\

Neuropsycholo`ia\ Vol[ 25\ No[ 6\ pp[ 514530\ 0887

0887 Elsevier Science Ltd[ All rights reserved
Pergamon PII] S99172821"86#990570 Printed in Great Britain
99172821:87 ,08[999[99

Role of the striatum\ cerebellum and frontal lobes

in the automatization of a repeated visuomotor
sequence of movements
JULIEN DOYON\$%' ROBERT LAFORCE JR[\$ GINETTE BOUCHARD\$
DANIELLE GAUDREAU\$ JOANNE ROY\% MARIE POIRIER\% PAUL J[ BE
DARD\%
FERNAND BEDARD& and JEAN!PIERRE BOUCHARD%
 Groupe de Recherche en Readaptation physique\ IRDPQ\ Site Centre Francois!Charon^ $ E  cole de Psychologie^ % Departement
des Sciences Neurologiques\ Hopital de l|Enfant!Jesus^ and & Departement de Radiologie\ Hopital de l|Enfant!Jesus\ Universite
Laval\ Quebec\ Canada

"Received 14 June 0885^ revised 4 May 0886^ accepted 11 September 0886#

Abstract*Recently\ Doyon et al[ 19 demonstrated that lesions to both the striatum and to the cerebellum in humans produce a
similar de_cit in the learning of a repeated visuomotor sequence\ which occurs late in the acquisition process[ We now report the
results of two experiments that were designed to examine whether this impairment was due to a lack of automatization of the
repeating sequence of _nger movements by using a dual!task paradigm and by testing for long!term retention of this skill[ In
Experiment 0\ the performance of groups of patients with Parkinson|s disease\ or with damage to the cerebellum or to the frontal
lobes\ was compared to that of matched control subjects on the Repeated Sequence Test "primary task# and the Brooks| Matrices
Test "secondary task#[ These two tests were administered concomitantly in both early and late learning phases of the visuomotor
sequence[ Overall\ the groups did not di}er in their ability to execute the primary task[ By contrast\ in accordance with the predictions\
patients in Stages 12 of Parkinson|s disease or with a cerebellar lesion failed to reveal the expected increase in performance on the
secondary task seen with learning\ suggesting that the latter groups of patients did not have access to the same level of residual
cognitive resources to complete the matrices compared to controls[ In Experiment 1\ the same groups of patients and control subjects
were retested again 0907 months later[ They were given four blocks of 099 trials each of the repeating sequence task\ followed by a
questionnaire and a self!generation task that measured their declarative knowledge of that sequence[ The results revealed a long!
term retention impairment only in patients who changed from Stage I to Stage II of the disease "suggesting further striatal
degeneration# during the one!year interval\ or who had a cerebellar lesion[ By contrast\ performance of the three clinical groups did
not di}er from controls on declarative memory tests[ These _ndings suggest that both the striatum and the cerebellum participate to
the automatization process during the late "slow# learning stage of a sequence of _nger movements and that these structures also
play a role in the neuronal mechanism subserving long!term retention of such a motor sequence behavior[ 0887 Elsevier Science
Ltd[ All rights reserved[

Key Words] Humans^ procedural memory^ lesion studies^ dual!task paradigm^ long!term retention^ automaticity[

Introduction explicitly such that they are available as a conscious rec!

A large body of research has demonstrated the exis!
tence of a functional dissociation between declarative and
procedural memory systems 80[ Declarative memory
corresponds to the ability to store events or facts
' Corresponding author] Julien Doyon\ Ph[D[\ Groupe de
Recherche en Readaptation Physique\ IRDPQ\ Site Centre
Francois!Charon\ 414\ Boul[ Wilfrid!Hamel\ Local B!66\ Que!
bec "Quebec#\ Canada\ G0M 1S7[ Fax] "307# 418!2437^ E!mail]
julien[doyonpsy[ulaval[ca
ollection[ This memory system is dependent upon the
integrity of the medial temporal "i[e[ the hippocampus
and the surrounding cortical areas# and diencephalic
structures 81\ 82[ By contrast\ procedural memory refers
to the capacity to acquire motor\ visuomotor\ vis!
uoperceptual\ cognitive or other skills gradually through
practice 89[ The anatomical substrate involved in the
incremental learning of skilled behaviors still remains a
source of debate[ However\ there is increasing evidence
from both animal and human studies\ which suggest that
the striatum and the cerebellum\ in concert with associ!
ated motor cortical regions of the frontal lobes\ par!

