TIME COURSE OF ATTENTIONAL MODULATIONS ON AUTOMATIC EMOTIONAL
PROCESSING
Au ho s: Sonia Doallo, Fe nando Cada ei a, Soco o Rod íguez Holguín
This is he pee e iewed e sion o he ollowing a icle: Doallo S, Cada ei a F; Rod íguez Holguín
S. (2007). Time cou se o a en ional modula ions on au oma ic emo ional p ocessing. Neu oscience
Le e s, 418, 111-116. doi:10.1016/j.neule .2007.03.009. This a icle may be used o non-comme cial
pu poses in acco dance wi h Else ie Te ms and Condi ions o Use o Sel -A chi ed Ve sions
2
Time cou se o a en ional modula ions on au oma ic emo ional p ocessing
Sonia Doallo, Fe nando Cada ei a, Soco o Rod íguez Holguín
Depa men o Clinical Psychology and Psychobiology, Uni e si y o San iago de Compos ela,
Co esponding au ho : Sonia Doallo. Facul y o Psychology. Uni e si y o San iago de Compos ela
Campus Su , E-15782 San iago de Compos ela, Galicia, Spain. Tel.: +34 981 563 100x13916; ax:
+34 981 528 071. E-mail add ess: [email p o ec ed] .
Abs ac
In a p e ious s udy using e en - ela ed po en ials (ERPs) [S. Doallo, S. Rod íguez Holguín, F.
Cada ei a, A en ional load a ec s au oma ic emo ional p ocessing: e idence om e en - ela ed
po en ials, Neu o epo 17 (2006) 1797–1801], we epo ed ha di e en ial esponses o una ended
pe iphe al a ec i e pic u es, as e lec ed by N1-P2 modula ions a pos e io egions, a e modula ed by
a en ional load a ixa ion. He e, new analyses o hese da a we e pe o med o e alua e whe he a
sus ained, b oadly dis ibu ed, nega i e shi in he una ended pic u es ERP wa e o ms, which
displayed la ge ampli udes o emo ional s imuli, e lec s an addi ional di e en ial esponse o he
emo ional con en . Unde low-load condi ions, unpleasan ( e sus neu al) pic u es elici ed g ea e
nega i i ies in he 80–140 ms la ency ange o e on ocen al si es and mo e cen opa ie ally
dis ibu ed om 200 o 280 ms. These indings p o ide u he e idence o he ime cou se o
emo ional p ocessing a una ended loca ions and i s modula ion by a en ional load.
Keywo ds
E en - ela ed po en ials; A en ion; Emo ion; Load; In e na ional a ec i e pic u e sys em
Pos -p in ( inal d a pos - e e eeing)
3
In oduc ion
An impo an issue on he ela ion be ween a en ion and emo ion e e s o he p ocessing o
emo ional s imuli p esen ed ou side he ocus o a en ion. Neu oimaging [14,20], lesion [19] and
e en - ela ed po en ials (ERPs) [1,2,18] s udies p o ide e idence o he cap u e o a en ion by
emo ional e en s. Howe e , da a indica ing ha he emo ional alue o ask-i ele an s imuli is
p ocessed when a en ion is ac i ely engaged on o he s imuli a e no unequi ocal. Some au ho s
epo ha ERPs elici ed by emo ional s imuli a e di e en om hose igge ed by neu al ones when
hey a e a ended, bu no when hey appea a ask-i ele an loca ions [6,8], sugges ing ha co ical
s ages o emo ional p ocessing a e s ongly modula ed by ocal a en ion. A ecen ERP expe imen
[7] ound ha he ex en o which he emo ional p ocessing is in luenced by a en ion depends on
ac o s such as o eal e sus pe iphe al p esen a ion. The c i ical ole o he ask- ele an a en ional
load on he p ocessing o ask-i ele an emo ional e en s has been also e idenced om unc ional
magne ic esonance imaging s udies [15,16]. In a p e ious epo [5], we ound ERP e idence
consis en wi h he hypo hesis ha he di e en ial b ain esponse o una ended emo ional s imuli
depends s ongly on he a en ional load o he ongoing ask. We eco ded ERPs elici ed by ask-
i ele an unpleasan and neu al pic u es b ie ly p esen ed a pe iphe al loca ions while pa icipan s
we e ac i ely moni o ing he ixa ion i o de o pe o m a disc imina ion ask a ying in load (low-
and high-load). Wi h he aim o de ec ing any cap u e o a en ion by ask-i ele an unpleasan
pic u es, he P2 componen was measu ed. P2 is specially sensi i e o nega i e isual s imuli [3,4] and
i is also elici ed in esponse o emo ional s imuli ou side he ocus o a en ion [1]. Resul s e ealed
ha unpleasan pic u es ( e sus neu al pic u es) p oduced enhanced N1-P2 ampli udes a
pa ie occipi al and occipi al si es only unde low-load condi ions. We concluded ha he b ain
esponses o he a ec i e alue o ask-i ele an pe iphe al pic u es a e modula ed by he a en ional
load a ixa ion. Al hough hese analyses we e ocused in he P2 componen , g and-a e aged
wa e o ms also e ealed ha he ERP o una ended s imuli p esen ed a sus ained, b oadly dis ibu ed,
nega i e shi wi h la ge ampli udes o emo ional pic u es han neu al pic u es [5]. He e, we e-
analyze ou da a wi h he aim o e alua ing whe he his di e ence e lec s an addi ional di e en ial
esponse o he emo ional con en o he pic u es and o in es iga e in mo e de ail he ime cou se o
his e ec .
