBRO. Published by Elsevier Ltd. All rights reserved.
*Correspondence to: P. Orban, University of Montreal, Geriatric Institute Research Center, Functional Neuroimaging Unit, 4565 Queen
Mary, Montreal, QC, Canada H3W1W5. Tel: 1-514-340-3540, ext:
4114.
E-mail address: pierre.orban@criugm.qc.ca (P. Orban).
Abbreviations: FDR, false discovery rate; fMRI, functional magnetic
resonance imaging; MNI, Montreal Neurological Institute; PPM, posterior probability maps.

0306-4522/11 $ - see front matter 2011 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2011.01.040

94

P. Orban et al. / Neuroscience 179 (2011) 94 103

ebellar systems in particular. Nonetheless, most of these

experimental paradigms have essentially explored the
subjects ability to acquire an abstract representation of
the order of the sequence elements, rather than investigating the nature of the motoric improvement measured
during skill sequential motor learning (Krakauer and Shadmehr, 2006). Indeed, the behavioral expression of learning
has usually been assessed through global measures of
performance such as the subjects overall improvement in
accuracy or reaction time, rather than through trial-by-trial
changes in different movement kinematics subtending the
unconstrained execution of a motor sequence. A recent
combined fMRI and kinematic approach however demonstrates how studying the precise relationship between
changes in neural activity and the improvement on a refined performance measure such as normalized jerk can
inform on motor sequence learning processes (Swett et al.,
2010). Nonetheless, it is still unclear how different aspects
of the motor sequence learning process, in particular performance changes in velocity and transitions between single movements, are individually mediated at the brain
level.
Using skill finger tapping tasks that favor the unconfined execution of a series of digit movements (Korman et
al., 2003; Walker et al., 2003; Hotermans et al., 2006),
recent behavioral studies have revealed that some movement transitions embedded within the motor sequence can
differently benefit from practice (Kuriyama et al., 2004;
Sheth et al., 2008). Such results indicate that the temporal
structure of the motor sequence comes to be reorganized
during learning through the development of chunking and
coarticulation mechanisms, which enable grouping individual motor items into larger units (Gobet et al., 2001; Sakai
et al., 2003, 2004). However, the neural substrates specifically involved in the overall transition gains induced by
training have not yet been identified. Furthermore, the
behavioral effect of training on velocity of finger pinch
movements and its associated brain mechanisms have not
been specifically assessed in the context of a sequence
learning task involving multiple fingers. Indeed, velocity
gains, which reflect dynamic motor adaptation processes,
have only been tested while subjects produce repetitive
ballistic contractions of a single finger, typically the thumb
(Classen et al., 1998; Muellbacher et al., 2001, 2002).
Thus, how changes in elementary parameters of single
movements may affect the behavioral manifestation and
brain mechanisms engaged during the course of motor
sequence learning still remains unknown.
We therefore sought to provide a refined behavioral
and neurophysiological description of the effects of improved performance on distinct movement kinematics during the course of skill finger sequence learning. In particular, this study aimed at better characterizing the functional
roles that motor regions like the cerebellum, the putamen,
and other motor-related cortical areas bear on genuine
motoric properties (compared to more cognitive aspects)
as subjects acquire a new motor sequence. To do so, we
used an event-related functional magnetic resonance imaging (fMRI) paradigm and a dedicated keypad that can

95

precisely measure the kinematics of finger displacements

during a sequential tapping task. This approach allowed us
to test the hypothesis that the performance improvements
related to velocity (V) and transitions (T) contribute differently to motor sequence learning, and that these kinematic
properties are mediated by partially segregated networks
of motor areas in the human brain.

EXPERIMENTAL PROCEDURES
Participants
Twelve volunteers (six females; group mean age 26.53.8 years)
gave informed consent to take part in this study, which was
approved by the local Ethics Committee at the Geriatric Institute
Research Center, University of Montreal. All subjects were righthanded as assessed by a questionnaire (Oldfield, 1971) and had
no history of neurological or psychiatric disorder. Musicians and
professional typists were excluded in order to control for preexisting skills that require highly coordinated finger dexterities.

