.lounrul ol rhe lntarnutionul i\taux4ts.rr'hologicul Stx iclr' (2004), 10. 647 654.
Copyright c 2004 INS. Pubiished by Cambridge Unir'crsiry Press. Prinled in the USA
DOI: 10. I 0l 7/S I l-556 I 7704 I 0501 8
Procedural and declarative memory
in obsessive-compulsive disorder
ROBI,RT M. ROTH.I.J JACIN'IHE tsARItsI,AU.2,1 DENISE MILOVAN.s.{ KIERON O'CONNOR.I
rx» CRISTO TODOROV'
rNeuropsychology PrÙgranr- I)!-partment ofl'sychiatry. Dartmouth Medical School, Lebanon, NH
:Laboratory oi Human Neuropsychology and Neurrrphysiology, Déparlemcnl de Psychologre, Unirersiti' Laval, Qucbec, Canada
rl)cparlnrcnl trf Psvchologv, C'oncordia Unircrsity'. \{ontrcal, Qucbec. Canada
rcentre dc Rccherche Fcmand Seguin. Hopital Louis-H. Lalbntainc, Montreal. Quebec. Canada
5Hopil;tl Louis-H. Lalirnlaine, Montl!'â1.
Quebcc" C'anada
(Rri( FrvFr) May 8. 20()-1; Rr:r'rsr.:o Oclober 29. 200]: Ac(-Êrpr Ft) Fcbruary 2, 2004)
Âbstract
Obsessivc-compulsivc disorder (OCD) has been associate<i with lrontostriatal abnormality. This has led to the
hypothesis that thc disordc-r is characterizcd by abnorrnality ofprocedural nrenrory. However, evidencc for either
procedural ordeclarative lrcrnory disturbance has been mixed, and ferv studies have dircctly assessed both ofthesc
fbnns ol'r.nenror-v- in thc sanre patient group. In thc present study. we assessed encoding and retrieval in declalative
r.rlcr.nory using the Rey Auditory Verbal Leaming Tesr ( RAVLT). and procedural Inelnory using the Pursuit Rotor
Task. in 27 adults q,ith OCD and 29 nralclied hcalthy controls. Groups did not dilfèr with respcct to salient
dernographic characteristics or nlenlory on lhe R,AVLT. ln contrast. patients with OCD pcrlbrmcd significantly
brlter than controls during thc early^ but not latcr trial blocks of the Pursuit Rotor Task. This pattern ol results
indicatcs intact encoding and retricval in declalative meurory. but abnorrnally enhanced procedural rnemory during
the early course of'learning in OCD. These findings uray be consistent rvith striatal overactivalion observed in
neuroinraging studics ofOCD, as well as lhe p«rnrinent role ofthe striatuur during early stages ofproceclural
lrrenrory. (J/^§. 2004. 10.611 654.)
Kcywords: OC'D. Procedural nreurory. Declarative nlcnlory. Striaturn
OCD has been associated witlr tiont«:striatal circuitry
abnonnality. Positron ernissioll tolllography ( PET) studies
have reported abnormally increased blood f'low in several
brain regions while patients were rcsting or during symp-
INTRODUCTION
Obsessive-compulsive disorder (OCD) is a neuropsychiat-
ric condition charactelized by intrusive, repetitive. and
unrvantcd thoughts that usually prornpt repetitive overt
tom provocation ( Rauch et al.. 200 I I Saxena & Rauch. 2000).
These r-egions have generally included the striatum (especially the caudate nucleus). orbitofrontal gyrus and other
fiontal lobe regions. thalarnus, and cingulate gyrus. Tteatment with selective serotonin reuptake inhibitors or behavioral therapy has been found to produce a nonnalization of
regional ovemctivation (Saxcna et al., 2001, 2002). Ciornputerized tornography and magnetic resorrance irnaging studies have reported structural abnormalities in striatum and
orbitofrontal gyrus. although inconsistently (Aylward et al.,
i996; Robinson ct al.. 1995; Rosenbcrg et al., 1997; Szcszko
ancl/or co'r,crt behaviors intcndcd to rcduce anxiety associated with the thoughts. Lifetirnc prcvalence rates for OCI)
range liom approximately one to three percent in the adult
population (tlebbinglon, 1998; Honvath & Weissrnan, 2000).
Thc disorder generally has its onset in childhood or adolescence, and is characterized by a chronic. rvaxing and waning course (Skoog & Skoog. 1999). Signiticantly reduced
quality of lit'c, as well as social, f-tunily and occupational
problerns are cornmon in OCD (Amir et a[.. 2000; Bystritsky
et al.. 2001).
Rcprinl rctlucrls to: Rohcrt
et
i, *,,t', *.n. n.,'.n".n","*t
al., 1999).
The presence of frontostriatal ciLcuitry abnorrnality sug-
Progranr. Departnrent of Psychiatry. Dartntouth \'lcdical School, One
\lcdical Cenler [)r'irc. [-ebanon. NH 0.1756-000 l. [-nrail: Robcrt.lv{.Rothiri
gests that patieuts with OCD nray dcrnonstrate pertbrmauce dcficits on procedural melllory tasks. Procedural
Darlnrtrrrth.ed u.
647
R.M. Roth et al.
648
lnclnory may be conccptualized as leanling without awarellcss and can be obserrvcd in the irnprovernent ofspeed and/or
accuracy ou tasks such as implicit seqtlerlce learning. rnirror rcading, probabilistic classitlcation, star mirror tracing.
or the Pursuit Rotor Task (Squire. 1986). lt should be noted
that procedural rnemory likely involvc's several processes,
as dernonstratcd by dissociations in perfortnance on dillèrcnt proccdural rncmory tasks u,ithin thc samc group of
'l
patiellts (Cabricli et al.. c)97). Nonethcless. uumerous studies using a variety oftasks have shorvn that aspects ofproccdural rncrrory are abnorrnal in patients rvith basal ganglia
dyslirnctiorr such as thosc rvith Tourette's syndrotne,
Parkinson's alld Huntington's diseasc. as lvcll as anitnals
rvith damage- to tl'ontostriatal circuitry ( Bylsma et al.. 19901
Gorncz Bcldarrain et al.. 1999; Hcindcl ct al., 19881 Miyachi ct al.. 2002: Packard & Krrorvlton, 2002; Pascual-Leone
et al., 1995; Sarazin et aI.,2002; Stebbins et al., 1995).
