B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

ava i l ab l e a t www.sc i enced i rec t . com

www.e l sev i e r. com/ l oca te /b ra in res

Research Report

Explicit versus implicit gaze processing assessed by ERPs

Roxane J. Itiera,⁎, Claude Alaina,b, Natasa Kovacevica, Anthony R. McIntosha,b

aThe Rotman Research Institute, Baycrest Centre for Geriatric Care, 3560 Bathurst Street, Toronto, Ontario, Canada M6A 2E1bDepartment of Psychology, University of Toronto, Ontario, Canada

A R T I C L E I N F O

⁎ Corresponding author. Fax: +1 416 785 2862.E-mail address: ritier@rotman-baycrest.on

0006-8993/$ – see front matter © 2007 Elsevidoi:10.1016/j.brainres.2007.07.094

A B S T R A C T

Article history:Accepted 11 July 2007Available online 31 August 2007

Gaze processing was investigated using event-related potentials in two different tasks inwhich front-view and 3/4-view faces were presented, with eyes gazing straight ahead oraverted. Task alternated between an explicit gaze direction judgment and a judgment onhead orientation where gaze was irrelevant. Accuracy and reaction times were affected bythe congruency of gaze and head directions in both tasks suggesting gaze was processedimplicitly in the head orientation task. In both tasks, larger P1 and N170 were found for 3/4-view faces compared to front-view faces that were not due to the luminance or contrast ofthe pictures. The N170 was also larger for averted than straight gaze but for front-view facesonly. In contrast, larger amplitudes for straight than averted gaze were reliably measuredaround 400–600 ms regardless of head orientation or task demands, and likely reflected theoutcome of gaze processing. The results suggest that head orientation and gaze directiondiscrimination occur regardless of task demands and interact at the decision making level.Neural markers of head orientation occur before those for gaze direction and the earlystructural encoding stages of face processing are view-dependant.

© 2007 Elsevier B.V. All rights reserved.

Keywords:GazeHead orientationEyesFaceSocial attention

1. Introduction

Gaze processing bears a fundamental role in human socialcognition. Direct (straight) gaze seems to be a particularlyimportant stimulus and the eye-to-eye gaze is a threat signalfor most primates (Emery, 2000). Even human neonates andinfants can discriminate between averted and direct gaze inadult faces (Farroni et al., 2002; Hains and Muir, 1996) andprefer direct gaze faces because they engage in social contact(Farroni et al., in press; Hains and Muir, 1996; Hood et al., 1998;Maurer, 1985). Behavioral studies have shown that direct gazeinfluences the speedof face processing in various tasks suchasgenderdiscrimination or identity recognition (Hoodet al., 2003;Macrae et al., 2002; Senju and Hasegawa, 2005; Vuilleumieret al., 2005), although this depends on the orientation of theface (Itier et al., 2007; Langton, 2000).

.ca (R.J. Itier).

er B.V. All rights reserved

While many neuroimaging studies have focused on theneural basis of gaze processing, with the superior temporalsulcus region (STS) as a core area (Allison et al., 2000; Haxbyet al., 2000; Puce et al., 1998), fewer studies have investigatedthe temporal aspect of gaze discrimination. Scalp electro-physiological studies of gaze processing have mainly focusedon the N170, a face-sensitive event-related potential (ERP)component (Bentin et al., 1996; George et al., 1996; Itier andTaylor, 2004a) which is also sensitive to eyes presented inisolation (Bentin et al., 1996; Itier et al., 2006; Jemel et al., 1999;Taylor et al., 2001a; Taylor et al., 2001c). A larger and earlierN170 has been reported for gazemovements going away from,rather than back to the observer (Puce et al., 2000), suggestingthe N170 is sensitive to the apparent motion of eyes. Theamplitude and source location of the M170, a face-sensitivecomponent recorded in magnetoencephalography (MEG)

.

80 B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

around the same time as the N170 (Halgren et al., 2000; Luet al., 1991; Sams et al., 1997), are also influenced by apparentgaze motion (Watanabe et al., 2001) with eye movementsdirected at the viewer eliciting the largest effects (Watanabeet al., 2006).