Experimental task
Participants were trained on a sequential finger tapping task
adapted for use in an event-related fMRI design. The task was
about 20 min long and included 60 practice trials that were interspersed with rest epochs lasting 12 s on average (jittering ranging
from 6 s to 18 s). Before scanning began (i.e., during the pretraining session) subjects were asked to memorize the sequence
using a verbal code (3 4 1 3 2 1 4 2; where 1, 2, 3, and 4
respectively refer to the index, middle, ring, and little fingers),
without actual training on the keypad. This was done so as to
study brain mechanisms related to implicit motor learning processes rather than to the explicit acquisition of the sequence
order. During scanning, each trial required subjects to prepare,
and then execute the explicitly known eight-element sequence.
Each rest epoch, during which a black screen was displayed, was
followed by a preparation and an execution phase. The time to
prepare for the execution of a sequence (i.e., planning phase) was
indicated to the subject by the brief appearance (500 ms) of a
yellow square at the center of the black screen. Subjects were
asked to prepare for sequence execution for a few seconds and
then to feel free to start typing it at the moment of their choice, with
no further external cuing, in order to promote self-initiation of the
series of movements. Results revealed that the preparation phase
lasted 4.24 s (SD0.91 s) on average (data for the preparation
phase are further explored in a separate paper). As soon as the
first of the eight sequential finger movements was initiated, a blue
square was displayed for 500 ms at the center of the black screen,
confirming the beginning of the execution phase. Subjects were
required to produce the motor sequence only once on each trial,
as fast and accurately as possible.

Material and data analysis

We used a custom-made MR compatible keypad allowing to measure precise finger movement kinematics (Fig. 1). The response
box was built using four industrial push button switches fixated on
a plastic enclosure. All electrical contacts were removed to keep
only the actuator and spring mechanisms. Total displacement of
the actuator was 5 mm. Pressing down a button moved a linear
encoder strip in front of an optical reading module that sensed
motion and direction, and that was used to send the corresponding digital impulses to the interface unit located outside the MR
room. The linear encoder strip was a thin Mylar strip with alternating lines and transparent areas (250 lines per inch). The reading head used two optical sensors in phase quadrature, meaning
that four impulses were sent to the interface (one count for every

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P. Orban et al. / Neuroscience 179 (2011) 94 103

Fig. 1. Experimental task and material. The finger tapping task required the self-initiated execution of an 8-element sequence (3 4 1 3 2
1 4 2) with the left hand. A custom-made keypad allowed recording,
through sensing motion modules, the precise displacement of four
button switches. In the right-sided graph, the grey curve (four channels
are shown as one) depicts the sequential finger motions over time (ms)
for the eight button presses of one early representative sequence. An
individual finger movement was considered to be initiated, completed
and released at respectively 10%, 70%, and 10% of the maximum
button switch press. Button press duration (velocity, V) was obtained
by calculating the duration difference between the initiation and completion of each individual movement (yellow dots illustrate the second
key press). Transition duration (transition, T) was calculated, for
each pair of individual movements, through the time difference
between the release of a given finger movement and the initiation of
the next one (blue dots illustrate the second transition).

transition) for every full cycle. Motion resolution was 1000 counts
per inch (one count every 25 m). Position counts received by the
interface module were stored in a 12 bits counter and those values
were continuously fed to a digital-to-analog converter. The resulting signal was then digitized using a 12 bits digitizer module
(National Instruments USB-6008, National Instruments Inc., Austin, TX, USA) at a sampling rate of 400 Hz per channel.
Data recorded for each key press were initially saved as
arbitrary voltage values, which were directly proportional to the
displacement of each button. They were temporally smoothed with
a triangular smoothing function to reduce noise. Minimum and
maximum voltage measures obtained for each of the four keys
were normalized to respective values of 0 and 100 (% of vertical
displacement) such that reliable comparisons of movement kinematics between fingers could be made. Several time points of
interest on each trial were then computed (see Fig. 1): initiation,
completion, and release of each button press. Button press duration (i.e., velocity [V]) was obtained by calculating the difference in
duration between the initiation and completion of each individual
movement (yellow markers in Fig. 1). Although velocity is typically
described as a measure of distance per time unit, time alone was
considered here as a measure of velocity because the amplitude
of finger movements remained constant throughout training. The
duration between movements (i.e., transition [T]) was calculated,
for each pair of individual movements, by measuring time differences between the release of a given finger movement and the
initiation of the next one (blue markers in Fig. 1). Incorrect sequences of finger presses were identified as errors and were
rejected from the analyses (see below).