Il1 contrast to procedural lnelnoly, cleclarative memory
involves thc couscious lcarning and lccall of infbrnration
such as Iists olrvords or images (Gabricli, 1998). Dysfurrction in the encoding and retrieval of declartrtive tnetnot'ies
has bcen most coulmorrly associated rvith darnagc to mesial
tcrnporal lobe structures, particularly thc hippocampus
(Cabeza & Nyberg, 2000: SqLrire & Zola. 1996). Double
dissociations may bc observed rvhereby patients rvith basal
ganglia abnonnality pcrtbrrn poorly on procedural memory
tasks and relativcly rvcll in their encoding and rctriel'al of
declalative rrL'lnories, rvhilc patier-rts with mesial ternporal
lobe abnonnalitics sholv thc revcrse pattern (Gabrieli, 1 9981
Sabc ct al., 1995). To datc. no consistcnt cvidencc fbrnresial
temporal lobc abnomrality has beerr tbund in OCD.
It has been hypothesized that because of a procedural
rnenlory dcficit, infonnation that would othcrwisc be processed without awarelress rnust be plocessetl with full awareness bv patients with OCD. resulting in incleased arousal
and misallocation of attcntion ( Rauch & Savage. 2000:
Rauch ct al.. t9!)7). Dcclaratil'c rlemory circuitry is recruited
in order to colrlpcnsatc for abrtonnal procedr.rral melnory.
albeil somovhal inelliciently. F unclional ncuroimaging studics using procedural mcrnory tasks have observed abnormal
recruitrncnt of l'r'ontostriatal circuitry and increascd lrippocampal acti!'atioû relative to hc'althy controls. supporting
this hypothesis (Rauch et al., 1997: Rotl.r et al..2003).
Fcrv bchavioral studics have assesscd proccdural mcmoly in OCD, and only a subset has cvaluated both procedural and declarative mernory iu the same group of patients.
Patienfs with OCD rvcre shorvlt to perfbnn more poorly
than hcalthy controls on thc proccdural tnctnory cotnponeltt
of the Torver of Hanoi (Cavedini et al.. 2001). as rvell as on
an irnplicit sequence learning task rvhere the opportunity to
recluit declarative rncmoty rvas intertèr'ed rvith through dual
task dcmands ( Dcckersbach et al.. 2002). I11 corltrast. olle
study reported poor delayed recall fbr a rvord list but intact
Pursuit Rotor Task pcrfbrurance ( Martin et al.. 1993). Other
invcstigations of declarative rnclnory in OCD have yiclded
inconsistent lin<lings (Christensen ct al., 1992: ['lollander
et al.. 199(): Savage et al.. 1996). When dellcits iu eucodin-e
and retrieval in declarative mcmory are observed in OCD,
evidence suggests that thcy arc largely due to in-rpaircd usc
of strategic processes subserved by frontostriatal circuitry
rathcr tharl processes subserved by rncsial ternporal lobe
circuitry (Deckelsbach et al., 2000; Savage et al., 1999,
2000).
The conflicting rcsults reported rvith respect to proce«lural rncmory in OCD rnay be partly due to thc usc of
relatively small sample sizes, the inclusion of medicated
patients, and tàilure to exclude patients rvith comorbid rnajor
deplessive disordcr. With regard to thc latter possibility.
patients rvith prirnary rnajor depressive disorder have bcen
rcportcd to pcrfonx poorly on procedural memory tasks
(Sabe et al.. 1995), and even non-clinical levels ofdepression have becn associatcd with reduced procedural lnemory
(Kalechstein et al., 1998). In the prcsent study, rve sought to
evaluate the hypothesis that procedural memory is abnormal in a sample of unmedicated and non-clinically depressed
paticnts with OCD. We hypothcsized that, relative to healthy
controls. the patient group rvould show poorer performance
on the Pursuit Rotor Task. a lneasure of procedural rnemory. and norrnal pcrforrnance on thc Rey Auditory Verbal
Learr-ring Test, a task designed to assess encoding and
retrieval in declarative lnelnol'y.
METHODS
Research Participants
Participants rvere 27 adult outpatients with OCD and 29
healthy controls. All participants were right-handed by selfrcportcd hand preferencc for rvriting, and u'ere betwcen thc
ages of I 8 and 65 years. None of the participants had a
history olsubstâuce abuse. neurolo-qical illness, head injury
resulting in a loss ofconsciousness, elcctroconvulsive therapy or psychosurgcry, or othcr mcdical illncss r,r,ith potcntial effects on cognitivc tinctioning. Paticnts met diagrlostic
criteria tbr OCD as detlned by the Diagnostic and Statisti-
cal Manual of Mental Disorders-Fourth Edition criteria
(Aurcrican Psychiatric Association, 1994). Diagnosis was
establishcd using the Anxiety Disorders Intervierv Schedule (ADIS). a structurcd diagnostic interview for anxiety
disorders and exclusionary conditions bascd on DSM-lV
criteria (l3rown et al.. 1994). The ADIS rvas administered
by either a psychiatrist or psychologist with extensivL- expericncc in OCD. Patie nts rvere excludcd if they had a comorbid DSM-lV diagnosis of rnajor deprcssivc disorder or
dysthyrnia. Arnong the patients rvitlr OC D.4 mct diagnostic
criteria lbr comorbid generalized anxiety disorder. -l had
social phobia. and 1 had parlic disorder. However. in all
câscs OCD was clcarly the prirnary diagnosis. OCD syrnptorn severity was assessed using the Yale-Brorvu ObsessiveCornpulsive Scale (YBOCS: Goodrnan et al.. 1989). The
YBOCS is a structurcd clinical intervierv specilÏcally
designed to detennine the naturc. extent and severity of
obscssions and compulsions. Ten items pertaining to the
Metnor.t'in OCI)
649
severity of obsessions and compulsions arc rated or1 a fbur
point scale of seve'r'ity, u,ith higher scores reflecting greater
severity of illness. Arnong our patienls with OCD. l9 were
ncver prescribed psychotropic mcdications and 8 had discoutinued thc usc ofselectivc serotonin reuptake inhibitors
lbr a minirnurn of trvo weeks prior to their participation in
the study. None of the patients werc undergoing cognitivebchavioral therapy at thc tirnc of participation. Hc'althy controls were recruited frorn a subject pool at the Centre de
Recherche Fernand Seguin (a dedicated research center
affil-
iated with the University of Montreal and Hopital Louis H.
Lafbntaine) and advertiscrnents in a local nervspapcr, antl
Irad no irersonal lristory ofpsychiatric illncss based on self-
report. All participants plovided written inlbrmed conserlt
al'ter cornplete dcscription of the study.
spced during baseline at which they were able to track the
targct closest to au averagc of5 s was used exclusively for
the test trials. This procedure was ernployed to minirnize
absolute group dillerence in motor coordination or spced,
and is consistent with prior studies using this task (van
Gorp et al.. 1999). Participants next completed a total of six
test blocks of four twenty second trials each. The inter-trial
resting pcriod was 20 s, while the inter-block resting pcriod
was 60 scconds. Thirty nrinutes of other cognitive tests
(results to be reported elsewhere) were completed betrveen
Blocks two and three. and again between Blocks 4 and 5.
