Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa
Xosé Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain).
Email: [email p o ec ed]
1
Ti le: Changes in isual memo y in mild cogni i e impai men . A longi udinal s udy
wi h CANTAB.
Au ho s: Ma ía Campos-Magdaleno1, Da id Lei a2, A u o X. Pe ei o1, C is ina Lojo-
Seoane1, Sabela C. Mallo1, Da id Facal1 & Onésimo Juncos-Rabadán1
Filia ions: 1. Depa men o De elopmen al Psychology, Uni e si y o San iago de
Compos ela, Galicia, Spain. 2. Depa men o Me hodology o Beha iou al Sciences,
Uni e si y o Ba celona, Ca alunya, Spain
Numbe o wo ds: 5658
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa
Xosé Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain).
Email: [email p o ec ed]
2
Abs ac
Backg ound: Mild cogni i e impai men (MCI), as a s age in he cogni i e con inuum
be ween no mal aging and demen ia, is mainly cha ac e ized by memo y impai men .
The aims o his s udy we e o examine CANTAB measu es o empo al changes o
isual memo y in MCI and o e alua e he use ulness o he baseline sco es o
p edic ing changes in cogni i e s a us.
Me hods: The s udy included 201 pa icipan s aged o e 50 yea s wi h subjec i e
cogni i e complain s. Visual memo y was assessed wi h ou CANTAB es s (PAL,
DMS, PRM and SSP) adminis e ed a baseline and on wo u he occasions, wi h a
ollow-up in e al o 18-24 mon hs. Pa icipan s we e di ided in o h ee g oups
acco ding o he change in hei cogni i e s a us: pa icipan s wi h subjec i e cogni i e
complain s who emained s able (SCC-S able), MCI pa icipan s who emained s able
(MCI-S able) and MCI pa icipan s whose cogni i e de e io a ion con inued (MCI-
Wo sened). Linea Mixed Models we e used o model longi udinal changes, wi h
e alua ion ime as a ixed a iable, and mul inomial eg ession models we e used o
p edic changes in cogni i e s a us.
Resul s: Isola ed signi ican e ec s we e ob ained o Age and G oup wi h all CANTAB es s
used. In e ac ions be ween E alua ion Time and G oup we e iden i ied in he PAL and DMS
es s, indica ing di e en empo al pa e ns depending on he changes in cogni i e s a us.
Reg ession models also indica ed ha CANTAB sco es we e good p edic o s o changes in
cogni i e s a us.
Conclusions: Decline in isual memo y measu ed by PAL and DMS es s can success ully
dis inguish di e en ypes o MCI, and conside ed oge he PAL, DMS, PRM and SSP can
p edic changes in cogni i e s a us.
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
3
Keywo ds: isual memo y; CANTAB es s; mild cogni i e impai men ; linea mixed models;
longi udinal assessmen .
In oduc ion
Cogni i e decline in he elde ly can be conside ed a con inuum anging om a
cogni i ely unimpai ed s a e (CU), o he p esence o subjec i e cogni i e complain s (SCC)
wi hou objec i e cogni i e impai men , also called Subjec i e Cogni i e Decline (SCD)
(Jessen e al., 2016; Molinue o e al., 2017), ollowed by Mild Cogni i e Impai men (MCI),
cha ac e ized by p esence o cogni i e complain s, objec i e cogni i e de e io a ion and
p ese a ion o minimal impai men o ins umen al ac i i ies o daily li ing (Pe e sen, 2004;
Pe e sen e al., 2018), and inally demen ia, which is cha ac e ized by cogni i e and
beha iou al symp oms ha impai no mal unc ioning in daily li e (APA, 2013). The single
and mul iple domain sub ypes o amnes ic and non-amnes ic MCI ha in ol e de e io a ion in
only one o in mo e han one cogni i e domain may also ep esen di e en le els o
cogni i e decline, wi h he mul iple domain sub ype being he mos ex eme clinical s a e
(B amba i e al., 2009; Han e al., 2012). P og ession along he con inuum is a complex
p ocess cha ac e ized by cogni i e changes, ansi ions and diagnos ic ins abili y a SCD and
MCI s ages, con e sion o demen ia and eco e y o CU (Facal, Guà dia-Olmos & Juncos-
Rabadán 2015; Pe e sen e al., 2018). Howe e , aking he ins abili y in o accoun , MCI and
he sub ypes cha ac e ized by only memo y impai men s (amnes ic single-domain) o by
impai men s in memo y and in o he cogni i e domains (amnes ic mul i-domain) a e
conside ed high- isk s a es o p og ession o demen ia, mainly Alzheime ’s Disease (AD).
Ea ly de ec ion o he di e en s ages o cogni i e decline and he p og ess o decline is a
p essing esea ch challenge in he p e en ion and ea men o demen ia (Albe e al., 2011;
Pe e sen e al., 2018).
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
4
P e ious s udies ha e shown ha isual memo y impai men can di e en ia e MCI
pa ien s om cogni i ely unimpai ed con ols (Alescio-Lau ie e al., 2007; Ba beau e al.