Me hods
Ten emale olun ee s (21–30 yea s old, mean = 26.4, S.D. = 2.5) we e assessed. All we e igh -
handed, had no mal o co ec ed- o-no mal ision, and had no his o y o psychia ic o neu ological
diso de s. Pa icipan s ga e in o med consen .
Pos -p in ( inal d a pos - e e eeing)
4
The a ge s imuli we e sho (0.6◦ × 2.3◦) o long (0.6◦ × 3.4◦) e ical ba s equip obably lashed o
50 ms in he cen e o he display. Ve ical ba s we e sequen ially p esen ed, acco ding o a s imulus 1
(S1)–s imulus 2 (S2) pa adigm. Du ing he delay pe iod be ween S1 and S2, 40 nega i e and 40
neu al pic u es (8◦ × 5.7◦) selec ed om he In e na ional A ec i e Pic u e Sys em (IAPS)1 [11] we e
occasionally p esen ed (nega i e p = .15, neu al p = .15) a 5.7◦ o he le o o he igh om a
ixa ion c oss o 50 ms. The wo ca ego ies signi ican ly di e ed om each o he in he alence
a ing (2.1 ± 0.6 e sus 5.2 ± 0.3; (39) = −26.314, p = .000) and in he a ousal a ing (7.2 ± 0.4 e sus
3.2 ± 0.5; (39) = 38.901, p = .000) on he basis o he no ma i e alues o IAPS in he Spanish
popula ion [13]. Valence and a ousal a ings o each pic u e a e shown in Tables 3 and 4 in
supplemen a y ma e ial online. S a is ical compa isons con i med ha he wo g oups o pic u es did
no signi ican ly di e in luminance o spa ial equency. The di icul y o he ele an cen al ask
was inc eased in a di e en expe imen al block, in which size disc imina ion was ende ed di icul by
educing he di e ence be ween he ba s (sho ba s: 0.6◦ × 2.3◦; long ba s: 0.6◦ × 2.5◦). Pa icipan s
we e equi ed o main ain eye ixa ion on he cen al c oss, and o disc imina e whe he he second ba
o he ma ch (S2) was equal o di e en in size om he i s ba (S1), p essing one bu on wi h one
hand i equal in size and ano he bu on wi h he o he hand i di e en in size, while igno ing he
pe iphe al pic u es. The assignmen o he esponse hand was balanced ac oss pa icipan s. The
in e al om S1 onse o dis ac o onse (SOA) andomly a ied om 100 o 1100 ms. SOA be ween
S1 and S2 andomly a ied om 1200 o 1500 ms. The in e ial in e als andomly a ied om 2000
o 2300 ms. In o de o amilia ize he pa icipan s wi h he ask, he low-load condi ion was p esen ed
i s . Each expe imen al condi ion consis ed o eigh ial blocks. The maximum numbe o ials pe
block was 125.
ERPs (bandpass 0.1–50 Hz, 500 Hz/channel) we e eco ded om 16 ac i e elec odes (F3, F4, FC3,
FC4, C3, C4, T5, T6, CP3, CP4, P3, P4, PO3, PO4, O1, and O2), e e ed o a nasal elec ode.