The average pcrcent time on target fbr each block was calculated by averaging tlre tirne ou larget for all four trials
within a block.
Data Analysis
Procedure
Group differences in demographic and clinical characteristics were analyzed using independent samples r tests and
Mood
Thc Beck Depression Inventory (BDl) is a 21-item sell'report scalc designed to assess ibr cognitive, emotional and
somalic syrnptonls ofdepression ( Bcck. 1 987). Scores range
liom 0 to 63. with higher scores indicating a greater level of
deprcssion. Situational anxiety u,as rneasured u,ith thc Spiclbcrger Statc-Trait Anxicty Inventory. Statc subscale (STAI-S;
Spielberger ct al.. 1970). Scores ou the STAI-S range fion.r
20 to U0, rvith higher scores indicating a greâter degree of
anxiety.
nonparametric statistics, as appropriate. Group X Trial and
Group X Block rnixed model repeated measures analysis of
variance were conducted for the RAVLT learning trials and
Pursuit RotorTask, rcspectively. Indcpendcnt sarnple l-tests
rvere carried out to evaluatc group dilferences on the iudividual trials of the RAVLT and blocks of the Pursuit Rotor
Task. All tests uscd two-tailed comparisons with signiticance lcvcl set at p < .05.
RESULTS
Declarative nrcnlonl
On the Rey Auditory Verbal Learning Test (RAVLT; Spreen
& Strauss. 19981, participarlts were rcad aloud a list of
flfteen rvords and aske«I to recall as many as possible. The
procedure was repeated fbr a total ol five leaming trials.
Irollorving thc trtth leaming trial. an interf'erencc list of
flfieerr nerv rvords rvas preseuted followed by frce recall of
the new list. Participants wcre subsequently asked to recall
the rvords tiorn the flrst list (short dclay). Subjects were
asked to recall thc llrst list a-eain afler a 30-min dclay (long
delay), arrd then complcted a yes/no rccognition menlory
trial. Total wolds recalled. as rvell as pcrcent retained relative to thc last lcarning trial. are presc'nted.
Procedw'ul nremot\
On thc' Pursuit Rotor Task (Photoelectric Pursuit Rotor.
Modcl 300I4; Lafiryette Instrunrent Cornpany. Lai'iryctte,
Indiana). participants rverc rc'quircd to hold a curved light
sensor wand with their right hand and track the motion of
a
îwo centimeter liglrt ernitting disk (the target) rotating insidc
a 30.5 centirnctcr in diarnctcr tnmtablc. Participants initially cornpleted a baseline ofthrec trvcnty sccond trials at
each of four ditlcrent disk rotation speeds ( I 5, 30, 45. and
60 rpm) and thc tilne-on-target rvas rccordccl. Thc avcrage
tilne-on-târget for each ofthc thrce baselinc rotation speed
trials was then calculated. For each participant. the rotation
Derno_eraphic and clinical characteristics of the patient and
control groups are presented in Table 1. The groups did not
diflbr significantly in terms of age, ycars of education. scx
composilion and handedness. The mean total score on the'
l.
Table
Denrographic and clinical characteristics of OCD and
control groups
OC'D ( ()ntrol
(n:21) (n - 29)
MSDLISDT'p
37.19 I 1.2 I 35.14 9.83 0.71 .448
Measurc
Ase
Yearsofeducation 14.87 .3.91 16.38.1.66 1.,19 .l4l
BDI
15.09 7.48 4.18 4.25 7.00 .001*
STAI S
13.26 10.77 3?..14 9.71 4.06 .001*
YBOC'S
'lbtal
28.33
YBOCS-Obsessions 13.71
YROC'S C'ompulsions
Fentale (o,i,)
40.7
Right-handcd ('2,;
il)egrees ol' fice dorn
*p
<
14.59
4.29
2.65
2.06
100
=
5,1
58.6
93.1
X2
0.18 0.29
0.49 0.26
tbr all comparisons,
.05.
llDl = Beck Depression ln\entory: S1Âl-S = Slale-l'raii An\iety
lnventtrry-State subscale: \'BO( S : Yale-Bros'n Obsessive Conrpulsive
Àot<,.
Scal.'.
650
R.M. Roth et al.
Tablc
2. Descriptive statistics lor pertbrnrance on procetlural
OCD
(n: 271
M
Measure
RAVLT (No. items recalled)
Trial
Trial
Ttial
t7.10
14.45
15.22
l 6.41
18.64
I 8.63
44.82 18.33 2.49
47.73 t7 .99 3.04
61.39 19.42 2.08
62.17 20.5.1 | .7 I
64.67 19.52 1.25
66.49 19.82 0.74
Trial
t3.67
Pursuit Rotor
Block
I
lllock
2
(
rl)egrees ol fieedonr
*/'<
I
l.4l
82.4t
I 1.44
82.78
tinrc-on-targct)
Block 3
[]lock 4
Block 5
!ilock 6
tl
56.68
61.87
10.87
70.ti5
71.36
70.44
12.19
13.33
(Zr
SD
14.00
3
Trial 4
5
lV
.sD
7.07 2.05 0.22
10.28 2.20 0.28
12.07 t.77 0.26
13.00 I .81 0.73
3.03 2. 18 t.23
I 1.66 2.88 0.32
88.44 t2.42 1.46
I | .72
2.99 0.3(r
1i9.39 15.29 1.50
t4.21, l.l l 0.67
ll
Short delay
Short delay, perccnt rccall
Long delay
Long dclay. percent recall
Recognition List A
Conlrol
= 29)
1n
1.45
2.t7
t.57
l .59
I .59
2.86
18.l.l
2.87
t] .67
1.27
6.96
t0.
I
2
and dcclarative memory lests
I
.825
.779
.797
.469
.223
.748
.t49
.723
.140
.505
.016+
.004*
.041+
.093
.215
.464
= 54 t'or all conrparisons.
'05'
YBOCS for the patient group was in the moderate symptom
scverity rauge. Despitc excluding patients rvith a diagnosable dcpressivc disordcr, thc paticnt group rcported significantly more symptorns oldepression and anxiety than the
control group.
Descriptive statistics for the RAVLT and Pursuit Rotor
Task are presented in Table 2. The mean number of rvords
recalled on each learning trial of RAVLT is preser.rted in
Fi-eure 1 for illustration. Neither the Group main elÏèct
[f (1.,§4):0. 18. p: .671] nor the Group X Trial interaction IF(4,54) : 0.83.p : .5l0] reached statistical significance. As expccted, there was a significant main efï-cct of
trial. indicating better recall with repeated exposure to the
word list lF(4,54) :231.55.
p:
.0011.
