CLINICAL TRIAL
published: 26 Augus 2016
doi: 10.3389/ nhum.2016.00421
Vi ual A a a o Emo ion
Recogni ion in Pa ien s wi h
Schizoph enia: A Pilo S udy
Samuel Ma cos-Pablos1*, Emilio González-Pablos2,Ca los Ma ín-Lo enzo2,
Luis A. Flo es1,Jaime Gómez-Ga cía-Be mejo3and Edua do Zalama3
1Ca i Founda ion, Pa que Tecnológico de Boecillo, Valladolid, Spain, 2Resea ch Uni , He manas Hospi ala ias Cen o
Sociosani a io Palencia, Palencia, Spain, 3ITAP-DISA, Uni e si y o Valladolid, Valladolid, Spain
Edi ed by:
Mikhail Lebede ,
Duke Uni e si y, USA
Re iewed by:
Pablo Billeke,
Uni e sidad del Desa ollo, Chile
Fe an A gelague ,
In ia, F ance
*Co espondence:
Samuel Ma cos-Pablos
[email p o ec ed]
Recei ed: 25 Ap il 2016
Accep ed: 08 Augus 2016
Published: 26 Augus 2016
Ci a ion:
Ma cos-Pablos S,
González-Pablos E,
Ma ín-Lo enzo C, Flo es LA,
Gómez-Ga cía-Be mejo J and
Zalama E (2016) Vi ual A a a o
Emo ion Recogni ion in Pa ien s wi h
Schizoph enia: A Pilo S udy.
F on . Hum. Neu osci. 10:421.
doi: 10.3389/ nhum.2016.00421
Pe sons who su e om schizoph enia ha e di icul ies in ecognizing emo ions in o he s’
acial exp essions, which a ec s hei capabili ies o social in e ac ion and hinde s hei
social in eg a ion. Pho og aphic images ha e adi ionally been used o explo e emo ion
ecogni ion impai men s in schizoph enia pa ien s, bu hey lack o he dynamism ha
is inhe en o acial exp essi eness. In o de o o e come hose incon eniences, o e
he las yea s di e en au ho s ha e p oposed he use o i ual a a a s. In his wo k,
we p esen he esul s o a pilo s udy ha explo ed he possibili ies o using a ealis ic-
looking a a a o he assessmen o emo ion ecogni ion de ici s in pa ien s who su e
om schizoph enia. In he s udy, 20 subjec s wi h schizoph enia o long e olu ion and
20 con ol subjec s we e in i ed o ecognize a se o acial exp essions o emo ions
showed by bo h he said i ual a a a and s a ic images. Ou esul s show ha
schizoph enic pa ien s exhibi ecogni ion de ici s in emo ion ecogni ion om acial
exp essions ega dless he ype o s imuli (a a a o images), and ha hose de ici s
a e ela ed wi h he psychopa hology. Finally, some imp o emen s in ecogni ion a es
(RRs) o he pa ien g oup when using he a a a we e obse ed o sadness o su p ise
exp essions, and hey e en ou pe o m he con ol g oup in he ecogni ion o he
happiness exp ession. This leads o conclude ha , apa om he dynamism o he
shown exp ession, he RRs o schizoph enia pa ien s when employing anima ed a a a s
may depend on o he ac o s which need o be u he explo ed.
Keywo ds: schizoph enia, acial ecogni ion o emo ions, ealis ic i ual a a a
INTRODUCTION
Schizoph enia is a se ious men al diso de ha a ec s abou 1% o he popula ion. I is he mos
expensi e men al illness in e ms o di ec heal h cos s, indi ec p oduc i i y losses, and he impac
on he amily and socie y. The e is also a no able impai men o he pe son pe o mance in a eas
such as employmen , amily and social in eg a ion (APA, 2002). This diso de is cha ac e ized by a
a ie y o symp oms: hallucina ions, delusions, a ec i e la ening, diso ganized beha io , apa hy,
social wi hd awal, cogni i e impai men , and o he s.
Among hose symp oms, social cogni ion is a majo cons uc o in es iga e in schizoph enia.
Social cogni ion has been de ined as he human abili y and capaci y o pe cei ing o he s’
in en ion and p edisposi ion (B o he s, 1990). Fo G een e al. (2005), social cogni ion
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Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
e e s o he men al ope a ions unde lying social in e ac ions,
which include p ocesses in ol ed in pe cei ing, in e p e ing,
and gene a ing esponses o he in en ions, disposi ions, and
beha io s o o he s. In he case o pa ien s wi h schizoph enia,
impai men s in social cogni ion a e p esen be o e he onse
o psychosis, sugges ing ha social cogni ion may be a ai
ma ke o he illness. Al hough he e is s ill a lack o comple e
consensus abou he conc e e scope and signi icance o hose
impai men s, some ini ia i es ha e a isen which y o s udy
cogni i e impai men s in schizoph enia ha include social
domains. Examples o such s udies a e he Measu emen and
T ea men Resea ch o Imp o e Cogni ion in Schizoph enia
(MATRICS; G een e al., 2000, 2008), and he Cogni i e
Neu oscience o T ea men Resea ch o Imp o e Cogni ion
in Schizoph enia (CNTRICS; Ca e e al., 2009). Following
hese amewo ks, h ee majo a eas o social cogni ion
in Schizoph enia can be conside ed: he heo y o mind,
a ibu ion s yle and he acial ecogni ion o emo ions (Penn
e al., 2008). The p esen s udy ocuses on he las o hose
a eas.