Ve ical and ho izon al eye mo emen s we e eco ded bipola ly om abo e and below he le eye
and om he ou e can hus o each eye. Reac ion ime (RT) and pe cen age o co ec esponses we e
eco ded o each ial. Da a we e collec ed o e epochs om 60 ms be o e s imulus o 600 ms a e
s imulus. T ials wi h eye blinks o ho izon al eye mo emen s we e ejec ed. Fo each pa icipan ,
ERPs elici ed by neu al and emo ional dis ac o s we e a e aged (digi al bandpass o 0.1–30 Hz)
sepa a ely o each isual ield and condi ion.
1 The IAPS numbe s o nega i e pic u es we e: 1050, 1300, 2120, 2800, 2900, 3000, 3010, 3030, 3051, 3053,
3060, 3071, 3100, 3102, 3120, 3130, 3150, 3170, 3230, 3350, 3400, 3550, 6212, 6250, 6260, 6313, 6510, 6550,
6560, 6570, 9040, 9050, 9400, 9410, 9421, 9520, 9630, 9800, 9810, 9920; o neu al pic u es: 2190, 2200,
2210,2840, 5500, 5510, 5520, 5530, 5531, 5532, 5533, 5534, 6150, 7000, 7002, 7006, 7009, 7010, 7025, 7030,
7034, 7035, 7040, 7050, 7060, 7080, 7090, 7150, 7170, 7190, 7207, 7217, 7224, 7233, 7235, 7490, 7500, 7550,
7820, 7830. The alence and a ousal no ma i e a ings o he Spanish popula ion [13] a e a ailable in he web
page: h p://www. edap.es/Ibe Psicologia/ibe psi5-1/iaps/iaps.pd .
Pos -p in ( inal d a pos - e e eeing)
5
Visual inspec ion o wa e o ms e ealed ha he ERP o dis ac o s imuli was a ec ed by a sus ained
nega i e shi which showed la ge ampli udes o emo ional pic u es han o neu al pic u es. To
e alua e whe he his di e ence e lec s a di e en ial esponse o he emo ional con en , he mean
ol age alues wi hin wel e la ency windows o 20 ms each one, om 60 o 300 ms, we e analyzed.
Repea ed-measu e ANOVAs we e pe o med o each la ency window wi h i e wi hin-subjec
ac o s: egion ( on al / on ocen al / cen al / cen opa ie al / pa ie al / empo al / pa ie ooccipi al /
occipi al), hemisphe e o eco ding (le / igh ), load condi ion (low / high), emo ional con en
(neu al / nega i e) and isual ield (le / igh ). Signi icance le els we e de e mined using deg ees o
eedom a e applying he G eenhouse–Geisse co ec ion when app opia e. Pos -hoc compa isons
we e pe o med using he Bon e oni adjus men o mul iple compa isons.
The RT and accu acy da a we e subjec ed o epea ed measu es ANOVAs wi h load ( wo le els) and
dis ac o (none/le neu al/ igh neu al/le emo ional/ igh emo ional, i e le els) as ac o s.
Resul s
Beha io al pe o mance con i med ha he cen al a en ional load was e ec i ely manipula ed: (1)
esponses we e slowe o a ge ba s p eceded by i ele an s imuli (neu al and emo ional) han o
hose no p eceded by dis ac o s (F(4,36) = 3.329, p = .020). This in e e ence e ec was only
signi ican in he low-load condi ion (F(4,36) = 2.998, p = .031); (2) hi a es we e also lowe du ing
he high-load (63.8 ± 9.8) han low-load (91.9 ± 7.9) condi ion (F(1,9) = 351.622, p = .000).
ERPs mean ampli udes o neu al and emo ional s imuli we e signi ican ly di e en du ing he 80–140
ms and 200–280 ms pos -s imulus in e als, wi h la ge nega i e ampli udes o unpleasan s imuli
han o neu al s imuli (all F(1,9) > 1.367, all p < .046). To u he explo e he ime cou se and he
opog aphical dis ibu ion o hese di e ences, and based on s a is ically signi ican in e ac ions
be ween emo ional con en , egion and load in hese wo ime anges (all F(7,63) > 3.242, all p <
.019), addi ional analyses we e conduc ed on 20-ms ime windows, sepa a ely o each expe imen al
condi ion and egion (see Tables 1 and 2).