Additional analyses
showed that the patients and controls performed similarly
in the number ofrvords recalled and percent ofwords recalled
at short and long delays, as well as on the recognition mem-
ory trial.
On thc Pursuit Rotor Task. the groups did not differ rvith
respect to the rotation speed used for test trials, as determined by the baseline evaluation (X2 :0.203, p: .299).
The majority of participants in both the patient (88.9%) and
control (75.9%) groups perfonned the tcst trials at thc 60 ryrn
setting, while the remainder used the 45 rym setting. Higure 2 shorvs the mcan percerlt time on-talget fbr the six test
blocks of thc Pursuit Rotor Task. A significant main effect
ID
14
12
10
of Group was present. indicating llrat. overall, the OCD
group stayed on-target significantly longer than the control
: 4.30. p : .0431. A main ef]ect of block
group [F( I .54)
was also observcd in<iicating bettcr pcrfbrmance with
12345
RAVL'l"hial
*ü** OCD "'^ '' Control
Fig.
l.
N{ean
Test by group.
wordspertrial on the ReyAuditory Verbal Learning
increasing task experience across the groups If'(5,54) :
46.92. p: .0011. The Group x Block interaction was also
significant [.F (5, 54) : 2.77 , p : .019]. Group comparisons
on thc individual test block performance indicated that the
OCD group stayed on-target significantly longer than controls for the first three blocks. Groups did not differ on the
last three blocks.
Statistical comparison of patients with (n : 8) and without (r = l9) a comorbid anxiety disorder did not reveal any
Menu»v in OCD
651
must be cxertcd in linking neuropsychological pertbr-
80
mance changes 1o specilic underlying neural circr.ritry, tentative support {br this hypothesis may be found in research
on brain regions involved in early lersu.r later stages of
procedural lnemory tasks. Studies rvith primates and healthy
humans indicate that the caudate nucleus aud rostral putamen tend to be most active during the carly stages of novel
ploccdural mernory tasks ( Krebs et al., I 998; Miyachi et al.,
2002). In contrast. later stages oflearning appear to involve
corticocerebellar circuitry and rnore caudal portions ofthe
putalnen (GralIon et al.. 1994: Krebs et al.. 19981 Miyachi
et al., 2002). Horvcver, it shoul«l be notcd that neither regional
overactivation nor underactivation on furrctional neuroirnaging are consistently associatcd rvith perfbrmance differenccs ou a variety of tasks in cither hcalthy controls or
75
70
65
60
55
50
45
40
12345b
Trial tslock
-'-l--OCD
Fig.
2.
''a-"
Control
Percent tirnc on larget on the Pursuil Rotor Task by groulr
patient populations (e.9.. McAllister et al.. 2001: Rauch
al.. 1997.1.
Only trvo functional neuroimaging studics to date have
applied proccdural mclnory tasks to OCD, both with small
et
sarnple sizes. One snrdy used PE,T and an irnplicit sequence
significant difÈrenccs or1 either the RAVLT or Pursuit Rotor
Task (allp > .05). No significant comelation (allp > .05)
u,as obselvcd betwecn percent tirne ou target for any ofthe
Pursuit Rotor blocks an«.l overall OCD syrnptom scvcrity
(YBOCS total score), or sevcrity of obsessions (YBOCS
Obsession subscale) or compulsions (YBOCS Cornpulsion
subscalc). F'inally, group diflèrences in mood did not accottt.tt
fbr thc Pursuit Rotol Task findings in analysis of covariancc-.
DISCUSSION
Thc prescnt study rcvc-alcd that uurnedicatcd paticnts with
OCD pertbrmed better than hcalthy controls on a procedural memory task. while group differences were ltot
observed tbr either encoding ol retricval in declarative rnernory. Specitically. thc OC'D paticnts l'cnraincd on-target during the' Pursuit Rotor Task for a sigrrificantly gl'cater percent
of tirne overall thau controls. This effect rvas largely dr-rc to
significantly bettcr pcltbrrnancc by the patients during the
carly but not latcr trial blocks of the- task. No association
was fbund bet*'ecn procedural rnemory and rnood or the
scverity of eithcr obsessions ol compulsions in thc patient
group.
'fhat our OCD group shorved bettcr procedural tnetrory
than controls, especially during the early block of trials,
was uncxpccted. Patients rvith Tourctte's syndrome, a disordcr hypothcsized to bc genctically rclated to OCD (Sheppard et al.. 1999;, have been shorvn to pcrtbrrn rnore poorly
than healthy controls orr the Pursuit Rotor Task (Stebbins
et al.. 1995). Howcver. iu coutrast to OCD. Tourette's syndronrc is associatcd rvith striatal underactivation (llraun et al..
1993; E,idclberg et al.. 1997). tt may be speculated that
enhanccd procedural lnemory during the early stages of
learning in OCD is associatcd rvith thc striatal ovelactivation reported in nunrerous firnctional neuroimaging studies
of the disorder (Saxer.ra & Rauch, 2000). Although caution
learning task (Rauch et al., 1997). r,r'hile the other (Roth
et al.. 2003) employed f'unctional MRI and a probabilistic
classification task (Knorvltou ct al., 1994;. Despite the use
of different tasks, both studies reported that adults with
OCD showed prorninent hippocampal but little striatal activation, while healthy controls showed prorniner,t striatal
and little to no hippocampal activation. Perfonnance differeuces were not observed in either study. These results were
interpreted as consistent rvith fiontostriatal dysfunction in
OCD. Sincc neithcr of thc studics spccifically reported on
temporal changes ir-r the degree of striatal activation during
the course ofthe tasks, the hypothesis that diff'erential striatal activalion in OCD is related to the carly stage of procedural mcnlory tasks could not be addressed.
Taken together. results frorn neuroirnaging studies dur'ing rest, sylnptom provocation and procedural metnory tasks
suggest that the directionality of thc striatal abnormality
seen in OCD. whether it be overactivation or underactivation, may depend on the stage of procedural memory interrogated and/or the naturc of the task ernploycd. With respect
to task requirerncnts. both sequence learning and probabilistic classification involve "cognitive" procedural mcmory. ln contrast. the Pursuit Rotor Task involves a niore
pulely "motor'" procedural n'lcmory. Activation of thc ltippocalnpus durirrg cognitive procedural memory tasks in OCD
has been interpreted as suggesting that these patients have
abnormal tiontostriatal circuitry and theretbre rnust rcly on
thc declarative lncmory systcm to adequately perform procedural rnernory tasks (Rauch & Savage,2000). lt rctnaius
unknown rvhether patients with OCD would also activate
the hippocampus. or show diilèrential striatal activation.
during a motor proccdural mcmory task such as that
employed in the present investigation. Further functional
lucuroimaging studies of OCD, ernploying both cognitive
and rrotor procedural mcmory tasks, and assessiug activation both during the early and later stages ofthe tasks. will
be necessary to evaluate these hypothcses.
