Affective Priming by Eye Gaze Stimuli : Behavioral and Electrophysiological Evidence

ORIGINAL RESEARCH published: 07 Decembe 2016 doi: 10.3389/ nhum.2016.00619 A ec i e P iming by Eye Gaze S imuli: Beha io al and Elec ophysiological E idence Tingji Chen ,Mikko J. Pel ola ,Lo a J. Ran a and Ja i K. Hie anen * Human In o ma ion P ocessing Labo a o y, School o Social Sciences and Humani ies/Psychology, Uni e si y o Tampe e, Tampe e, Finland Edi ed by: A hu M. Jacobs, F ee Uni e si y o Be lin, Ge many Re iewed by: La s Kuchinke, In e na ional Psychoanaly ic Uni e si y Be lin, Ge many Benny Bjö n B iesemeis e , In e na ional Psychoanaly ic Uni e si y Be lin, Ge many *Co espondence: Ja i K. Hie anen [email p o ec ed] Recei ed: 23 Sep embe 2016 Accep ed: 21 No embe 2016 Published: 07 Decembe 2016 Ci a ion: Chen T, Pel ola MJ, Ran a LJ and Hie anen JK (2016) A ec i e P iming by Eye Gaze S imuli: Beha io al and Elec ophysiological E idence. F on . Hum. Neu osci. 10:619. doi: 10.3389/ nhum.2016.00619 The p esen s udy employed he a ec i e p iming pa adigm and measu emen s o e en - ela ed po en ials (ERPs) o in es iga e implici a ec i e eac ions elici ed by gaze s imuli. Pa icipan s ca ego ized posi i e and nega i e wo ds p imed by di ec gaze, a e ed gaze and closed eyes. The beha io al esponse ime (RT) esul s indica ed ha di ec gaze implici ly elici ed mo e posi i e a ec i e eac ions han did closed eyes. Analyses o he ERP esponses o he a ge wo ds e ealed a p iming e ec on he N170 and an in e ac ion on la e posi i e po en ial (LPP) esponses, and cong uen ly wi h he beha io al esul s, sugges ed ha , compa ed o closed eyes, di ec gaze was a ec i ely mo e cong uen wi h posi i e wo ds and mo e incong uen wi h nega i e wo ds. The p iming e ec on he N170 esponse indica ed ha gaze s imuli in luenced he subsequen a ec i e wo d p ocessing a an ea ly s age o in o ma ion p ocessing. In conclusion, he p esen beha io al and elec ophysiological e idence sugges s ha di ec gaze au oma ically ac i a es mo e posi i e a ec i e eac ions han closed eyes. Keywo ds: eye gaze, a ec i e p iming, e en - ela ed po en ial, sel - a ings, a ec i e e alua ion INTRODUCTION Gaze and eye con ac a e c ucial social signals, which p o ide in o ma ion abou indi iduals’ di ec ion o a en ion and in en ions. A gaze looking owa ds he pe cei e is likely o be in e p e ed as signaling a endency o app oach and in en ion o communica e, whe eas eyes looking away may signal a endency o a oid (A gyle and Cook, 1976). Eye gaze no only signals he sende ’s app oach-a oidance endencies, bu i also ac i a es co esponding mo i a ional endencies in he pe cei e s. Seeing ano he pe son’s di ec gaze, as compa ed o a e ed gaze o closed eyes, elici s g ea e ela i e le -side on al Elec oencephalog aphic (EEG) ac i i y, associa ed wi h app oach endency (Ha mon-Jones, 2003; Hie anen e al., 2008; Pönkänen e al., 2011b; Kylliäinen e al., 2012). S udies in es iga ing he skin conduc ance esponse (SCR), a measu e o physiological a ousal, ha e shown g ea e SCRs in esponse o di ec gaze as compa ed o a e ed gaze o closed eyes (Nichols and Champness, 1971; Hie anen e al., 2008; Helminen e al., 2011). These indings indica e ha eye gaze is a powe ul s imulus elici ing a ec i e-mo i a ional esponses in he pe cei e . In addi ion o elici ing physiological a ousal and mo i a ional esponses, eye gaze has also been shown o elici a ec i e esponses in he pe cei e . Howe e , s udies measu ing explici esponses, such as sel - a ed a ec i e alence, ha e indica ed somewha con adic ing indings o bo h nega i e and posi i e a ec i e esponses o ano he indi idual’s di ec gaze. F on ie s in Human Neu oscience | www. on ie sin.o g 1Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli Di ec gaze can signal dominance and agg ession, hus elici ing a e si e esponses in bo h animals and humans (Eme y, 2000; Skuse, 2003). Acco dingly, s udies in es iga ing sel - epo ed a ec i e esponses o eye gaze ha e e ealed ha , o emo ionally neu al aces, di ec gaze is e alua ed as less posi i e han a e ed gaze and closed eyes (Hess e al., 2007; Hie anen e al., 2008; Pönkänen e al., 2011a). On he o he hand, di ec gaze can be pe cei ed as a signal o posi i e communica i e in en ion (Kleinke, 1986). S udies in es iga ing sel - epo ed likabili y and a ac i eness o aces ha e shown ha pa icipan s e alua e aces wi h di ec gaze as mo e likable and a ac i e han aces wi h a e ed gaze (Mason e al., 2005; Kuzmano ic e al., 2009; Ewing e al., 2010). Some s udies using physiological measu emen s o indi ec beha io al measu