Tables 1 and 2
Fo he low-load condi ion, he e ec s o he emo ional con en o he pic u es we e obse ed in he
i s la ency windows (80–140 ms) wi h a p edominan ly on ocen al dis ibu ion (all F(1,9) > 5.814,
all p < .039), wi h la ge nega i e ampli udes o unpleasan pic u es han neu al pic u es. E ec s o
emo ional con en we e also p esen o e mo e pos e io si es in he 120–140 ms la ency ange (all
F(1,9) > 5.213, all p < .048). F om 80 o 120 ms, he e ec on hese pos e io elec odes was no so
Pos -p in ( inal d a pos - e e eeing)

6
ma ked, al hough he e we e emo ional con en × isual ield (all F(1,9) > 5.445, all p < .045) and
emo- ional con en × hemisphe e × isual ield (all F(1,9) > 5.559, all p < .043) in e ac ions. A he
la e in e al (200–280 ms), he di e en ial esponse o he emo ional con en had a mo e
cen opa ie al dis ibu ion (all F(1,9) > 8.522, all p < .017).
Fo he high-load condi ion, he e ec s o he emo ional con en we e modula ed by he hemisphe e o
eco ding and he isual ield (all F(1,9) > 5.228, all p < .048). The e we e no eliable emo ional
con en e ec s a any egion o hemisphe e.
Figs. 1 and 2 show he ERPs o unpleasan and neu al pic u es in he low-load condi ion, o he mos
ele an scalp loca ions.
Figu e 1 and 2
Discussion
In a p e ious epo [5], di e en ial b ain esponses o ask-i ele an emo ionally salien s imuli, as
e lec ed by ampli ude modula ions o he N1-P2 componen a pa ie occipi al and occipi al egions,
we e obse ed when a en ion was ac i ely engaged in a low-load p ima y ask, bu no when he load
was inc eased. We concluded ha unpleasan s imuli ecei e p io i ized p ocessing compa ed wi h
neu al s imuli e en when hey a e p esen ed ou side he a en ional ocus, and ha his p ocessing is
s ongly a enua ed by he a en ional load o he ongoing ask. He e, we pe o med new analyses o
ou ERP da a, o e alua e whe he a sus ained nega i e shi , p esen in he dis ac o pic u es ERP
wa e o ms, b oadly dis ibu ed and which showed a la ge ampli ude o emo ional s imuli, migh
indica e an addi ional di e en ial b ain esponse o he emo ional alue o s imuli. These new
analyses e ealed ha unpleasan pic u es p oduced g ea e nega i i ies, wi h a p edominan ly
on ocen al dis ibu ion, om 80 o 140 ms pos -s imulus, and mo e cen opa ie ally dis ibu ed
om 200 o 280 ms. Again, hese e ec s we e only signi ican in he low-load condi ion. Taken
oge he , hese indings con i m ha a en ional cap u e by emo ionally salien e en s depends on he
a ailabili y o a en ional esou ces.
The ea ly di e en ial neu al esponse (80–140 ms) o he emo ional con en o s imuli a on ocen al
loca ions migh e lec he ac i a ion o he p e on al co ex, which has been in ol ed in he as
ca ego iza ion o emo ion (see below). An ea ly ERP di e en ia ion be ween pleasan and unpleasan
s imuli ( acial exp essions) has been also epo ed by p e ious s udies [17] du ing passi e obse a ion
condi ions. Al hough o he s [6,8] ha e no ound ERP emo ional modula ions unde una ended
Pos -p in ( inal d a pos - e e eeing)
7
condi ions, no iceable di e ences in he expe imen al designs migh explain he disc epancies (see [5]
o a u he discussion).
The ea ly e ec o emo ional con en is also consis en wi h s udies epo ing an elec ophysiological
on al esponse o unpleasan s imuli in sho la encies [1,2,9]. Kawasaki e al. [9] eco ded
di e en ial neu al esponses o nega i e isual s imuli in he 120–170 ms la ency ange a
en omedial p e on al a eas (see also [10]). These au ho s sugges ed ha he p e on al ci cui s
migh p o ide a as ca ego iza ion o emo ion, which migh modula e he p ocessing o isual
in o ma ion in o he b ain egions. In a simila ein, Ca e ie´ e al. [2] obse ed ha unconsciously
pe cei ed signals o h ea ( e sus nonnega i e pic u es) p oduced a la ge ac i a ion in he
en omedial p e on al co ex (VMPFC) a ound 150 ms. They p oposed ha he VMPFC is in ol ed
in he op-down egula ion o a en ion, inc easing he subsequen isual co ex ac i a ion, and
esul ing in a acili a ion o dange p ocessing.