514
515 J[ Doyon et al[:Automatization of a visuomotor skill
ticipate in this type of memory 8\ 08\ 21\ 25\ 40\ 51\ 83
85[
Evidence in favour of a striatal contribution in
incremental learning has come from the study of cell
physiology 02\ 22\ 71 and neurochemistry 5\ 6\ 72\ as
well as from lesion experiments in rodents 46 and non!
human primates 62\ 63\ 85[ Although some scepticism
about the validity of this hypothesis has recently been
expressed 16\ 092\ research in patients with either Par!
kinson|s or Huntington|s disease 19\ 11\ 24\ 26\ 27\ 38\
51\ 66\ 091 and in normal control subjects using modern
brain imaging techniques\ such as positron emission tom!
ography "PET# and functional magnetic resonance imag!
ing "fMRI#\ have also corroborated the notion that the
striatum plays a critical role in the learning of a variety
of skills 08\ 10\ 29\ 20\ 25\ 33\ 65\ 74[ Likewise\ evidence
in accord with a cerebellar participation in gradual learn!
ing after repeated trials has originated from physiological
2\ 8\ 31\ 32\ 44\ 55\ 85 and ablation studies in animals
09\ 58\ 76\ 77\ as well as from clinical 19\ 17\ 60\ 68\ 86
and brain mapping studies in humans 08\ 10\ 13\ 14\ 20\
33\ 64\ 73\ 74[ Finally\ in addition to the striatum and
the cerebellum\ some researchers have suggested that the
motor cortical areas of the frontal cortex "e[g[ pre!SMA\
SMA\ premotor cortex and primary motor cortex# are
involved in skill acquisition as well\ especially those
necessitating the learning of ordered sequences 51\ 83\
84\ 090[ The latter proposal is supported by anatomical
evidence which shows that the striatum and the cer!
ebellum project back to these cortical areas and the pre!
frontal cortex 3\ 47\ 70[ This is also corroborated by a
series of physiological 34\ 59\ 53\ 54 and ablation studies
50 in non!human primates\ as well as by PET and fMRI
experiments in which learning!associated changes in cer!
ebral blood ~ow in motor and pre!frontal regions have
been observed in healthy normal volunteers 19\ 10\ 29\
20\ 25\ 33\ 35\ 61\ 64\ 68\ 73[
Recent investigations in humans have demonstrated
that the striatum and the cerebellum do not only play a
critical role in the early "fast# learning stages of a vis!
uomotor skill 14\ 33\ 60 in which considerable improve!
ment in performance can be seen within a single training
session\ but that they may also participate in the {{auto!
matization|| process which occurs in the late "slow# phase
of the acquisition process 08\ 10\ 20\ 33\ 65\ 74[ In the
latter phase of learning during which further gains can
be observed across several sessions "and even weeks# of
practice 35\ 36\ it is believed that the execution of the
task becomes automatic\ hence reducing the mental e}ort
and attention to be directed in performing the skill as
well as the load on the subjects| working memory capacity
4[ In accordance with this notion\ Doyon et al[ 19
have recently compared the performance of patients with
Parkinson|s disease\ with a cerebellar lesion\ or with dam!
age circumscribed to the frontal lobes on a version of the
Repeated Sequence Test 56[ This test consists of a visual
reaction!time task with a _xed embedded sequence of
_nger movements[ The subjects received four blocks of
trials "i[e[ 39 presentations of a 09!item sequence# per day
over six training sessions\ which took place once a week
during six consecutive weeks[ The results revealed that
the performance of Parkinsonian patients with a bilateral
striatal dysfunction "i[e[ Stages 12 of the disease accord!
ing to Hoehn and Yahr|s scale 30# and patients with
damage circumscribed to the cerebellum\ but not those
with a lesion limited to the frontal cortex\ failed to
improve as much as their matched control subjects in the
last three training sessions only[ Moreover\ correlational
analyses showed that the learning de_cit in patients with
either PD or with a cerebellar lesion was not related to a
cognitive deterioration\ mood disturbance\ or to a motor
de_cit per se[ By contrast\ no signi_cant di}erence
between the three clinical and control groups was seen
with respect to their level of declarative knowledge of
the sequence[ Based on these _ndings\ Doyon et al[ 19
proposed that\ unlike declarative memory\ the incremen!
tal acquisition of a visuomotor skill depends upon the
integrity of the striatum and the cerebellum[ Further!
more\ because the impairment was observed in the second
half of the training sessions\ they also suggested that these
two structures are particularly important in advanced
"slow# learning stages of a visuomotor sequence\ possibly
in the {{automatization|| phase\ during which the for!
mation of a pattern of response is consolidated 4[
Several investigators have proposed the use of dual!
task methodology to investigate the level of auto!
matization of a skill[ This method is thought to test for
the level of attentional resources that subjects can devote
to a second cognitive task as they become more e.cient
at performing a learned behavior 7\ 03\ 04\ 29\ 25\ 42[
Indeed\ it has been suggested 28\ 39\ 75 that training on
a skill learning task modi_es the performance resource
functions of the individual 69\ such that the capacities
needed to execute the task decline with practice hence
leaving room for a second task to be executed[ Other
researchers have proposed that testing for long!term
retention of a skill can also be useful to measure the
subjects| level of automatization of that behavior\ as per!
formance on tasks that are well learned are less likely to
deteriorate due to the simple passage of time 49\ 42\ 78[
In the present study\ these two approaches were used to
determine whether the de_cit seen in Doyon et al[ 19 in
PD patients with a bilateral striatal dysfunction and in
patients with a cerebellar lesion\ was indeed due to a
di.culty in automatizing a sequence of well!learned
movements[ It is important to note that the data in the
dual!task condition were gathered concomitantly with
those reported in the skill learning study 19[
Experiment 0] Automatization of a Visuomotor Skill
Assessed Using a Dual!Task Paradigm
In our previous study 19\ the impairment in learning
the repeating sequence after a bilateral striatal dys!
function or damage to the cerebellum was observed only
 J[ Doyon et al[:Automatization of a visuomotor skill
in late phase of the acquisition process[ Furthermore\
the de_cit in these two groups was not related to other
confounding factors "e[g[ mood disturbance\ motor de_!
cit\ or cognitive deterioration#[ The present experiment
was thus designed to examine whether the learning
impairment was due to a lack of automatization of the
sequence of _nger movements using a dual!task para!
digm[ The performance of the same groups of patients
with Parkinson|s disease\ with a cerebellar lesion\ or with
damage circumscribed to the frontal lobes who par!
ticipated in the study by Doyon et al[ 19\ was compared
to that of their matched control subjects on the Brooks|
Matrices test 09 "i[e[ secondary task#\ as they were per!
forming concomitantly the Repeated Sequence Test "i[e[
primary task#[ These two tasks were administered twice]
First\ at the beginning "i[e[ early learning stage# after
subjects had been exposed 39 times "Session 0# to the
repeating sequence^ and second\ at the end "late learning
stage# after they had been given 139 repetitions of the
sequence and thus had achieved high pro_ciency on this
new skill "Session 5#[
The automatization phase of a skill constitutes a stage
during which the pattern of responses is consolidated
and the processing resources necessary to execute other
cognitive tasks become increasingly available with prac!
tice 4[ It was thus predicted that only the groups of
patients who showed a learning impairment in late phase
of the learning process "PD patients in Stages 12 of the
disease and those with a lesion to the cerebellum\ 19#\
would not demonstrate a signi_cant improvement in per!
formance across the six training sessions on the Brooks|
Matrices Test 01[ We also expected that such impair!
ment would be due to a reduced level of cognitive
resources available to perform the matrices "i[e[ sec!
ondary task# because of a lack of automatization of the
sequence of movements "i[e[ primary task#[
Method
Subjects
Three groups of patients and of normal control subjects were
tested in this dual!task condition "Table 0#[ All of the patients
were recruited via the Departments of Neurological Sciences
and Neuroradiology at the Enfant!Jesus Hospital in Quebec\
Canada[ By contrast\ the normal control subjects were either
acquaintances of the experimenters or volunteers from the com!
munity[ The patients in each clinical group were screened using
a basic neuropsychological evaluation in order to exclude those
showing signs of depression or dementia 19[ All subjects gave
informed written consent for their participation in this experi!
ment[ This study was approved by the Ethics Review Board of
the Hopital de l|Enfant!Jesus\ Quebec\ Canada[
Parkinson|s disease `roup "PD#[ This group was composed of
00 patients who had received a diagnosis of idiopathic Par!
kinson|s disease "PD# "Table 0#[ They were divided into two
subgroups based on the severity of the disease using Hoehn and
Yahr|s scale 30] Stage 0 "n  5#^ Stages 12 "n  4#[ When
prescribed\ patients were taking optimal levels of levodopa
medication at the time of testing[ Patients with drug!induced
516
Parkinsonism\ multiple system atrophy\ cerebro!vascular
disease\ epilepsy\ history of alcoholism\ head injury or tumor\
cerebellar disturbances\ or with disproportionate oculomotor
and autonomic dysfunction were excluded from this study[
Cerebellar `roup "CE#[ A group of 00 patients with a radio!
logically!documented lesion in the cerebellum was also tested[
Eight of them had damage restricted to the cerebellum proper\
whilst the rest had lesions extending into the brain stem or
spinal cord[ All of these patients had dysarthria\ ataxia and
dysmetria\ although the severity of these cerebellar signs
di}ered between patients[
Frontal!lobe `roup "FL#[ A heterogeneous group of nine pat!
ients with damage circumscribed to the frontal cortex was also
seen[ There were 4 patients with left!sided lesions\ 1 with right!
sided lesions and 1 with bilateral lesions "Table 0#[
Normal!control `roups "NC#[ Three separate groups of
healthy control subjects were included to match the clinical
groups with respect to sex distribution\ mean age and mean
level of education "Table 0#[ Thus\ groups of 8\ 00 and 03
subjects were used as controls for the patients with PD\ with a
cerebellar lesion or with damage to the frontal cortex\ respec!
tively[ None of the control subjects had any positive history of
a psychiatric or neurological disorder[
Materials and procedure
Experimental tasks
The subjects| levels of processing resources available while
executing the visuomotor sequence at di}erent stages of the
learning process was measured with a dual!task paradigm using
a version of the Repeated Sequence Test as the primary task
and the Brooks Matrices Test 01 as the secondary task[
Primary task
This task consisted of a short version of the same Repeated
Sequence Test that was used in the skill learning aspect of the
study 19[ Brie~y\ this test was administered using a response
box that has four identical lights "stimuli# and four buttons\
one below "0[64 cm# each light[ The lights and buttons were
arranged horizontally at equidistance from one another[ This
box was connected to an IBM PC computer that controlled
stimulus presentation and recorded the two measures of interest
for this task] i[e[ the subject|s reaction time and accuracy on
each trial "Fig[ 0#[
The subjects were instructed to use the middle and index
_ngers of each hand\ and to keep one _nger on each of the four
keys[ They were asked to press the button corresponding to the
light that was illuminated as quickly as possible\ while making
as few errors as possible[ The stimulus remained displayed until
the subject made a response[ After the response\ the light went
o} and was immediately followed 499 ms later by the display
of another stimulus[ The location of the stimuli was pro!
grammed in a speci_c sequence of 09 positions[ Hence\ if one
were to designate the four possible locations as 0\ 1\ 2 and 3
from left to right\ the sequence was the following] 3!1!2!0!2!1!
3!2!1!0[ In this dual!task condition\ each block of trials was
composed of three continuous repetitions of this 09!item
sequence without any pause between them\ so that each block
appeared as a continuous series of 29 trials[ The subjects were
not informed of the presence of the repeating sequence\ nor did
they receive feedback concerning the latencies or accuracy of
their responses[
517 J[ Doyon et al[:Automatization of a visuomotor skill