FMRI procedures
Brain imaging data were acquired on a 3.0 Tesla MRI scanner
(Magnetom Tim Trio, Siemens) with a 12-channel head coil. Functional T2*weighted volumes were obtained using a blood-oxygen-level-dependent (BOLD) sensitive, single-shot echo planar
sequence (TR1000 ms; TE30 ms; FA70; FoV220220
mm2; matrix size6464; voxel size3.43.47 mm3; gap
25%; 16 slices). Structural T1*-weighted MRI scans were also
acquired, using a turbo flash sequence with an inversion pulse
(TR2300 ms; TE2.91 ms; FA09; FoV256256 mm2; ma-

trix size256256; voxel size111.2 mm3; gap50%; 160

slices).
Processing and statistical analyses of brain images were
performed using SPM2 (Wellcome Department of Cognitive Neurology, London, UK) implemented in Matlab 7 (Mathworks Inc.,
Sherbom, MA, USA). Spatial preprocessing included realignment
and adjustment for in-scanner head movement related effects,
coregistration of functional and anatomical images, spatial normalization into the stereotactic Montreal Neurological Institute
(MNI) space, and spatial smoothing using a Gaussian kernel of 7
mm full width at half maximum (FWHM). Statistics were performed
using the linear general model (Friston et al., 1995). At the intraindividual level, the design matrix included two regressors that
modelled the preparation and execution epochs, respectively.
Activation effects related to the preparation phase of the task were
not investigated in the present study, and thus the corresponding
regressor was modelled as a covariate of no interest. Variables of
interest were related to motor execution and practice-related effects linked to performance on specific kinematic variables (i.e.
velocity and transitions) measured during the execution of the
motor sequence. Hence, the design matrix included two additional
linear parametric regressors associated with the execution epochs, modulated respectively by the trial-averaged duration of
individual finger button presses (V) and the trial-averaged duration
of transitions between finger movements (T). Linear contrasts
testing for the main effect of execution, as well as for the effects of
execution modulated by performance (V or T), were convolved
with a canonical hemodynamic response function (HRF), generating fixed-effects statistical maps (Friston et al., 2002). It should
be noted that the parametric contrasts that tested for performance-related effects took into account the heterogeneity of the
kinematic learning curves observed across subjects, as these
analyses were performed at the individual level.
Summary statistic maps obtained for each contrast were subsequently entered into random-effects level models to allow inferences at the population level. Given the a priori knowledge based
on existing literature, loci of activations for performance-related
effects were identified within the striato-cortical and cerebellocortical motor loops. The brain network of interest encompassed
the striatum and cerebellum, their related cortical motor and premotor regions as well as the thalamus. An inclusive mask delineating this brain network of interest (size30,000 voxels) was
thus created using the WFU PickAtlas software toolbox (Maldjian
et al., 2003). For the main effect of motor sequence execution,
activation maps were thresholded and considered significant at
P0.05 after false discovery rate (FDR) correction for multiple
comparisons (Genovese et al., 2002). Activation maps obtained
for parametric modulation effects were thresholded at P0.005
(uncorrected) to reveal the full extent of activation, but only brain
regions that showed peak voxels surviving a threshold of P0.001
(uncorrected) were considered to be significantly activated.
Direct comparisons, using classical inferences, between the
parametric effects for the two kinematic parameters did not yield
significant results. The absence of results likely comes from the
fact that parametric effects are typically weaker than main condition effects because the former is orthogonalized with respect to
the latter (Bchel et al., 1998). In addition, the learning curves for
the velocity and transition variables, which were entered as covariates with identical onsets in the design matrix, correlated to some
extent. Thus this may have lowered the likelihood of detecting
significant differences in parametric activation effects between
kinematic variables, although these were nonetheless found to
benefit from practice in significantly different proportions (see
Results). In order to partly address this concern, we computed
posterior probability maps (PPMs) that enabled conditional or
Bayesian inferences about regionally specific effects (Friston and
Penny, 2003). This type of analysis allows one to determine
whether a lack of significant statistical effect in a given contrast is

P. Orban et al. / Neuroscience 179 (2011) 94 103

97

Fig. 2. Trial-averaged behavioral results. The two left-sided plots depict the group learning curves over 60 trials for the velocity and transition
kinematic measures in yellow and blue respectively (mean trial-averaged durationSD). Thick lines show the logarithmic best fit curve for velocity
(dark yellow) and transitions (dark blue). The right-sided plot with green dots shows the correlation coefficient between the transition and velocity
measures in each participant (meanSD0.450.33).

merely due to a failure to detect it (i.e., error of type II/false

negative). After PPMs were computed for the contrasts of interest
(parametric effects for the transition and velocity parameters), the
probability (P%) that a voxel activation would exceed the threshold
defined based on the variance in parameters over all voxels was
identified. The interpretation of the result is thus that there is less
than P% probability that an area significantly activated in a given
contrast (e.g. transition) would also be activated in the other
contrast (e.g. velocity).