2008; Juncos-Rabadán, Facal, Pe ei o & Lojo-Seoane, 2014a; Wes e be g e al., 2013). O he
s udies ha e success ully p edic ed he p og ession om MCI o AD (De Anna e al., 2014;
De ancesco e al., 2013; Didic e al, 2013; Ol a-Cuca ella e al., 2018; Reijs e al, 2017;
Sax on e al., 2004) and e en comple e neu odegene a i e p og ess om he cogni i ely
impai ed s a e o MCI and AD (Mis idis, K umm, Monsch, Be es & Taylo , 2015). These
indings indica e he impo ance o including eliable isual memo y es s o diagnosing MCI
and o s udying he cou se o decline in di e en aspec s o isual memo y in p og ession o
AD.
Compu e ized assessmen o isual memo y using he Camb idge Neu opsychological
Tes Au oma ed Ba e y (CANTAB; Camb idge Cogni ion L d., 2012; Sahakian e al., 1988)
has been used o di e en ia e con ols, MCI and AD pa icipan s in c oss-sec ional s udies
(Alladi, A nold, Mi chell, Nes o & Hodges 2006; de Ro e e al., 2011; Juncos-Rabadán e
al, 2014a; Junkkila, Oja, Laine & Ka asch, 2012; Swaison e al., 2001). CANTAB includes
es s ha assess isual Episodic Memo y (EM) and isual Wo king Memo y (WM). Bo h
ypes o memo y ha e been shown o be impai ed ea ly on in AD (Belle ille, Syl ain-Roy,
de Boysson & Ména d, 2008; Economou, Papageo giou & Ka ageo giou, 2011; an Geld op
e al., 2015). De e io a ion in EM has been ound o be a pa icula ly s ong p edic o o
p og ession o AD (Belle ille e al., 2008; Landau e al., 2010).
Longi udinal e idence om esea ch using he CANTAB isual memo y es s emains
sca ce (Cacciamani e al., 2017; Juncos-Rabadán e al., 2016; Mi chell, A nold, Dawson,
Nes o & Hodges, 2009; Summe s and Saunde s, 2012). Summe s and Saunde s (2012) ound
ha he decline in isual memo y pe o mance assessed wi h CANTAB measu es (Pai ed
Associa es Lea ning, Spa ial Span, Spa ial Wo king Memo y) in combina ion wi h he Rey
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
5
Audi o y Ve bal Lea ning Tes iden i ied 100% o cases o MCI pa ien s who p og essed o
AD a e 20 mon hs. Howe e , Cacciamani e al. (2017) epo ed imp o emen s in Spa ial
Wo king Memo y, Spa ial Recogni ion Memo y and Pai ed Associa ed Lea ning a e a
ollow-up pe iod o 12 mon hs in a small sample o MCI pa ien s. Fu he in es iga ion
including la ge sample sizes and longe in e als be ween assessmen s mus be ca ied ou o
analyze he disc iminan alue and e olu ion o hese memo y measu es.
The main pu pose o he p esen s udy was o de e mine longi udinal pa e ns o
pe o mance o isual memo y CANTAB es s in pa ien s diagnosed a baseline wi h MCI and
assessed wice wi h a ollow-up in e al o a ound 18 mon hs o measu e s abili y o
de e io a ion o he condi ion. A seconda y aim was o assess he use ulness o baseline
CANTAB measu es o p edic ing changes in cogni i e s a us a he inal ollow-up s age.
Me hodology
Pa icipan s
Pa icipan s we e selec ed om he Compos ela Aging S udy (CompAS), an ongoing
longi udinal p ojec in ol ing he de ec ion and ollow-up o Mild Cogni i e Impai men in
pa ien s wi h subjec i e cogni i e complain s and no p io diagnos ic o demen ia, psychia ic
o neu ological diso de s a ending p ima y ca e cen es in Galicia, an au onomous egion in
no hwes Spain (Juncos-Rabadán e al., 2012). We selec ed 201 pa ien s aged o e 50 yea s
who had comple ed 3 isi s (a Baseline, Time 1 and Time 2) wi h a be ween- es in e al o
a ound 18 mon hs. The mean in e al was 18.49 mon hs (3.64 s anda d de ia ion, SD)
be ween Baseline and Time 1, 17.72 mon hs (3.81 SD) be ween Time 1 and Time 2, and
36.83 mon hs (5.17 SD) be ween Baseline and Time 2. None o he pa icipan s had
p e iously been diagnosed wi h MCI o demen ia, clinical s oke, auma ic b ain inju y,
mo o -senso y de ec s, alcohol o d ug abuse/dependence, o any neu ological o psychia ic

Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