In line wi h hese p oposals, he ea ly di e en ial emo ional esponse o e an e io egions obse ed
in he p esen s udy, migh be conside ed as a co ela e o he in ol emen o he p e on al co ex in a
mechanism o op-down acili a ion o he isual p ocessing sys em. The subsequen signi ican ERP
modula ions, desc ibed in ou p e ious wo k [5], a he le el o N1-P2 componen o e he pos e io
scalp egion, migh e lec he esul o hese modula o y e ec s o he p e on al co ex on isual
egions. In addi ion, he p esen indings allow o app ecia e ha hese ea ly e ec s o emo ional
con en on ERPs a e in luenced by he a ailabili y o a en ional esou ces.
Emo ional modula ions o he ERPs om 200 o 280 ms pos -s imulus, cen opa ie ally dis ibu ed,
unde low-load condi ions, we e also ound. ERP ampli ude modula ions in his la ency ange, wi h
la ge nega i i ies o unpleasan s imuli, ha e been epo ed in se e al ecen s udies. Liddell e al.
[12] ound la ge ampli udes o he N2 componen , wi h a cen al dis ibu ion, in esponse o he
subliminal p esen a ion o ea ul aces as compa ed wi h neu al ones. Schupp e al. [18] ound an
a ec i e disc imina ion o IAPS pic u es ( e lec ed by la ge nega i i ies o a ec i e pic u es a
empo o-occipi al si es) when he op-down a en ional con ol was di ec ed o a p ima y ask. The
me hodological di e ences be ween s udies make di icul a de ailed compa ison be ween esul s o
an explana ion o he opog aphical dis ibu ion di e ences. In spi e o his, he p esen indings
p o ide con e ging e idence suppo ing an au oma ic esponse o emo ional s imuli, ei he aces [12]
o IAPS pic u es [18], which does no depend o hei explici ca ego iza ion and ha can be p esen
when a en ion is ocused in a main ask [18]. The p esen da a ex end hese indings indica ing ha
he elec ophysiological esponse o he a ec i e alue o ask-i ele an IAPS pic u es is s ongly
in luenced by he a ailabili y o esou ces o a en ion. E en hough no de ini e conclusions can be
ex ac ed om hese da a because o he small sample size, he esul s appea o p o ide new
elec ophysiological suppo o he hypo hesis ha a en ional load o he ongoing ask may be
Pos -p in ( inal d a pos - e e eeing)
8
c ucial in de e mining he ex en in which ask-i ele an emo ional s imuli a e p ocessed [15,16].
The e is ano he me hodological limi a ion ha should be no ed. Only nega i e and neu al s imuli
we e employed, which make i di icul o dis inguish he con ibu ions o he obse ed e ec s o
alence and a ousal. Addi ional expe imen s including also a ousing pleasan pic u es a e necessa y o
each s ong conclusions on au oma ic a en ion o ask-i ele an a ec i e pic u es as a unc ion o
hei wo basic dimensions.
In conclusion, he p esen indings p o ide e idence suppo ing ha he p io i ized p ocessing o
s imuli wi h emo ional alue p esen ed a ask-i ele an loca ions s ongly depends on he a en ional
load a ele an loca ions. They also e eal ha he ime cou se o emo ional alue p ocessing o
una ended s imuli is cha ac e ized by an ea ly (80–140 ms) modula ion o he on al
elec ophysiological esponse which p ecedes he di e en ial p ocessing a pos e io co ical egions.
Acknowledgemen s
This s udy was suppo ed by Spain’s Minis e io de Educación y Ciencia (SEJ2004-01377) and Xun a
de Galicia (PGIDT05PXI21101PN). The au ho s hank o D . S. Ba á (Op ics A ea, Applied Physics
Depa men a he Uni e si y o San iago de Compos ela) o me hodological assis ance.
Supplemen a y da a
Supplemen a y da a associa ed wi h his a icle can be ound, in he online e sion
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