ORIGINAL RESEARCH
published: 01 No embe 2018
doi: 10.3389/ nhum.2018.00437
O bi o on al Lesion Al e s B ain
Dynamics o Emo ion-A en ion and
Emo ion-Cogni i e Con ol
In e ac ion in Humans
Venla Kuusinen1,2,Elena Cesnai e1,3,Ja i Pe äkylä1,2,Kei h H. Ogawa4
and Kaisa M. Ha ikainen1,2*
1Beha io al Neu ology Resea ch Uni , Tampe e Uni e si y Hospi al, Tampe e, Finland, 2Facul y o Medicine and Li e Sciences,
Uni e si y o Tampe e, Tampe e, Finland, 3Depa men o Neu ology, Max Planck Ins i u e o Human Cogni i e and B ain
Sciences, Leipzig, Ge many, 4Depa men o Psychology, Sain Ma y’s College o Cali o nia, Mo aga, CA, Uni ed S a es
Edi ed by:
Shuhei Yamaguchi,
Shimane Uni e si y, Japan
Re iewed by:
Poppy L. A. Schoenbe g,
Vande bil Uni e si y Medical Cen e ,
Uni ed S a es
Giuliana Lucci,
Fondazione San a Lucia (IRCCS),
I aly
*Co espondence:
Kaisa M. Ha ikainen
[email p o ec ed]
Recei ed: 23 Ap il 2018
Accep ed: 04 Oc obe 2018
Published: 01 No embe 2018
Ci a ion:
Kuusinen V, Cesnai e E, Pe äkylä J,
Ogawa KH and Ha ikainen KM
(2018) O bi o on al Lesion Al e s
B ain Dynamics o Emo ion-A en ion
and Emo ion-Cogni i e Con ol
In e ac ion in Humans.
F on . Hum. Neu osci. 12:437.
doi: 10.3389/ nhum.2018.00437
Pa ien s wi h lesion o he o bi o on al co ex (OFC) expe ience challenges in emo ional
con ol and emo ion-guided beha io s. The OFC is known o pa icipa e in execu i e
unc ions and a en ional con ol o emo ion and ou p e ious esea ch sugges s OFC
lesion al e s he balance be ween olun a y and in olun a y a en ion and cogni i e
con ol wi hin he con ex o emo ion. To be e unde s and how OFC lesion a ec s
he dynamics and in e ac ion o hese unc ions, we s udied EEG and pe o mance o
12 pa ien s wi h lesion o he OFC and 11 con ol subjec s wi h in ac OFC in a Go/NoGo
isual eac ion ime (RT) ask wi h neu al a ge s and in e ening h ea - ela ed emo ional
dis ac o s (Execu i e RT Tes ). E en - ela ed po en ials (ERPs), speci ically N2P3 peak-
o-peak ampli ude and he ollowing la e posi i e po en ial (LPP), we e used o measu e
alloca ion o a en ion and cogni i e con ol o emo ional dis ac o s. Task pe o mance
and Beha io Ra ing In en o y o Execu i e Func ions—Adul e sion (BRIEF-A) sco es
we e used o assess execu i e unc ions. As expec ed, he Con ol g oup showed
inc eased N2P3 ampli ude in he con ex o h ea - ela ed dis ac o s, pa icula ly o e
he igh hemisphe e, while LPP was no modula ed by hese dis ac o s. In con as ,
pa ien s wi h OFC lesion showed no such impac o h ea - ela ed dis ac o s on
N2P3 ampli ude bu exhibi ed inc eased and p olonged le -la e alized impac o h ea
on LPP in he Go-condi ion. In NoGo-condi ion, he N2P3 ampli ude was inc eased in
bo h g oups due o h ea , bu he impac was seen ea lie , i.e., a he N2 peak in he OFC
g oup and la e a he P3 peak in Con ols. The OFC g oup commi ed mo e e o s in
he Execu i e RT Tes and epo ed mo e p oblems in BRIEF-A, hus bo h objec i e and
subjec i e e idence o challenges in execu i e unc ions was ob ained in pa ien s wi h
o bi o on al lesion. Fu he mo e, he ime-cou se o a en ion alloca ion and cogni i e
con ol owa ds ask-i ele an emo ional s imuli was al e ed as e idenced by ERPs. We
conclude ha o bi o on al lesion is associa ed wi h al e ed neu al dynamics unde lying
he in e ac ion o in olun a y a en ion o emo ion and cogni i e con ol. These al e a ions
in b ain dynamics may unde lie some o he challenges pa ien s encoun e in e e yday
li e when emo ional e en s in e ac wi h cogni i e demands.
Keywo ds: a en ion, cogni i e con ol, execu i e unc ion, emo ion, EEG, ERP, o bi o on al co ex, human s udies
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
INTRODUCTION
While li le is known o human o bi o on al co ex (OFC)
unc ion i is hough o be in ol ed in emo ional con ol and
emo ion-guided beha io s. The OFC wi h i s wide connec ions
o o he limbic and p e on al egions allows o in eg a ing
in o ma ion o emo ional alue in o a en ional and execu i e
unc ion ne wo ks (A mony and Dolan, 2002; Wallis, 2007).
Lesion o he OFC esul s in challenges in emo ion-guided
beha io s (Rolls and G abenho s , 2008) and expe ienced
di icul ies in execu i e unc ions necessa y in daily li e (Lø s ad
e al., 2012a). Howe e , neu opsychological es s ypically ail o
cap u e any de ici s in a en ional, execu i e o a ec i e unc ions
in pa ien s wi h lesion o OFC despi e hei sel - epo ed
occu ence (Manes e al., 2002; Zald and And eo i, 2010).
Al e a ions in emo ion-a en ion and emo ion-cogni i e con ol
in e ac ions ha e been obse ed in hese pa ien s wi h e en -
ela ed po en ials (ERPs; Ha ikainen e al., 2012a; Mäki-
Ma unen e al., 2017), sugges ing a lack o sensi i i y on he
pa o adi ional es ing me hods. Mo e de ailed knowledge,
including possible changes in he dynamics o hese in e ac ions,
is needed o u he insigh in o he neu al basis unde lying
he beha io al, emo ional and cogni i e challenges hese pa ien s
encoun e as well as o de eloping accu a e assessmen and
a ge ed ehabili a ion ools o hem.
To ob ain insigh in o he empo al dynamics o emo ion-
a en ion and emo ion-cogni i e con ol in e ac ions and he
ole o human OFC in hese unc ions, we s udied pa ien s
wi h ocal lesion o OFC using ERPs while hey pe o med a
compu e -based es o execu i e unc ions, Execu i e Reac ion
Time (RT) Tes , in he con ex o emo ional dis ac o s. This
pa adigm is designed o mimic e e yday challenges in execu i e
unc ions whe e simul aneous demands o mul iple execu i e
unc ions and unexpec ed emo ional e en s mee . As pa ien s
wi h OFC lesion epo challenges in execu i e unc ions in
e e yday si ua ions bu do no show de ici s in adi ional
neu opsychological es ing, we assumed ha a pa adigm
in oducing bo h emo ional and cogni i e challenge migh be
mo e sensi i e han adi ional es s in objec i ely cap u ing
di icul ies hese pa ien s encoun e . The Execu i e RT Tes has
been shown o be sensi i e in de ec ing emo ional in e e ence
o ask pe o mance in heal hy young subjec s e lec ing no mal
emo ion-a en ion in e ac ion (Ha ikainen e al., 2012b; E kkilä
e al., submi ed). Mo eo e , exagge a ed a en ion cap u e
by h ea (i.e., al e ed emo ion-a en ion in e ac ion) has also
been shown wi h his pa adigm in pa ien s wi h mild head
inju y and pe sis en symp oms (Ha ikainen e al., 2010b) and
in pa ien s wi h e ac o y epilepsy ea ed wi h deep b ain
s imula ion and agus ne e s imula ion (Ha ikainen e al.,
2014; Sun e al., 2015, 2017). In line wi h hese p e ious s udies,
we ocused on emo ional modula ion o la e a en ional and
cogni i e con ol phases e lec ed in N2 and P3 peaks and
used N2P3 peak- o-peak ampli ude as an elec ophysiological
bioma ke o emo ion-a en ion in e ac ion. Fu he mo e, we
assessed he subsequen emo ional modula ion o la e posi i e
po en ial (LPP), e lec ing con inued emo ional p ocessing a e
N2P3 po en ial.