6
disease. A baseline, pa icipan s we e classi ied as single-domain amnes ic MCI (sda-MCI),
mul iple-domain amnes ic MCI (mda-MCI), single-domain non amnes ic MCI (sdna-MCI) o
mul iple-domain non amnes ic MCI (mdna-MCI), acco ding o s anda d c i e ia (Albe e al.,
2011; Dubois e al., 2007; Pe e sen, 2004). The c i e ia o diagnosis o MCI included he
ollowing: (a) sel - epo ed, in o man -co obo a ed conce ns abou cogni ion, assessed by a
sho e sion o he subjec i e memo y complain s ques ionnai e (SMCQ; Benede and
Seisdedos, 1996); (b) pe o mance o 1.5 s anda d de ia ions (SD) below age and educa ion
no ms in one o mo e cogni i e domains, assessed by he subscales o he Spanish e sion o
he Camb idge cogni i e examina ion, CAMCOG-R (Huppe e al., 1996; Spanish e sion:
López-Pousa, 2003; Pe ei o, Ramos-Lema, Juncos-Rabadán, Facal & Lojo-Seoane, 2015),
excep o memo y, assessed by he sho and long delay ee ecall om he Spanish e sion
o he Cali o nia e bal lea ning es (Delis e al., 1987; Spanish e sion: Benede and
Alejand e, 1998); (c) no signi ican o minimal impac on ac i i ies o daily li ing, assessed
by ins umen al ac i i ies o daily li ing scale (Law on and B ody, 1969); and (d) he absence
o demen ia as es ablished by he DSM-IV and NINCDS-ADRDA c i e ia. Pa icipan s
pe o ming as cogni i ely no mal adul s in gene al unc ioning and speci ic domain es s,
acco ding o no ms by age and yea s o educa ion, and p esen ing subjec i e cogni i e
complain s (SCC), we e included in he SCC g oup. This g oup me he ollowing c i e ia: (a)
a ending p ima y ca e heal h cen es wi h sel - epo ed cogni i e conce ns; and (b)
con i ma ion o hese conce ns by he sho Spanish e sion o he ques ionnai e o
subjec i e memo y complain s (Benede and Seisdedos, 1996) adminis e ed o pa icipan s
and a amily membe . The SCC g oup was conside ed a con ol g oup. All diagnoses we e
eached by consensus a a special mee ing o he esea ch eam.
In each successi e ollow-up assessmen , pa icipan s we e eclassi ied as SCC, sda-
MCI, mda-MCI, sdna-MCI, mdna-MCI and p obable demen ia (DSM-IV and NINCDS-
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
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ADRDA) by applying he same c i e ia as a baseline. A he hi d e alua ion, pa icipan s
we e classi ied in o h ee g oups acco ding o he changes in hei cogni i e s a us:
pa icipan s wi h SCC a Baseline who emained s able a Time 2 (SCC-s able g oup, n=148,
71.49%); pa icipan s diagnosed wi h MCI a Baseline who emained s able a Time 2 (MCI-
s able g oup, n= 31, 15.45%); and pa icipan s diagnosed as sda-MCI o sdna-MCI a Baseline
who p og essed o mda-MCI, mdna-MCI o demen ia a Time 1 o Time 2 (MCI-wo sened
g oup, n= 22, 13.04%). P obable AD o o he ypes o demen ia we e diagnosed acco ding o
he DMS-IV and NINCDS-ADRDA c i e ia, and p og ession o demen ia was con i med by
consul a ion o he medical his o y and eco ding he da e o neu ological diagnosis. We
assumed, in acco dance wi h B amba i e al. (2009) and Campos-Magdaleno, Díaz-Bó eda,
Juncos-Rabadán, Facal & Pe ei o (2016), ha he change om single-domain o mul iple-
domain co esponds o cogni i e wo sening, in which mul i-domain MCI ep esen s he mos
se e ely impai ed o he MCI sub ypes.
All pa icipan s ga e hei w i en in o med consen p io o pa icipa ion in he s udy.
The esea ch p ojec was app o ed by he Galician E hics Commi ee o Clinical Resea ch
(Xun a de Galicia, Spain), and he s udy was pe o med in acco dance wi h he e hical s anda ds
es ablished in he 1964 Decla a ion o Helsinki and e ised in Seoul 2008.
Ma e ials and P ocedu e
Fou CANTAB isual memo y es s we e adminis e ed: pai ed associa es lea ning (PAL),
pa e n ecogni ion memo y (PRM), delayed ma ching o sample (DMS) and spa ial span (SSP).