Table 0[ Subjects characteristics

PD NC Cerebellar NC Frontal NC
Group "n  00# "n  8# "n  00# "n  00# "n  8# "n  03#

Age] Mean years "S[D[# 43[7 "5[2# 42[6 "3[6# 24[5 "7[7# 27[6 "00[5# 39[8 "06[0# 35[2 "00[9#
Education] Mean years "S[D[# 02[9 "4[0# 02[6 "1[8# 01[4 "2[2# 02[6 "2[0# 00[2 "2[3# 02[5 "2[0#
Sex "female:male#] 5:4 3:4 7:2 3:6 3:4 6:6
Diagnostic] VCA] 1 Vasc[ malf[] 1
OPCA] 0 Astrocytoma] 1
CA] 5 Meningioma] 2
SP] 1 Kystic lesion] 0
Abcess] 0

Stage of the disease0 I] 5

II] 1
III] 2

Duration of the disease] 94 years] 2 94 years] 5

509 years] 1 509 years] 4
0010 years] 5

Side of lesion Left] 1 Left] 0 Left] 4

Right] 2 Right] 0 Right] 1
Bilateral] 5 Bilateral] 8 Bilateral] 1

Site of lesion Orbitofrontal] 2

Dorsomedial] 0
Dorsolateral] 4

Medication L!Dopa] 00
Anticholiner!
gics
Artane] 2
Cogentin] 0
Parsitan] 2

VCA] Vascular cerebellar accident^ OPCA] Olivo!ponto!cerebellar atrophy^ CA] Cerebellar atrophy^ SP] Spino cerebellar atrophy^
Vasc[ malf[] Vascular malformation[
0
Source] Hoehn + Yahr|s Scale "0856#[