Fo adap i e beha io s, e icien cogni i e and a en ional
con ol is needed o ei he selec he app op ia e beha io al
esponses o supp ess undue emo ional eac ions in ace
o emo ional e en s. To ha end, ask-i ele an emo ional
in o ma ion compe e o a en ional and execu i e esou ces
equi ed o pe o m he ask and hus ask-i ele an
emo ional e en s equen ly in e e e wi h pe o mance in
asks equi ing a en ion and execu i e unc ions in heal hy
subjec s (Ha ikainen e al., 2000, 2010a, 2012b; Hodsoll e al.,
2011). In con as o heal hy subjec s, we ha e p e iously shown
ha pa ien s wi h lesion o he OFC show s onge han no mal
bias o olun a y a en ion suppo ing ask pe o mance bu
a he expense o in olun a y a en ion alloca ion ha migh
be bene icial ou side he cu en ask demands (Ha ikainen
e al., 2012a; Mäki-Ma unen e al., 2017). In a ecen s udy
wi h OFC lesion pa ien s, non-emo ional audi o y s imuli
e oked educed ampli ude o N1 po en ial which is known
o be modula ed by op-down a en ion con ol (Kam e al.,
2018). O he elec ophysiological s udies ha e epo ed al e ed
a en ional p ocessing o emo ion and no el y a e OFC
lesion, al hough wi h equi ocal esul s. Rule e al. (2002) ound
enhanced P3 po en ials o a e si e ask-i ele an soma osenso y
s imuli. Dec eased P3 o no el i ele an audi o y s imuli along
wi h no mal P3b o a ge s has been p e iously epo ed
in pa ien s wi h OFC lesion (Lø s ad e al., 2012b). In line
wi h educed a en ion- ela ed ERPs o no el and emo ional
s imuli, ask-i ele an emo ional pho og aphs esul ed in
a enua ed N2P3 peak- o-peak ampli udes in pa ien s wi h
OFC lesion whe eas inc eased N2P3 ampli udes o immedia ely
ollowing a ge s we e obse ed (Ha ikainen and Knigh ,
2003; Ha ikainen e al., 2012a). Enhanced N2P3 ampli udes
we e also obse ed in he con ex o ask- ele an h ea -
ela ed s imuli in OFC lesion (Mäki-Ma unen e al., 2017).
These esul s sugges ha he OFC has a ole in guiding
a en ion o emo ionally o o he wise signi ican e en s e en
when i ele an o he cu en ask, modula ing he ex en o
emo ional impac on ask- ela ed a en ional and cogni i e
con ol p ocesses and in con ibu ing o he balance be ween
olun a y and in olun a y a en ion especially in he con ex o
emo ion.
The a eas in ol ed in emo ional p ocessing, like he
OFC and he amygdala, a e hough o in e ac wi h he
on opa ie al a en ion ne wo k, including he la e al p e on al
co ex, pa ie al co ex and he on al eye ields (Pessoa,
2010), o allow o no mal emo ion-a en ion in e ac ion.
OFC e alua es he alue and signi icance o emo ional
s imuli (W igh e al., 2008) and di ec s his in o ma ion
o o he b ain a eas esponsible o a en ional con ol and
execu i e unc ions. A en ion modula es he alue coding
in OFC (Xie e al., 2018) and dopamine gic modula ion
o OFC has been shown o al e a en ional pe o mance
(Wins anley e al., 2010). The pos e io OFC has been
shown o ac i a e oge he wi h empo opa ie al a eas and
he an e io cingula e co ex in esponse o salien e en s
ha occu ou side he cu en ocus o a en ion bu equi e
e alua ion o po en ial beha io al ele ance (G ube e al.,
2010). Thus, OFC may be pa o he neu al sys em ha allows
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
o moni o ing he en i onmen o po en ially signi ican
in o ma ion e en when ou side he cu en ask o ocus o
a en ion.
In ac communica ion be ween a en ional and emo ion-
ela ed ne wo ks, and hei key nodes such as he OFC, is needed
o app op ia e emo ion-a en ion in e ac ion allowing o
success ul emo ion-guided beha io s. Emo ional and a en ional
in e ac ions a e mul idi ec ional, in e wined and dynamic
wi hin senso y, limbic and a en ional ne wo ks ha in e ace
in OFC. Thus, ins ead o assessing emo ion-a en ion in e ac ion
as a s a ic phenomenon in a single ime poin i is impo an o
e alua e he empo al e olu ion and dynamics o his in e ac ion
in heal hy subjec s and how he dynamics a e al e ed in pa ien s
wi h OFC lesion. ERPs wi h empo al esolu ion compa ible
wi h apidly e ol ing men al e en s a e sui able o such an
app oach. Wi h his app oach i is possible o gain in o ma ion
ha e en ually allows o be e insigh in o de ici s hese pa ien s
encoun e in eal li e si ua ions ha cu en ly elude adi ional
assessmen .
No mal emo ional modula ion o a en ion- ela ed b ain
po en ials is ypically e lec ed in enhanced N2, P3 o N2-P3
po en ials (Dennis and Chen, 2007; Olo sson e al., 2008;
Mäki-Ma unen e al., 2015) o inc eased slow posi i i y
du ing LPP (Hajcak e al., 2009) depending on he ask. The
obse ed impac o ask-i ele an emo ional in o ma ion on
ask- ela ed a en ional p ocesses is ypically la e alized o he
igh hemisphe e dependen unc ions as well as a ge - ela ed
b ain po en ials o e he igh pa ie al egion (Ha ikainen
e al., 2000, 2007, 2010a). In o de o isola e he pu e impac
o emo ion, he impac o isual s imuli can be sub ac ed
by means o di e ence wa e o ms whe e an ERP e oked by
a condi ion wi h emo ionally neu al dis ac o is sub ac ed
om an ERP e oked by a condi ion wi h h ea - ela ed
emo ional dis ac o wi h exac ly he same basic physical
ea u es. Such di e ence wa e o ms e lec he me e impac
o emo ion wi h b ain po en ials ela ed o isual p ocessing
sub ac ed (Ha ikainen e al., 2007). In he cu en s udy, we
used black line d awings o biologically ele an h ea - ela ed
s imuli, i.e., spide s and emo ionally neu al con ol images
cons uc ed om iden ical line componen s bu in a di e en
con igu a ion ha did no ha e emo ional alue. Such simple
h ea - ela ed s imuli used in he cu en s udy a e known o
be p io i ized o a en ion ne wo ks (Vuilleumie and Schwa z,
2001) and p o ide means o ap in o po en ial al e a ions in
emo ion-a en ion in e ac ion due o OFC lesion. Because he
N2 po en ial e lec s ea ly cogni i e con ol, pa icula ly in a
esponse inhibi ion/NoGo ask (Donke s and an Box el, 2004;
Megías e al., 2017), and he P3 po en ial e lec s esponse
inhibi ion and possibly esponse cancella ion in a NoGo ask
(Kok e al., 2004; Randall and Smi h, 2011; G oom and C agg,
2015) as well as a en ion alloca ion (Polich, 2007), hey a e
sui able candida es o s udying he in e ac ion o emo ion
and a en ion/cogni i e con ol. We u he combined hese
ampli udes o N2P3 peak- o-peak ampli ude as ou p e ious
s udies wi h clinical popula ions ha e sugges ed ha in con as
o single peak measu emen s, N2P3 peak- o-peak ampli ude
may p o ide a mo e obus measu e o a en ion (Mäki-
Ma unen e al., 2015, 2017) and help con ol o abno mal
EEG shi s and slow wa es equen ly obse ed in clinical
popula ions.