The PAL es assesses isuospa ial episodic memo y and lea ning (Sahakian e al., 1988). One
o mo e boxes con aining a pa e n a e displayed on he sc een and a e opened in a andom
o de . The pa e ns shown in he boxes a e hen displayed in he middle o he sc een, one a a
ime, and pa icipan s a e asked o ouch he box in which he pa e n was o iginally loca ed. I
he pa icipan makes an e o , he pa e ns a e shown again as a eminde o he loca ions. The
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
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le el o di icul y (2, 4, 6 and 8 pa e ns) was inc eased h oughou he es s. The ou come
a iable was he o al numbe o e o s adjus ed o le el 6, which ep esen s a high le el o
di icul y and has been used by se e al esea che s o s udy MCI and AD (Alladi e al., 2006;
Chambe lain e al., 2011; Lenehan e al., 2016; Mi chell e al., 2009; Polche e al., 2017). The
PRM es assesses isual pa e n ecogni ion memo y in a wo-choice o ced disc imina ion
pa adigm (Swainson e al., 2001). The pa icipan s we e p esen ed wi h wo blocks o 12 isual
pa e ns, each displayed sepa a ely. In he ecogni ion phase, subjec s a e equi ed o choose
be ween a pa e n hey ha e al eady seen and a no el pa e n. The ou come measu e was he
pe cen age o co ec esponses, conside ed in some p e ious s udies as a speci ic episodic
memo y ou come (de Jage , Milwain & Budge, 2002; Juncos-Rabadán, Pe ei o, Facal,
Rebo edo & Lojo-Seoane, 2014b; Na han e al., 2017). Delayed ma ching o sample (DMS)
assesses bo h simul aneous and sho - e m isual memo y (Sahakian e al., 1988; Owen e al.,
1993). Pa icipan s mus selec he pa e n ha exac ly ma ches he sample om among ou
abs ac choices ha include dis ac o s. In some ials, he sample and he choice pa e ns a e
shown simul aneously, while in o he s he e is a delay o 0 ms, 4,000 ms o 12,000 ms. The
ou come measu e was he pe cen age o co ec esponses, also conside ed an episodic memo y
measu e ask (Juncos-Rabadán e al., 2014b, 2016; Sweeney, Kmiec & Kup e , 2000). Spa ial
span (SSP) is a compu e ised e sion o he Co si blocks ask ha assesses isual wo king
memo y capaci y (Owen e al., 1990). A pa e n o whi e squa es is shown on he sc een. Some
o he squa es change colou , one a a ime, in a a iable sequence. A he end o he p esen a ion
o each sequence, a one indica es ha he pa icipan should ouch each o he boxes in he
same o de ha hey we e o iginally p esen ed. The numbe o boxes in he sequence is
inc eased om a le el o wo a he s a o he es un il a inal le el o nine, wi h h ee
sequences a each le el. The ou come a iable, he span leng h, was calcula ed o he longes
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9
sequence success ully ecalled and was used as index o he SSP ask (Saunde s and Summe s,
2010).
The ou CANTAB es s we e adminis e ed in a mo e ex ensi e coun e balanced
assessmen ca ied ou by ained psychologis s. To con ol o he e ec o isual acui y on
pe o mance o he CANTAB, we measu ed he isual acui y o bo h eyes wi h he Ligh house
nea isual acui y es .
S a is ical analysis
C oss-sec ional analyses we e ca ied ou a baseline o socio-demog aphic and
p incipal neu opsychological measu es, which we e modelled using non-pa ame ic es s (e.g.
K uskal-Wallis and Mann-Whi ney es s) o de e mine di e ences be ween g oups, gi en he
skewed empi ical dis ibu ions and he small sample size in some cases. In o de o model
longi udinal changes in he CANTAB measu es, we ini ially used (gene alized) linea mixed
models -(G)LMM- wi h andom in e cep s and andom slopes. We conside ed ha he
in e cep s migh di e acco ding o he memo y ajec o ies o he pa icipan s and ha di e en
slopes would ep esen a ious empo al pa e ns o change in memo y pe o mance. We inally
disca ded andom slopes in he es ima ed models due o con e gence issues. The s a is ical
models included he ollowing independen a iables o p edic o s as ixed e ec s: E alua ion
Time (Baseline, Time 1 and Time 2), G oup (SCC-s able, MCI-s able and MCI-wo sened), and
hei in e ac ion (E alua ion Time x G oup). By speci ying G oup and E alua ion Time as ixed
ac o s we can es pai wise compa isons o he es ima ed ma ginal means o he dependen
a iables o each g oup and a each e alua ion ime. As all models included andom e ec s o
in e cep s and he e oskedas ici y due o he g oup, he co a ia e age a baseline was
s anda dized o enable in e p e a ion o he in e cep . Sepa a e models we e cons uc ed o each
dependen a iable: PAL o al e o s adjus ed o 6 shapes, PRM o al pe cen co ec , DMS
o al pe cen co ec , and SSP span leng h. The SCC-s able g oup was conside ed he e e ence
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16
ou comes di e en ia ed pa icipan s who showed no cogni i e impai men (SCC-S able) and
pa icipan s wi h MCI, and e en be ween MCI pa icipan s who emained s able o wo sened.
The esul s indica e ha assessing isual memo y wi h CANTAB measu es may be use ul o
di e en ia ing be ween di e en s ages o MCI in he cogni i e con inuum o demen ia.
Es ima ed simple and mul iple mul inomial logis ic models used o assess he u ili y o
CANTAB sco es a he ini ial s age o p edic cogni i e e olu ion a he end o he s udy p o ed
o ha e a good o e y good p edic i e capaci y (AUCs be ween 0.71 o 0.86; see sec ion S1 o
Supplemen a y Ma e ial o u he in o ma ion ega ding he model es ima es and
pe o mance). In summa y, he models showed ha he highe he isual memo y sco e he
lowe he isk o being classi ied in he g oup wi h he wo s cogni i e ou look.