Secondary task

The Brooks Matrices Test was used as the secondary task in

Fig[ 0[ Diagram illustrating the materials used and a rep!
resentative experimental trial in the dual!task performance situ!
ation[
order to interfere with the visuospatial processing that is elicited
while executing the repeating visuomotor sequence[ In this test\
subjects were required to keep in mind a visuospatial pattern
made of _ve digits in a 33 matrix\ the location of each digit
being dependent upon auditory instructions that were com!
municated to them via a cassette player "Fig[ 0#[ They were _rst
asked to follow directives\ which instructed them to always
place the _rst digit in the same {{Starting|| box "1nd row\ 1nd
column of the matrix# and to position the remaining four digits
in separate\ but connecting boxes[ Following completion of a
trial\ subjects were given a template on which a matrix was
illustrated and were then required to indicate the location
of the _ve digits from memory[ A di}erent set of auditory
instructions representing a unique visuospatial pattern of digits
was administered on each experimental trial[ The dependent
measure of interest was the number of directional movements
per matrix that were correctly reproduced based on the auditory
instructions[ A total of 05 di}erent sets of instructions were
recorded and were divided into two groups "A and B#\ which
were administered on separate occasions "see Experimental
design#[
Before the dual!task session began\ the subjects were given
 J[ Doyon et al[:Automatization of a visuomotor skill
appropriate instructions and a number of practice trials to
familiarize themselves with the Brooks| matrices task[ First\
two trials were given in which a template of the matrix was
placed in view of the subjects who were required to write down
the digits in the appropriate boxes at the same time as they were
hearing the instructions[ Second\ two other practice trials were
administered in which a template was again placed in view of
the subjects who were now asked to wait until the end of the
auditory instructions before writing the digits in the appropriate
boxes[ Finally\ _ve additional trials were given in which the
subjects were required to wait until the end of the auditory
instructions before writing the digits in the boxes[ This time\
however\ the template was hidden from the subjects view during
the instructions[ Performance in the latter condition was used
as a control measure of the subjects| ability to perform the
Brooks| Matrices Test 01 alone[
Experimental design
Both the primary and the secondary tasks were administered
concurrently in two separate testing sessions\ which were held
after subjects were given either 39 or 139 repetitions of the 09!
item repeating sequence "i[e[ after Sessions 0 and 5 in the pre!
vious skill learning study 19#[ On each experimental trial\ they
were asked to execute a block of 29 trials with the repeating
sequence task\ at the same time as they were completing a
matrix[ Eight experimental trials were administered in both
testing sessions[ Finally\ the order of presentation of the two
groups of instructions "A and B# was counterbalanced within
each group of subjects[
Results
The results of the primary and secondary tasks were
analysed using mixed!design analyses of variance "ANO!
VA|s# for repeated measures[ These analyses were con!
ducted comparing the performance of each clinical group
"or subgroup in the case of the PD patients# to that of
their respective group of normal control subjects[ When
necessary\ post hoc comparisons were performed using
the NewmanKeuls procedure[
Primary task
Accuracy[ Subjects in the three clinical and control
groups were very accurate on this task\ the mean number
of correct responses per sequence "max  09# ranging
from 7[788[89[ Results of separate ANOVA|s revealed
that all the patients| groups made signi_cantly more
errors than their respective groups of control subjects
"PD] F"1\06#  3[61\ P 9[94^ CE] F"0\19#  05[16\
P 9[990^ FL] F"0\10# 05[1\ P 9[990#[ Although the
Group main e}ect was signi_cant for the PD patients\
the results of post!hoc comparisons conducted on the
data of each subgroup of PD patients did not reach
signi_cance[ The only other signi_cant main e}ect was
that of Session in the analysis with the CE group and
their controls\ indicating that these subjects were overall
more accurate on Session 5 than on Session 0[ None of
518
the double\ nor of the triple interactions were signi_cant[
The latter _ndings suggest that patients and control sub!
jects did not di}er in their pattern of correct responses[
Reaction time[ Figure 1a\ 1c and 1e illustrate the geo!
metric mean RT of all subjects| groups for the two exper!
imental conditions "single vs dual tasks# in Sessions 0 and
5[ Note that Fig[ 1a shows the performance of the two
subgroups of patients with PD and their matched control
group "so that it is possible to compare with the results
obtained on the secondary task#\ but that the statistical
analysis was performed using the data from the entire
group of PD patients[ The reaction times of all subjects
were transformed to logarithms to reduce skewness in the
distribution and the subsequent ANOVA|s were per!
formed using this transformation[ These analyses
revealed a main e}ect of Group for the cerebellar!control
comparison only "F"0\19#  03[4\ P 9[990#[ Highly sig!
ni_cant e}ects of practice and of experimental condition
were obtained in the three analyses\ all subjects being
faster on Session 5 than on Session 0\ while being slower
in the dual than in the single task condition "Session] PD\
F"0\06#  57[7\ P 9[9990^ CE\ F"0\19#  44[5\
P 9[9990^ FL\ F"0\10#  67[4\ P 9[9990^ Condition]
PD\ F"0\06#  099[86\ P 9[9990^ CE\ F"0\19#  156[5\
P 9[9990^ FL\ F"0\10#  134[6\ P 9[9990#[ Except for
a SessionGroup and a ConditionGroup interaction
in the comparison involving the CE group\ all of the
other double and triple interactions did not approach
signi_cance[ These results suggest that\ in general\ the
performance of the subjects| groups was a}ected similarly
by dual!task condition in both testing sessions[
Secondary task[ The results of separate ANOVA|s for
repeated measures on the number of directional move!
ments correctly reproduced "Fig[ 1b\ 1d and 1f# revealed
that PD patients "F"1\06#  2[89\ P 9[94# and those
with a cerebellar lesion "F"0\19#  8[62\ P 9[90# made
signi_cantly more errors on this test than their controls[
In addition\ a signi_cant main e}ect of Session was
observed in the comparisons between the PD\ CE and FL
groups and their controls "PD] F"1\06#  4[63\ P 9[94^
CE] F"0\19#  7[38\ P 9[90^ FL\ F"0\10#  38[13\
P 9[9990#\ indicating that subjects in these groups
improved their performance from Session 0 to Session 5[
More importantly and as predicted\ however\ a sig!
ni_cant GroupSession interaction was obtained for
both PD and CE groups "PD] F"1\06#  4[61\ P 9[91^
CE] F"0\19#  02[95\ P 9[90#\ but not for the FL group[
Subsequent analyses comparing the performance of each
subgroup of PD patients to the normal control subjects
with a repeated!measures ANOVA yielded a signi_cant
interaction for the patients in Stages 12 of the disease
only "F"0\01#  7[06\ P 9[91#[ Further analyses
revealed that the de_cit observed in the groups of patients
with PD "Stages 12#\ or with damage to the cerebellum\
in the secondary task could not be due to an inability to
perform the Brooks| Matrices Test for two reasons[ First\
there was no di}erence in performance between the clini!
cal groups and their respective groups of control subjects
529 J[ Doyon et al[:Automatization of a visuomotor skill

Fig[ 1[ Results of the subjects| groups for the Repeated Sequence Test "primary task# "a\ c\ e# and the Brooks Matrices Test "secondary
task# "b\ d\ f #[ The data points in the single condition of the primary task correspond to the mean reaction times of Blocks of trials
0 and 3 that were administered in Session 0 and 5 of the skill learning study 19[
 J[ Doyon et al[:Automatization of a visuomotor skill
with respect to the number of directional movements
reproduced in the _ve matrices that were used in the
introduction session to control for the subjects| ability to
perform the Brooks| Matrices Test when administered
alone "PD] F"1\06#  1[94\ P  9[05^ CE] F"0\19#  1[34\
P  9[02^ FL] F"0\10#  9[93\ P  9[74#[ Second\ no sig!
ni_cant group di}erence was obtained "using a one!way
ANOVA# when they were compared on Session 0 only\
"PD] F"1\06#  9[12\ P  9[68^ CE] F"0\19#  1[35\
P  9[02^ FL] F"0\10#  0[87\ P  9[85#\ suggesting that
the level of performance of the patients did not di}er
from that of the controls when they were _rst tested in
the dual!task condition[ Also\ the latter _nding suggest
that the patients had a similar level of cognitive resources
available to perform the secondary task at the beginning
of learning[
Discussion
The results of the three clinical groups on the primary
task indicate that\ overall\ patients did not di}er from the
control subjects in their ability to execute the repeating
sequence when another visuo!spatial task was intro!
duced[ Each group showed a signi_cant e}ect of
condition\ as they were much slower to respond in the
dual!task than in the single!task condition[ In addition\
this di}erence in performance was still evident on Session
5[ This suggests that\ even after 139 repetitions of the
embedded sequence\ the patients and control subjects had
not achieved complete automatization of the sequence of
movements and thus that they were still in the pro!
ceduralization process 4[ Such a _nding is consistent
with the elegant work of Karni et al[ and his colleagues
35\ 36 who have shown that healthy control subjects
could only reach asymptotic performance of a simple 4!
item sequence of _nger movements after 3 weeks of daily
practice "0419 min:day#[ More importantly\ however\
the fact that performance of the patients| groups in the
dual!task condition did not di}er from that of their mat!
ched control subjects\ suggests that the divergence in the
results on the secondary task observed in the PD Stages
12 and the cerebellar groups cannot be due to a di}er!
ence in the way subjects were performing the repeating
sequence task[
By contrast\ the results of the present study dem!
onstrate that\ as predicted\ patients in Stages 12 of PD
or with damage to the cerebellum\ but not those with a
frontal!lobe lesion\ were impaired on the Brook|s Matr!
ices Test 01[ Further analyses showed that this de_cit
did not result from an incapacity to perform the matrices
per se\ because the performance of patients in both PD
and CE groups did not di}er from that of their respective
groups of control subjects\ both when this task was
administered alone in the practice session and when it
was _rst given in a dual!task condition "Session 0#[ Fur!
thermore\ such an impairment could not be due to a
di.culty in attentional capacities\ as the performance of
520
the clinical and control groups on Brooks| matrices did
not di}er on Session 0[ If a de_cit in dividing attention
following a bilateral striatal dysfunction or damage to
the cerebellum was the source of impairment on the sec!
ondary task\ di.culties should have been observed\ not
only on Session 5\ but on Session 0 as well[ Instead\ the
fact that only patients in advanced stages of PD and in
the CE group did not improve on Session 5 "i[e[ after 139
presentations of the 09!item sequence 19#\ suggests that
they did not have the same level of cognitive resources to
devote to performing the matrices[ It is important to note
that this impairment was observed in the same groups of
patients who showed a learning impairment in late phases
of the acquisition process of the repeating visuomotor
sequence in our parallel study 19[ Together\ these results
support the hypothesis that the impairment reported by
Doyon et al[ 19 in acquiring such a visuomotor skill
after damage to the striatum or the cerebellum was due
to a lack of automatization of the repeated sequence of
_nger movements in late "slow# learning phase 35\ 36[
Such a de_cit can be conceptualized as an inability
to combine the di}erent _nger movements into a single
integrated unit with extended practice and thus\ the pre!
sent _ndings suggest that both the striatum and the cer!
ebellum contribute to the automatization of this co!
articulation process[ This does not mean\ however\ that
the impairment following damage to these structures
results from the same underlying information processing
mechanisms[ Indeed\ Laforce and Doyon 40 have
recently demonstrated a double functional dissociation
between the striatum and the cerebellum and have sug!
gested that the striatum plays a critical role in per!
ceptivomotor learning mechanisms based on stimulus!
response types of associations\ whereas the cerebellum is
preferentially involved in the ability to integrate separate
movements into a ~uid sequence[ Thus\ although similar\
the de_cit observed following damage to both structures
would suggest that the impairment in automatizing the
sequence of _nger movements could be due to di}erent
cognitive processes[
The notion that the striatum and the cerebellum are
involved in the automatization phase of a visuomotor
skill is consistent with several functional imaging studies
with PET and fMRI\ in which a change in hemodynamic
responses in both of these structures have been associated
with the learning of a repeating sequence of movements
using a very similar paradigm 08\ 10\ 14\ 33\ 65\ 74[ This
is also in accord with single!cell recording experiments in
the striatum and the cerebellum 8\ 02\ 22\ 71\ 85\ which
have demonstrated the existence of highly speci_c _ring
patterns during the learning of a motor skill[ Indeed\ the
hypothesized role of the striatum in the automatization
process is reminiscent of the work by Shultz et al[ 71
who have described a decrease in the sensitivity of dopa!
minergic brain stem neurons to rewarding stimuli as the
animal becomes over!trained on a conditioning para!
digm[ This is also consistent with the studies by Graybiel
et al[ 23 who have demonstrated in the striatum the
521 J[ Doyon et al[:Automatization of a visuomotor skill