In he cu en s udy, we aimed a assessing he impac o
OFC lesion on he empo al dynamics o emo ion-a en ion
and emo ion-cogni i e con ol in e ac ion. We assessed
how ask-i ele an emo ional dis ac o s modula e he N2,
P3 and LPP du ing a ask equi ing a en ion and cogni i e
con ol in heal hy subjec s and in pa ien s wi h OFC lesion.
In line wi h ou p e ious s udies (Ha ikainen e al., 2007,
2010a), we expec ed heal hy con ol pa icipan s o show
igh -la e alized modula ion o a en ion- ela ed ERPs o
ask-i ele an emo ion which would e lec no mal emo ion-
a en ion in e ac ion domina ed by he igh hemisphe e. In
compa ison, we expec ed al e ed modula ion o a en ion
and cogni i e con ol ela ed ERP componen s in pa ien s
wi h OFC lesion. In addi ion, we s udied whe he pa ien s
wi h OFC lesion expe ience inc eased di icul ies in e e yday
execu i e unc ions as p e iously epo ed (Lø s ad e al.,
2012a; Mäki-Ma unen e al., 2017) and assessed wi h he
Beha io Ra ing In en o y o Execu i e Func ions—Adul
e sion (BRIEF-A; Ro h e al., 2005) sel - epo ques ionnai e.
We also assessed whe he he e is any objec i e e idence
o execu i e dys unc ion as e lec ed in pe o mance in a
compu e -based Execu i e RT Tes ha engages se e al
execu i e unc ions simul aneously in he con ex o h ea -
ela ed dis ac o s.
MATERIALS AND METHODS
Subjec s
Twel e pa ien s (mean age = 58 yea s, male = 11, emale = 1,
mean yea s o educa ion = 13) wi h acqui ed lesion o he
OFC o med he OFC lesion g oup. Lesion e iologies we e
auma ic b ain inju y (n= 8), ope a ed meningioma (n= 3) and
aneu ysma ic suba achnoidal hemo hage (n= 1). All pa ien s
had pa icipa ed in a p e ious s udy o ou esea ch g oup
pe o ming a modi ied e sion o he cu en execu i e unc ion
es . The Con ol g oup consis ed o 12 neu ologically heal hy
subjec s (mean age = 53 yea s, male = 6, emale = 6, mean
yea s o educa ion = 15) ec ui ed as a con enience sample
om subjec s who had p e iously pa icipa ed in a s udy o ou
esea ch g oup, o educe he e ec o lea ning on be ween-g oup
di e ences. The g oups did no di e signi ican ly in e ms o age
and yea s o educa ion. Howe e , subjec sex dis ibu ion was
no balanced as he e was only one emale in he OFC lesion
g oup and six emales in he Con ol g oup. Gene al exclusion
c i e ia o bo h g oups included his o y o subs ance abuse,
p e ious neu ological diso de (such as ADHD), and cu en
mode a e o se e e dep ession. The s udy was app o ed by
he E hical Commi ee o he Tampe e Uni e si y Hospi al and
pa icipan s p o ided hei w i en in o med consen acco ding
o he Decla a ion o Helsinki go e ning he use o human
subjec s.
In i a ions o pa icipa e in he s udy we e based on
neu o adiological e alua ions o sui able lesion loca ion by
an expe ienced neu o adiologis who e e ed pa ien s o he
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
esea ch g oup. Lesion cha ac e iza ion was based on magne ic
esonance imaging (MRI) excep o one pa ien whose MRI
scan was una ailable. This pa ien ’s lesion e alua ion was
de e mined by compu ed omog aphy (CT) scan. Lesion loca ion
and size we e subsequen ly e alua ed by a neu ologis , and
pa ien s wi h mul iple o ex ensi e lesions ex ending beyond
he OFC we e excluded om he s udy. The mos se ious
inju y class in his s udy was mode a e b ain inju y, based
on he Finnish diagnos ic guidelines o b ain inju ies (B ain
Inju ies. Cu en Ca e Guidelines, 2017). Mode a e b ain inju y
in Finnish classi ica ion co esponds o mild complica ed o
mode a e b ain inju y in b ain inju y li e a u e (Williams e al.,
1990) and in Ame ican diagnos ics guidelines (Depa men o
Ve e ans A ai s and Depa men o De ense, 2016). Lesion
econs uc ions we e ca ied ou using MRIc on e sion 11
(Ro den e al., 2007) and a e p esen ed in Figu e 1. Lesion
cha ac e is ics, including ype o inju y, size and loca ion, a e
p esen ed in Table 1.
Ques ionnai es
BRIEF-A (Ro h e al., 2005) was used o assess pa icipan s’
subjec i e judgmen o hei execu i e unc ions in daily
li e. The ques ionnai e p esen s 70 s a emen s conce ning
di e en si ua ions employing execu i e unc ions equi ing
he esponde o assess whe he he/she exhibi s he kind o
beha io ‘‘ne e ,’’ ‘‘some imes’’ o ‘‘o en.’’ Nine di e en
aspec s o execu i e unc ions a e assessed (Inhibi ion,
Shi ing, Emo ional Con ol, Sel -Moni o ing, Ini ia ion,
Wo king Memo y, Planning/O ganizing, Task Moni o ing,
O ganiza ion o Ma e ials) and la e combined o p oduce
FIGURE 1 | Lesion econs uc ions o he o bi o on al co ex lesion g oup. Ele en ho izon al slices a e p esen ed o each pa ien . The op panel ep esen s g oup
o e lay o all lesions, whe e he colo ba indica es he numbe o pa ien s ha ing he lesion on he same a ea, wi h da ke colo s indica ing ewe pa ien s and ligh e
colo s ep esen ing mo e pa ien s. In he MRI lesion econs uc ion images o single pa ien s he ed colo indica es he lesion loca ion.
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
TABLE 1 | Lesion cha ac e is ics o he o bi o on al co ex lesion g oup.