The age o pa icipan s a baseline signi ican ly in luenced pe o mance o all es s o e
ime. Olde pa icipan s sco ed lowe on all measu es, ega dless o he diagnos ic g oup (SCC-
s able, MCI-s able, MCI-wo sened). The in luence o age on he pe o mance in he CANTAB
isual memo y es s o old adul s wi h MCI and wi hou cogni i e impai men has been
documen ed in c oss sec ional s udies (Juncos-Rabadán e al., 2014a). The cu en indings add
new e idence om a longi udinal design.
The s udy indings also show a main e ec o G oup, wi h he MCI-wo sened g oup
ob aining he wo s sco es in all CANTAB measu es used a he h ee e alua ion imes. This
g oup comp ised pa icipan s wi h g ea e cogni i e impai men , who we e ound o ha e
p og essed o mul iple-domain MCI o demen ia a ei he o he ollow-up e alua ions. The
p o ile wi h wo s pe o mance in isual memo y es s o mul iple-domain MCI has al eady
been shown in p e ious s udies (Juncos-Rabadán e al., 2014b). Ou esul s suppo he capaci y
o he CANTAB isual memo y es s o show di e en pe o mance p o iles and disc imina e
be ween g oups in he cogni i e con inuum om no mal aging o demen ia, and sugges he use
o hese es s o ea ly diagnosis o cogni i e impai men . The indings ob ained wi h CANTAB

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sco es a e consis en wi h some addi ional analyses done o e i y ha cogni i e decline is
signi ican ly mo e p onounced in MCI g oups. The indings showed ha he changes di e ed
signi ican ly in he h ee s udy g oups and ha he indi iduals included in he MCI-wo sened
g oup showed he mos nega i e changes in he gene al cogni i e pe o mance.
Rega ding he main e ec o he a iable E alua ion Time, he PAL es was he only
measu e ha indica ed signi ican di e ences a he h ee e alua ion momen s in all
pa icipan s. This signi ican main e ec adds new e idence o p e ious s udies on he u ili y
o he PAL o assess isual memo y and lea ning in old adul s wi h and wi hou cogni i e
impai men (Fowle , Saling, Conway, Semple & Louis, 2002; Junkkila e al., 2012; O'Connell
e al., 2004; Polche e al., 2017). Mo eo e , ou esul s indica e ha he PAL measu e can
de ec changes in longi udinal pe o mance ela ed o e olu ion along a con inuum o cogni i e
decline. Taking in o accoun ha longi udinal esea ch is sca ce, his inding is an impo an
con ibu ion and adds e idence o he pionee ing wo k by Blackwell and colleagues (Blackwell
e al., 2004), who obse ed ha he same CANTAB measu e was signi ican ly co ela ed wi h
he deg ee o subsequen cogni i e de e io a ion in he ea ly s ages o AD.
The mos in e es ing indings o he p esen s udy a e he signi ican in e ac ions be ween
E alua ion Time x G oup in he PAL and DMS measu es. Rega ding he PAL o al e o s
adjus ed-6 shapes, he in e ac ion was signi ican o he MCI-s able and he MCI-wo sened
g oups, indica ing he exis ence o speci ic longi udinal pa e ns o pe o mance o each. The
ma ginal means indica e a small inc ease in e o s in he SCC-s able g oup be ween he baseline
and he ollow-up e alua ions, while in bo h MCI g oups he e o s inc eased signi ican ly in
he same pe iods. The inc ease was mo e impo an o he MCI-wo sened g oup. The
di e ences in PAL empo al pa e ns indica e a decline in he pe o mance o e ime o all
g oups; howe e , hey also enable disc imina ion be ween he leas cogni i ely impai ed g oup
(SCC-s able) and he MCI g oups, as well as be ween he MCI g oup ha emain s able (MCI-
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[email p o ec ed]
18
s able) and he MCI g oups in which u he de e io a ion occu s (MCI-wo sened). Ou indings
add a new pe spec i e o hose epo ed by Cacciamani e al. (2017), who obse ed a ma ked
imp o emen in PAL when compa ing he baseline pe o mance wi h he 6-mon h ollow-up,
bu no di e ence in pe o mance be ween 6- and 12-mon h ollow-ups. This imp o emen may
be he esul o a p ac ice e ec due o he sho ollow-up pe iod; howe e , he p ac ice e ec
may disappea when longe ollow-up in e als be ween PAL es s a e used in longi udinal
assessmen s.
Rega ding he DMS, he E alua ion Time x G oup in e ac ion was only signi ican in he
MCI-wo sened g oup, in which he es pe o mance declined o e ime. The pe o mance o
he o he wo g oups, SSC-s able and MCI-s able, did no a y signi ican ly. The E alua ion
Time x G oup in e ac ion was no signi ican o ei he he PRM o al pe cen co ec o SSP
span leng h. Howe e , he es ima ed ma ginal means showed signi ican di e ences be ween
SCC-s able and MCI-wo sened g oups, indica ing a clea decline in he la e g oup o e ime.