Facial Recogni ion o Emo ions
Conce ning emo ion ecogni ion, subjec s wi h schizoph enia
show a de ici in acial emo ion disc imina ion and iden i ica ion.
Also, his de ici has been obse ed in o he diseases such as
dep ession, mania, demen ia, b ain inju y, au ism, e c. (Mandal
e al., 1998; Penn e al., 2001; Pinkham e al., 2003).
Se e al wo ks ha e ocused on he abili y o schizoph enic
pa ien s o ecognize ace emo ions. Rega ding he clinical
condi ion o pa ien s wi h schizoph enia, he de ici in he
acial ecogni ion o emo ions is a pe manen ea u e o he
disease. This de ici is p esen om he beginning o he illness
and ends o s ay in mo e ch onic s ages (Kee e al., 2003).
Pa ien s ha e mo e di icul y o ecognize nega i e emo ions
such as ange o ea , in e p e ing hem w ongly as neu al
exp essions (Kohle e al., 2003). In ela ion o he symp oms, i
seems ha subjec s wi h delusions o pe secu ion and pa anoia
ha e be e ou comes han subjec s wi h schizoph enia, bu
wi hou pa anoia (Lewis and Ga e , 1995). Pa ien s wi h
nega i e symp oms would ha e u he de e io a ion in hese
es s (G een and Nuech e lein, 1999). Wi h espec o gende ,
women misin e p e neu al aces as sad ones mo e o en han
men, and males epo ed neu al aces as ang y ones (Weiss
e al., 2007). The abili y o ecognizing acial emo ions seems
o be ela ed o o he cogni i e unc ions, as well as o a ious
aspec s o social unc ioning and he quali y o li e (Kee e al.,
2003; Kohle e al., 2010). Fo example, in Sil e e al. (2002)
some au ho s ela e social cogni ion impai men s o al e a ions
in he memo y, abs ac hinking, language p ocessing and
a en ion.
Apa om emo ional ecogni ion impai men diagnosis,
many psychosocial in e en ion p og ams in he ield o
social cogni ion (including emo ion ecogni ion) ha e
been used o yea s: Social Skills T aining (SST; Libe man
e al., 1985), In eg a ed Psychological The apy (IPT; Rode
e al., 1996) and T aining in Emo ional In elligence (TEI;
Vau h e al., 2001). Also, speci ic social cogni ion ea men
echniques ha e also been de eloped mo e ecen ly: Social
Cogni ion and In e ac ion T aining (SCIT; Penn e al.,
2005), Social Cogni ion Enhancemen T aining (SCET; Choi
and Kwon, 2006), Me aKogni i es T aining (MKT; Mo i z
and Woodwa d, 2007) and T aining o A ec Recogni ion
(TAR; Wölwe e al., 2005). Mos o hose s udies and
ea men p ocedu es ocus on indi idual mechanisms and
obse a ional pe spec i es. Howe e , du ing he las yea s,
esea che s ha e s a ed o s udy schizoph enic pa ien s
du ing in e ac i e si ua ions (Pa k e al., 2011; Lee e al.,
2013). The main goal is o make use o i ual en i onmen s
and a a a s o p o ide new objec i e me hods o assessing
pa ien s’ in e pe sonal beha io cha ac e is ics in a social
se ing.
In e ms o emo ion ecogni ion, one d awback o cu en
diagnosis and ea men p ocedu es esides in he ac ha he e
is a lack o a me hodology ha allows co ela ing he exis ing
me hods o encoding and pa ame e izing acial mo emen s
wi h he di e en cogni i e impai men s. To da e, se e al
me hods ha e been p oposed o acial mo ion pa ame e iza ion:
Facial Ac ion Coding Sys em (FACS; Ekman and F iesen, 1978;
Ekman e al., 2002), Maximally Disc imina i e Facial Mo emen
Coding Sys em (MAX; Iza d, 1983), and AFFEX (T onick e al.,
2002). Howe e , mos p og ams o he iden i ica ion and
ea men o a ec ion ecogni ion diso de s in pa ien s wi h
schizoph enia ha e been based on he use o s a ic images
o acial emo ions. These images a e ob ained om di e en
exis ing acial coding sys ems, he FACS being one o he
mos accep ed ones. The use o his kind o image esul s in
a ha dly-pa ame e izable iden i ica ion and ea men p ocess.