Subjec E iology o inju y Time since inju y (mon hs) Lesion size (cm3) Lesion side B odmann a eas
OF1 T auma ic b ain inju y 36 2.94 Righ 10, 11
OF2 Suba achnoidal hemo hage 120 11.58 Righ 10, 11, 25, 32
OF3 Ope a ed meningioma 40 34.25 Bo h 9, 10, 11, 24, 25, 32, 45, 46, 47, 48
OF4 T auma ic b ain inju y 39 2.43 Bo h 11, 20, 36, 38
OF5 Ope a ed meningioma 41 49.29 Bo h 9, 10, 11, 25, 32, 45, 46, 47, 48
OF6 T auma ic b ain inju y 183 1.36 Righ 10, 11
OF7 Ope a ed meningioma 71 4.34 Le 10, 11
OF8 T auma ic b ain inju y 24 10.65 Bo h 10, 11, 20, 25, 28, 34, 38, 46, 47, 48
OF9 T auma ic b ain inju y 46 1.57 Righ 10, 11
OF10 T auma ic b ain inju y 24 3.62 Bo h 10, 11, 20, 38
OF11 T auma ic b ain inju y 19 2.99 Le 11, 25, 48
OF12 T auma ic b ain inju y 46 19.13 Bo h 10, 11, 20, 21, 25, 34, 36, 38, 46, 47, 48
Mean 57.4 12.0
Lesion e iology, side, size in cubic cen ime e s, a ec ed B odmann a eas and ime om he inju y in mon hs a e p esen ed.
h ee summa y indices (Beha io al Regula ion Index (BRI),
Me acogni ion Index (MI) and Global Execu i e Composi e
(GEC)). The BRIEF-A is sui able o assessing sel - epo ed
execu i e dys unc ion in b ain inju ed pa ien s (Waid-Ebbs
e al., 2012). Beck’s Dep ession In en o y (BDI; Beck e al.,
1996) was used o measu e possible dep essi e symp oms
o pa icipan s because dep ession was one o he exclusion
c i e ia and could impai ask pe o mance (Aus in e al.,
2001) and bias a en ion alloca ion o nega i e emo ional
s imuli (Go lib e al., 2004). Ri e mead Pos -Concussion
Symp oms Ques ionnai e (RPQ; King e al., 1995) was used o
measu e he amoun o pos -concussion ela ed symp oms in
pa ien s and de e mine whe he hey we e s ill symp oma ic.
Pa icipan s also comple ed a basic demog aphic in o ma ion
ques ionnai e.
Execu i e Reac ion Time Tes
The Execu i e RT Tes , de eloped by Ha ikainen e al.
(2010b) is a compu e -based Go/NoGo ask ha inco po a es
non-emo ional a ge s imuli and emo ion- ela ed (neu al and
h ea ening) i ele an dis ac o s imuli. The ask equi es
se e al ypes o execu i e unc ions, including esponse
inhibi ion, se shi ing and upda ing, wo king memo y and
selec i e a en ion. Schema ic diag am and ask desc ip ion o
he Execu i e RT Tes a e p esen ed in Figu e 2.
Pa icipan s pe o med he Execu i e RT Tes while sea ed
app oxima ely one me e away om a compu e sc een in
a sound a enua ed boo h. They we e ins uc ed o eac as
as and as accu a ely as possible o he o ien a ion o he
iangle. The emo ional igu e se ed as an i ele an dis ac o ,
hus he pa icipan s need no consciously eac o i , bu i
may cap u e a en ional esou ces ia bo om-up mechanism
and he eby c ea e a en ional compe i ion. Th ee e o ypes
a e possible in pe o ming he es : Miss, i.e., missing he
bu on p ess al hough bu on p ess was equi ed; Inco ec
bu on p ess, i.e., p essing he w ong bu on, o example
p essing down bu on e en hough he iangle was poin ing
upwa ds; and Commission e o , i.e., p essing he bu on e en
hough one was equi ed o wi hd aw om esponding ( he
so called ‘‘NoGo-e o ’’). Misses e lec p oblems in ini ia ing
a esponse o lapses in a en ion, Inco ec bu on p esses
FIGURE 2 | Schema ic illus a ion o he Execu i e Reac ion Time Tes by
Ha ikainen e al. (2010b), an in eg a ed es o execu i e unc ions wi h
ask-i ele an emo ional dis ac o s. This es mimics e e yday demands o
execu i e unc ions as i equi es mul iple di e en execu i e unc ions o be
engaged simul aneously, including wo king memo y, esponse inhibi ion and
he abili y o change beha io al se s lexibly. Co esponding o eal-li e
si ua ions whe e success ul beha io equi es sha ing cogni i e con ol
esou ces be ween he cu en ask and in e ening emo ional e en s, he es
equi es cogni i e con ol o su icien ly con ol emo ional in e e ence in o de
o pe o m well. Thus, his es allows o sensi i e assessmen o execu i e
unc ions as well as emo ion-a en ion and emo ion-execu i e unc ion
in e ac ion. Each ial begins wi h a whi e iangle appea ing on he sc een
poin ing ei he upwa ds o downwa ds. The pa icipan s mus a end o he
poin ing di ec ion o he iangle and keep i in wo king memo y. A Go o a
NoGo signal in o m o a a ic ligh is p esen ed 150 ms a e he o se o he
iangle in he middle o he sc een. The colo o he a ic ligh signals whe he
he pa icipan is supposed o espond o wi hhold om esponding; g een
ligh = Go and ed ligh = NoGo. In hal o he blocks he a ic ligh ule o
esponding is e e sed equi ing he subjec o lexibly change se s and
espond acco ding o a new ule. In Go-condi ion, pa icipan s we e ins uc ed
o p ess a esponse pad bu on co esponding o he iangle o ien a ion
memo ized ( iangle up = middle inge , iangle down = index inge ).
Task-i ele an emo ional dis ac o s we e p esen ed in he middle posi ion o
he a ic ligh . The emo ional dis ac o s we e composed o iden ical
line-elemen s bu in a di e en con igu a ion o ming ei he a igu e o a spide
(nega i e, h ea ening dis ac o ) o a lowe (neu al dis ac o ).
e lec lapses in wo king memo y, while Commission e o s
indica e p oblems in esponse inhibi ion. In summa y, he
ask equi es e icien con ol o execu i e unc ions, selec i e
a en ion and es s he e ec o ask-i ele an emo ional s imuli
on hese p ocesses and he abili y o he subjec s o con ol
o i .
The numbe o Go/NoGo blocks, h ea - ela ed and neu al
dis ac o s and o ien a ion o he iangle we e all balanced o a
50:50 a io and p esen ed in andom o de . Each block consis ed
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
o 64 ials and he o al leng h o he ask was 16 blocks, esul ing
in 1,024 ials pe pa icipan . Hal o he blocks we e pe o med
using he igh hand and he o he hal pe o med using he
le hand. RT and numbe o e o s se ed as measu es o ask
pe o mance. The emo ional igu es we e composed o iden ical
black lines in o de o con ol o physical p ope ies (size, colo ,
complexi y, luminance) and p e en s imuli p ope ies o he
han emo ional con en om in luencing isual a en ion and
ERPs.
EEG Reco ding and P ep ocessing
The EEG signal was eco ded using 64 Ag/AgCl ac i e elec odes
(ac iCAP, Gilching, Ge many) along wi h a QuickAmp-ampli ie
sys em and B ain Vision Reco de so wa e (B ain P oduc s,
GmbH). The sampling a e used o digi ize EEG was 500 Hz.