The measu es in which a signi ican E alua ion Time x G oup in e ac ion was obse ed
co espond o he wo CANTAB es s (PAL and DMS) mos closely ela ed o episodic memo y
(de Jage e al., 2002; Juncos-Rabadán e al., 2014a, 2014b, 2016; Na han e al., 2017; Sweeney
e al., 2000). PAL in ol es isuospa ial episodic memo y and lea ning, and DMS in ol es
sho - e m memo y o complex isual pa e ns. Decline in episodic memo y has been desc ibed
as one o he mos po en p edic o s o p og ession o Alzheime 's disease (Belle ille e al.,
2008; Landau e al., 2010), and ou esul s show ha he PAL o al e o s adjus ed-6 shapes and
he DMS o al pe cen co ec enable de ec ion o longi udinal changes ha may be indica i e
o p og ession in he con inuum o cogni i e de e io a ion.
Howe e , he measu es he PRM o al pe cen co ec and he SSP span leng h ha di e ed
signi ican ly be ween g oups (G oup main e ec ) did no indica e di e ences be ween g oups
o e ime (E alua ion Time x G oup in e ac ion). PRM in ol es memo y and subsequen
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[email p o ec ed]
19
ecogni ion o sequences o isual pa e ns, which may be ela ed o he a en ional span
capaci y, which is associa ed wi h wo king memo y. In p e ious s udies, con adic o y indings
ega ding span leng h as a measu e o wo king memo y ha di e en ia es pa icipan s
acco ding o diagnosis and p og ession ha e been epo ed. While a la ge numbe o s udies
suppo he exis ence o impai men in span leng h p io o diagnosis o demen ia (Belle ille e
al., 2017; Economou e al., 2006; Gagnon and Belle ille, 2011; an Geld op e al., 2015;
Saunde s and Summe s, 2010), o he s udies ob ained con adic o y o non-meaning ul esul s
(G i i h e al., 2006; Gua ch, Ma cos, Salame o, Gas ó, & Blesa, 2008; Kessels, O e beek, &
Bouman 2015), ques ioning he alue o he measu e o ea ly de ec ion o cogni i e
impai men . Ou indings indica e ha he PRM measu e and he SSP span canno di e en ia e
longi udinal pa e ns be ween g oups.
We conclude ha isual episodic memo y declines in people wi h MCI o e ime and ha
his decline may be a cogni i e indica o o he p og ession in he con inuum anging om he
s age cha ac e ized by p esence o cogni i e complain s wi hou objec i e cogni i e impai men
o demen ia, h ough he di e en le els o se e i y o MCI. PAL o al e o s adjus ed-6 shapes
ou come, and DMS pe cen co ec o al measu es di e en ia e he changes in pa icipan s in
he con inuum o cogni i e de e io a ion: people wi h and wi hou objec i e de e io a ion, and
people who wo sen o emain s able o e ime. In addi ion, he be ween-e alua ion in e als
used in longi udinal s udies should be wide enough o p e en p ac ice e ec s.
Membe ship o g oups cha ac e ized by change in cogni i e s a us de eloped a he second
ollow-up s age (T 2) has p o en o be accu a e in he ligh o di e en ypes o e idence. Fi s ,
a di e en pa e n o change was obse ed in CANTAB measu emen s acco ding o his
classi ica ion. Secondly, di e en pa e ns o change we e also obse ed in o he cogni i e
sco es such as MMSE and CAMCOG-R when compa ing he g oups included in his s udy.
Finally, compa ison o membe ship in g oups ob ained by he p ocedu e desc ibed in his s udy
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20
wi h a classi ica ion ob ained by means o non-pa ame ic clus e ing o mul i a ia e ajec o ies
(i.e. indi idual ajec o ies in he 4 CANTAB sco es) e ealed a simila i y index o 0.74, which
indica es a good le el o ag eemen . In summa y, we demons a ed ha he isual CANTAB
sco es a) a e use ul o p edic ing cogni i e e olu ion in he ime-pe iod included in his s udy,
b) di e o e ime depending on he change in cogni i e s a us o indi iduals, and c) allow
esea che s o classi y indi iduals consis en ly in compa ison wi h o he cogni i e ou comes
(i.e. clinical assessmen a he second ollow-up).
The limi a ions o he p esen s udy include he ac ha only one g oup o pa ien s wi h
MCI ha wo sened o e ime was conside ed. By no ha ing a la ge numbe o pa icipan s in
whom de e io a ion ended o wo sen, i was no possible o di e en ia e people who p og ess
o mul iple-domain MCI om hose who p og ess o demen ia, and bo h we e included wi hin
he same g oup. This hinde s in e p e a ion o he esul s, as al hough he pa icipan s p og ess
in he same di ec ion o he con inuum o cogni i e de e io a ion, hey show impo an
di e ences ega ding he deg ee o cogni i e impai men and unc ional capaci y. Di e ences
be ween bo h ypes o pa icipan s in hei CANTAB longi udinal p o iles should be conside ed
in u u e s udies. On he o he hand, he in e al o hi y-six mon hs be ween baseline and he
inal e alua ion may no be long enough o ull assessmen o he p og ess. We hope in he
u u e o be able o collec longi udinal da a o e a longe pe iod o ime, as he cu en
longi udinal esea ch is s ill ongoing. We expec o conduc a hi d ollow-up e alua ion o
assess changes ha ha e occu ed in a pe iod o app oxima ely 54 mon hs (4.5 yea s) a e
baseline.