In addi ion, s a ic images lack he impo an in o ma ion ha
is inhe en o ace o ace social in e ac ions, so he pe son
unde s udy (ei he su e ing om schizoph enia o no ) may
no co ec ly di e en ia e he ac ual emo ion (Lemay e al.,
2000; Weh le e al., 2000; Adams e al., 2003; Klucha e and
Sams, 2004; Joyal e al., 2014). The e o e, he sea ch o o he
e alua ion and ea men ools o hese pa ien s is an in e es ing
challenge.
One powe ul ool o enhance expe imen al con ol o e
such dynamic social in e ac ions has been he use o a a a s
o i ual eali y (Wu e al., 2014), and also he use o pic u e
mo phing in e aces (Fuku a e al., 2014). Fo example, a ecen
s udy shows ha he use o i ual eali y ools may p esen
a numbe o ad an ages when dealing wi h pa ien s su e ing
om schizoph enia, such as symp om assessmen , iden i ica ion
o symp om ma ke s, o he in es iga ion o he di e en ial
p edic ion o symp oms (F eeman, 2008). I has also been shown
ha he use o i ual cha ac e s (a a a s) can cha ac e ize, in a
simple way, dis o ions in he social pe cep ion o pa ien s (Kim
e al., 2007). O he s udies show ha he dis o ions o eali y
and memo y can be assessed using i ual en i onmen s (So kin
e al., 2008; Wenige and I le, 2008). This ype o en i onmen s
has also been applied as a he apy o con e sa ional aining
p og ams in pa ien s wi h schizoph enia (Ku e al., 2006, 2007).
Focusing on he emo ional ecogni ion h ough acial
exp essions, he use o a a a s has a numbe o ad an ages
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Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
o e con en ional me hods based on s a ic images, as hey
allow including he dynamic aspec o he acial exp essi eness,
as well as he con ol and pa ame e iza ion o he exp ession
iming and in ensi y, o he symme y le el and he du a ion
o each exp ession. The e o e, he use o a a a s could p o ide
an e icien ool o he diagnosis and ea men o de iciencies
in social and emo ional beha io . Howe e , while a a a s a e
well sui ed o s udy human cogni ion (Joyal e al., 2014), he e
a e s ill many open ques ions conce ning bo h he heo e ical
aspec s o employing i ual a a a s in psychology and hei
p ac ical applica ion (Ayme ich e al., 2014). As such, u he
in es iga ion needs o be done in o de o assess he sui abili y
o employing i ual a a a s in schizoph enia diagnosis and
ea men .
Expe imen al Goals and Hypo heses
The use o i ual agen s cons i u es a po en ial in e media e link
be ween s anda dized es s and eal-li e unc ioning, and also
o e s he possibili y o being used as an inno a i e medium o
cogni i e emedia ion (Oke e al., 2015). As such, he objec i e o
he p esen s udy is o explo e he possibili ies o using a ealis ic-
looking a a a p e iously in oduced in Ma cos e al. (2010) o
he assessmen o emo ion ecogni ion de ici s in pa ien s who
su e schizoph enia.
Al hough hey a e ou o he scope o his pilo s udy, some
o he bene i s o an a a a o e s a ic images include: o allow
he pa ame e iza ion and ine uning o he shown exp essions;
o o co ela e he di e en exp ession in ensi y, iming and
o he cha ac e is ics o acial exp essi eness wi h he pa ien
ecogni ion a es (RRs) and psychopa hology.
In his con ex , we compa ed he esponse o a g oup o
pa ien s wi h schizoph enia and a con ol g oup using bo h a
classical emo ion ecogni ion es based on s a ic images, and
a new es based on a dynamic a a a . Conside ing p e ious
s udies (Ku e al., 2006, 2007; Dyck e al., 2010) he e is
e idence ha schizoph enia pa ien s would also show de ici s in
he ecogni ion o emo ional exp essions displayed by a i ual
a a a . As such, ou i s hypo hesis was:
Hypo hesis 1: Compa ed wi h con ols, pa ien s will show wo se
ecogni ion sco es, ega dless he ype o s imuli (a a a o images).
The bene i s o dynamic acial exp essions ha e been
discussed la ely. Some s udies sugges ha he dynamic
p ope ies o human acial mo emen s may play a su p isingly
small ole in people’s abili y o in e he emo ional s a es o o he s
om hei acial exp essions (Gold e al., 2013).
O he s show ha he e is no di e ence in he use o dynamic
o s a ic images as a combina ion o hype sensi i i y o s a ic
emo ions and hyposensi i i y o dynamic emo ions in people
wi h schizoph enia migh unde lie he absence o di e ences in
esponse o hese s imuli (Fuku a e al., 2014).
On he o he hand, he e is also e idence ha he use o
dynamic acial exp essions, apa om being ecologically mo e
alid and he e o e mo e app op ia e o emo ion esea ch, helps
in he pe cep ion o emo ions (K umhube e al., 2013). Based
on he abo e assump ions, he second hypo hesis we wan ed o
con as was:
Hypo hesis 2: The a a a would u n ou o ha e be e
ecogni ion sco es han s a ic images.