Fig[ 2[ Results of the subjects| groups on each block of trials of the Repeated Sequence Test in both Session 5 of training and the
retention session[ The data points in Session 5 correspond to the mean reaction times of Blocks of trials 03 that were administered
in Doyon et al[ 19[
 J[ Doyon et al[:Automatization of a visuomotor skill
existence of tonically active neurons that begin to signal
rewarding stimuli only as a conditioning task becomes
well!learned[ The proposal that the cerebellum par!
ticipates as well in the automatization phase of learning
is supported by a recent study by Bloedel et al[ 00
who recorded the modulation of multiple single neurons
located in the di}erent cerebellar nuclei as cats were learn!
ing to move a manipulandun through a groove maze[
These authors found a signi_cant increase in amplitude
of the cells| response\ which was correlated with an
improvement of the cat|s performance on the task[ They
suggested that the cerebellum is involved actively in the
incremental acquisition of a motor skill\ especially in
the process during which the strategy for performing a
learned movement becomes established[
Patients with frontal!lobe lesions did not di}er in per!
formance from their group of control subjects in both
primary and secondary tasks[ Further qualitative analy!
ses of the performance of the individual patients within
this group did not reveal any di}erence in the pattern of
results when the e}ect of side or site of lesion "i[e[ dividing
the patients into those who had damage in the dorso!
lateral\ orbitofrontal or medial region of the frontal
lobes# was analysed[ These results\ together with the fact
that the same patients did not reveal any learning impair!
ment of the repeating sequence in the skill learning aspect
of the study 19\ implies that the frontal cortex does not
play a signi_cant role in the acquisition of a visuomotor
sequence\ nor in its automatization phase[ There is ample
evidence which suggests\ however\ that the frontal lobe\ in
particular\ the primary motor cortex\ the lateral premotor
regions and supplementary motor areas\ contributes to
the learning and production of willed sequences of actions
0\ 18\ 3436\ 61\ 83\ 84\ 86[ Consequently\ the apparent
discrepancy between the latter results and our _ndings
may simply be explained by the fact that the patients in
this group had lesions that did not encroach on these
motor cortical regions[
Experiment 1] Automatization of a Visuomotor Skill
Assessed by Testing for Long!Term Retention
The results of Experiment 0 suggest that the learning
impairment reported by Doyon et al[ 19 following a
bilateral striatal dysfunction\ or a lesion to the cerebel!
lum\ could be due to a di.culty in automatizing the
repeating sequence of movements[ In the present study\
the {{automatization hypothesis|| was tested again\ but
with a di}erent theoretical approach[ Instead of using a
dual!task paradigm\ we sought to determine\ for the _rst
time\ whether damage to the striatum and the cerebellum
impairs the long!term retention of a repeated visuomotor
sequence[ Patients with either Parkinson|s disease\ or
with damage involving the cerebellum or the frontal cor!
tex and their respective groups of normal control subjects\
were retested once 705 months later on the same
Repeated Sequence Test[ The subjects were given four
522
blocks of 099 trials followed by the administration of two
tests "a short questionnaire and a self!generation task#
that measured the subject|s declarative knowledge of the
sequence[ It was predicted that the groups of patients who
showed a learning de_cit late in the acquisition process\
possibly because of a lack of automatization of the
sequence of movements "i[e[ patients in Stages 12 of PD
or with a cerebellar lesion#\ would exhibit an impairment
in long!term retention of this visuomotor skill[ By
contrast\ the performance of the clinical groups on the
declarative memory tests would not di}er from their con!
trol subjects[
Method
Subjects
Three groups of patients and of normal control subjects were
included "Table 1#[ These subjects had participated in the skill
learning study 19 and in Experiment 0 with the dual!task
condition[ Again\ all subjects gave informed\ written consent
for their participation in this experiment\ which was approved
by the Ethics Review Board of the Hopital de l|Enfant!Jesus\
Quebec city[
Parkinson|s disease `roup "PD#[ This group consisted of 04
patients who had received a diagnosis of idiopathic Parkinson|s
disease "Table 1#[ At the time of testing for retention\ subgroups
composed of 2 and 6 PD patients\ did not show any sign of a
signi_cant clinical deterioration and thus were still considered
to be\ respectively\ in Stage 0 and Stages 12 of the disease[ By
contrast\ _ve patients had changed from Stage 0 to Stage 1
"called PDCS# during the approximate one!year delay period[
It is important to note that the clinical status of the PD patients
who showed a motor deterioration during the delay and those
who did not\ was assessed by a neurologist "Dr P[ J[ Bedard#
associated with our research team using the Hoehn and Yahr|s
scale 30[ On average\ these patients were tested 01[0 months
"S[D[  9[5# after the last training session in the skill learning
study 19[ Again\ when prescribed\ patients were taking optimal
levels of levodopa medication at the time of testing[ Patients
with drug!induced Parkinsonism\ multiple system atrophy\ cer!
ebro!vascular disease\ epilepsy\ history of alcoholism\ head
injury or tumour\ cerebellar disturbances\ or with dis!
proportionate oculomotor and autonomic dysfunction\ were
also excluded from the present experiment[
Cerebellar `roup "CE#[ Twelve patients with a radiologically!
documented lesion in the cerebellum were also tested "Table 1#[
Eight of them had damage restricted to the cerebellum proper\
whilst the rest had lesions extending into the brain stem or the
spinal cord[ All of these patients had dysarthria\ ataxia and
dysmetria\ although the severity of these cerebellar signs
di}ered between patients[ They were retested on average 02[1
months "S[D[] 1[1# after the last training session[
Frontal!lobe `roup "FL#[ A group of 7 patients with di}erent
etiologies\ but whose damage was nevertheless circumscribed
to the frontal cortex\ were also seen "Table 1#[ There were 3
patients with left!sided lesions\ 1 with right!sided lesions and 1
with bilateral lesions[ This group was seen on average 09[4
months "S[D[  9[7# after the last practice session[
Normal control `roups "NC#[ A total of 27 normal control
subjects were also included in this study[ They were subdivided
into three groups to match the clinical groups with respect to
sex distribution\ mean age and mean level of education "Table
1#[ The delay between the training and the retention sessions
ranged\ on average\ from 00[702[4 months[
523 J[ Doyon et al[:Automatization of a visuomotor skill