emen s, sugges he e alua ion o di ec gaze in a mo e posi i e manne (Kampe e al., 2001; Lawson, 2015). Fo example, using he Implici Associa ion Tes , Lawson (2015) showed a obus p e e ence o aces looking owa ds he pe cei e , han looking away. Thus, i can be specula ed ha he na u e o a ec i e esponses o gaze di ec ion may depend on whe he explici o implici a ec i e eac ions a e measu ed. As compa ed wi h implici esponses, explici esponses a e mo e suscep ible o ask demands, mo i a ional biases, and o he op-down in luences (Ho mann e al., 2005). By con as , implici esponses, which do no ely on in ospec i e expe ience, may be less suscep ible o mo i a ional in luence, and may e lec pe cei e s’ ins inc ual esponse o a di ec gaze. In suppo o his specula ion, we ecen ly showed ha implici and explici measu es, indeed, esul ed in di e en ial a ec i e e alua ions (Chen e al., 2016). We used he a ec i e p iming pa adigm (Fazio e al., 1986) o in es iga e au oma ic (implici ) a ec i e esponses elici ed by eye gaze. In a ypical a ec i e p iming expe imen , pa icipan s a e equi ed o make speeded e alua ions o a ec i e a ge s p eceded by b ie ly p esen ed a ec i e p imes. Typically, he esponse la ency o a ge s is sho e o he a ec i ely cong uen p ime- a ge pai s compa ed o a ec i ely incong uen pai s (Fazio e al., 1986). This inding has been in e p e ed o indica e ha he p esen a ion o he p ime au oma ically elici s he associa ed a ec i e e alua ion and acili a es he decoding o a ec i ely cong uen a ge s (Fazio e al., 1986; Fazio, 2001). Since he seminal wo k by Fazio e al. (1986), he a ec i e p iming e ec has been epo ed in a la ge numbe o s udies and demons a ed o be a eplicable and obus phenomenon (Fazio, 2001; Klaue and Musch, 2003). In ou p e ious a ec i e p iming s udy, he gaze s imuli we e b ie ly p esen ed as p imes and immedia ely ollowed by posi i e and nega i e wo ds as a ge s. The pa icipan s e alua ed he alence o he wo ds as as as possible. Responses o posi i e wo ds we e as e a e di ec gaze han a e closed eyes, while esponses o nega i e wo ds we e as e a e closed eyes han a e di ec gaze. These esul s we e in e p e ed o indica e ha he pe cep ion o di ec gaze au oma ically ac i a es mo e posi i e e alua ions han closed eyes (Chen e al., 2016). Ins ead, he explici a ings showed ha di ec gaze was e alua ed as less posi i e han closed eyes. Howe e , wi h he beha io al esponse ime (RT) da a alone, i is impossible o know a which s age o p ocessing gaze p imes s a o exe hei in luence on a ge p ocessing. The high empo al esolu ion o e en - ela ed po en ials (ERPs), which p o ide a con inuous ime-window on neu al p ocesses du ing s imulus p esen a ion, may shed ligh on his ques ion. Impo an ly, p e ious s udies ha e demons a ed ha some ERP componen s a e modula ed by he a ec i e cong uence be ween a ge s and p eceding con ex s. In es iga ion o hese componen s may p o ide indica ions abou he a ec i e (in)cong uence be ween gaze s imuli and a ec i e wo ds on he neu al le el. In he p esen s udy, we employed he a ec i e p iming pa adigm (as in Chen e al., 2016) and eco ded ERPs in esponse o he a ge wo ds p eceded by eye gaze. P e ious s udies employing a simila me hodology ha e sugges ed ha P1 is he ea lies componen o be modula ed in a ec i e p iming s udies, wi h la ge P1 ampli udes in esponse o a ec i ely incong uen s. cong uen a ge s (Hie anen and As ikainen, 2013; Sianipa e al., 2015). The ollowing N170 componen , wi h ime window a ound 150–200 ms a e a ge onse (ea lie o ace and la e o wo d a ge s), has also been epo ed o be modula ed in a ec i e p iming s udies wi h wo ds (Comesaña e al., 2013) and aces (Hie anen and As ikainen, 2013; Hinojosa e al., 2015) as a ec i e a ge s. Fo example, Hie anen and As ikainen (2013) showed ha happy aces p eceded by pic u es o posi i e emo ional scenes elici ed la ge N170 ampli udes, whe eas he N170 ampli udes we e la ge o sad aces p eceded by nega i e scenes. The N170 componen e lec s ea ly isual p ocessing o aces, wo ds, and objec s (Rossion e al., 2000). In he con ex o a ec i e p iming, modula ion o he N170 esponse by a ec i e p imes may indica e inc eased ac i i y in isual p ocessing a eas when he a ec i e con en s o he p ime and a ge ma ch. A ew s udies ha e shown p iming e ec s on he ea ly pos e io nega i i y (EPN), wi h enhanced EPN ampli udes (i.e., mo e nega i e mean ac i i y a a ound 250–400 ms), in esponse o incong uen s. cong uen a ge s (Hie anen and As ikainen, 2013; Rampone e al., 2014). The midline N400 componen is sugges ed o e lec seman ic in eg