Finally, many s udies ha e ela ed he acial emo ion
ecogni ion impai men s o schizoph enia pa ien s wi h hei
psychopa hology (Dyck e al., 2010; Gold e al., 2013) and o he s.
Fo ha eason, ou hi d hypo hesis is:
Hypo hesis 3: I p esen , ecogni ion de ici s o he pa ien s
g oup a e co ela ed wi h he psychopa hology.
MATERIALS AND METHODS
Fo he expe imen , bo h pa ien s and con ols we e asked
o en e an o ice indi idually and o ake a sea a a desk
which held a compu e sc een. The he apis hen explained
hem ha some acial exp essions co esponding o he six
basic emo ions: joy, sadness, ea , ange , su p ise and disgus
we e going o be shown on he sc een. I was also explained
ha exp essions we e going o be pe o med by an a a a
ha will s a in a neu al pose o be shown in a s a ic
image, and ha he goal was o y and guess he exp ession
shown. The he apis insis ed on he ac ha he e we e no
good o bad answe s, and ha he main pu pose o he es
was o collec he pa icipan s’ pe cep ion. The he apis hen
asked he pa icipan s i hey had unde s ood he ins uc ions
o he es , epea ing hem in he case he pa icipan did
no . The he apis ied o main ain a neu al one o oice
h oughou he expe imen , in o de no o in luence he
esponses.
When he pa icipan was eady, he he apis showed
he di e en emo ional exp essions on he PC sc een. Bo h
he s a ic images and he a a a we e in e spe sed andomly
and p esen ed o he use , and he he apis wai ed up o
20 s o a esponse o be gi en. Images showed a s a ic
emo ional exp ession (see Figu e 1). On he o he hand,
he exp ession pe o med by he a a a s a ed om a
neu al pose and ended in he exp ession maximum. A a a
main ained he maximum o he exp ession un il he he apis
mo ed on o he nex exp ession ei he because o a esponse
gi en o i he conside ed a imeou . Co ec answe s we e
labeled as 1, whe eas bo h w ong o lack o answe we e
labeled as 0.
Subjec s
Pa icipan s in he s udy consis ed on wo g oups: pa ien and
con ol. The pa ien g oup consis ed o 20 subjec s ea ed o
schizoph enia a he San Luis hospi al (Palencia, Spain). On
an a e age, hey a e middle-aged pa ien s and wi h a long
e olu ion o he disease. A e he esea ch eam checked ha
hei cogni i e le el allowed hem o unde s and ins uc ions
and he pu pose o he es , hey we e asked o olun a ily
pa icipa e in he s udy. The con ol g oup consis ed o 20
subjec s andomly ec ui ed among heal hy wo ke s o he
same cen e . Table 1 con ains a su ey o he demog aphics
o bo h g oups. Symp oma ology was assessed by e sion A o
he Posi i e and Nega i e Synd ome Scale (PANNS; Kay e al.,
1987).
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Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
FIGURE 1 | The chosen s a ic emo ions.
Ma e ials and Equipmen
S a ic Images
Fo he s a ic images, six pho os om he Paul Ekman model
e lec ing six uni e sal emo ions pe o med by di e en ac o s
we e selec ed. Images we e selec ed so ha he shown exp ession
was isually simila o he one pe o med by he a a a , bu also
looking ha he ac o s ha pe o med hem we e om di e en
aces and gende s in o de o a oid biased esul s. Figu e 1 shows
he selec ed images o he di e en exp essions.
A a a In e ace
The de eloped a a a ollows a bio-inspi ed design looking o
ealis ic esul s and consis ing o wo majo s eps: modeling and
anima ion. The modeling s ep is ca ied ou using a lase scanne
ha allows h ee-dimensional in o ma ion o a eal ace o be
ob ained. Measu ed poin s a e hen meshed in o de o ob ain a
3D su ace model. Face ex u e (colo ) is ob ained om sepa a e
pho og aphs ha a e mapped on o he 3D su ace. This allows
a deg ee o ealism highe han ha p o ided by o he modeling
me hods o be achie ed. Ce ain elemen s (eyes, ee h, o al ca i y)
ha e been modeled sepa a ely and hen included in he whole
model, since hey could no be scanned.
The anima ion has been done h ough pseudo-muscles
g ouped in o a hie a chical skele on. The pseudo-muscles achie e
a good app oxima ion o he eal acial muscles and ha e he
ad an age o equi ing a lowe compu a ional e o , which
makes hem ideal o in e ac i e eal- ime applica ions. The
pseudo-muscle anima ion p ocess has been ca ied ou aking
in o accoun bo h he ac ual muscula physiognomy and
ana omy. Once posi ioned, he pseudo-muscles a e used o
p ope ly bend he h ee-dimensional mesh. The subsequen
de o ma ion is also based on he ana omy o he human ace
in he egions o muscle inse ions in o he skin. Figu e 2
shows a scheme o he di e en s ages o he p ocess o
TABLE 1 | Demog aphics o bo h con ol and pa ien g oups.