RESULTS
Behavioral results
The number of erroneous sequences over the entire training period was very low (3.25 out of 60 trials, SD3.67). In
addition, the error rate did not change with practice, as
indicated by the absence of significant difference between
the first (1.67, SD2.53) and second half (1.58, SD1.62)
of the training trials [t(11)0.13; P0.9]. Incorrect trials
were excluded from the behavioral and brain imaging analyses. Group learning curves based on trial-averaged durations for button presses of individual elements (V) and for
transitions between sequence elements (T) are shown in
Fig. 2. The subject-specific trial-averaged learning curves
were used in the analysis of brain imaging data to investigate the neural correlates of each kinematic parameter. A
repeated measures analysis of variance (ANOVA) including trial-averaged durations for the 60 events revealed
that the main effect of practice (events) was significant
[F(59,649)24.84; P0.0001], as were the practice effects observed for each kinematic measure considered
separately [V: F(59,649)3.52; P0.0001; T: F(59,649)
24.36; P0.0001]. These results suggest that a general
decrease in sequence duration results from the combined
improvement in performance on both the velocity of individual elements and transition between elements. Although a positive correlation between the two different
kinematic learning curves was observed [r0.450.33],
the interaction effect between the two kinematic measures
[V vs. T] and the amount of practice was highly significant
[F(59,649)5.39; P0.0001], hence showing that the nature and amplitude of the improvement in performance
differed between the two kinematic measures. Changes in
velocities show a fast and short improvement process,
while modifications in transitions demonstrate a slower but
larger gain in performance. Indeed, the gain in velocity of

individual movement elements was about 20 30%, and

reached asymptote after 20 trials, whereas the improvement in transition durations between individual movements
was about 70 80%, but required 50 trials to reach asymptotic performance.
The behavioural data for the transition (T) and velocity
(V) variables were further analysed at the within-sequence
level for the sake of completeness, although these behavioural results could not be incorporated into the functional
brain imaging analyses. A repeated measures analysis of
variance (ANOVA) was performed over all durations extracted for the velocity (3, 4, 1, 3, 2, 1, 4, 2) and transition
(3-4, 4-1, 1-3, 3-2, 2-1, 1-4, 4-2) kinematic parameters. At
the group level, the main effects of type of button press
(i.e., 1, 2, 3 or 4) and practice were significant for the
velocity variable [F(7,77)4.47; P0.001 and F(59,649)
3.52; P0.0001]. The type of button press effect was
significant for the first trial [F(7,77)4.10; P0.001], but
the eight elements of the sequence were not performed at
significantly different velocities on the last trial [F(7,77)
0.78; P0.6]. This finding was further confirmed by a
significant interaction effect showing that all sequence elements did not benefit in the same proportion from motor
training [F(413,4543)1.18; P0.01]. More specifically, it
appears that button presses executed with the ring and
little fingers (3 and 4) were performed at a slower speed at
the beginning of training, but were characterized by velocities similar to that of the index and middle fingers (1 and 2)
at the end of the allocated period of motor sequence
practice. With respect to the analysis on transitions, the
main effects for the individual transitions and practice were
also shown to be significant [F(6,66)3.75; P0.01 and
F(59,649)24.36; P0.0001]. The analysis revealed that
the seven element-to-element transitions were characterized by significantly different durations for both the first
[F(6,66)2.84; P0.05] and last [F(6,66)2.55; P0.05]
trials. Furthermore, the significant interaction revealed that
the decrease in transition time was not similar between
transition types [F(354,3894)1.19; P0.01], hence indicating that some transitions benefited more than others
from practice. The finding that transitions times between
different pairs of finger movements are unequal and are
unevenly affected by practice is in agreement with the
development of chunking mechanisms that temporally restructure the sequence of movements during training. It

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P. Orban et al. / Neuroscience 179 (2011) 94 103

Table 1. Brain imaging results for the main effect of motor sequence
execution
Brain region

Cerebellum lobule 8 L
Cerebellum lobule 8 R
Cerebellum lobule 4-5 L
Cerebellum lobule 4-5 R
Cerebellum lobule 6 L
Cerebellum lobule 6 R
Thalamus R
Thalamus L
Putamen R
Pre-supplementary motor area
Supplementary motor area
Primary motor cortex R
Primary motor cortex L

17
14
10
7
21
17
17
17
28
3
3
45
38

55
62
52
55
52
55
17
24
0
10
0
17
21

49
49
14
14
28
21
7
14
7
49
63
56
63

3.11
3.04
5.13
3.70
4.72
4.77
3.53
2.81
3.08
3.86
3.52
4.66
3.70

Peak voxels from activation maps significant at P0.05 (FDR-corrected). x, y, and z are stereotactic coordinates in the Montreal Neurological Institute (MNI) space. Z, Z-statistic score; R and L, right and
left.

tivation levels in the supplementary motor area and primary motor cortex (including and extending outside the
hand representation area). The probabilities (P) that areas
with significant increases in activity as a function of one
kinematic parameter would be similarly activated in relation to the other kinematic variable are provided in Fig. 4.
Such results indicate that velocity and transition engaged
overlapping networks of brain regions (left cerebellar lobules 4-5 and 6 as well as right primary motor cortex), but
nonetheless suggest that subsets of brain areas are more
specifically recruited to support gains in velocity (left lobule
8 and right lobule 4-5 of the cerebellum) and transition
performance (lateral cerebellar lobules 6 bilaterally, putamen, SMA, and primary motor cortex).