Table 1[ Subjects characteristics

PD NC Cerebellar NC Frontal NC
Group "n  04# "n  04# "n  01# "n  01# "n  7# "n  00#

Age] Mean years "S[D[# 45[6 "5[6# 43[2 "7[0# 26[2 "09[2# 39[1 "02[2# 27[8 "05[4# 39[8 "03[5#
Education] Mean years "S[D[# 02[4 "3[5# 01[8 "1[7# 01[4 "2[5# 02[2 "1[5# 00[2 "2[3# 02[5 "2[0#
Sex "female:male# 6:7 7:6 7:3 6:4 3:3 5:4
Delay between training and 01[0 "9[5# 02[4 "2[2# 02[1 "1[1# 01[0 "0[5# 09[4 "9[7# 00[7 "1[2#
retention in months "S[D[#

Diagnostic VCA] 1 Vasc[ Malf[] 1

OPCA] 0 Astrocytoma] 1
CA] 5 Meningioma] 1
CACGP] 0 Kystic lesion] 0
SP] 1 Abcess] 0

Stage of the disease0 I] 2

IIIII] 01

Duration of the disease 94 years] 94 years] 6

509 years] 2 509 years] 4
0010 years] 7

Side of lesion Left] 0 Left] 0 Left] 3

Right] 1 Right] 0 Right] 1
Bilateral] 01 Bilateral] 09 Bilateral] 1

Site of lesion Orbitofrontal] 2

Dorsomedial] 0
Dorsolateral] 4

Medication L!Dopa] 04
Anticholiner!
gics
Artane] 3
Cogentin] 0
Parsitan] 2

VCA] Vascular cerebral accident^ OPCA] Olivo!ponto!cerebellar atrophy^ CA] Cerebellar atrophy^ CACGP] Cerebellar atrophy
with calci_cations of the globus pallidus^ SP] Spinocerebollar atrophy^ Vasc[ Malf[] Vascular malformation[
0
Source Hoehn + Yahr|s Scale "0856#[