Age Sex PANNS posi i e PANNS nega i e PANNS psychopa ology PANNS o al
Mean S.D. Male Female Mean S.D. Mean S.D. Mean S.D. Mean S.D.
Con ol 42.7 10.8 7 13 – – – – – – – –
Pa ien s 55.0 8.3 11 9 21.8 7.5 27.4 9.3 47.1 11.3 97.0 27.8
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Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
FIGURE 2 | S ages o he p ocess o cons uc ion o he a a a .
Modeling (le ) and anima ion ( igh ).
modeling and anima ion. A mo e de ailed desc ip ion o he
a a a cons uc ion and de elopmen is gi en in Ma cos e al.
(2010).
Figu e 3 shows he se o pseudo-muscles used and hei
posi ion on he i ual ace.
The ac ion o hese pseudo-muscles p oduce de o ma ions on
he i ual 3D model in he same way as eal acial muscles do
on he ace su ace. The pseudo-muscle mo emen s a e based
on he minimum ac ion uni s (AUs) om he FACS. Complex
exp essions can be gene a ed h ough he combina ion o AUs
wi h di e en in ensi ies, as shown in Figu e 4.
Fo his expe imen , we ha e gene a ed six basic dynamic
exp essions: happiness, disgus , ange , ea , sadness and su p ise
(See Figu e 5).
Also, he con ol in e ace o he a a a has been simpli ied
in he cu en s udy, in such a way ha he he apis only has
o p ess a keyboa d key o make he a a a pe o m a gi en
exp ession. Al hough a iables like in ensi y and iming can be
modi ied, hey ha e been kep cons an in o de o s anda dize
he exp essions shown o he pa icipan s o he expe imen .
FIGURE 3 | Pseudo-muscles used in he a a a . 1. F on ; 2. Co uga o
supe cilii; 3. P oce us; 4. The eye muscles and o bicula o he eye; 5.
Quad a uslabiisupe io is; 6. Zygoma icus majo ; 7. Zygoma icus mino ; 8
Neck; 9. Buccina o ; 10. Giggly; 11. O bicula mou h; 12. Jaw; 13. T iangula
om bea d.
P ocedu e
The s udy was ca ied ou indi idually o each pa icipan . Facial
s imuli in he o m o s a ic images and eal- ime dynamically
gene a ed a a a exp essions we e p esen ed o each pa icipan ,
h ough a compu e sc een, in a andom o de . In o al,
pa icipan s we e asked o iden i y he emo ional exp essions
exhibi ed by six s a ic images and six a a a exp essions, each
co esponding o he six uni e sal emo ional exp essions: ange ,
ea , disgus , su p ise, sadness and happiness.
Responses we e eco ded as success ul i he emo ional
exp ession is co ec ly iden i ied o as a ailu e i he emo ional
exp ession is w ongly iden i ied o no esponse is gi en o a 20 s
ime limi .
E hics
This c oss-sec ional s udy was app o ed by he Clinical Resea ch
E hics Commi ee o he Hospi al i was pe o med in. In o med,
olun a y, w i en consen was ob ained om he pa ien s and
con ols a e a ho ough explana ion o he p ocedu es, in
acco dance wi h he Decla a ion o Helsinki.
ANALYSIS AND RESULTS
All analyses we e pe o med using he so wa e SPSS, wi h he
alpha le el a 0.05 o s a is ical signi icance, unless o he wise
s a ed.
Desc ip i e S a is ics
In e ms o desc ip i e s a is ics, a compa ison o RRs o each
o he emo ional exp essions o he wo g oups o pa icipan s
has been done, by conside ing he esponses ob ained o he
a a a agains hose ob ained o s a ic images. The RRs o
he each g oup (pa ien s/con ol) a e shown in Figu e 6. Fo
he g oup o pa ien s, i can be obse ed ha he success a e
o exp essions o ange and happiness a e highe o he s a ic
images, while exp essions o sadness and su p ise a e mo e easily
ecognizable o he anima ed a a a . The exp ession o ea
has simila RRs in bo h cases. Fo he con ol g oup, sadness,
happiness and ange we e be e ecognized in he case o images,
while sadness and su p ise exp essions we e be e ecognized in
FIGURE 4 | Neu al exp ession and ange exp ession wi hin he ac ion
uni s (AUs) o he acial ac ion coding sys em (FACS) ha gene a e i .
F on ie s in Human Neu oscience | www. on ie sin.o g 5Augus 2016 | Volume 10 | A icle 421

Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
FIGURE 5 | The six emo ional exp essions gene a ed by he a a a . F om op o bo om and om le o igh : happiness, disgus , ea , ange , su p ise and
sadness.
he case o he a a a . Finally he ea exp ession has a qui e low
RR.
I has o be no ed ha in he case o he exp ession o disgus ,
he exp ession gene a ed by he a a a was no ecognized by any
pa icipan , hus i was excluded om u he analysis. We plan
o ebuild his exp ession o u u e ealiza ions.