DISCUSSION
Practice on a complex series of repeating finger movements usually leads to a gradual decrease in the time
required to execute the whole motor sequence (Korman et
al., 2003; Walker et al., 2003; Kuriyama et al., 2004; Ho-

should be noted, however, that this group analysis only

shows effects common to most subjects, and thus likely
overshadows specific differences with regards to the precise improvement profiles observed between participants.
Imaging results
The main effect of execution of the finger tapping sequence over 60 trials was characterized by a global increase in activity in a series of brain areas composing the
striato-cortical and cerebello-cortical motor loops (Table 1,
Fig. 3). Large cerebellar activity was detected bilaterally in
lobules 8, 4-5 and 6. Increased activity was also observed
in the contralateral putamen and thalamus bilaterally. At
the cortical level, the primary motor cortex as well as lateral
and medial premotor areas showed motor execution-related activity bilaterally.
In order to determine the precise role played by the
brain regions reported above during the course of motor
sequence learning, additional parametric analyses were
carried out to look for specific correlations between the
increases in brain activity and the practice-related decreases in duration for button presses of the sequence (V),
as well as for delays between them (T) (Table 2, Fig. 4).
First, the results revealed that movements velocity modulated the magnitude of neural responses in the spinocerebellum as significant activations were observed in the
ipsilateral (left) lobule 8, in lobules 4-5 bilaterally, and in the
medial lobule 6 ipsilaterally. A similar modulation effect
was observed in the left thalamus and the contralateral
(right) primary motor cortex (encompassing the hand representation area). Second, improvements in movements
transitions were accompanied by increased responses in
both right and left putamen, as well as in the right thalamus. Increased transition-related activity in the cerebellum
was mostly localized in lobules 6 of the neocerebellum
bilaterally, extending into cerebellar lobule 4-5 on the ipsilateral side. Finally, changes in transition performance at
the cortical level correlated with bilateral increases in ac-

Fig. 3. Brain imaging results for sequence execution. Main effect

activation maps (red blobs) are displayed at P0.05 (FDR-corrected)
on the group-averaged structural scan. Peak voxels are reported for
each brain region in Table 1. Coordinates are in the MNI space
(coronal slice, y; axial slice, z). Abbreviations: C4-5, C6, and C8,
cerebellar lobules; Put, Putamen; SMA, supplementary motor area;
M1, primary motor cortex; L, left; R, right.

P. Orban et al. / Neuroscience 179 (2011) 94 103

Table 2. Brain imaging results for the velocity and transition kinematic
variables
Brain region
Velocity
Cerebellum lobule 8 L
Cerebellum lobule 4-5 L
Cerebellum lobule 4-5 R
Cerebellum lobule 6 L
Thalamus L
Primary motor cortex R
Transition
Cerebellum lobule 4-5 L
Cerebellum lobule 6 L
Cerebellum lobule 6 R
Thalamus R
Putamen R
Putamen L
Supplementary motor area
Primary motor cortex R
Primary motor cortex L

31
10
7
24
21
41

45
52
55
58
21
17

49
14
14
21
7
49

3.46
3.66
3.32
3.30
3.26
3.49

7
38
34
14
24
28
0
45
31

55
52
58
21
7
3
7
21
17

14
28
28
0
7
7
56
63
70

3.53
3.51
3.66
3.22
3.28
3.97
3.05
3.65
3.09

8
67
77
12
12
44
120
27
9
9
17
20
4

Peak voxels are significant at P0.001 (uncorrected). x, y, and z are

stereotactic coordinates in the Montreal Neurological Institute (MNI)
space. Z, Z-statistic score (Z); C, cluster size that shows the full extent
of activation at P0.005 (uncorrected); R and L, right and left.