Elec ode impedances we e kep below 5 k h oughou he
eco ding. The EEG p ep ocessing and cons uc ion o ERPs
was done o line using B ain Vision Analyze 2 so wa e (B ain
P oduc s, GmbH). The EEG was down sampled o 250 Hz
and il e ed wi h IIR il e s o 0.01–70 Hz ollowed by blink
a i ac emo al by semiau oma ic, independen componen
analysis–based unc ion, me hod desc ibed by Jung e al.
(2000). An addi ional a i ac emo al was pe o med emo ing
in e als wi h mo e han 100 µV ol age di e ence o he
su ounding signal. The da a was hen e- e e enced o he
linked igh and le lobules au iculae and u he il e ed o
0.01–30 Hz be o e segmen a ion. Segmen a ion o c ea e ERPs
was pe o med by cu ing segmen s s a ing 200 ms be o e ial
onse , i.e., he appea ance o he iangle on he sc een, and
ending 1,800 ms a e . Segmen s we e baseline-co ec ed o
he base line o a ime ame om be o e 200 ms o he ial
onse .
The ERP segmen s we e a e aged based on condi ion (Go
o NoGo) and dis ac o ype (Emo ional, Neu al), esul ing in
ou di e en ERP condi ions o each subjec (Go Emo ional,
Go Neu al, NoGo Emo ional and NoGo Neu al, espec i ely).
The minimum cu -o o he numbe o segmen s pe condi ion
pe pa icipan was 50. Each ial began wi h he iangle,
i.e., loca ed a imepoin 0 ms. Go/NoGo signal, i.e., he a ic
ligh , appea ed 300 ms a e he ial onse . The N2 and
P3 componen s appea ing a e he Go/NoGo signal we e
iden i ied om he G and A e age wa e o ms based on isual
inspec ion and semiau oma ic peak de ec ion based on he
ime ames de ined by isual inspec ion. The N2 was de ined as
he mos nega i e peak in a ime ame anging om 450 ms
o 670 ms (i.e., 150–370 ms om he a ic ligh cue) and he
P3 as he mos posi i e peak in a ime ame om 600 ms
o 900 ms (i.e., 300–600 ms om he a ic ligh cue). We
expo ed he mean alue a ound he obse ed peak ±5 ime
poin s om he peak ma ke o analysis. N2 ampli ude is
no mally well depic ed in on ocen al egions whe eas he
a ge -e oked P3 ampli ude is seen on he pa ie al a eas and
we included elec odes ha bes cap u e hese componen s. Fo
his eason and in o de o educe he numbe o s a is ical
compa isons and o keep me hodology simila o ou p e ious
s udies (Mäki-Ma unen e al., 2015, 2017), we selec ed one
on al, cen al and pa ie al elec ode o e each hemisphe e
o s a is ical analysis: F3 (le on al), F4 ( igh on al), C3
(le cen al), C4 ( igh cen al), P3 (le pa ie al) and P4 ( igh
pa ie al). The N2P3 peak- o-peak ampli ude was cons uc ed by
sub ac ing he N2 ampli ude om he P3 ampli ude o each
elec ode.
S a is ical Analysis
Beha io al Analysis
The beha io al analysis was pe o med using R e sion 3.3.3
(R Co e Team, 2017). The dis ibu ion o RTs was skewed and
hey we e no malized using loga i hmic ans o ma ion be o e
he analysis. RT analysis was conduc ed wi h mixed model
ANOVA whe e G oup (OFC, Con ol) se ed as a be ween-
g oup ac o and Emo ion (Emo ional, Neu al) as a wi hin-
subjec s ac o . E o analysis was done using gene alized bina y
logis ic eg ession as sugges ed by Jaege (2008) and Dixon
(2008). In he bina y logis ic eg ession model, G oup (OFC,
Con ol) and Emo ion (Emo ional, Neu al) we e used as ixed
e ec p edic o s and Subjec as a andom e ec p edic o . Subjec
was classi ied as a membe o he OFC g oup o he Con ol
g oup in a hie a chical manne .
Fo he bina y logis ic eg ession analysis, e o da a
was dicho omized. Th ee ypes o e o s we e possible
(See ‘‘Execu i e Reac ion Time Tes ’’ sec ion); Go-e o s,
i.e., ‘‘Inco ec bu on p ess’’ and ‘‘Miss,’’ and NoGo-e o s,
i.e., ‘‘Commission e o s.’’ Inco ec bu on p esses we e
dicho omized as ei he ‘‘inco ec ’’ o ‘‘o he ’’ (i.e ‘‘co ec ’’ o
‘‘miss,’’ o he possible answe s in a Go-si ua ion) and Misses as
‘‘miss’’ o ‘‘o he ’’ (i.e., ‘‘co ec ’’ o ‘‘inco ec ’’ using a simila
logic as p e iously). Commission e o s we e dicho omized as
‘‘commission e o ’’ o ‘‘co ec ’’ (no o he e o ypes a ailable
in NoGo-si ua ion). To al e o s we e labeled as ‘‘e o ’’ o
‘‘co ec .’’ Following his, a sepa a e model o p edic p obabili y
o make an e o was c ea ed o each condi ion. We used he
‘‘lme4’’ package e sion 1.1–13 (Ba es e al., 2015) o bina y
logis ic eg ession modeling and analysis.
Be o e modeling, he da a was checked o ou lie s. A subjec
was conside ed an ou lie i his/he e o sum in any e o
ca ego y exceeded he g oup mean e o a e o ha e o
ca ego y by mo e han 2.5 s anda d de ia ions (SD). In case o
an ou lie , he da a was analyzed wi hou he ou lie and i he
esul s changed, he ou lie was excluded om he inal analysis.
Da a was also checked o ou lie and ‘‘w ong- ule’’ blocks. A
block wi h w ong ule was a block whe e he subjec appa en ly
answe ed using he w ong answe ing ule. I 75% o he answe s
we e Commission e o s and Misses, he block was conside ed a
w ong ule block and excluded. Ou lie block was a block whe e
he subjec ’s e o a e was mo e han h ee SD abo e his/he
mean e o a e. Nei he w ong ule blocks no ou lie blocks
we e de ec ed in he da a, i.e., no blocks we e excluded om he
analysis. Ou lie subjec c i e ia we e me se e al imes in bo h
g oups, howe e , he esul was a ec ed only once. Pa icipan
numbe 12 om he Con ol g oup was excluded om u he
beha io al and neu ophysiological analysis based on he highe
amoun o o al e o s compa ed o he es o he g oup (To al
e o s, g oup mean = 3% s. pa icipan 12 mean = 9.6%).
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
ERP and ERP Di e ence Wa e Analysis
The N2P3 peak- o-peak ampli ude was used o s a is ical
analysis. We used mixed model ANOVA ( epea ed measu es
and be ween-g oup measu es) o compa e be ween-g oup
and wi hin-subjec s ac o s simul aneously. G oup (OFC,
Con ol) was de ined as a be ween-g oup ac o and Emo ion
(Emo ional, Neu al), La e ali y (Righ , Le ) and Region
(F on al, Cen al, Pa ie al) as wi hin-subjec s ac o s. ERPs we e
analyzed sepa a ely o he Go- and NoGo-condi ions. Da a
sui abili y o ANOVA assump ions was es ed, no mali y es s
yielding no mal o close o no mal dis ibu ions.