Also, Table 2 shows a compa ison o emo ion ecogni ion
sco es be ween bo h g oups o pa icipan s. I can be seen ha
in he case o s a ic images he RRs o he con ol g oup a e
be e on a e age o all exp ession han hose o he pa ien
g oup. In he case o he a a a , howe e , con ol g oup only
ou pe o ms pa ien g oup in he case o su p ise and ange
exp essions.
Recogni ion Ra es A e aged o All
Emo ions
The answe s o he pa icipan s we e coded as a binomial
a iable labeled as ecogni ion ( ecogni ion success/ ecogni ion
ailu e), which in u n was conside ed as he dependen a iable
o ou s udy. A se o bi a ia e analysis was i s conduc ed
in o de o explo e he ela ionship be ween he dependen
a iable and he o he ac o s: g oup (con ol/pa ien s), ace ype
(a a a /images), sex,age and emo ion (happiness, sadness, ange ,
ea , su p ise). Table 3 su eys he esul s o he di e en es s
o each conside ed ac o . Simple bina y logis ic eg essions
we e employed o he ca ego ical a iables, whe eas a S uden ’s
- es was employed o he con inuous age a iable. Independen
F on ie s in Human Neu oscience | www. on ie sin.o g 6Augus 2016 | Volume 10 | A icle 421
Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
FIGURE 6 | Recogni ion a es ob ained o he a a a and o he s a ic images o each g oup (pa ien s/con ols).
samples - es showed no signi ican age di e ences be ween
g oups. As Table 3 shows, a iables ace ype and sex did
no esul s a is ically signi ican (p=0.614 and p=0.212
espec i ely o he Wald c i e ion). On he o he hand,
s a is ically signi ican esul s we e ob ained o he a iable
g oup (p<0.001) wi h an OR =0.466 when conside ing he
F on ie s in Human Neu oscience | www. on ie sin.o g 7Augus 2016 | Volume 10 | A icle 421
Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
TABLE 2 | Mean and s anda d e o o he di e en emo ions.
Con ol Pa ien s
A a a Images A a a Images
Ange 0.6/0.112∗0.90/0.069 0.35/0.109 0.60/0.112
Happiness 0.65/0.109 1/0 0.70/0.105 0.95/0.050
Sadness 0.70/0.105 0.25/0.099 0.60/0.112 0.25/0.099
Fea 0.2/0.092 0.50/0.115 0.30/0.105 0.35/0.109
Su p ise 1/0 0.80/0.092 0.45/0.114 0.20/0.092
∗Mean/SE.
con ol g oup as a e e ence, indica ing ha he RR o he con ol
g oup is o e all wo imes highe han he one o he pa ien
g oup.
S a is ically signi ican esul s we e also ob ained o he
emo ion a iable. In his case he emo ion a iable is poly omous,
so in o de o e alua e a eg ession model, one o i s alues
is conside ed as a e e ence (e.g., su p ise), while he es a e
conside ed as ‘‘dummy’’ binomial a iables, allowing o compu e
hei OR. I can be seen ha conside ing he su p ise exp ession
as a e e ence, he e esul s a is ically signi ican alues o all
exp essions bu ange , indica ing ha emo ion has a signi ican
con ibu ion o he RR. In he case o age, s a is ically signi ican
esul s we e ob ained o he - es (p<0.001). A u he logis ic
eg ession analysis was pe o med o e alua ing he e ec s o
age o e ecogni ion, and using age as independen and non-
ca ego ical co a ia e. Resul s indica ed ha age indeed had a
signi ican e ec o e he RR (p<0,001 o he Wald c i e ion)
and an OR =0.950, which indica es ha ecogni ion success
dec eases wi h age.
Fu he explo a ions showed no s a is ically signi ican
in e ac ions be ween co a ia es. To inc ease he powe o he
s a is ical model, non-signi ican co a ia es we e excluded o
he analysis. A e aged ac oss all emo ions, a logis ic eg ession
analysis was hen conduc ed using age, emo ion and g oup as
p edic o s, bu he esul ing model indica ed a weak ela ionship
be ween p edic ion and g ouping (Nagelke ke’s R2=0.214), and
o e all p edic ion o 69.8% (74.9% o ecogni ion success/63.0%
o ecogni ion ailu e).
TABLE 3 | Resul s o indi idual es s o he conside ed ac o s.
Independen a iable ∗P alue ∗∗ OR ∗∗∗ CI (95%)
In . Sup.
G oup <0.001 0.466 0.311 0.698
Face ype 0.614 1.107 0.745 1.645
Sex 0.212 1.288 0.865 1.917
Age <0.001 4.6 0.405 6.781
Ange ∗∗∗∗ 1 1 – –
Happiness∗∗∗∗ 0.003 2.983 – –
Sadness∗∗∗∗ 0.04 0.518 – –
Fea ∗∗∗∗ 0.001 0.322 – –
∗Wald c i e ion o dicho onomous a iables, - es o con inuous a iable age.