Experimental tasks
The subjects| levels of retention of a visuomotor skill was
assessed using an identical version of the Repeated Sequence
Test to that used by Doyon and colleagues 19\ whereas their
declarative knowledge of the sequence was measured with a
short questionnaire and a self!generated task[
Repeated sequence test] visuomotor skill learnin`[ The material
was the same as described in Experiment 0[ In this task\ the
subjects were again required to use the middle and index _ngers
of each hand and to keep one _nger on each of the four keys[
They were asked to press the button corresponding to the light
that was illuminated as quickly as possible\ while making as
few errors as possible[ The same sequence used by Doyon et al[
19 was repeated again[ The subjects were given four exper!
imental blocks of trials in a single retention session[ A short
period of rest "89 s# was allowed between each block of trials[
Repeated sequence test] declarative memory tasks[ Following
the last experimental block of trials of the Repeated Sequence
Test\ the subjects| declarative knowledge of the sequence was
assessed in two ways[ First\ they were asked to complete a short
questionnaire that comprised the following three questions] "a#
Did you notice anything about the task<\ "b# Did you ever
notice any pattern or sequence< and "c# What was the sequence<
Subjects were given one point per positive response "total  2
points# on Questions 0 and 1 and were given an additional point
only if they were able to reproduce the entire sequence of 09
stimuli in the right order[ Second\ they were required to com!
plete two blocks of 099 trials in a self!generated sequence task[
In the latter task\ subjects were told that\ instead of pressing
the button below the light that was illuminated\ they now had
to press the button corresponding to where they thought the
next stimulus should appear in the sequence[ In this task\ accu!
racy was more important than speed[ Again\ a rest period of 89
s separated the two blocks of trials[
These two tests were always administered after the subjects
had completed four blocks of trials in the repeated sequence
condition in order to warranty that the primary measure of
interest in this study "i[e[ the long!term retention of the skill#
would not be in~uenced by the fact that subjects were reac!
quainted with the sequence during the declarative memory
tasks[
 J[ Doyon et al[:Automatization of a visuomotor skill
Results
The dependent variables of interest in the present
experiment were the mean number of correct responses
and reaction time for the skill learning aspect of the
Repeated Sequence Test\ as well as the mean number of
accurate responses on the two tests measuring the level
of declarative knowledge of the sequence[
Repeated sequence test] visuomotor skill learning
Long!term retention for the repeating sequence was
assessed using three di}erent measures[ First\ subjects|
performance taken from the four blocks of trials in Ses!
sion 5 of training 19 was compared to that of the four
blocks of trials in the retention session "S5!R#[ Second\
data from Session 5 of learning were compared to those
of the _rst block of trials from the retention session "S5!
R[B0#[ Finally\ the results of the fourth block of trials
from the training session were compared to those of the
_rst block from the retention session "S5[B3!R[B0#[ For
each of these indices\ separate analyses of variance
"ANOVA|s# for repeated measures were conducted con!
trasting the results of each clinical group to that of their
respective groups of normal control subjects[ As for the
PD patients\ the analyses were _rst performed using the
data from each subgroup "Stage 0\ n  2\ Stages 12\
n  01# as they were evaluated clinically at the time
of the retention session[ Subsequent analyses using the
results of the _ve patients who changed from Stage 0 to
1 "PDCS# within the one!year delay period were also
carried out in order to examine the e}ects of further
nigrostriatal degeneration on retention of the visuomotor
skill[ However\ only the results of the statistical analyses
comparing the latter subgroup of PD patients to the
group of control subjects are reported in Table 2 and
Figure 2\ as they were the only subgroup who dem!
onstrated a signi_cant di}erent pattern of retention[
Three di}erent "instead of a single# measures of retention
were used to show that the results were robust and not
only a re~ection of the type of retention indices employed[
Accuracy[ Overall\ the subjects in this study were very
accurate\ the mean number of correct responses within a
sequence "max[  09# ranging from 7[68[6[ When the
PD patients who stayed in either Stage 0 or Stages 12
during the delay period were _rst compared\ the analyses
on each of the dependent measures taken separately
revealed main e}ects of Group "S5!R] F"0\14#  00[49\
P 9[90^ S5!R[B0] F"0\14#  09[54\ P 9[90^ S5[B3!
R[B0] F"0\14#  8[28\ P 9[90# and Session "S5!R[B0]
F"0\14#  4[81\ P 9[94^ S5[B3!R[B0] F"0\14#  4[80\
P 9[94# for those in the more advanced group only[
However\ there were no signi_cant GroupSession
interaction for either group on the dependent measures\
suggesting that the PD patients did not di}er from con!
trols in the number of errors made over time[ Also\ as
reported in Table 2\ comparisons of the PDCS\ CE and
524
FL groups with the control subjects revealed that they
did not di}er with respect to their level of accuracy\ as a
unique main e}ect of Group and a single GroupSession
interaction were observed\ respectively\ using the S5!R
measure with the PDCS subgroup "F"0\07#  6[77\
P 9[94# and the S5[B3!R[B0 indices with the CE group
"F"0\11#  5[59\ P 9[94#[
Reaction time[ The analyses comparing the reaction
time data of the PD patients who stayed in Stage 0 or in
Stages 12 of the disease with those of the control group
"Fig[ 2 and Table 2# yielded only a highly signi_cant main
e}ect of Session\ which was seen independently of the
retention measure used "Stage 0] S5R] F"0\05#  33[61\
P 9[9990^ S5!R[B0] F"0\05#  34[83\ P 9[9990^
S5[B3!R[B0] F"0\05#  32[95\ P 9[9990^ Stages 1!2]
S5!R] F"0\14#  23[27\ P 9[9990^ S5!R[B0] F"0\14# 
45[95\ P 9[9990^ S5[B3!R[B0] F"0\14#  37[67\
P 9[9990#[ No signi_cant GroupSession interaction
was observed on either measure when the PD patients in
Stage 0 were compared to control subjects[ Although
the latter _ndings are consistent with our expectations
because these patients did not show a learning impair!
ment in the _rst place 19\ this lack of _ndings may
simply be due to the small sample size "n  2# in this
group[ Contrary to our prediction\ however\ the Group
x Session interaction never reached the level of sig!
ni_cance in the PD patients who were in Stages 12
"n  01# at the time of testing[
The results of the PDCS\ CE\ FL and their respective
groups of control subjects in the four blocks of trials for
both Session 5 of training and the retention session are
illustrated in Fig 2a2c\ whereas the outcomes of the
statistical analyses using the di}erent dependent mea!
sures of retention for each of the groups comparisons are
summarized in Table 2[ As shown in the latter table\ a
signi_cant main e}ect of Group was only seen in the
cerebellar group "S5!R] F"0\11#  08[76\ P 9[990^ S5!
R[B0] F"0\11#  05[71\ P 9[990^ S5[B3!R[B0]
F"0\11#  06[43\ P 9[990#\ suggesting that these pat!
ients were slower than controls to respond when per!
forming the sequence[ All subjects| groups "including the
FL group# were also signi_cantly slower to respond in
the retention session compared to the last training session
"PDCS] S5!R] F"0\07#  22[67\ P 9[9990^ S5!R[B0]
F"0\07#  75[16\ P 9[9990^ S5!B3!R!B0]
F"0\07#  84[46\ P 9[9990^ CE] S5!R] F"0\11#  24[78\
P 9[9990^ S5!R[B0] F"0\11#  53[97\ P 9[9990^
S5[B3!R[B0] F"0\11#  53[66\ P 9[9990^ FL] S5!R]
F"0\06#  00[51\ P 9[90^ S5!R[B0] F"0\06#  10[63\
P 9[990^ S5[B3!R[B0] F"0\06#  06[06\ P 9[990#[
Most importantly\ however\ signi_cant GroupSession
interactions were observed in both PDCS and CE com!
parisons "PDCS] S5[R] F"0\07#  3[68\ P 9[94^ S5!
R[B0] F"0\07#  09[4\ P 9[90^ S5[B3!R[B0]
F"0\07#  02[02\ P 9[90^ CE] S5!R] F"0\11#  5[52\
P 9[94^ S5!R[B0] F"0\11#\ P  9[9415#[ These inter!
actions were due to the fact that these patients showed a
greater deterioration in performance over time than their
525 J[ Doyon et al[:Automatization of a visuomotor skill

Table 2[ Summary of results of the statistical analyses com! Session\ nor any GroupSession interaction on either
paring clinical and normal control groups on the Repeated task "Table 3#[
Sequence Test