To analyze di e ences in a en ion alloca ion o emo ion
be ween he g oups and o elimina e he e ec o o he isual
p ocesses and po en ial a i ac s on he obse ed di e ences, we
c ea ed di e ence wa e o ms by sub ac ing ERP ampli ude in
con ex o neu al dis ac o om ERP ampli ude in con ex
o emo ional dis ac o in bo h g oups (ERP Emo ional—ERP
Neu al). This di e ence wa e o m was used o in es iga e
di e ences in con inuous emo ional p ocessing in selec ed
ime windows and subjec ed o sepa a e s a is ical analysis.
In Go-si ua ion we chose ime windows co esponding o he
ime o P3 peak and he ollowing slow posi i e wa e o m, he
LPP, which is epo ed o be la ge when emo ional s imuli
is only a ended o bu educed wi h success ul eapp aisal o
emo ion (Hajcak and Nieuwenhuis, 2006), i.e., 700–800 ms
and 800–900 ms in ou pa adigm. In NoGo-si ua ion we
chose ime windows a ound he N2 peak and he P3 peak,
i.e., 600–700 ms and 700–800 ms, o u he analysis as hese
po en ials a e hough o e lec di e en phases o cogni i e
con ol equi ed o esponse inhibi ion and a e known o
be modula ed by emo ion wi h he ex en o modula ion
e lec ing ac o s in luencing emo ion-cogni ion in e ac ion such
as emo ional in elligence (Megías e al., 2017). The amoun
o selec ed ime windows was kep o minimum o con ol
o amilywise e o a e. Sub ac ion ERP emo ional—ERP
Neu al was conduc ed i s and he mean ampli ude in he
a o emen ioned 100 ms ime windows expo ed o s a is ical
analysis. The di e ence wa e o ms e lec ing me e impac o
emo ion we e subjec ed o ANOVA whe e ac o G oup (OFC,
Con ol) se ed as a be ween-g oup ac o and La e ali y (Righ ,
Le ) and Region (F on al, Cen al, Pa ie al) as wi hin-subjec s
ac o s.
Pos hoc analysis wi h ANOVA was pe o med when
signi ican in e ac ions we e me . When decomposing
in e ac ions o pos hoc ANOVAs, we chose o adjus
he signi icance le el based on he Bon e oni me hod, o
p= 0.017 on he inal ANOVA le el o co ec o mul iple
compa isons. S a is ical analysis was pe o med using R e sion
3.3.3 (R Co e Team, 2017) and he package ‘‘ez’’ e sion 4.4-0 o
ANOVA compa isons (Law ence, 2016). Sphe ici y co ec ions
we e applied whene e non-sphe ical da a was encoun e ed.
Ques ionnai e Analysis
The BRIEF-A composi e sco es and indices, he RPQ subsco es
and o al sco es, and he BDI sco es we e analyzed using R
e sion 3.3.3 (R Co e Team, 2017). No mali y es s esul ed
in a non-no mal dis ibu ion in mos cases, hus Wilcoxon
ank-sum es s o nonpa ame ic compa isons we e applied
using package coin (Ho ho n e al., 2006, 2008). BRIEF-A
aw sco es we e ans o med o no ma i e -sco es and he
-sco es used o be ween-g oups compa ison, as hey allow
compa ison o a s anda d coe al sample (Ro h e al., 2005).
F om he RPQ we compa ed he cu en epo ed symp oms
be ween he g oups. The alidi y o he RPQ o al sco e
has been ques ioned because pos -concussion symp oms a e
nonspeci ic, i ing many o he condi ions as well. Di iding
he o al sco e o emo ional, soma ic and cogni i e symp om
ca ego ies has been sugges ed in se e al s udies, hus we di ided
he o al sco e in o hose ca ego ies acco ding o Smi h-Seemille
e al. (2003) and Po e e al. (2006), and analyzed hem
sepa a ely.
RESULTS
Task Pe o mance
RT analysis esul ed in no signi ican main e ec s o in e ac ions;
he e was no di e ence be ween he g oup RTs (OFC lesion
g oup, RT = 476.87 ms ±191.61 ms s. Con ol g oup
RT = 459.09 ms ±180.16 ms). The OFC lesion g oup
was 2.3 imes mo e likely o commi an e o o any ype
compa ed o he Con ols (To al e o s, Main e ec o G oup,
OFC s. Con ols: OR 0.43, (95% CI = 0.21–0.88), 4.7%
s. 2.1%). The OFC lesion g oup was 5.2 imes mo e likely
o miss a esponse compa ed o he Con ol g oup (Miss,
Main e ec o G oup, OFC s. Con ols: OR 0.19, (95%
CI = 0.041–0.90), 0.9% s. 0.2%). The inc eased p obabili y
o commi an e o o any ype o miss esponding in
he OFC lesion g oup was no dependen on he emo ional
dis ac o . The p obabili y o commi an Inco ec bu on
p ess was almos signi ican ly di e en (p= 0.059) be ween
he g oups, he OFC lesion g oup commi ing mo e Inco ec
bu on p esses (Main e ec o G oup, OFC s. Con ols: OR
0.39, (95% CI = 0.15–1.04), 2.9% s. 1.2%). Bina y logis ic
eg ession o Commission e o s did no yield signi ican
esul s.
ERPs
Go-Condi ion
The mean ampli udes and SD o he N2 and P3 ERP
componen s as well as he N2P3 peak- o-peak ampli udes
o bo h g oups in each condi ion a e lis ed in Table 2.
In he Go-condi ion, analysis o he N2P3 peak- o-peak
ampli ude yielded no s a is ically signi ican main e ec s.
The e was a signi ican in e ac ion o G oup ×Emo ion
(F(1,21)= 10.36, p= 0.0041, η2
G= 0.0026) which was in es iga ed
u he by di iding he da a by G oup and analyzing hem
sepa a ely wi h pos hoc ANOVAs. In he Con ol g oup,
he N2P3 ampli ude in con ex o he emo ional dis ac o
was la ge compa ed o he neu al dis ac o (F(1,10)= 6.31,
p= 0.031, η2
G= 0.0031; Emo ional = 7.10 µV±3.74 µV
s. Neu al = 6.71 µV±3.59 µV). Howe e , unde he
Bon e oni-adjus ed signi icance c i e ia his e ec was only
app oaching signi icance. In he OFC lesion g oup, he
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Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
TABLE 2 | N2, P3 and N2P3 ampli udes and s anda d de ia ions (in µV) p esen ed o each condi ion (Go and NoGo), o bo h g oups and sepa a ely o bo h emo ional
dis ac o s and o each elec ode o e he le and igh on al (F3, F4), cen al (C3, C4) and pa ie al (P3, P4) scalp si es used in he analysis.