a ion o wo ds wi h he p eceding con ex (Ku as and Hillya d, 1980) and i has been epo ed o be modula ed by he a ec i e cong uence be ween wo ds and he p eceding con ex (Zhang e al., 2006, 2010; Ede e al., 2011). Typically, g ea e N400 ampli udes a e obse ed o a ec i ely incong uen han o cong uen pai s. La e posi i e po en ial (LPP) modula ion by a ec i e cong uence has been epo ed in p iming s udies wi h wo ds (Zhang e al., 2010), aces (We heid e al., 2005; Hie anen and As ikainen, 2013), and scenes (He ing e al., 2011) as a ec i e a ge s. The esul s ha e e ealed g ea e LPP ampli udes a a ound 400–700 ms o a ec i ely incong uen han cong uen a ge s. EPN and LPP a e bo h sugges ed o e lec selec i e a en ion o emo ionally signi ican s imuli (Schupp e al., 2004). In he p esen s udy, we aimed o: (i) eplica e ou p e ious esul s o implici and explici a ec i e esponses o eye gaze; (ii) p o ide physiological e idence ela ed o a ec i e cong uence o gaze-wo d pai s by in es iga ing hose ERP componen s which ha e been demons a ed o be modula ed by he a ec i e cong uence be ween a ge s and p eceding p imes; F on ie s in Human Neu oscience | www. on ie sin.o g 2Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli and (iii) by measu ing ERP esponses, examine he ea lies s age o p ocessing a which gaze s imuli s a o exe hei in luence on he p ocessing o a ec i e wo ds. We expec ed o eplica e he beha io al esul s o ou p e ious s udy (Chen e al., 2016). Namely, in he a ec i e p iming ask, posi i e wo ds would be esponded o as e a e di ec gaze han a e closed eyes, while nega i e wo ds would be esponded o as e a e closed eyes han a e di ec gaze (i.e., posi i e wo ds being a ec i ely mo e cong uen wi h di ec gaze han closed eyes). In he sel - a ing ask, on he o he hand, di ec gaze would be e alua ed as less posi i e compa ed o closed eyes. Based on he p e ious ERP s udies (Zhang e al., 2010; He ing e al., 2011; Hie anen and As ikainen, 2013), we expec ed a ec i e p iming e ec s on he P1, N170, EPN, N400 and LPP componen s. To be speci ic, P1, EPN, N400 and LPP esponses o posi i e wo ds we e expec ed o be la ge when p eceded by closed eyes s. di ec gaze, whe eas hese esponses o nega i e wo ds would be la ge when p eceded by di ec gaze s. closed eyes. The N170 esponse o posi i e wo ds was expec ed o be g ea e when p eceded by di ec gaze s. closed eyes, whe eas N170 o nega i e wo ds would be g ea e when p eceded by closed eyes s. di ec gaze. MATERIALS AND METHODS Pa icipan s Thi y- wo na i e Finnish speake s (17 emales; 19–32 yea s, mean = 25 yea s), wi h no mal o co ec ed- o-no mal ision, pa icipa ed. Th ee pa icipan s we e excluded om he ERP da a analyses due o echnical e o s. All pa icipan s we e in o med abou he expe imen al p ocedu e, and a signed consen was ob ained om each pa icipan . The pa icipan s we e gi en a mo ie icke o hei pa icipa ion. The esea ch p o ocol was app o ed by he E hics Commi ee o he Tampe e egion. S imuli Simila o he s udy by Chen e al. (2016), he p imes we e g ayscale images showing a ec angula shaped a ea o he eye egion o anima ed aces. Fou male and ou emale aces wi h di ec gaze, a e ed gaze (20◦le / igh ), and closed eyes (Figu e 1A) we e c ea ed by using a 3D anima ion so wa e, Digi al A Zone [Daz] 3D S udio1. The size o he p imes was 2.0◦×6.9◦ e ically and ho izon ally, espec i ely. The a ge s we e 48 posi i e and 48 nega i e Finnish wo ds selec ed om he s udy by Söde holm e al. (2013) (Figu e 1B). Acco ding o he a ings made by 20–30-yea - old pa icipan s (Söde holm e al., 2013), posi i e and nega i e wo ds di e ed signi ican ly in alence a ings, (94)= 34.56, p<0.001 (Mposi i e = 5.62; Mnega i e = 2.55), bu no in a ousal (p= 0.579), wo d leng h (p= 0.691), o absolu e o ela i e su ace equency (bo h ps = 0.787). The a ge s we e displayed in Calib i on and he size o he wo ds p esen ed on he sc een was 1.5◦ e ically and 3.8◦–6.9◦ ho izon ally. 1h p://www.daz3d.com/ Design and P ocedu e The expe imen consis ed o a p iming ask and an explici a ing ask. The p iming ask had a 3 (gaze: di ec , a e ed, closed) ×2 (wo d alence: posi i e s. nega i e) design, including six blocks wi h 96 ials in each. Each o he 96 a ge s (48 posi i e and 48 nega i e wo ds) we e pai ed wice wi h a di ec gaze, a e ed gaze and closed eyes p ime ac oss he blocks. Thus, in o al, he expe imen con ained 96 ials o each p ime × a ge condi ion. Each expe imen al ial consis ed o he ollowing e en s in sequence (Figu e 1C): a ixa ion c oss (500 ms), a gaze p ime (100 ms), a blank sc een (200 ms), and a wo d a ge p esen