R.M. Roth et ul.
652
Thc f'unctional signilicancc of better procedural mcmory
in our paticnts is nnclear. One aspect of procedural lnemoty
subserved by lrontostriatal circuitry that lray be relevant to
OCD is thc fbrrnatiou ol stirnulus-rcsponse associatious
( Mishkin ct al.. 1984; Packard & Knorvlton, 2002; Poldrack
,l995).
ln the casc of OCD. this
et al., 2001; Saint-Cyr et al.,
rnay be exprcssed as thcilitated acquisition ofassociations
bctwccn potcntially threatcnine cogrtil ive- ol cnvirorttnental
stirnuli such as irrtrusive thoughts ar-rd anxiety-reducing conrpulsive behaviors. Exposure and respouse prevention, a fotm
of behavior thcrapy that is hi-ehly ctï'ective fbr trcating OCD.
involves irr part repcated presentation of anxicty-provoking
stirnuli and gradual rvittrhotding of compulsive responscs
(Foa et al. 2001). This treatrncnt. rvhich has been shown to
rcduce resting t'r'or-ltostriatal overactivation in patients rvith
OCD on positron emission tornography scans (Schwal'tz.
1998), may rvork in part through the breaking of maladaptive stimulus-rcsponsc associat ions.
Our OCD and control groups did not cliller rvith rcspect
to encoding and rctrieval in declarative tnernory. Prior
research has yielded inconsistent findings lbr both verbal
and r.'isual declarative mclnory in the disorder (Grcisberg &
McKay. 2003). Rcccnt studics havc indicatcd that lesser
use oforganizational strategies during encoding. rather than
inTpailed retricval processes, accourlts lbr ve-r'bal and visual
declarativc memory dellcits rvhcn observed in OCID (Deckersbach ct al.. 20001 Savage ct al.. 1999). This has been
interpreted as ret'lecting a deficit in the use of frontostriatal
circuitry rnediatcd stratcgic processes rather than a ntesial
tcrnporal circuitry rnediated retrieval deficit lSavagc et al.,
1999). The lack of gloup dit-fèrence for declarative memory
in the plesent study may thus be due in part to the natule of
thc RAVLT. Unlike sornc othcr declarativc mcrnoly tcsis
such as the ('alifbntia Verbal Leaming Test (CVLT; Delis
et al., 1987). the iterns on the RAVLT cannot be readily
organized on thc basis of semantic or other relationships
beîrn'cen iterns, and thclelble thc potential advantage in recall
afforded to controls rvas likely limited. L,vcn if a test such
as the CVLI had been ernployed, previous findings (Savage et aI..2000; suggcst that group diflerences in learning
and rccall rvould likcly lravc been due to thc paticnt groups
lesser usc of strategic proccsses rather than a retlicval def-
icit per se.
The prescnt tindiugs colltrast with tlrc only prior study
using the Pursuit Rotor'l-ask in OCD, u,hich found no differences betrveen healthy controls and patierlts ( Martin et al.,
I 993 ). ln attelnpting to account for their results. Martin and
collcagucs proposcil that thc high [cvcl oleducation ofthcir
participants (Â1 age OCD : 15.4: içl age controls : 15.9
years) may have rendered it difficult to obse'rve group diffèrences. Horvever, thc level of education of participants in
thc prcscrlt study is cornparable to that leport. Furthennole,
both studies uscd unmedicated patients, and treatment rvilh
selective serotonin rcuptake inhibitors does not appear to
havc a significant irnpact on procedural lucmory in OCD
(Mataix-Cols ct al.. 2002). Thus. educati<m and tredication
status are unlikely to explain the discrepancy in findings. lt
is possible that thc larger samplc size employed in the cur-
rent stucly may have contributcd to the detection of group
differences.
It may be questioned rvhether the better procedural memory by our patient group is an artifàct ofpoor perfbnnance
by the control group. Howevcr, the percent time-on-target
for our controls during all stages ofthe Pursuit Rotor Task
is cornparable or better than that observed in scveral other
studies using healthy controls rvith similar agcs arrd educa-
tiorr levels (Martin et al., 19931 Stebbins et al., l995: van
Gorp et al., 1999). It may also be qr.restioned whether the
comparison of tests that employ diilbrent stimulus modalities. auditory.-verbal ( RAVLT) r'ersls visuomotor ( Pursuit
Rotor), r.nay have impacted our findings. The methodology
and results ofthe present study do not perrnit resolution of
this issuc. Further studies employing both auditory-verbal
dcclarative lrernory tests arrd auditory-verbal procedural
memory tests such as prir-ning tasks rvould help address this
issue.
Our OCD group shorvcd grcater time-orl-target than con-
trols as early as the flrst block of test trials on thc Pursuit
Rotor Task. This raises the possibility that the patients had
greater skill than controls at baseline. Our groups did not
differ significantly in the rprn levcl at rvhich their ability to
stay on target was closest to 5 s during baseline trials: this
has been thc standard n-rethod to cstablish baseline equivalcncc in rnotor abilities on the task (Heindel ct al., 1989;
Stebbins ct al., 1995; van Gorp et al.. 1999). Horvever. significant group differeuces in the rate of improvernent in
actual time on target during the baseline trials rnay have
resulted in the patient group starting the tcst blocks rvith an
already higher level of pertbrmance. We therefore analyzed
the time on target for the last baseline trial to gauge level of
perfonnance prior to the first tcst block. This was fourrd to
be significantly bettcr for the patient group [t(l):2.18,
.034). lt is possible that the nrultiple baseline trials
were sutïcient to pennit group dilterences in procedllral
memory to manifcst, which rvere thcn maintaincd until the
fourth block rvhen the patient group reached a plateau in
their rate of inrprovement. F uture studies would benefit from
using sizably larger sarnples in ordcr to permit statistical
cvaluation of thc ratc of lcarning during both thc baseline
p:
and test phases of the task. Altemately. beginning test blocks
at the same rpm rate tbr all subjects and elirninating pre-test
block basclinc trials altogether may bc hclpful fbr detcrmining differenccs in procedural rnemory in early and late phases
rvithout extensive pre-exposure to the task (e.g., Cranholrn
et al., 1993).