∗∗ Odds Ra io (OR) o dicho onomous a iables, mean di e ence o con inuous
a iable age. ∗∗∗ Con idence in e al (CI). ∗∗∗∗ E alua ed using Su p ise emo ion as
e e ence.
Recogni ion Ra es o Each Emo ion
Sepa a ed logis ic eg ession analyses we e hen conduc ed o
each emo ional exp ession (see Table 4 o a su ey o he
esul s). In he case o ange , simple bi a ia e logis ic eg ession
analyses showed a s ong ela ionship be ween he dependen
a iable ecogni ion and ace ype (p=0.013 o he Wald
c i e ion), g oup (p=0.013), and age (p=0.003). No s a is ically
signi ican in e ac ions be ween co a ia es we e ound. Logis ic
eg ession conduc ed using hose h ee ac o s p oduced a
s a is ically signi ican model (chi squa e =19.33, p<0.001 wi h
d =3). Nagelke ke’s R2o 0.291 indica ed a weak ela ionship
be ween p edic ion and g ouping. P edic ions success o e all was
72.5% (83.7% o ecogni ion success and 54.8% o ecogni ion
ailu e). The Wald c i e ion showed ha only ace ype and
age made a signi ican con ibu ion o he model. The OR
(Exp(B)) indica ed ha success in ecogni ion dec eased wi h age,
and ha pa icipan s we e 4161 imes mo e likely o ecognize
ange exp ession in he case o images. Howe e , due o he
said weakness o he model, we conclude ha in he case o
ange he model is unable o co ec ly p edic he ecogni ion
success.
In he case o happiness bi a ia e logis ic eg ession
analyses showed a s ong ela ionship be ween he dependen
a iable and ace ype (p=0.006, OR =18.778). No o he
co a ia es o in e ac ions we e ound o be signi ican . Fo
explo a o y easons, age and g oup we e also included in he
model. The eg ession model was s a is ically signi ican (chi
squa e =14.738, p<0.002, d =3). O e all p edic ion
success was o 82.5%. Wald’s c i e ion showed no signi ican
con ibu ion o age and g oup, bu in he case o ace ype
i showed a signi ican con ibu ion (p=0.006, OR =18.98)
indica ing a signi ican ly highe RR in he case o he images.
In he case o sadness only ace ype (p<0.01) and age
(p=0.037) we e ound signi ican ly ela ed o he dependen
a iable and so we e in oduced in he model. The es o he
ull model agains he cons an only model esul ed s a is ically
signi ican (chi squa e =18.890, p<0.001 wi h d =2).
P edic ion success was 72.5% (69.4% success, 75% ailu e) wi h
a Nagelke ke’s R2o 0.281. Again, he RR dec eased wi h age
(OR =0.948 o a con inuous a iable). Fo he ace ype he OR
using he a a a g oup as a e e ence was 0.156 indica ing ha
he ecogni ion success was signi ican ly highe in he case o he
a a a .
In he case o ea , bi a ia e analyses indica ed no s a is ically
signi ican ela ionship be ween he dependen a iable and any
o he co a ia es.
In he case o su p ise, simple bi a ia e logis ic eg ession
analyses showed a ela ionship be ween he dependen a iable
ecogni ion and ace ype (p=0.041 o he Wald c i e ion),
g oup (p<0.001), and age (p<0.001). No addi ional s a is ically
signi ican in e ac ions be ween co a ia es we e ound. Logis ic
eg ession conduc ed using hose h ee ac o s p oduced a
s a is ically signi ican model (chi squa e =37.903, p<0.001
wi h d =3). Nagelke ke’s R2o 0.512 indica ed a mode a e
ela ionship be ween p edic ion and g ouping. P edic ions
success o e all was 80% (81.6% o ecogni ion success and
77.4% o ecogni ion ailu e). The Wald c i e ion showed
F on ie s in Human Neu oscience | www. on ie sin.o g 8Augus 2016 | Volume 10 | A icle 421
Ma cos-Pablos e al. A a a o Emo ion Recogni ion in Schizoph enia
TABLE 4 | Su ey o he esul s o he indi idual emo ions.
Exp ession Main e ec s ∗∗ OR Signi icance
Ange Face ype (p=0.013) 4.161 Highe RR∗ o images
Age (p=0.003) 0.78 RR dec eases wi h age
Happiness Face ype (p=0.006) 18.98 Highe RR o images
Sadness Face ype (p=0.04) 0.156 Be e RR in he case o he a a a
Age (p=0.003) 0.948 RR dec eases wi h age
Fea NO SIG NO SIG NO SIG
Su p ise Face ype (p<0.001) 0.2 Highe RR in he case o he a a a
G oup (p<0.001) 20 Highe RR in he case o he con ol g oup
∗RR, Recogni ion Ra e. ∗∗ Odds Ra io (OR) o dicho onomous a iables, mean di e ence o con inuous a iable age.
ha only ace ype and g oup made a signi ican con ibu ion
o he model. The OR (Exp(B)) indica ed ha ecogni ion
success is likely o be 5×highe in he case o he a a a ,
and ha he OR is 20×highe in he case o he con ol
g oup.