ed un il he pa icipan ’s esponse. S imulus-onse -asynch ony (SOA) was 300 ms. The pa icipan s we e sea ed 70 cm away om he sc een and equi ed o classi y he a ge wo ds as posi i e o nega i e, as quickly and accu a ely as possible, by p essing he ‘‘+’’ o ‘‘−’’ key ( esponse key loca ion was coun e balanced ac oss pa icipan s). A e he esponse, he e was a 2000-ms in e al be o e he nex ial. Be ween he blocks, he e was a 1-min b eak. In he explici a ing ask, he gaze pic u es we e shown o he pa icipan s one by one. The pa icipan s we e equi ed o e alua e he a ec i e alence and a ousal o each gaze s imulus on he 9-poin Sel -Assessmen Manikin (SAM; B adley and Lang, 1994) scales (1 = unpleasan /calm, 9 = pleasan /a ousing). Each gaze s imulus was p esen ed on he sc een, i s oge he wi h he a ousal scale and hen wi h he alence scale. Each ace emained on he sc een un il he pa icipan esponded on bo h scales. Analyses o he Beha io al Da a Recogni ion accu acy and RTs we e calcula ed om he p iming ask. T ials wi h inco ec esponses o he wo d alence (5.54%) and ials wi h esponse la encies sho e han 2.5 s anda d de ia ions (SDs) below o abo e each pa icipan ’s mean (2.88%) we e excluded. Log10- ans o m was applied o co ec o non-no mal dis ibu ion. A 3 (gaze: di ec , a e ed, closed) ×2 (wo d alence: posi i e s. nega i e) epea ed measu es analysis o a iance (ANOVA) was pe o med on bo h ecogni ion accu acy and RT da a. Fo he a ing ask, one-way ANOVAs we e conduc ed o es di e ences in he alence and a ousal a ings o di ec gaze, a e ed gaze and closed eyes. All s a is ical analyses we e pe o med using he SPSS package. Huynh- Feld co ec ion was applied when app op ia e. Bon e oni co ec ion was pe o med o all mul iple compa isons. Fo he sake o cla i y, unco ec ed deg ees o eedom a e epo ed. EEG Reco ding and Analyses Elec oencephalog aphic (EEG) ac i i y was con inuously eco ded om 64 elec odes moun ed in an elec ode cap (ac iCAP), ampli ied wi h a QuickAmp ampli ie , and moni o ed wi h B ain Vision Reco de (B ain P oduc s GmbH, Munich, Ge many). The analog signal was ampli ied 26.55 imes and he sampling a e was se o 1000 Hz. Using a common a e age e e ence, he EEG signals we e e e enced F on ie s in Human Neu oscience | www. on ie sin.o g 3Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli FIGURE 1 | Examples o he p ime (A) and a ge (B) s imuli. The sequence o e en s on a single ial is illus a ed in (C). online o an a e age o all scalp elec odes. Addi ionally, e ical elec o-oculog am (VEOG) was eco ded wi h a pai o elec odes placed abo e and below he le eye. The FT9 elec ode was used o eco ding ho izon al elec o- oculog am (HEOG). Elec ode impedances we e educed unde 30 k. O line, he EEG signal was digi ally il e ed wi h a 0.5–30 Hz band-pass il e (24 dB/oc slope) and ocula -co ec ed using he G a on/Coles algo i hm (G a on e al., 1983). Then, he co ec ed signal was segmen ed in o 800-ms long epochs s a ing 100 ms p io o a ge onse . The mean ol age du ing he 100-ms p e- a ge pe iod was used o baseline co ec ion. Because we we e mainly in e es ed in ERPs a e he a ge , using p e- a ge baseline, ins ead o p e-p ime baseline, may be mo e app op ia e as he p e- a ge ERPs may be shi ed di e en ly by di e en gaze p imes (Hie anen and As ikainen, 2013). A i ac s we e de ec ed based on he ollowing c i e ia: ol age s ep o e 50 µV/ms, ampli ude exceeding ±100 µV, and ac i i y lowe han 0.5 µV. T ials con aining a i ac s (8.0%) we e ejec ed. A e age wa e o ms in each expe imen al condi ion we e calcula ed o each pa icipan . Selec ion o he elec ode si es and ime windows was based on isual inspec ion o he a e aged wa e o ms and he indings om p e ious s udies (Rossion e al., 2000; Kissle e al., 2009; Ede e al., 2011; Ci on, 2012; Hie anen and As ikainen, 2013). Fo example, acco ding o he p e ious li e a u e, N170 and EPN ha e an occipi o empo al scalp dis ibu ion (Rossion e al., 2000; Ci on, 2012), N400 is acqui ed om midline elec odes (Ede e al., 2011; Hie anen and As ikainen, 2013) and LPP peaks o e he pa ie al lobe (Kissle e al., 2009). The e o e, he peak ampli ude (an a e age o ampli udes wi hin ±5 ms o he de ec ed peak) and la ency o P1, N170 and he mean ampli ude o he EPN we e de e mined om occipi o empo al channels P7 and P8, wi hin a ime window 80–160 ms, 160–260 ms and 300–400 ms, espec i ely. The mean ampli ude o N400 was de e mined a midline elec odes Cz and CPz, wi hin he ime in e al o 250–400 ms. Mean LPP ampli ude was analyzed om channels CP1, CP2, P1, P2, CPz and Pz, wi hin a ime window o 400–700 ms. All