In surrmary, the prescnt findings revealcd signiticantly
better procedural memory duling the early stages of lcarning in unrnedicated patients rvith OCD as compared to
healthy controls. in the absencc of group differences for
cncoding and rctricval in declarativc mclrrory. This pattern
of findings appears to be consistent rvith evidence of frontostriatal circuitry abnormality in OCD. Replication in a
largcr sarnplc of paticnts with OCD. and direct comparison
with patients rvith Tourette's syndrome, rvould be infonnative. Finally, further lirnctional neuroimaging studies would
be hclpful to directly cvaluate the relationship between cog-
653
Lletnor.r,in OCl)
nitive and rnotor procedural mcrnory task pcrlbrmancc and
frontostriatal circuitry activation in OCD.
ACKNOWLEDGMENTS
Psychological Corporation.
This study \vas supported by grants tiorr the F'onds Pour La Forrnation de Chercheurs et L'Aide a la Recherche (l{MR). and the
Fond cle la Recherche en Santé Québec (KO and JB). We thank
Laura F'lashnran and three anonyrnous revic-wers for their helplul
comrnents on this manuscril'rt.
REFERENCES
Anrir. N.. l-reshrnan. ÿ1., & Foa. I"-.8. (2000). Farnily distress and
involvernent in relatives of obscssive-contpulsir,'c disorder
patients. Journol ol .4ntiet.v Disorders. 14,209-217.
Arnerican Psychiatric Association. (19911. Di ugno.slic' nd sloti.sti<'ul munuol ol mentul disonlcrs (4th ed.). Washington, DC:
Arne-rican Psychiatric Association Press.
u
Aylrr,ard.
E.ll.. Ilanis.
&
G.J.,
lloehn-Salic. R., Barta. P.E.. N{achlin.
Peallson. G.D. (1996).
Nortlal caudate nucleus in
obsessivc-conrpulsir'e <lisordel assessed by quantitative neuroirnaging. .4rchives ol Getrcral Ps.t'chiutrl'. -r3.577 584.
Bcbbington. P.lr., ( I998). Epidemiology of obsessive-cotnpulsive
S.R..
disorder: Brirish,lourna\ d Ps1'c'hiur.t' Supp|ementun (35),2 6.
Beck. A.T. (1987). BecÀ Depression lnventory. San Antonio. TX:
The Psychologieal ('ttlporation.
Braun. A.R.. Stoetter. 8.. Randolph. C.. Ilsiao. J.K.. Vladar. K..
Gernert..l.. ( arson. R.Fl.. Ilerscovitch. P. & Chase. T.N. ( 1993).
Thc f'unctional Neuroanatorny ol Tourcttc's Syndronrc: An
F
DG-PET Study. I: Regional change's in cercbral glucose ntetab-
olisnr dilierentiating patients and controls. Neurops.r'chttphur-
mutolog.t,.9. l5l 168.
Brown. T.A.. Di Nardo. PA.. & Barlo*. D.H. (1994). Antiery
disonlers inten'iev'schedule.li» DSI'{ ly. Albany, NY: Graywind Publications.
Bylsnra. F'.W.. Branclt. J.. & Strauss. M.E. (1990). Aspccts of plocedural urenror! arc diTterenlially inrpatrcd in Iluntington's
cliscase. .4rz'lilr,r,s o/ C' Ii ni ca I N artntps.t'choIo91, 5. 287 297.
Bystritsky. A.. [-iberman. R.P, Hwang. S.. Wallacc. C.J., Vapnik.
T., Maindnrent. K.. & Saxena. S. (2001). Social tunctioning
and quality
ollilè
conrparisons bctwecn obscssive-cotnpulsivc
and schizophrenic disorders. Dt'pressiott ttnd An.tiety. 14,
ll4
218.
C'abeza. R. & Nybcrg. L. (2000). Inraging cognition Il: An eurpirical rer'icw o1275 PF,T and {'lvlRI studics. Jorrrrrrl of Cognitnt'
Neuroscientc. l:. | 17.
Cavcdini. P., (lisinra. lvt.. Riboldi, (i.. D'Annucci. A.. & Ilcllodi.
L. (200 I ). A neuropsychological sturly of dissociation in cor-
tical antl sr.rbcortical firnctioning in obsessive-cotnpulsive dis-
order by Toiler
357 363.
of IIanoi
with obsessivc-conrpulsive disorder. .4nrerican Jourttul oJ Psyc'hiatr.y, 159. 1780 1182.
Delis, D.C.. Kramer. J.H.. Kaplan. E., & Ober, Il.A. (1987). &r/i/brniu l/erbul Leurning Test Adult lâr.srort. New York: The
tâsk. Bruin anrt C'ognition, 46,
Christenscn. K.J., Kirn, S.W.. Dyskcn. IV.W.,
&
Hoover, K.M.
obscssirc-
in
Psychiatr.v. J/.4
(1992). Ncuropsychological perfortnance
18.
cornpulsivc disorder. Biologicol
Deckersbach. T.. Olto. M.W., Savage. C.R.. Baer, L.. & Jenike,
M.A- (2000). The relationship lretween senrantic organization
and rnernory in obsessive-cornpulsi ve disorder. P,s1't' lntheru pl'
unl Pst<ltoso»rutit's, 69. l0l l()7.
Deckersbach. 'f.. Savage. C.R.. Curran. T.. Bohne. A.. Wilhelnt.
S.. Baer. L.,.lcnike. N'I,A.. & Rauch. S.L. (2002). A study of
parallel implicit and cxplicit inf-orntation processing in putients
Eidelberg, D.. Moeller. J.R,. Antonini,4., Kazumata, K.. Dhawan.
V.. Budnran. C.. & Feigin. A. (1997). The rnetabolic anatomy
ol Tourelte's syndronre. N e u ro lo g1'. 4 B, 927 934.
F'oa. E., Wilson, R., & Wilson. R.R. (200 I ). Stop obsessing!: How
îo overconte _rour ohse.ssiotts and compul.:iotts ( Rev. ed.). New
York: Bantanr Doubleday Dell Publishers.
Gabrieli. J.D. ( 1998). Cognitivc neuroscience of hurnan melrory.
.4tnuul Review of Psycholog.r', 49,81 ll5.
Gabtieli, J.D., Stebbins, G.T.. Singh, J.. Willinghanr. D.. & Goetz,
C.G. ( 1997). lntact mirror-tracing and impaircd rotary-pursuit
learning in patients with lluntington's disease: Evidence for
dissociable rnel.nory systems in skill leaming. Neuropsl;<'hol-
ogv. 11.272'281.
Gonrez Beldarrain, M., Grafman. J.. Pascual-Leonc. A.. & GarciaMonco. J.C. ( 19991. Procedural learning is irnpaired in patients
with prciiontal lesions. À'erln1rlg1,.52. I853 I8(r0.