Co ela ions wi h Psychopa hology
Conside ing only he pa ien g oup, success in he ecogni ion
o emo ions p o ed o be co ela ed wi h he posi i e deg ee
o symp oma ology acco ding o he PANNS. A simple bina y
logis ic eg ession ac oss all emo ions and o bo h he a a a
and images using ecogni ion success as dependen a iable
showed ha i was signi ican ly ela ed wi h he PANNS
o al (p=0.039 o he Wald c i e ion). The Odds Ra io
(Exp(B) =0.989) indica ed ha he RR slowly dec eases
as PANNS inc eases. O he bi a ia e analysis wi h he es
o he co a ia es showed no signi ican ela ion wi h he
dependen a iable. Indi idual analysis o each exp ession
did no show signi ican di e ences in e ms o PANNS
sco es.
DISCUSSION
Consis en wi h ou hypo hesis, desc ip i e esul s show ha
schizoph enia pa ien s p esen de ici s in he ecogni ion
o i ual emo ional exp essions when compa ed wi h he
con ol g oup. As Table 3 shows, he odds a io o he
a e age RRs o he con ol g oup is almos wice as high
as hose o he schizoph enia pa ien s. Also, a e aged ac oss
all emo ions and o bo h con ol g oups, he eg ession
model showed ha di e ences in RRs be ween he a a a and
he images we e no s a is ically signi ican . These indings
ma ch hose p e iously p esen ed by Kim e al. (2007)
and Dyck e al. (2010), showing a educ ion in social
pe cep ion o schizoph enia pa ien s e en when employing
i ual cha ac e s.
Fo he o he conside ed co a ia es, sex did no p oduce
s a is ically signi ican e ec s o e he RR, while age p oduced
signi ican a ia ions, sligh ly dec easing he RRs as age
inc eases. In he con ol g oup, his e ec is somehow expec ed
as he e ec s o age o e exp ession ecogni ion displayed
by i ual cha ac e s has been ela ed in he li e a u e o
he ac ha elde ly people is less used o echnology and
i ual en i onmen s (Ma cos e al., 2010). I has also been
ela ed wi h he ac ha isual acui y ends o decline wi h
ad ancing age o e en o he ac ha olde adul s ha e
an a en ional bias owa ds old-age aces (Campbell e al.,
2015). In he case o he g oup o pa ien s, u he s udies
ha ela e age wi h o he ac o s due o he e olu ion o he
schizoph enia shall be done in o de o p ope ly add ess his
e ec .
Rega ding he ela ionship be ween ecogni ion de ici s and
psychopa hology, ou indings also e eal an expec ed associa ion
be ween symp oma ology and emo ion ecogni ion, as RRs
dec ease as PANNS sco es inc ease. Howe e , no s a is ically
signi ican di e ences we e ound be ween he na u al images
and he i ual ones, sugges ing ha his ela ionship is
independen o he ype o acial s imuli employed. These esul s
ma ch hose o Fuku a e al. (2014), and could be ela ed o a
combina ion o hype sensi i i y and hyposensi i i y o s a ic and
dynamic emo ions espec i ely.
Howe e , in he case o ou second hypo hesis, he
ecogni ion sco es ob ained by he a a a do no ou pe o m
hose ob ained om he images as expec ed. Analyzing each
emo ional exp ession indi idually, o he ange exp ession
s a is ically signi ican esul s we e ound be ween he g oups o
pa ien s and con ol as well as when compa ing esul s o he
a a a and s a ic images. In his case, he ange exp ession is
be e ecognized when using s a ic images and he con ol g oup
clea ly ou pe o ms he pa ien g oup. In he case o happiness,
s a is ically signi ican di e ences we e ound be ween ace ype,
being he exp ession be e ecognized in he case o he s a ic
images. In he case o sadness, ace ype was again ound
o be a main e ec o e he RR along wi h age. I can be
seen, howe e , ha in his case he a a a clea ly ou pe o ms
he s a ic images. No s a is ically signi ican main e ec s we e
ound o he ea exp ession. Finally, in he case o sadness,
bo h he ace ype and he g oup o pa icipan s u ned ou
o be s a is ically signi ican o he di e ences ound in he
RR.
As Kohle e al. (2003) s a es, in he case o images pa ien s
ha e mo e di icul y o ecognize nega i e emo ions such as
ange , ea , o sadness. Al hough o he s udies ha e shown sligh
imp o emen s in he ecogni ion o nega i e emo ions when
using i ual aces (Dyck e al., 2010), in ou case his is only ue
o sadness bu in a highe deg ee.
I is also in e es ing o poin ou ha pa ien s ou pe o m
he con ol g oup in he ecogni ion o he happiness exp ession
F on ie s in Human Neu oscience | www. on ie sin.o g 9Augus 2016 | Volume 10 | A icle 421