termans et al., 2006; Sheth et al., 2008). This process is

known to be contingent on proper functioning of various
motor-related brain areas (Hikosaka et al., 1999, 2002;
Doyon and Benali, 2005; Ashe et al., 2006; Orban et al.,
2008; Doyon et al., 2009). In particular, it has been shown
that the gradual improvement in normalized jerk during the
course of graphomotor sequence learning is tightly accompanied by changes in activity in the striatum, cerebellum,
and associated motor cortical areas (Swett et al., 2010).
The exact pattern of brain activity reorganization that account for the global change in performance however likely
depends on the precise structure of the task and its exact
underlying learning processes. Our findings further indicate that the overall improvement in performance arises
from combined and simultaneous modifications in distinct
but complementary aspects of sequential movement kinematics, namely velocity of individual movements and transitions between them. Velocity and transitions were found to be
mediated by partially overlapping and segregated subnetworks embedded within the striato-cortical and cerebellocortical motor loops. As will be discussed later, it is worth
noting that our results identifying the brain correlates of either
velocity or transition refer to both learning-dependent and
learning-independent neural mechanisms that ultimately subtend together the expression of improved performance for
velocity and transitions (Orban et al., 2010).
Movement kinematics during motor sequence
learning
The experimental paradigm used here allowed to study
motor sequence learning without superimposing constraints on the execution of individual movements such as
pacing or cueing. This enabled the measurement of both
velocity and transition kinematic parameters as well as the

99

description of their respective contribution to the overall

improvement in performance. The results reveal that the
single finger movements that build up the sequence benefit
from motor training. This suggests that a fast adaptation in
elementary finger motions, reflected through improved
movement velocity, does not only take place during practice of repetitive ballistic contractions performed with a
single finger (Classen et al., 1998; Muellbacher et al.,
2001, 2002), but that it can also occur during learning of
sequences that comprise multiple serial finger movements.
Previous work has shown that brief practice of pinch movements, typically performed with the thumb, results in a
rapid adaptation of ballistic motor behaviors, as reflected
through the optimization of movements direction, acceleration, and force (Classen et al., 1998; Muellbacher et al.,
2001, 2002). The present results show that a similar experience-dependent effect on individual movements produced in sequence contributes to the overall improvement
in speed when executing an entire motor sequence.
In addition to changes in velocity, a gradual improvement was observed at the level of the element-to-element
transitions embedded within the sequence, a finding in
agreement with studies that reported such an effect using
skill finger tapping tasks similar to ours (Kuriyama et al.,
2004; Sheth et al., 2008). As shown by the analysis of the
within subjects trials, the performance improvement was
not due to a global decrease in all transition times between
movements, but rather to a more pronounced positive
effect of practice on some of the pairs of finger movements. The fact that some transitions benefited more from
practice than others suggests that the structure of the
motor sequence underwent a learning-dependent temporal reorganization. Consequently, we interpret the overall
decrease in transition durations as arising from the emergence of chunking processes, which enable disparate
subs-sequence memory units to be gradually amalgamated into a larger single memory representation with practice (Gobet et al., 2001; Sakai et al., 2003, 2004). Because
this qualitative reorganization of the hierarchical structure
of a motor sequence is tightly coupled to the subjectspecific spontaneous emergence of rhythmic performance,
the gains in transitions performance are also thought to
reflect the optimization of the temporal control of sequential movements (Janata and Grafton, 2003; Ivry and Spencer, 2004; Sakai et al., 2004).
Altogether, such findings complement those from independent investigations showing that different aspects of
motor learning can develop in parallel, presumably without
interfering with one another (Overduin et al., 2008; Moisello et al., 2009). The latter studies indicate that learning
to respond to the spatial order of a series of arm-reaching
movements may occur simultaneously to motor adaptation of
these movements. Our results extend such findings by showing that the gains in speed of movements on a skilled finger
tapping task arise not only from the development of chunking
processes but also from the concomitant motor adaptation of
individual movements. It is worth noting that the improvement
profiles related to those two kinematic measures show that
velocity gains are smaller and occur on a shorter time-scale

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P. Orban et al. / Neuroscience 179 (2011) 94 103

Fig. 4. Brain imaging results for the kinematic parameters. The left-sided panel shows parametric activation effects for the velocity (yellow blobs) and
transition (blue blobs) kinematic variables. Overlap of the two effects is shown in green. Correlation effect activation maps are displayed at P0.005
(uncorrected) on the group-averaged structural scan. Brain regions including peak voxels that survived a threshold of P0.001 (uncorrected) are
reported in Table 2. Coordinates are in the MNI space (coronal slice, y; axial slice, z). Abbreviations: C4-5, C6, and C8, cerebellar lobules; Put,
Putamen; SMA, supplementary motor area; M1, primary motor cortex; L, left; R, right. The right-sided panel shows the probability value (P) of activation
for different brain areas in either the velocity contrast (yellow circles) or the transition contrast (blue circles). MNI coordinates (x, y, z) for the different
regions: C8L (31, 45, 49), C4-5L (10, 52, 14), C4-5R (7, 55, 14), C6L (24, 58, 21), C6L (38, 52, 28), C6R (34, 58, 28),
PutL (28, 3, 7), PutR (24, 7, 7), SMA (0, 7, 56), M1R (41, 17, 49), M1R (45, 21, 63), M1L (31, 17, 70).