ERP da a we e analyzed using epea ed measu es ANOVA wi h gaze and wo d alence as wi hin-subjec ac o s. RESULTS Beha io al Da a The ANOVA o he esponse accu acy da a showed a signi ican main e ec o wo d alence, F(1,31)= 26.41, p<0.001, η2 p= 0.460. Response accu acy o posi i e wo ds (98%) was signi ican ly highe han ha o nega i e wo ds (91%). Fo he RTs, he ANOVA showed a main e ec o wo d alence, F(1,31)= 46.84, p<0.001, η2 p= 0.602. Pa icipan s esponded as e o posi i e wo ds (M= 636 ms) han o nega i e wo ds (M= 695 ms). Impo an ly, he analyses showed he expec ed in e ac ion be ween eye gaze and wo d alence, F(2,62)= 5.36, p= 0.010, η2 p= 0.148. Fo posi i e wo ds, a one-way ANOVA showed a main e ec o gaze di ec ion, F(2,62)= 6.31, p= 0.003, η2 p= 0.169. Pai wise compa isons showed ha esponses o posi i e wo ds we e as e a e di ec gaze (M= 629 ms) han a e closed eyes (M= 646 ms, p= 0.002, Cohen’s d= 0.69). The RT o posi i e wo ds a e a e ed gaze (M= 634 ms) did no di e signi ican ly om he RTs o posi i e wo ds p eceded by di ec gaze (p= 0.330, d= 0.29) and closed eyes (p= 0.265, d= 0.33). No e ec o gaze F on ie s in Human Neu oscience | www. on ie sin.o g 4Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli FIGURE 2 | Means and s anda d e o s o esponse imes (RTs) o posi i e and nega i e a ge s p eceded by di ec gaze, a e ed gaze and closed eyes p imes (∗∗ p<0.01). di ec ion was ound on he RTs o nega i e wo ds (p= 0.401; Figu e 2). ERP Da a Figu e 3 shows he g and a e age ERP opog aphies o he P1, N170, EPN, N400 and LPP componen s wi hin he espec i e ime windows. P1 Fo he P1 ampli udes, he main e ec o gaze was signi ican , F(2,56)= 15.97, p<0.001, η2 p= 0.363. P1 ampli udes we e la ge a e closed eyes (2.58 µV) han di ec gaze (1.77 µV, p<0.001, d= 0.92) and a e ed gaze (1.97 µV, p<0.001, d= 0.90) p imes (Figu e 4). The e was no signi ican main e ec o wo d alence (p= 0.900) o an in e ac ion be ween gaze and wo d alence (p= 0.454). Fo P1 la ency, he analyses showed signi ican main e ec s o gaze, F(2,56)= 4.73, p= 0.013, η2 p= 0.144. Speci ically, he la ency o P1 was sho e a e a e ed gaze (118 ms) han closed eyes (122 ms, p = 0.017, d= 0.56) p imes. The P1 la ency a e di ec gaze (120 ms) did no di e om ha a e a e ed gaze o closed eyes (p = 0.197, d= 0.36; p = 0.854, d= 0.21, espec i ely). The in e ac ion be ween gaze and wo d alence on P1 la ency was no signi ican (p = 0.347). N170 The analyses o he N170 ampli udes e ealed a signi ican in e ac ion be ween gaze and wo d alence, F(2,56)= 3.89, p= 0.026, η2 p= 0.122 (Figu e 4). Sepa a e one-way ANOVAs we e conduc ed o in es iga e he e ec o gaze p imes on posi i e and nega i e wo ds. Fo he posi i e wo ds, a one-way ANOVA showed a main e ec o gaze, F(2,56)= 5.20, p= 0.008, η2 p= 0.157. Pai wise compa isons showed signi ican ly la ge N170 ampli udes in esponse o posi i e wo ds a e di ec gaze (−8.68 µV) han a e closed eyes p imes (−8.01 µV, p= 0.005, d= 0.66). The N170 ampli udes o posi i e wo ds p eceded by a e ed gaze did no di e om hose p eceded by di ec gaze FIGURE 3 | G and a e age e en - ela ed po en ial (ERP) opog aphies o he P1, N170, ea ly pos e io nega i i y (EPN), N400 and la e posi i e po en ial (LPP) componen s a he indica ed ime windows. F on ie s in Human Neu oscience | www. on ie sin.o g 5Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli FIGURE 4 | G and a e age ERPs o he P1, N170, EPN and LPP componen s o posi i e and nega i e wo ds p imed by di ec gaze, a e ed gaze and closed eyes a he de e mined elec ode si es (P7 and P8 o P1, N170 and EPN; CP1, CP2, P1, P2, CPz and Pz o LPP). The ol age maps show he ERP di e ence (di ec gaze minus closed eyes) o posi i e (le ) and nega i e ( igh ) wo ds in he LPP ime window. F on ie s in Human Neu oscience | www. on ie sin.o g 6Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli (p= 1.000, d= 0.06) o by closed eyes (p= 0.111, d= 0.43). Fo nega i e wo ds, he e was no e ec o gaze (p= 0.689). No signi ican e ec s we e ound in he analyses o N170 la ency. EPN The EPN analyses showed a main e ec o gaze p ime, F(2,56)= 8.89, p<0.001, η2 p= 0.241 (Figu e 4). O e all, he EPN ampli ude was la ge (i.e., mo e nega i e) a e a e ed gaze (−3.52 µV) han di ec gaze (−3.18 µV, p= 0.008, d= 0.64) and closed eyes (−2.98 µV, p<0.001, d= 0.73) p imes. No o he signi ican e ec s we e ound. N400 The analyses o he N400 mean ac i i y showed ha he main e ec s o gaze and wo d alence we e signi ican . O e all, he N400 ampli ude was smalle (i.e., mo e posi i e) a e a e ed gaze (2.24 µV) han closed eyes (1.78 µV, p= 