F on al F3 (le ) F4 ( igh )
Condi ion G oup Dis ac o N2 P3 N2P3 N2 P3 N2P3
Go Con ol Emo ional −5.3 (3.8) 1.5 (3.2) 6.8 (3.3) −3.9 (4.4) 3.1 (2.8) 7.0 (3.3)
Neu al −5.1 (3.8) 1.4 (3.1) 6.5 (3.3) −3.6 (4.7) 2.8 (3.0) 6.4 (3.0)
OFC Emo ional −3.5 (6.0) 4.4 (7.2) 7.9 (4.0) −2.5 (4.9) 5.6 (5.2) 8.2 (3.5)
Neu al −3.6 (5.6) 4.7 (7.0) 8.3 (4.7) −2.8 (4.8) 5.7 (5.3) 8.4 (4.4)
NoGo Con ol Emo ional −3.0 (2.1) 7.4 (4.2) 10.4 (4.5) −3.0 (2.3) 6.3 (3.8) 9.3 (4.6)
Neu al −2.6 (2.7) 7.1 (3.9) 9.7 (4.1) −2.8 (2.9) 5.8 (3.7) 8.5 (4.1)
OFC Emo ional −2.3 (3.6) 10.4 (4.8) 12.7 (5.5) −2.6 (3.9) 10.3 (4.9) 12.8 (5.2)
Neu al −1.9 (3.7) 10.1 (4.4) 12.0 (5.2) −1.9 (3.3) 10.2 (4.7) 12.0 (5.0)
Cen al C3 (le ) C4 ( igh )
Condi ion G oup Dis ac o N2 P3 N2P3 N2 P3 N2P3
Go Con ol Emo ional −6.5 (3.9) 0.7 (3.0) 7.2 (4.0) −4.3 (3.2) 3.2 (4.3) 7.5 (4.3)
Neu al −6.5 (3.9) 0.6 (3.1) 7.1 (3.8) −4.3 (3.5) 2.7 (3.8) 7.1 (4.0)
OFC Emo ional −4.7 (6.4) 3.4 (6.3) 8.2 (3.8) −4.1 (6.1) 4.5 (4.8) 8.6 (4.4)
Neu al −4.8 (6.2) 3.5 (6.1) 8.4 (4.2) −4.6 (5.8) 4.9 (5.0) 9.5 (4.6)
NoGo Con ol Emo ional −2.1 (2.2) 7.6 (3.9) 9.6 (4.0) −1.8 (1.7) 7.0 (4.1) 8.7 (4.6)
Neu al −1.9 (2.3) 7.1 (3.8) 9.0 (3.9) −1.6 (1.7) 6.5 (4.0) 8.1 (4.3)
OFC Emo ional −1.5 (3.8) 9.1 (3.6) 10.7 (5.0) −2.0 (3.7) 9.1 (4.5) 11.1 (4.8)
Neu al −1.1 (4.3) 9.2 (3.6) 10.3 (5.1) −1.2 (3.8) 8.9 (4.4) 10.1 (5.0)
Pa ie al P3 (le ) P4 ( igh )
Condi ion G oup Dis ac o N2 P3 N2P3 N2 P3 N2P3
Go Con ol Emo ional −2.8 (4.7) 4.4 (3.6) 7.2 (4.7) −1.4 (4.3) 5.5 (3.8) 6.9 (4.6)
Neu al −2.9 (5.1) 4.0 (4.0) 6.9 (4.8) −1.2 (4.8) 5.0 (4.1) 6.2 (4.5)
OFC Emo ional −2.7 (4.4) 5.6 (4.4) 8.3 (3.2) −2.6 (3.7) 5.9 (3.4) 8.5 (3.8)
Neu al −3.2 (4.5) 5.2 (4.0) 8.4 (3.1) −2.8 (3.8) 6.0 (3.3) 8.8 (3.7)
NoGo Con ol Emo ional −0.7 (3.7) 6.1 (4.6) 6.9 (4.0) −0.4 (3.8) 6.4 (4.0) 6.8 (4.6)
Neu al −0.9 (4.0) 6.2 (3.9) 7.1 (3.8) −0.5 (3.8) 6.4 (3.8) 6.9 (4.3)
OFC Emo ional −0.9 (3.4) 7.2 (3.5) 8.1 (3.8) −0.4 (2.5) 7.5 (3.6) 7.9 (3.1)
Neu al −0.7 (4.1) 7.0 (3.6) 7.7 (4.2) −0.3 (2.8) 7.4 (3.4) 7.6 (3.2)
alence o he dis ac o had no signi ican e ec on he
N2P3 ampli ude (F(1,11)= 4.49, p= 0.058, η2
G= 0.0031,
Emo ional = 8.25 µV±3.39 µV s. Neu al = 8.64 µV±
3.74 µV).
The e was also an in e ac ion e ec o G oup ×
Emo ion ×La e ali y (F(1,21)= 4.48, p= 0.046, η2
G= 0.0004). The
da a was di ided by G oup and he g oups analyzed sepa a ely.
Pos hoc ANOVA e ealed signi ican in e ac ion e ec o
Emo ion ×La e ali y in he Con ol g oup (F(1,10)= 9.19,
p= 0.013, η2
G= 0.0006) bu no in he OFC lesion g oup
(F(1,11)= 1.04, p= 0.33, η2
G= 0.0003). Fu he analysis o he
in e ac ion was pe o med by di iding Con ol g oup da a by
La e ali y and conduc ing sepa a e pos hoc ANOVAs on he
igh and le hemisphe es, e ealing N2P3 ampli ude was la ge
in con ex o he emo ional dis ac o o e he igh hemisphe e
(F(1,10)= 8.47, p= 0.016, η2
G= 0.0061; Emo ional = 7.13 µV±
3.89 µV s. Neu al = 6.57 µV±3.64 µV; Figu e 3). The
alence o he dis ac o had no signi ican e ec on he
N2P3 ampli ude o e he le hemisphe e in he Con ol g oup
(F(1,10)= 2.78, p= 0.13, η2
G= 0.0010). The e was also an
in e ac ion e ec o G oup ×Emo ion ×La e ali y ×Region
(F(2,42)= 3.45, p= 0.041, η2
G= 0.0001). In addi ion o he
a o emen ioned e ec s in he Con ol g oup, decomposing
his in e ac ion by pos hoc ANOVAs e ealed an in e ac ion
o Emo ion ×Region ×La e ali y in he OFC lesion g oup
(F(2,22)= 4.14, p= 0.03, η2
G= 0.0005). The OFC lesion g oup
da a was di ided by La e ali y and pos hoc ANOVAs pe o med,
howe e , no u he signi icance was de ec ed on ei he
hemisphe e.
NoGo-Condi ion
In he NoGo-condi ion, analysis o he N2P3 peak- o-peak
ampli ude showed Main e ec o Emo ion (F(1,21)= 8.64,
p= 0.008, η2
G= 0.0033) and Main e ec o Region (F(2,42)= 37.4,
p<0.001, η2
G= 0.11) bu no s a is ically signi ican di e ence
be ween he g oups. Main e ec o Emo ion indica ed ha he
N2P3 ampli ude in con ex o he emo ional dis ac o was
la ge han N2P3 ampli ude in con ex o he neu al dis ac o
(Emo ional = 9.62 µV±4.76 µV s. Neu al = 9.13 µV±
4.55 µV). Main e ec o egion indica ed ha he size o he
N2P3 ampli ude di e ed signi ican ly be ween each b ain egion,
being la ges on he on al egion and smalles on he pa ie al
egion (pos hoc - es F on al s. Cen al, p<0.001, F on al
s. Pa ie al, p<0.001 and Cen al s. Pa ie al, p<0.001;
F on al = 11.0 µV±4.83 µV s. Cen al = 9.74 µV±4.47 µV
s. Pa ie al = 7.39 µV±3.70 µV). A signi ican in e ac ion o
Emo ion ×Region was also obse ed (F(2,42)= 5.31, p= 0.009,
η2
G= 0.0011). Pos hoc ANOVAs we e pe o med o each
egion sepa a ely, e ealing la ge N2P3 ampli udes in con ex
o he emo ional dis ac o on on al and cen al egions bu
no on he pa ie al egion (F on al egion: F(1,22)= 14.78,
p= 0.0009, η2
G= 0.0060; Emo ional = 11.36 µV±4.99 µV s.