Goodnran" W.K.. Price. L.H., Rasnrussen. S.A., lv'lazure, C.. Delgado. P.. Ilcninger. G.R.. & Charney. D.S. (1989). The YaleBrorvn Obsessive-Cornpulsil'e Scalc. I: Developrncnt. use. and
reliability. Archives of Gene rol Psy'chiatr.t',46. l0l2-1016.
Grafton, S.T., Woods. R.P. & Tyska, M. (1994). Functional imaging ofprocedural niotor leaming: Relating cerebral blood flow
with individual subject perlbnnance. Ilumun Brain lllopping.
t.221 214.
Granhohr. Fl.. Éiartzokis. G.. Asamou R.F'.. & Marder. S.R. ( 1993 ).
Prclirninary associations betlvcen rnotor procedural learning.
basal ganglia T2 relaxation times. and tardive dyskincsia in
schizophrenia. Ps)'cltiatry Reseorch. 50. 33 44.
Greisberg. S. & McKay, D. (2003). Neuropsychology ofobsessivcconrpulsive disorder: A revierv and trea{lnent irnplications. C/il-
icol Psycholog.tt Review. 2 3, 95 I 17.
Heindel" W.C.. Butters, N.. & Salnron, D.P (1988). lmpaired leaming of a nrdor skill in patients rvith Huntington's disease. r9cftar.
ioral Neuroscien<:e, 102. l4I 147.
Fleindel, W.C--.. Saluron. D.P.. Shults. C.W.. Walicke. PA., & Butters. N. (l9ti9). Neuropsychological evidence for nrultiple
inrplicit nlelnory systerns: A cor:rparison of Alzheinter's,
lluntington's, and Parkinson's disease patients. Journal ol
Ne urosc ien<'e. 9. 582-587.
Hollander, E.. Schillman, E.. Cohen,8.. Rivcra-Stein, M.4.. Rosen.
W., Gorrlan. .1.M.. Fyer, A..1.. Papp. 1... & Lietroivitz. M.R.
(1990). Signs of ccntral nervous systenr dyslunction in
obsessivc-compulsive disordcr.,!rc'ltives of Generu| Ps.t'chiutry, 17.27 32.
Horwath, I-.. & Weissrman. lvl. M. (2000). Thc epiderniology and
cross-national presentation of obsessive-compulsive disorder.
Ps.t,chiatric Clinics tl North ,4nterica. 23.493 507.
Kalechstein. A.D., IIinkin. C.H.. van Gorp, W.G.. Castcllon, S.A..
& Satz. P ( 1998). Depression predicts procedural but not episodic nrerrory in HIV- I infection. Jotrrnutl o/'Clinitul uud Experinentu I Neun4tsycholog.r'. ) 0. 529 535.
Knowlton. 8.J.. Squire. L.R.. & Gluck, I\'1.A. ( 1994). Probabilistic
classitlcation learning in arnnesia. Leorning ond Menrory,, l.
t06
120.
Krcbs. ll.l.. lirashcrs-Krug.'f.. Rauch. S.L.. Savagc. C.R.. Hogan.
N.. Rubin, R,ll.. f-ischrnan. A.J.. & Alpert. N.M. ( 1998). Robotaided firnctional irnaging: Application to a motor learning study.
Human Broin lllapping,6,59 72.
R.M. Rorh et al.
654
Martin, A.. Pigolt. T.A.. L:rlonde. F-.M.. Dalton. I.. Dubbert. 8.. &
Murphy. D. L. ( 1993 ). Lack of evitlence lor Huntington's diseaselikc cognitive dysfunction in obsessivc-conrpulsive disorder.
lliologit:ul Psychiurrv,
-?J,
345 353.
lvlataix-Cols. D., Alonso, P. Pifarre, J.. Menchon, J.M.. & Vallejo,
l. (2002l'. Neuropsychological perlbrnrance in rnedicated vs.
unrnedicated patients with obsessive-colnpulsive disorder. Ps_rh io tt'.t' Re s eo rt' h, I 09. 255' 264.
McAIlistsr. T.W., Sparling, M.8.. I-lirshman. L.A., Guerin. S..1.,
Ivlarnourian. A.C.. & Saykin. A.J. (2001 ). Differential r.r'orking
nrenroly load effccts al'ter milcl trauuratic brain injury. Neuroinrage. 14. I004 1012.
Mishkin. M.. Ivtalamut. 8.. & Bachcvalicr, J. (1984). Iv{emolies
<'
and habits: Trvo neural systerrts. In G. Lynch, J.L. McGaugh. &
N.lvl. Wcinbcrgor ( Eds.). Neurobiolog.t, ol learning; atrul Dten-
o/r'(pp. 287 296). Ncw York: Guilf'old Press.
Mi1,achi, S., Ilikosaka. O.. & Lu. X, (2002). Diffèrential activation of nronkey striatal neurons in the early and late stages
ol' prcrcedural learning. Experincntttl Bruin Reseurch. 146.
122 t26.
Packard. I\4.G. & Knowlton, ll..l. (2002). Lcarning and nrcrnory
frrnctions ofthe basal ganglia. ,lnnunl Revie:l ol Neuroscit'nce,
l-r.563-593.
Pascual-Leone, A.. Gralirran. J., & IIallett, IVI. (1995). Procedural
Iearning and lrretiontal co(lèx. .4nnals fi the Neu' htrk Acadenty of Sciences. 769.61 70.
Poldrack. R.A.. Clark, .1." Pare-tllagocv. ti.J.. Shohamy, D., Cleso
Moyano. J., Myers, C'.. & Ciluck. N'I.4. (2001). lntcractive rnemory syslcrl.rs in the huuran brain. Norure. 411. 516-550.
Rauch. S.L. & Savage. C.R. (2000). lnvestigating cottico-striatal
pathophysiology in obsessive-cornpulsive tlisorders: Proce-
dural lcarning and irnaging probes. ln Vy'.K. Coodrnan, M.\'.
Rudorfèr & J.D. Maser ( [:ds. ). O|.rre.s.si le-compulsive tlisonler
(pp 133 154). Mahwah, NJ: Lai.vrence Erlbaurn Associates.
Inc.
Rauch. S.L.. Savagc. C'.R., Alpert. N.M., Dougherty. D.. Kendrick. A.. Curran. T.. Brorvn. ll.f).. Manzo" P. F-ischrnan. A.J..
&.lcnike. M.A. (1997). Probing striatal lunction in obscssiveconrpulsive disorder: A PliT study of'iniplicit sequcnce learning. Jourrrul of Neurops.vchiatr.t' arul Clinicul Neuroscicnces,
9.5(18-571.
Rauch. S.l-.. Whalcn, P.J.. Curran. T.. Shin. L.ivl.. (loffey. B.J..
Savage. Ci.R.,lvtclnerney, S.C., Baer, L.. &.lenike. M.A. (2001).