than transitions gains, hence suggesting that the latter contributes to a larger extent to the overall improvement in sequential motor performance.
Brain correlates of velocity performance
The imaging results reveal that the subjects improvement
in velocity was mediated by activity in ipsilateral lobules
4-5, 8 and 6 of the spinocerebellum, as well as the contralateral primary motor cortex. Single-unit electrophysiological studies in non-human primates have repeatedly
shown that primary motor cortex neurons encode multiple
kinematic parameters such as velocity, acceleration, position, and force (Stark et al., 2007, 2009). In addition, repetitive transcranial magnetic stimulation (Classen et al.,
1998; Muellbacher et al., 2001, 2002) and fMRI (Morgen et
al., 2004) studies in humans have shown that short prac-

tice on repetitive ballistic pinch movements elicits cortical

representational changes in the primary motor cortex, hence
reflecting the creation of a short-term memory trace. Consistent with such findings, our results suggest that one function
of the primary motor cortex (hand representation area) during
the course of learning novel motor sequences is to give rise
or implement a rapid process of motor adaptation of the
elementary components composing the sequence.
Importantly, the present study also lends support to the
view that the cerebellum contributes to this fast process of
motor adaptation, or allows its expression. Cerebellar activity related to velocity gains was found predominantly in
territories composing the ipsilateral spinocerebellum, with
significant activation effects being precisely localized in
lobule 8 and lobules 4-5, extending into the most medial
lobule 6 ipsilaterally. Functional MRI data in humans have

P. Orban et al. / Neuroscience 179 (2011) 94 103

shown that these cerebellar territories contain somatotopic

representations of the forelimb, notably encompassing the
fingers and wrist areas (Grodd et al., 2001; Manni and
Petrosini, 2004). This suggests that these cerebellar regions may cooperate with the primary motor cortex in
mediating gains in velocity performance on individual finger movements. This hypothesis is consistent with recent
resting-state functional connectivity work that points to the
existence of segregated functional cerebello-cerebral networks in humans, including a sensorimotor network encompassing the cerebellar lobules 8 and 4-5 and the primary
motor cortex (Krienen and Buckner, 2009; OReilly et al.,
2009). Moreover, research using transneuronal tracers in
monkeys has demonstrated the existence of anatomical projections between the arm areas of both cerebral and cerebellar motor regions (Kelly and Strick, 2003), hence providing an
anatomical substrate for the occurrence of interactive processes between these brain regions.
Brain correlates of transition performance
The most prominent locus of transition-related activity was
located in the lobule 6 of the neocerebellum bilaterally.
Activations in this cerebellar area have been repeatedly
observed in motor sequence learning tasks (see Desmond
and Fiez, 1998, for a review). Over the last decades, one
of the core functions of the cerebellum has been linked to
the representation of temporal information (Janata and
Grafton, 2003; Ivry and Spencer, 2004). The cerebellar
hemispheres, in particular the lobules 6, have been shown
using fMRI to be engaged during tasks requiring complex
processing of timing needed for rhythm elaboration (Aso et
al., 2010; Bengtsson et al., 2004, 2005; Thaut et al., 2008),
while patients with cerebellar lesions fail to accurately master
the timing component of tasks that involve movement production (Spencer et al., 2007). Thus, the integration of sensory-motor inputs in specific areas of the cerebellar cortex in
tasks with high degrees of timing complexity may be an
essential part of the process leading to rhythm formation and
optimized chunking during motor sequence learning (Janata
and Grafton, 2003; Sakai et al., 2004).
Bilateral activity in the putamen was linked to transition
performance, thus arguing for a complementary function
for this subcortical area in processing timing and rhythms
processes. Accordingly, data from neuroimaging studies in
healthy subjects and reports of Parkinsons disease patients highlight a role for the putamen in the internal generation of timing and beat during rhythmic performance of
sequential movements (Grahn, 2009; Grahn and Rowe,
2009). Such findings are also in agreement with reports of
strong basal ganglia activation during learning of timed
motor sequences (Penhune and Doyon, 2002, 2005). In
addition, basal ganglia dysfunction is accompanied with
motor learning deficits thought to be due, in part, to the
inability to construct or express chunked responses (Graybiel, 1995, 1998). Accordingly, individuals that suffer basal
ganglia stroke fail to hierarchically organize movement
sequences into chunks as efficiently as neurologically intact controls (Boyd et al., 2009). In monkeys, blockade of
striatal type-2 dopamine receptors prevents from chunking