F on ie s in Human Neu oscience | www. on ie sin.o g 8No embe 2018 | Volume 12 | A icle 437
Kuusinen e al. O bi o on al Co ex in Emo ion-A en ion In e ac ion
FIGURE 3 | G ea e modula ion o la e posi i e po en ial (LPP) by h ea due o
o bi o on al lesion. Abo e e en - ela ed po en ial (ERP) wa e o ms illus a e
N2P3 complex and he ollowing LPP in he Con ol g oup (ERP on he le )
and in he OFC lesion g oup (ERP on he igh ) in he P3 elec ode.
Signi ican ly enhanced and p olonged posi i i y was de ec ed due o
h ea - ela ed emo ional dis ac o s in he OFC lesion g oup bu no in he
Con ol g oup in he 700–900 ms ime window depic ed wi h a ec angle.
S a is ical signi icance is ma ked wi h an as e isk. Dashed ed line a 300 ms
ep esen s onse o he esponse cue (i.e., he a ic ligh ). Below opog aphy
o he di e ence wa e o m isola ing emo ional modula ion o b ain ac i i y
(ERP Emo ional—ERP Neu al) o h ee subsequen 100 ms ime windows in
each g oup. Time ange 700–900 ms shows inc eased le -la e alized posi i i y
on pa ie al egion in he OFC lesion g oup (lowe ow) in con as o Con ol
g oup (uppe ow). In he Con ol g oup he inc eased posi i i y o emo ion
de ec ed in analysis o he N2P3 peak- o-peak ampli ude was mo e ocal,
igh -la e alized and limi ed in ime ( opog aphy ime window 600–700 ms) as
opposed o he OFC lesion g oup, who exhibi ed mo e di use, le -la e alized
and p olonged posi i i y.
Neu al = 10.63 µV±4.71 µV. Cen al egion: F(1,22)= 13.27,
p= 0.0014, η2
G= 0.0054; Emo ional = 10.06 µV±4.49 µV s.
Neu al = 9.42 µV±4.49 µV), suppo ing he obse ed main
e ec s.
ERP Di e ence Wa e o m Window
Analysis
Go-Condi ion
In addi ion o assessing he impac o emo ional dis ac o s
on a en ion- ela ed ERP peaks wi h peak- o-peak analysis,
we assessed he impac o emo ion on selec ed 100 ms ime
windows. We isola ed he impac o me e emo ional alue
wi h ERP di e ence wa e o m (ERP Emo ional Go—ERP
Neu al Go) and analyzed he mean ampli ude o he di e ence
wa e o m wi hin a 700–800 ms ime window. This analysis
esul ed in no main e ec s, bu an in e ac ion e ec o
G oup ×La e ali y ×Region (F(2,42)= 3.51, p= 0.039,
η2
G= 0.024) was obse ed. To in es iga e his in e ac ion
u he , he da a was di ided by G oup and g oups we e
analyzed sepa a ely wi h pos hoc ANOVAs. In he OFC
lesion g oup, pos hoc ANOVA e ealed La e ali y ×Region
in e ac ion (F(2,22)= 4.75, p= 0.019, η2
G= 0.055). Pos hoc
ANOVAs conduc ed sepa a ely o each egion showed ha
o e he pa ie al egion, he mean ampli ude o he di e ence
wa e o m signi ican ly di e ed be ween he wo hemisphe es
(F(1,11)= 13.15, p= 0.004, η2
G= 0.16, Le Pa ie al = 0.61 µV±
0.83 µV s. Righ Pa ie al = −0.019 µV±0.67 µV). In
he OFC g oup emo ional s imuli we e associa ed wi h g ea e
posi i i y o e he le pa ie al co ex and he ampli udes in
con ex o emo ional compa ed o neu al dis ac o s di e ed
on he le pa ie al egion (Figu e 3). In he Con ol g oup,
he e we e no main e ec s o in e ac ions wi hin his ime
window.
ERP di e ence wa e o m analysis o he mean ampli ude
wi hin ime window 800–900 ms esul ed in Main e ec o
Region (F(2,42)= 3.58, p= 0.037, η2
G= 0.036), indica ing
emo ional modula ion o b ain ac i i y di e ed signi ican ly
be ween he cen al and pa ie al egions (pos hoc - es Cen al
s. Pa ie al, p= 0.031; Pa ie al = 0.33 µV±0.68 µV s.
Cen al = −0.029 µV±0.75 µV). Fu he mo e, in e ac ion
e ec G oup ×La e ali y ×Region (F(2,42)= 5.38, p= 0.008,
η2
G= 0.019) was obse ed and he da a was di ided by G oup
and g oups analyzed we e sepa a ely wi h pos hoc ANOVAs.
In he OFC lesion g oup, Main e ec o Region (F(2,22)= 5.42,
p= 0.012, η2
G= 0.064) showed ha he mean ampli ude o he
di e ence wa e o m wi hin he analyzed ime window di e ed
signi ican ly on he on al and pa ie al egions (pos hoc -
es F on al s. Pa ie al, p= 0.043; F on al = −0.08 µV±
0.84 µV s. Pa ie al = 0.41 µV±0.84 µV) bu no on
he o he egions (F on al s. Cen al, p= 0.93; Cen al s,
Pa ie al, p= 0.07). In e ac ion e ec La e ali y ×Region
was also obse ed (F(2,22)= 5.96, p= 0.009, η2
G= 0.030).
Pos hoc ANOVAs pe o med sepa a ely o each egion
showed ha he mean ampli ude on he le pa ie al egion
was signi ican ly la ge compa ed o he mean ampli ude
on he igh pa ie al egion (F(1,11)= 8.71, p= 0.013,
η2
G= 0.072; Le Pa ie al = 0.65 µV±0.89 µV s. Righ
Pa ie al = 0.18 µV±0.89 µV). The e was also a end,
unde he Bon e oni-adjus ed signi icance c i e ia, owa ds a
di e ence in he mean ampli udes on he igh on al and
le on al egion (F(1,11)= 5.16, p= 0.044, η2
G= 0.024; Righ
F on al = 0.05 µV±0.80 µV s. Le F on al = −0.21 µV±
0.92 µV). Inspec ion o he o iginal ERP wa e o ms showed
p olonged and enhanced LPP o e he le pa ie al egion in
OFC g oup in con ex o emo ional dis ac o s (Figu e 3). In
he Con ol g oup, no u he Main e ec s o In e ac ions we e
de ec ed.
NoGo-Condi ion
In NoGo-si ua ion, analysis o he mean ampli ude o he
di e ence wa e o m e lec ing emo ional modula ion o b ain
ac i i y du ing a esponse inhibi ion ask (ERP Emo ional
NoGo—ERP Neu al NoGo) in 600–700 ms ime window
esul ed in Main e ec o G oup (F(1,21)= 4.53, p= 0.045,
η2
G= 0.11; OFC = −0.50 µV±0.66 µV s. Con ol =
0.18 µV±0.88 µV), wi h opog aphy showing p onounced
nega i i y in he OFC lesion g oup (Figu e 4). As his ime
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