Probing striato-thalamic f unction in obsessir,'e-conrpulsive disordcr and Tourette syndronre using neuroinraging nrcthods.
-4dt'Ltnce,s in Neurolog.r,. I 5. 207 224.
Robirrson, D., Wu. I I.. lVlunne, R.A.. Ashtari. ivl.. Alvir, J.M., Lemer
G.. Koreen. A. Colc. K.. & Bogcrts. B. (199-5). Reduced caudate nucleus volume in obsessive-conrpulsivc disorder.
lrcltives
ol Generttl Ps.r'<hiatrl', Jl. 393 398.
Rosenberg. D.R.. Keshavan. M.S.. O'llearn. K.M.. Dick. E.L..
Bagwell. W.W.. Seynrour'. A.8.. It{ontrosc, D.M.. Picrri. J.N.,
Sainl-Cyr, .1.A.. Taylor. A.E.. & Nicholson, K. (1995). Behavior
and thc basal ganglia. Atlvances in Neurolog.t,,65, I 28.
Sarazin, M.. Deweer. 8.. Merkl. A.. Von Poser. N.. Pillon. 8., &
Dubois. B. (2002). Procedural learning and striatofrontal dysfunction in Parkinson's disease. ,ÿlovement Disorders, 17,
265 273.
Savage, C.R.. Baer, L., Keuthen, N.J.. Brorvn. H.D.. Rauch. S.L.,
& Jcnike. M.A. (1999). Organizational strategics nrediate nonverbal r.nernory irnpairment in obscssive-compulsive disorder.
Biological Ps1'chiatry.4j, 905 916.
Savage. C.R.. Deckersbach. T., Wilhelnr, S., Ratrch. S.L.. Baer, L.,
Reid. T., & .lenike, M.A. (2000). Strategic processing and episodic nrenrory inrpairnrent in obsessive compulsive disordcr.
Neuropsycholog.r,. 14. l4l l5l.
Savage. C'.R.. Keuthen. N.J.. Jenike. M.A., Brown, ILD.. Baer. L..
Kendrick. A.D.. Miguel. E.C.. Rauch. S.L., & Alpert. lv4.S.
996). Recall and recognition nlelrory in obsessive-compulsive
disorder. .kturnul of Neurops.w:hiatry uncl CIinic'ttl Neuros<:i(
1
ent'es.8.99
103.
Saxena, S.. Bota, R.G.. & Brody, A.L. (2()0 11. Brain-behavior
relationships in obsessive-compulsive disorder. Senrinors in
Clinical Ncutopsl'chiatr.r,. 6. 82 l0l.
Saxena. S.. Brotly.4.L.. Ho, M.L., Alborzian. S.. Maidnrent. K.M.,
Zohrabi, N.. Ho. M.K. FIuang. S.C., Wu. H.M., & Baxter, L.R.
(2002). Differc-ntial cerebral rnetabolic changes with paroxetine treatlnent ofobsessivc-compulsive disorder vs. major depression. ,4irliives o/ General Ps.t'chiatr.r,^ 59,250 261.
Saxentr. S. & Rauch. S. L. (2000). Functional neuroinraging and
the neuroanatolry ol'obsessive-compulsivc disorder. Psychiatric' Olinics ol Norrh .lntericu.2J. 563 586.
Schwartz, .1.M. (1998). Ncuroanatornical aspects of cognitivcbehavioural therapy response in obsessive-corripulsive disor-
der. An evolving perspective on brain and behaviour. Bnllslr
Journal oJ Psla'hiqlvy 5upplemenîum (35), 38-41.
Sheppard. f).M.. Bradsharv. J.L.. Purcell. R.. & Pantelis. C. (1999).
Tourctte's and conrorbid syndromes: Obsessive conrpulsive and
attention deficit hyperactivity disorder. A conrmon etiology'l
Clinical Psvcholog.r' Àelleu', 19.531 552.
Skoog. G. & Skoog. I. (1999). A 40-year follow-up of patients
n,ith obsessive-compulsive disorder. .4rchiyes ol GeneruI Ps1-
chiittry, 56, l2l-127.
Spielbergcr, C.. Montouri. F-.. & Luschene. R. (1970). Stote-Troit
An.riery lnvenror.l, (STAI l"orm C I ). Palo Alto. CA: Consulting
Psychologists Press.
& Strauss" E. (1998). A conpeniliunt ol neuropst,chologicol tests (2ntl ed.). New York: Oxfbrd University Press.
Squire. t-.R. (1986). lVlechanisms ol menrory. Sr:ience. 2.]2.
Spreen, O.
I
612 l6l
9.
Squire. L.R. &Zola, S.M. (1996). Structureand functionofdeclarative and nondeclarative memory systems. Ptoceedings of tlte
National .4caclenrv ol St'ie nces ol the United States of Anrcrita.
9J. t3515 13522.
& Birmaher, B ( I 997 ). Frontostriatal lueasurernent in treâtmentnaive childrcn rvith obscssive-conrpulsive disorder. .4rchives
ol Generul Ps.t'chiatr.t.54. 824 ti30.
Roih, R.M.. Saykin. A.J.. Wishart. l'1.A." F-lashrnan. L.A., Ward. J..
& Marnourian. A.C. (2003 ). An flvlRI study ot'brain actir ation
during irnlrlicit learning in OCD. Journul oJ Nerntps.lchiutry
Stebbins, G.T.. Singh. .1.. Weiner. J., Wilson, R.S.. Goetz. C.G., &
Gabricli. J.D.E. ( 1995). Selective impairmcnts of rncmory functioning in unnredicated adults rvith Gilles de la Tourette's syndrorne. Àtro o7r.ry'c hologl', 9, 329 337 .
Szeszko, PR., Robinson. D.. Alvir. J.lr'1.. Bilder, R.M.. Lensz. T..
Ashtari. M.. Wu. H.. & Bogerts. B. ( 1999). Orbital lrontal and
atul Clini<'ul Neuro,tc ien<'es, I 5, 262.
Sabc, L.. Jason. L., Juejati. NL. Lciguartia. R., & Starkstein, S.E.
( I 995). Dissociation betrvecn dcclarative and procedural leârning in derrrcntia and dcpression. Journttl ol Clinical und Expcr-
anrygdala volurne reductions in obsessive-compulsive disordcr. .4rcftilc,s ol Generul Ps.tchiatn', -16. 913 919.
van Gorp. W.C.. Altshuler, L.. Theberge, D.C.. & Mintz, J. ( 1999).
Declarative and procedural melnory in bipolar disorder. Biologic a I Ps.t <:lt iatry. 4 6, 525 -53 l.
inerial Nettropsrchologv.
1
Z.
841
84t1.