Financial suppo
This esea ch was suppo ed h ough FEDER ounds by he Spanish Di ec o a e Gene al
o Scien i ic and Technical Resea ch (P ojec Re . PSI2014-55316-C3-1-R), he Na ional
Resea ch Agency (Spanish Minis y o Science, Inno a ion and Uni e si ies) (P ojec Re .
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
21
PSI2017-89389-C2-1-R) and by he Galician Go e nmen (Conselle ía de Cul u a, Educación
e O denación Uni e si a ia; axudas pa a a consolidación e es u u ación de unidades de
in es igación compe i i as do Sis ema Uni e si a io de Galicia; GI-1807-USC: Re . ED431-
2017/27).
Con lic s o in e es .
None.
E hical s anda ds
The au ho s asse ha all p ocedu es con ibu ing o his wo k comply wi h he e hical
s anda ds o he ele an na ional and ins i u ional commi ees on human expe imen a ion and
wi h he Helsinki Decla a ion o 1975, as e ised in Seoul 2008.
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Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
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Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
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Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
32
Table 1. Mean and s anda d de ia ions (in pa en heses) o he demog aphic and
neu opsychological measu es a baseline o he h ee g oups: subjec i e cogni i e complain s
(SCC) ha emain s able (SCC-s able); mild cogni i e impai men ha emain s able (MCI-
s able); mild cogni i e impai men ha wo sened (MCI-wo sened).
No e: MMSE= MiniMen al S a e Examina ion CCI=Cha lson Como bidi y Index. SCC: Subjec i e Cogni i e
Complain s (pa ien ). CAMCOG= Camb idge Cogni i e Examina ion ( o al sco e). CVLT SDFR= Cali o nia
Ve bal Lea ning Tes , Sho Delay F ee Recall. CVLT LDFR= Cali o nia Ve bal Lea ning Tes , Long Delay F ee
Recall. Visual Acui y = Ligh house es .
*= p < .05
**= p < .01
SCC-s able
G oup 1
N=149
MCI-s able
G oup 2
N=32
MCI-wo sened
G oup 3
N=27
K uskal Wallis
χ²(gl)
G oup
compa ison
Age
64.26 (8.83)
Range:50-87
70.94 (7.54)
Range: 54-83
75.44 (7.14)
Range: 61-87
39.46 (2)**
G3 > G2 > G1
Gende
Women: 70.3%
Men: 29.7%
Women: 68.8%
Men: 31.3%
Women: 55.6%
Men: 44.4%
Yea s o
Educa ion
10.28 (4.71)
Range: 2-22
9.15 (3.40)
Range: 2-17
9.30 (4.79)
Range: 4-25
1.09 (2)
SCC
18.84 (4.54)
Range: 7-31
20.25 (4.09)
Range: 10-32
18.07 (4.64)
Range: 13-33
6.83 (2)*
G2 > G1, G3
Law on-
B ody
7.55 (.95)
Range: 4-8
6.8 (1.55)
Range: 3-8
6.15 (2.08)
Range: 2-8
17.29 (2)**
G1 > G2, G3
CCI
.76 (.84)
Range: 0-3
1.09 (1.02)
Range: 0-4
.70 (.86)
Range:0-3
3.65 (2)
MMSE
28.34 (1.34)
25.13 (2.89)
24.04 (2.53)
73.39 (2)**
G1 > G2, G3
CAMCOG
89.88 (6.96)
77.40 (8.99)
70.92 (10.08)
81.74 (2)**
G1 > G2 > G3
CVLT-
SDFR
11.01 (2.50)
4.50 (3.00)
2.37 (2.04)
113.20 (2)**
G1 > G2 > G3
CVLT-
LDFR
11.85 (2.57)
5.53 (3.77)
2.48 (2.43)
105.13 (2)**
G1 > G2 > G3
Visual
Acui y
.55 (.17)
Range: .20-1.00
.52 (.16)
Range: .20-.80
.53 (.18)
Range: .33-.80

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33
Table 2. Summa y o models compa ed o PAL o al e o s adjus ed-6 shapes. All models
include andom e ec s o in e cep s and age a baseline as co a ia e. Model 1 is he null
mixed model (i.e. andom in e cep s and age co a ia e only); Model 2 is he mixed model
wi h main e ec s; Model 3 is he mixed model wi h main e ec s and in e ac ions.
Coe icien s and s anda d e o s (in pa en heses) a e shown on a log scale o numbe o e o s
(i.e. na u al log o he esponse).
No e: ***p< 0.01
Dependen a iable: PAL o al e o s adjus ed-6 shapes
Model 1
Model 2
Model 3
Age a baseline
0.559***
(0.054)
0.379***
(0.051)
0.377***
(0.051)
E alua ion Time
0.036***
(0.009)
-0.032***
(0.012)
MCI-wo sened
1.065***
(0.153)
0.888***
(0.156)
MCI-s able
0.904***
(0.131)
0.780***
(0.134)
E alua ion Time x
MCI-wo sened
0.280***
(0.030)
E alua ion Time x
MCI-s able
0.137***
(0.021)
In e cep
3.403***
(0.054)
3.105***
(0.056)
3.170***
(0.057)
Obse a ions
624
624
624
Log Likelihood
-3,005.318
-2,965.740
-2,911.160
Akaike In . C i .