Comparison
Discussion
PDCS vs NC CE vs NC FL vs NC
Measure d[f["0\07# d[f["0\11# d[f["0\06# The main _ndings of this study are that\ compared to
Accuracy matched control subjects\ PD patients who changed from
S5!R G Stage 0 to Stage 1 of the disease "hence suggesting further
S5!R!B0 striatal degeneration#\ as well as those with damage to
S5[B3!R!B0 S S GS the cerebellum\ did not show as much retention of the
ability to produce the repeating visuomotor sequence\
Reaction time
S5!R S GS GS S approximately a year after they had been exposed to
GS extensive training of this skill[ Interestingly\ such an
S5!R[B0 S GS$ GS S impairment in the retention of this skill was observed in
GS% a group of patients who had developed a striatal dys!
S5[B3!R!B0 S GS GS S function that was similar to those "in the case of the PD
PDCS  subgroup of PD patients who changed from Stage 0 CS subgroup#\ or were the exact same patients "in the
to Stage 00 of the disease during the one!year delay period[ case of the CE group#\ who had previously demonstrated
CE  cerebellar group[ FL  frontal!lobe group[ NC  nor! a learning de_cit in late phase of the acquisition process
mal control group[ S5FS1 last training session from our 19[ Thus\ similarly to the declarative memory system
previous study[ S5[B3  fourth block of trials in Session 5[ that is critical for both explicit learning and long!term
R  retention session[ R[B0  _rst block of trials in the reten!
tion session[ G  main e}ect of group[ S  main e}ect of retention of information\ these results suggest that the
session[ GS  interaction groupsession DF  degree of striatum and the cerebellum are not only critical for the
freedom[ acquisition of a visuomotor sequence\ but that they may
 P 9[94\  P 9[90\  P 9[990\ %P  9[9415\ also play a role in the neuronal mechanism subserving
$ P  9[9460[ long!term retention of such a skill[ Indeed\ the present
_ndings suggest that damage to these two structures
would disrupt the consolidation of visuomotor skilled
behaviors and the development of further long!term rep!
respective groups of control subjects "Figs 2a2c#[ Inter! resentational changes that can occur in both motor cort!
estingly\ such interactions were also observed for all of ical and subcortical structures with extended practice[
the di}erent types of retention measures\ except for the The latter notion is in accord with that of Gabrieli et al[
S5[B3!R[B0 measure in the CE vs NC comparison which 15 who proposed that the striatum and the cerebellum
failed to reach the level of signi_cance[ participate to the learning of visuomotor skills\ but that
Subsequent analyses comparing the subjects| per! the long!term representation of this skill would be located
formance on Session 5 vs the last block of trials on the at a cortical level and not within those structures[ This is
retention session "S5!R[B3# were also performed in other also consistent with a slightly di}erent idea proposed by
to verify that the loss in speed seen on Block 0 of the Doyon 08 who suggested that both the striatum and the
retention session was caused by a de_ciency in retention cerebellum play a critical role in the automatization phase
of the skill rather than by a general slowing of response[ of learning of a skill\ but when normal control subjects
The results of all the group comparisons did not reveal have learned an ability and have practiced it until it
any signi_cant e}ect of Group\ Session or Group! becomes automatic and overlearned\ the long!term {{neu!
Session\ suggesting that di}erence in performance in ral representation|| of that skill may then be mediated by
the retention session of the PDCS and CE groups was a distributed cortical and subcortical system involving
not due merely to a motor deterioration per se[ only the motor related regions "e[g[ M0\ SMA\ pre!
Repeated sequence test] declarative memory tasks[ motor# of the frontal lobe and the striatum\ but not the
Explicit knowledge of the sequence was assessed by com! cerebellum[
paring the mean number of correct answers on the short The results of this experiment contrast with those in which
questionnaire that were obtained in Session 5 of training intact retention of a visuomotor skill has been reported in
with that observed in the retention session using an amnesic patients with heterogeneous etiologies using either
ANOVA for repeated measures[ A similar type of a very similar version of the Repeated Sequence Test 37\
ANOVA for the self!generation task was also performed 57 or other skill learning tasks 06\ 07[ Amnesia in humans
using the mean number of accurate responses on the is known to be produced following bilateral damage to
second block of trials of the sixth training session "S5[B1#\ medial and diencephalic regions 48\ 80[ By contrast\ no
and those on Block 0 of the retention session "R[B0#[ The de_cit in skill retention is usually observed following lesions
results of all the comparisons between clinical and control to this neural system\ nor to the frontal lobes[ Thus\ the
groups did not reveal any signi_cant e}ect of Group or present _ndings reinforce the notion that the striatum and
 J[ Doyon et al[:Automatization of a visuomotor skill
Table 3[ Results of the declarative memory tasks in Session 5 of training and the retention session for all the subjects| groups on the
Repeated Sequence Test
PDCS NC
Group "n  4# "n  04#
Questionnaire "Mean:2 "S[D[##
Session 5 1[9 "9[5# 1[0 "9[5#
Retention 1[9 "9[5# 1[0 "9[4#
Self!generated test "Mean:09 "S[D[##
Session 5 5[8 "0[2# 6[0 "1[5#
Retention 5[5 "1[4# 5[1 "1[9#
the cerebellum are part of a separate neural network\ which
allows a sequence of movements "and possibly\ other skills
as well# to become rapid and automatic with practice\ as
well as to be maintained over long periods of time[
The fact that a retention impairment was found in the
PDCS group "the same patients who had showed normal
learning of the sequence in the skill learning study 19#\
suggests that further dysfunction of the nigro!striatal
pathway causes subjects to loose an ability over time[
This last _nding would suggest that the striatum does
not only contribute to the learning and retention of a
visuomotor skill\ but that it also constitutes a potentially
important cerebral station within which the motor pro!
grams necessary for executing a skill e.ciently could be
stored[ Although much conjectural\ such idea would be
consistent with animal work\ which has shown that stri!
atal neurons undergo changes in responsiveness during
incremental learning 02\ 22\ 23\ 71[
Considering that the level of retention of a skill may
constitute a measure of the degree of automatization of
that particular ability 49\ 42\ 78\ the present _ndings
support the idea that the striatum and the cerebellum are
implicated in this latter phase of learning[ Such interpret!
ation is in accord with the results of Experiment 0\ in
which we have demonstrated a de_cit in the auto!
matization of the same repeating visuomotor sequence
using a dual!task paradigm in the groups of patients with
PD "Stages 12# or with a cerebellar lesion[ This is also
consistent with a recent PET imaging study 10\ in which
we observed peaks of cerebral blood ~ow "CBF# activity
in both the ventral striatum and the cerebellum when the
repeating sequence was well learned\ whereas no focal
increase in CBF was seen when subjects were beginning
to learn a new sequence[
Finally\ no signi_cant di}erence between each of the
clinical group and their respective group of control sub!
jects was observed on the declarative memory tasks[
These results agrees with our own _ndings 19\ as well
as those from other studies 06\ 66\ in which a functional
dissociation between declarative and procedural memory
systems has been reported in similar groups of patients[
However\ the last _ndings must be taken with caution as
the declarative memory tests were always administered
526
Cerebellar NC Frontal NC
"n  01# "n  01# "n  7# "n  00#
0[7 "9[6# 0[7 "0[9# 0[5 "9[0# 0[8 "9[6#
1[0 "9[6# 1[2 "9[5# 0[7 "9[7# 1[1 "9[5#
4[7 "1[2# 5[8 "2[7# 5[6 "1[8# 6[8 "1[3#
5[6 "0[8# 4[7 "1[7# 6[9 "1[0# 6[9 "1[3#
after the subjects had terminated the four blocks of trials
in the repeating sequence condition[ It is thus possible
that the lack of di}erence between groups could be due
to the fact that the subjects| declarative knowledge of the
sequence was reactivated while performing the repeating
sequence[
Conclusion
To our knowledge\ the results of Experiment 0 with
the dual!task paradigm constitute the _rst demonstration
in clinical populations\ that an impairment in the
incremental learning of a visuomotor skill following a
dysfunction in the striatum or cerebellum may be due to
a di.culty in the automatization process of the skill using
a dual!task paradigm[ Together with _ndings from pre!
vious investigations\ which have demonstrated an impair!
ment in the early stages of skill acquisition on a variety
of tasks following damage to these two structures 19\ 11\
12\ 66\ the present results suggest that the striatum and
the cerebellum are involved in the automatization phase
of learning a motor sequence[
Finally\ intact retention of a variety of skills has often
been reported after variable delays in normal control
subjects and amnesic patients 1\ 05\ 15\ 37\ 52\ 57[ This
study\ however\ constitutes a _rst attempt to test for
retention of a visuomotor skill a year later in groups of
patients who had or had not shown a learning impairment
in the _rst place[ The present results extend those of our
previous studies and suggest that the striatum and the
cerebellum are engaged in neuronal mechanisms that will
allow a skill to be maintained in long!term memory[
Acknowled`ements*We would like to express our appreciation
to the patients and control subjects who participated in the
present experiment[ We would also like to thank Rhonda Amsel
for her statistical advice\ as well as Dr Morris Moscovitch\ Dr
Adrian M[ Owen\ Philip Jackson\ Martin La~eur and Marie!
Christine Ouellet for their comments on an earlier version of
this text[
This work served as partial ful_lment for the requirements
of a Ph[D[ degree to R[ Laforce Jr[ and a master degree to G[
527 J[ Doyon et al[:Automatization of a visuomotor skill
Bouchard and D[ Gaudreau[ This research was supported in
part by grants to Julien Doyon from the Natural Sciences and
Engineering Research Council OGPIN 901 and the {{Fond!
ation de l|Hopital de l|Enfant!Jesus||\ Quebec city\ Canada[
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