101

movements into a smooth sequence of motor responses

(Levesque et al., 2007). Altogether, findings from the present study thus suggest that both the lateral cerebellum and
putamen mediate the optimization of the temporal structure of the motor sequence during learning, although it is
unclear how their precise functions may differ in subtending or expressing the improved timing, rhythmic and
chunking processes.
At the cortical level, a role for the supplementary motor
area and the primary motor cortex in supporting improved
transitions during motor sequence learning is consistent
with previous findings highlighting their roles in the expression of sequential movements. Medial premotor areas are
known to process temporal complexity in timing tasks (Aso
et al., 2010; Bengtsson et al., 2004, 2005) and to support
multiple functions linked to the organization of movements
produced in sequence, like coding for rank-order effects,
the ordinal position of elements, and the intervals between
elements or chunks (Nakamura et al., 1998; Shima and
Tanji, 2000; Tanji, 2001; Kennerley et al., 2004). With
respect to the primary motor cortex, a distinct activation
associated with transition gains was observed in addition
to that related to velocity performance, outside the hand
representation area. Single-cell recording experiments
conducted in monkeys have previously revealed that the
primary motor cortex contains neuronal populations that
may code for serial knowledge (Carpenter et al., 1999) and
sequential movements (Lu and Ashe, 2005), thus supporting the view that the role of neuronal populations within
and outside the hand representation area in the primary
motor cortex may extend beyond processing basic motor
parameters such as velocity.
Limitations and perspectives
The present findings provide evidence for the existence of
partly different quantitative relationships between two aspects of movement kinematics and neural activity in specific
brain regions during practice of novel motor sequences. However, it should be stressed that the present study does not
allow to dissociate between the brain regions that undergo a
genuine learning-dependent functional plasticity, which actively induces behavioral changes, from those that merely
implement and express the increase in performance occurring as a by-product of learning (Orban et al., 2010). In
other words, our findings do not allow to determine
whether neural activity within separate subareas of the two
kinematic-related brain networks is primary or secondary
to the observed behavioural change. Yet, the present results confirm the presence of partially distinct brain networks supporting velocity and transition movement kinematics. Both aspects of sequential movements concomitantly improve during the course of motor sequence
learning, although they follow different temporal dynamics.
In addition, the relatively low temporal resolution of fMRI
prevented us from directly investigating the neural mechanisms that may more specifically take place within each
practice trial. Consequently, the exact nature of the brain
substrates that dynamically subtend chunking during motor sequence learning could not be investigated in detail

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P. Orban et al. / Neuroscience 179 (2011) 94 103

here. A more refined understanding could be provided by

other brain imaging techniques that would allow comparing
the neural correlates of fast transitions (observed within
chunked segments) and slow transitions (i.e. the so-called
problem points within a motor sequence) (Kuriyama et
al., 2004; Sheth et al., 2008). For the same reason, it is
unclear how the brain could implement the optimization of
specific individual elements of the motor sequence in a
context-dependent manner, based on the fact that coarticulation does not only have an impact on between-elements segments, but also on the individual profiles of each
sequence element as a function of the preceding and
succeeding motor units (Jerde et al., 2003).

CONCLUSION
The present findings provide a dynamic perspective on
motor sequence learning, a property of the brain deemed
essential for humans and other mammalians. Our results
suggest that distinct but intertwined processes that simultaneously develop with motor practice exhibit different
learning shapes, and that their expression are subtended
by partially segregated brain networks. Specifically, our
results lend support to the view that the primary motor
cortex and anterior spinocerebellum preferentially contribute to performance changes in velocity with which elementary motor units that compose the sequence are produced,
whereas brain areas encompassing the anterior neocerebellum, the putamen, and a larger extent of the frontal
motor cortex mediates more specifically the improvements
in transition performance. These results thus help to tease
apart the neural underpinnings of the expression of chunking and rhythm, which are viewed as key mechanisms
involved in motor sequence learning, from those related to
more basic motor adaptation processes. These two kinematic features of motor sequence production contribute
together to the reorganization of brain activity usually observed with practice on novel motor sequences.
AcknowledgmentsThe authors are most grateful to Andr Cyr
for building the MR-compatible keypad and for technical assistance, to Estelle Breton and Vo An Nguyen for skillful help with
data acquisition and analysis, and to Maria Korman for early
discussions on this topic. This work was funded through a grant
from the Natural Sciences and Engineering Research Council
(NSERC, Canada) to JD. PO and PM are supported by the
National Funds for Scientific Research (FNRS, Belgium). OL is
supported by a fellowship from the Ministre du dveloppement
conomique, de linnovation et de lexportation (MDEIE, Canada).

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(Accepted 20 January 2011)

(Available online 26 January 2011)