0.017, d= 0.60), while he N400 ampli udes a e di ec gaze (2.13 µV) did no di e om hose a e a e ed gaze and closed eyes (p= 0.940, d= 0.18; p= 0.154, d= 0.39, espec i ely), F(2,56)= 5.31, p= 0.008, η2 p= 0.159. Finally, he N400 was smalle o posi i e (2.30 µV) han nega i e wo ds (1.80 µV), F(1,28)= 5.44, p= 0.027, η2 p= 0.163. LPP The analyses showed a ma ginal main e ec o wo d alence, F(1,28)= 4.01, p= 0.055, η2 p= 0.125. Posi i e wo ds (3.41 µV) elici ed a la ge LPP han did nega i e wo ds (3.07 µV). Impo an ly, he analyses showed a signi ican in e ac ion be ween gaze and wo d alence, F(2,56)= 3.30, p= 0.044, η2 p= 0.105 (see Figu e 4). Sepa a e one-way ANOVAs o bo h posi i e and nega i e wo d condi ions we e no signi ican (p= 0.296; p= 0.117, espec i ely). Howe e , as indica ed by he ERP wa e o ms in Figu e 4, he LPP ampli udes o nega i e wo ds p imed by di e en eye gaze condi ions seemed o di e . Thus, we pe o med pai ed - es s and he esul s sugges ed la ge LPP esponses o nega i e wo ds p eceded by di ec gaze (3.23 µV) s. closed eyes (2.83 µV, p= 0.033, d= 0.42). Explici Ra ings Fo he alence a ings, he analyses showed a ma ginal main e ec o gaze, F(2,62)= 3.09, p= 0.053, η2 p= 0.091. Closed eyes (M= 5.85) and a e ed gaze (M= 5.72) we e a ed sligh ly mo e posi i e han di ec gaze (M= 5.45), bu hese di e ences we e no signi ican (p= 0.086, d= 0.42; p= 0.204, d= 0.34, espec i ely). The e was a signi ican di e ence be ween gaze s imuli in a ousal a ings, F(2,62)= 7.22, p= 0.002, η2 p= 0.189. Di ec gaze (M= 3.94) was a ed mo e a ousing han a e ed gaze (M= 3.32, p= 0.002, d= 0.70) and closed eyes (M= 3.27, p= 0.021, d= 0.52; Figu e 5). DISCUSSION The p esen s udy employed a ec i e p iming and sel - a ing asks o in es iga e implici and explici a ec i e e alua ion o eye gaze. ERPs in esponse o he a ge wo ds we e eco ded FIGURE 5 | Means and s anda d e o s o he alence and a ousal a ings o he gaze s imuli (∗p<0.05; ∗∗ p<0.01). du ing he a ec i e p iming ask in o de o examine he ime cou se o he p iming e ec s. The esul s o he a ec i e p iming ask showed an in e ac ion be ween eye gaze and wo d alence in he beha io al RT da a, and e ealed a p iming e ec o posi i e wo ds, i.e., posi i e wo ds we e e alua ed as being posi i e as e a e di ec gaze han a e closed eyes. No p iming e ec was ound o he nega i e wo ds. The sel - a ing esul s showed ha di ec gaze was e alua ed as less posi i e han closed eyes. The ERP analyses showed a clea p iming e ec on he N170 esponse and an in e ac ion be ween eye gaze and wo d alence on he LPP esponse: a g ea e N170 ampli ude o posi i e wo ds a e di ec s. closed eyes, and a sligh ly g ea e LPP o nega i e wo ds a e di ec s. closed eyes. The beha io al esul s success ully eplica e hose o ou p e ious s udy (Chen e al., 2016), and indica e ha di ec gaze implici ly elici s mo e posi i e a ec i e eac ions han closed eyes, whe eas di ec gaze is explici ly e alua ed as less posi i e han closed eyes. Chen e al. (2016) sugges ed ha because humans ha e a undamen al need o belong, and a e mo i a ed o o m and main ain in e pe sonal ela ionships (Baumeis e and Lea y, 1995), di ec gaze, as a signal o indi iduals’ app oach endency and in en ion o social communica ion, ul ils hese needs and hus is au oma ically e alua ed as a posi i e signal. Howe e , when i comes o explici e alua ions, when indi iduals become awa e o o he people’s gaze and s a o e alua e hei co esponding eelings, hei esponses may become con olled and he ini ial and au oma ic esponses a e a enua ed and supp essed. They may espond o he gaze s imuli in a e lec i e and analy ic way, and may s a o analyze he eason o he eye con ac . Consequen ly, a di ec gaze may e oke a eeling o unce ain y and, he e o e, diminish posi i e eelings (Chen e al., 2016). Impo an ly, he ERP esul s showed an in e ac ion be ween eye gaze and wo d alence on he N170 and LPP esponses. Speci ically, a p iming e ec was ound o posi i e wo ds on he N170: esponses o posi i e wo ds we e g ea e when p eceded by di ec gaze as compa ed o closed eyes. P e ious esea ch has F on ie s in Human Neu oscience | www. on ie sin.o g 7Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli shown g ea e N170 esponses o a ge s p eceded by a ec i ely cong uen compa ed o incong uen p imes (Hie anen and As ikainen, 2013; Hinojosa e al., 2015). A plausible explana ion is ha he enhanced N170 in esponse o a ec i ely cong uen s. incong uen pai s may e lec he in eg a i e ac i a ion o a ec i e alence by he con ex s (p imes) and he a ge s imuli, and he e ec o his ac i a ion on isual