6,016.637
5,943.481
5,838.320
Bayesian In . C i .
6,029.561
5,969.329
5,872.785
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
34
Table 3. Summa y o model compa ison o PRM o al pe cen co ec . All models include
andom e ec s o in e cep s and age a baseline as co a ia e. Model 1 is he null mixed model
(i.e. andom in e cep s and age co a ia e only); Model 2 is he mixed model wi h main e ec s;
Model 3 is he mixed model wi h main e ec s and in e ac ions. Coe icien s and s anda d e o s
(in pa en heses)
No e: ***p< 0.01
Dependen a iable: PRM pe cen co ec o al
Model 1
Model 2
Model 3
Age a baseline
-5.430***
(0.656)
-3.439***
(0.599)
-3.460***
(0.599)
E alua ion Time
0.213
(0.379)
0.405
(0.405)
MCI-wo sened
-16.591***
(2.362)
-16.673***
(2.823)
MCI-s able
-12.344***
(1.645)
-10.625***
(1.967)
E alua ion Time x
MCI-wo sened
0.286
(2.471)
E alua ion Time x
MCI-s able
-1.974
(1.249)
In e cep
83.072***
(0.649)
85.735***
(0.731)
85.546***
(0.744)
Obse a ions
560
560
560
Log Likelihood
-2,055.846
-2,014.233
-2,010.012
Akaike In . C i .
4,123.691
4,046.466
4,042.024
Bayesian In . C i .
4,149.637
4,085.337
4,089.493
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
35
Table 4. Summa y o compa ed models o DMS o al pe cen co ec . All models include
andom e ec s o in e cep s and age a baseline as co a ia e. Model 1 is he null mixed
model (i.e. andom in e cep s and age co a ia e only); Model 2 is he mixed model wi h main
e ec s; Model 3 is he mixed model wi h main e ec s and in e ac ions. Coe icien s and
s anda d e o s (in pa en heses)
No e: ***p< 0.01
Dependen a iable: DMS o al pe cen co ec
Model 1
Model 2
Model 3
Age a baseline
-6.170***
(0.565)
-4.555***
(0.554)
-4.456***
(0.546)
E alua ion Time
0.212
(0.387)
0.563
(0.423)
MCI-wo sened
-12.014***
(1.831)
-7.677***
(2.038)
MCI-s able
-5.990***
(1.470)
-6.597***
(1.738)
E alua ion Time x
MCI-wo sened
-7.506***
(1.610)
E alua ion Time x
MCI-s able
-0.684
(1.096)
In e cep
78.252***
(0.565)
80.170***
(0.707)
79.847***
(0.720)
Obse a ions
555
555
555
Log Likelihood
-2,001.541
-1,975.448
-1,961.768
Akaike In . C i .
4,011.083
3,964.896
3,941.536
Bayesian In . C i .
4,028.344
3,995.065
3,980.292
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
36
Table 5. Summa y o models compa ed o SSP span leng h. All models include andom
e ec s o in e cep s and age a baseline as co a ia e. Model 1 is he null mixed model
( andom in e cep s and age co a ia e only); Model 2 is he mixed model wi h main e ec s;
Model 3 is he mixed model wi h main e ec s and in e ac ions. Coe icien s and s anda d
e o s (in pa en heses) a e shown on he log scale o numbe o co ec esponses (i.e. na u al
log o he esponse).
No e: **p<0.05; ***p< 0.01
Dependen a iable: SSP span leng h
Model 1
Model 2
Model 3
Age a baseline
-0.078***
(0.019)
-0.053**
(0.021)
-0.054***
(0.021)
E alua ion Time
0.006
(0.024)
0.025
(0.026)
MCI-wo sened
-0.248***
(0.085)
-0.254**
(0.113)
MCI-s able
-0.107
(0.058)
-0.044
(0.085)
E alua ion Time x
MCI-wo sened
0.025
(0.113)
E alua ion Time x
MCI-s able
-0.071
(0.072)
In e cep
1.581***
(0.019)
1.610***
(0.032)
1.601***
(0.034)
Obse a ions
624
624
624
Log Likelihood
-1,013.299
-1,007.706
-1,007.200
Akaike In . C i .
2,032.597
2,027.413
2,030.400
Bayesian In . C i .
2,045.570
2,053.359
2,064.994
Co esponding au ho : Ma ía Campos-Magdaleno, Depa men o De elopmen al Psychology, Rúa Xosé
Ma ía Suá ez Núñez, s/n. Campus Su . 15782 San iago de Compos ela, (Galicia, Spain). Email:
[email p o ec ed]
37
Figu e 1. Es ima ed ma ginal means and e o s ba s om Model 1 o PAL, PRM, DMS and
SSP in he h ee g oups ac oss he h ee e alua ion imes.
No e: SE= S anda d E o ; BL = Baseline assessmen ; T1= Time 1 assessmen ; T2= Time 2
assessmen .