p ocessing (Hie anen and As ikainen, 2013; Diéguez-Risco e al., 2015). Thus, he N170 modula ion indica es ha di ec gaze is a ec i ely mo e cong uen wi h posi i e wo ds han closed eyes. An in e ac ion be ween eye gaze and wo d alence was also ound on he LPP wi h sligh ly g ea e LPP o nega i e wo ds p eceded by di ec gaze as compa ed o closed eyes. P io s udies ha e epea edly epo ed ha he LPP is modula ed by a ec i e cong uence be ween he a ge s and p eceding con ex s, wi h a ec i ely incong uen a ge s elici ing la ge LPP ampli udes compa ed o a ec i ely cong uen a ge s (We heid e al., 2005; Zhang e al., 2010; He ing e al., 2011; Hie anen and As ikainen, 2013). An enhanced LPP in esponse o a ec i ely incong uen a ge s is in e p e ed as e lec ing inc eased a en ional esou ce alloca ion when he a ge s a e unexpec ed o do no a ec i ely ma ch he p eceding p imes (We heid e al., 2005; Zhang e al., 2010; Diéguez-Risco e al., 2015). Thus, he p esen LPP esul indica es ha di ec gaze is a ec i ely mo e incong uen wi h nega i e wo ds compa ed wi h closed eyes. I should be no ed, howe e , ha he one-way ANOVAs o bo h posi i e and nega i e wo d condi ions we e no signi ican . This implies ha he e ec s on he LPP we e no obus . Acco ding o he abo e in e p e a ion o social needs being ul illed by di ec gaze, one may aise a ques ion o why he e ec o a e ed gaze did no signi ican ly di e om di ec gaze in bo h implici a ec i e e alua ion and ERP measu es, as a e ed gaze signals a endency o a oidance. A possible explana ion o his esul migh be he use o s a ic gaze s imuli as p imes, a he han dynamic gaze shi s o gaze o eal pe sons. As compa ed wi h s a ic gaze, dynamic and eal gaze is mo e ealis ic and ecologically alid, and may lead o ela i ely s onge a ec i e esponses. S udies ha e shown ha dynamic s imuli, ela i e o s a ic s imuli, enhance neu al esponses and in ensi y judgmen s (Sa o e al., 2004; Weye s e al., 2006). A se ies o s udies by Hie anen e al. (2008) has demons a ed ha gaze s imuli p esen ed as pic u es o by a eal li e pe son elici di e en ial beha io al and physiological esponses (Pönkänen e al., 2011a,b). Fo example, Pönkänen e al. (2011a) epo ed g ea e N170 and EPN ampli udes o di ec s. a e ed gaze and closed eyes o he li e gaze s imuli, bu no o he gaze pic u es. Simila ly, a g ea e N170 o di ec s. a e ed gaze was epo ed in a s udy using dynamic gaze s imuli (Con y e al., 2007). Thus, we specula e ha he employmen o mo e ealis ic gaze s imuli may yield a clea e dis inc ion be ween di ec and a e ed gaze. In he p esen s udy, he p iming e ec on N170 ampli udes was obse ed only wi h posi i e a ge wo ds and he e ec on LPPs only wi h nega i e a ge wo ds. I is no ewo hy ha he p iming e ec s shown on b ain po en ials a e no always epo ed o bo h posi i e and nega i e a ge s. Fo example, Zhang e al. (2010) epo ed p iming e ec s on LPP only o posi i e wo ds; speci ically, LPP o posi i e wo ds was la ge p eceded by nega i e s. posi i e pic u es. They specula ed ha his was due o nega i e pic u es gene ally elici ing s onge emo ional eac ions han posi i e pic u es. This explana ion can also be applied o he p esen esul s. As compa ed wi h closed eyes, he p esen as well as p e ious s udies show ha di ec gaze is usually e alua ed as emo ionally mo e a ousing and ac i a ing s onge au onomic esponses (Helminen e al., 2011; Pönkänen e al., 2011a; Chen e al., 2016). As a esul , di ec gaze p imes may lead o ela i ely s onge p iming e ec s han closed eyes p imes. Thus, o he N170 esponse, posi i e wo ds p esen ed in he con ex o di ec gaze may elici a s onge addi i e e ec o in eg a i e ac i a ion as compa ed wi h nega i e wo ds p esen ed in he con ex o closed eyes. Wi h espec o he LPP, nega i e wo ds p esen ed in he con ex o di ec gaze may elici a s onge incong uency e ec as compa ed wi h posi i e wo ds p esen ed in he con ex o closed eyes. I should be no ed, howe e , ha he obse ed in e ac ions be ween he gaze s imuli and he posi i e and nega i e wo ds canno be explained by he di e en ial a ousal o di ec gaze and closed eyes alone. We me ely sugges ha he au oma ic a ec i e e alua ions and he ollowing a ec i e p iming e ec s may also depend on he a ec i e a ousal elici ed by he p imes. Fo he beha io al esul s, we obse ed he p iming e ec wi h posi i e wo ds bu no wi h nega i e wo ds. We ha e no ob ious explana ion o his inding. I should be no ed ha , in ou p e ious s udy (Chen e al., 2016), he beha io al p iming e ec s we e obse ed o bo h posi i e and nega i e wo ds. The p esen s udy had a simila expe imen al design as he p e ious s udy, wi h he excep ions ha he p esen s udy included mo e a ge wo ds and ials, only one p ime— a ge SOA (ins ead o wo), and he p imes we e sup aliminally p esen ed (wi hou an addi ional subliminal condi ion). Ne e heless, we belie e ha his sligh di e ence in he esul s shall no e u e ou conclusion. The ERP analyses showed ha he p iming e ec s began o be e lec ed on b ain ac i a ion as ea ly as a he le el o he N170 componen . P io s udies in es iga ing language comp ehension ha e indica ed ha he in luence o con ex ual in o ma ion on lexical p ocessing occu s app oxima ely wi hin he ini ial 200 ms ollowing s imulus onse (Se eno e al., 2003). The p esen esea ch acco ds wi h and ex ends he ea lie indings by demons a ing ha a gaze s imulus se ing as an a ec i e con ex also exe s an in luence on a ec i e wo d p ocessing a an ea ly s age o neu al p ocessing. The p esen s udy showed ha he P1, EPN and N400 componen s we e no modula ed by he a ec i e cong uence be ween p imes and a ge s. A ew p io a ec i e p iming s udies ha e epo ed p iming e ec s on he P1 and EPN (Hie anen and As ikainen, 2013; Rampone e al., 2014; Sianipa e al., 2015). The easons o he disc epan indings may be ela ed o di e ences in he me hods be ween he s udies. Fo example, he a ge s imuli used by Hie anen and As ikainen (2013) we e acial exp ession pic u es, whe eas isually p esen ed wo ds we e used in he p esen s udy. As F on ie s in Human Neu oscience | www. on ie sin.o g 8Decembe 2016 | Volume 10 | A icle 619 Chen e al. A ec i e P iming by Eye Gaze S imuli compa ed wi h a ec i e aces, he a ec i e meaning o wo ds is on ogene ically lea ned and symbolic and, he e o e, he p ocessing o a ec i e in o ma ion om wo ds and aces may be di e en (Schach and Somme , 2009). Se e al a ec i e p iming s udies wi h wo ds as a ge s ha e epo ed a la ge N400 in esponse o a ec i ely incong uen a ge s (Zhang e al., 2006, 2010; Ede e al., 2011). Howe e , some s udies ha e no obse ed an N400 modula ion (He ing e al., 2011; Kissle and Koessle , 2011), o ha e e en epo ed e e sed a ec i e p iming e ec s (Aguado e al., 2013; Hie anen and As ikainen, 2013). He ing e al. (2011) conduc ed h ee a ec i e p iming expe imen s wi h ei he a ec i e pic u e o wo d pai s and epo ed a p iming e ec on he LPP, bu no on he N400. They a gued ha hese esul s may sugges a dissocia ion in he p ocesses o seman ic and a ec i e p iming: he LPP is modula ed by a ec i e misma ch, whe eas he N400 may la gely depend on he seman ic connec edness be ween he p imes and a ge s. A limi a ion ha should be add essed in u u e esea ch is ela ed o isual low-le el di e ences be ween di e en gaze s imuli. Fo example, di ec gaze has a highe scle a-i is con as han closed eyes, and is geome ically mo e symme ic han a e ed gaze. One may specula e ha he e ec s epo ed in ou s udies we e d i en by low-le el ea u es o he eyes when p esen ed b ie ly, a he han by social e alua ion as we sugges ed. To examine his, u u e s udies could include ace s imuli wi h on al and o a ed head o ien a ions, and app op ia e con ol s imuli, such as sc ambled aces wi h di ec gaze, a e ed gaze and closed eyes. CONCLUSION Co esponding o ou hypo heses, he p esen s udy ound ha he beha io al da a success ully eplica ed p e ious indings (Chen e al., 2016), indica ing ha di ec gaze is implici ly e alua ed as mo e posi i e han closed eyes, whe eas i is e alua ed as less posi i e in explici e alua ions. The ERP analyses showed a p iming e ec on he N170 and an in e ac ion on LPP esponses: a la ge N170 o posi i e wo ds a e di ec s. closed eyes and a sligh ly la ge LPP o nega i e wo ds a e di ec s. closed eyes. These esul s indica e ha di ec gaze, as compa ed wi h closed eyes, is pe cei ed as mo e a ec i ely cong uen wi h posi i e wo ds, and as mo e a ec i ely incong uen wi h nega i e wo ds. The obse ed p iming e ec on he N170 also indica es ha gaze s imuli in luence he subsequen a ec i e wo d p ocessing a an ea ly s age o in o ma ion p ocessing. AUTHOR CONTRIBUTIONS All he ou au ho s we e in ol ed in he expe imen al design, da a collec ion and analysis. 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Looking a you o looking elsewhe e: he in luence o head o ien a ion on he signal alue o emo ional acial exp essions. Mo i . Emo . 31, 137–144. doi: 10.1007/s11031-007- 9057-x Hie anen, J. K., and As ikainen, P. (2013). N170 esponse o acial exp essions is modula ed by he a ec i e cong uency be ween he emo ional exp ession and F on ie s in Human Neu oscience | www. on ie sin.o g 9Decembe 2016 | Volume 10 | A icle 619