While gazemotion clearly influences early face processing,the picture is less clear for static stimuli with most studies inadults reporting no gaze effects on the N170 (Grice et al., 2005;Klucharev and Sams, 2004; Schweinberger et al., 2007; Tayloret al., 2001c). As far as we know, only one study reported largerN170 amplitudes for averted than direct gaze which wasrestricted to the right hemisphere, with no latency differences(Watanabe et al., 2002). When isolated eyes rather than fullfaces were used, longer N170s for eyes-closed compared toboth averted and direct gaze conditions were found, but nodifferences were found between averted and direct gaze, andno amplitude effects were reported (Taylor et al., 2001c). Incontrast, the M170 component showed a significantly shorterlatency for averted than direct gaze but only for isolated eyesand again no amplitude modulations (Taylor et al., 2001b).

Altogether, the inconsistency of these results precludes anyfirmconclusionas towhether gaze canbeprocessed early on inthe visual pathway (∼170 ms) for static stimuli, or later on,given the absence of later ERP analyses. Only one recent studysuggested that gaze direction could be processed around 250–300 ms (Schweinberger et al., 2007). Furthermore, behavioralstudies have shown that face orientation can modulategaze perception (Emery, 2000; Hietanen, 1999; Langton, 2000;Langton et al., 2000) but the timing of this influence is un-known as all previous studies used front-view faces only.Finally, as previous gaze studies used semi-passive or totallypassive tasks (e.g. Puce et al., 2000; Taylor et al., 2001c;Watanabe et al., 2002), the possible influence of directedattention onto the eye region for discriminating gaze is un-known. In the present ERP study, we testedwhether the neuralcorrelates of gaze processingwere influenced by task demandsand byhead orientation. Our goalwas to clarify the gaze effectson the N170 and to explore possible later effects. Subjectsperformed an explicit gaze discrimination task (Gaze task) anda head orientation task in which gaze was irrelevant (Headtask). Faceswere presented in 3/4-viewor front-viewwith gazedirected at the viewer or away. Head and gazewere oriented tothe right or to the left side (see Experimental procedures for afull description).

2. Results

2.1. Behavioral data

For behavioral analyses, left and right sides were collapsed,yielding four main conditions: head-turned-gaze-averted,head-turned-gaze-straight, head-front-gaze-averted, head-front-gaze-straight. Hits and response times (RTs) wereanalyzed using a 2 (tasks: Gaze or Head) × 2 (gaze direction:averted or straight) × 2 (head orientation: front-view or 3/4-view) ANOVA.

Overall performances were comparable between the twotasks (91.8% hits for the Gaze task, 92.3% for the Head task). Amain effect of Head orientation was found (F(1,15)=9.4, p<.01)

due to slightly better accuracy for front-view than 3/4-viewfaces. No effect of gaze was found but a head×gaze interaction(F(1,15)=27.18, p< .0001) was due to better accuracy forcongruent conditions, i.e. when head orientation and gazedirection matched (Fig. 1). No interaction with task was found.Faster RTs were found in the Head compared to the Gaze task(main effect of task, F(1,15)=17.07, p<.001). Front-view andgaze-straight conditions elicited faster RTs than 3/4-view andgaze-averted conditions, respectively (effect of head orienta-tion, F(1,15)=98.7, p<.0001 and gaze direction, F(1,15)=42.43,p< .0001). The head× gaze interaction (F(1,15) = 106.25,p<.0001) was caused by faster RTs for congruent conditions(Fig. 1). The task×head×gaze was also significant (F(1,15)=4.6,p<.05). For front view faces, t-tests confirmed faster RTs forstraight than averted gaze in both the Head task (t(15)=11.19,p<.0001) and the Gaze task (t(15)=9.62, p<.0001). In contrast,for 3/4-view faces, RTs were faster for averted than straightgaze in the Head task (t(15)=−3.82, p<.005) but not in the Gazetask for which no difference was found (p=.09).

Thus, for both tasks, congruent conditions elicited betteraccuracy and faster RTs than incongruent conditions, with thehead-front-gaze-straight condition eliciting the best accuracyand the fastest RTs.

2.2. Electrophysiological data

2.2.1. The N170 componentLatency and amplitude measures were analyzed separatelyusing a 2 (task: Gaze or Head)×2 (gaze direction: straight oraverted)×2 (head orientation: front-view or 3/4-view)×2(side)×2 (electrodes: parietal or cerebellar)×2 (hemisphere)ANOVA.

In the latency analysis, the N170 was slightly delayed for 3/4-view than front-view faces (effect of head, F(1,15)=18.07,p<.001) as well as for averted compared to straight gaze(effect of gaze, F(1,15)=7.11, p< .05). No effect of task wasfound. For N170 amplitude, main effects of head orientation (F(1,15)=12.56, p<.005) and electrode (F(1,15)=8.08, p<.05) werefound. This was due to larger amplitudes for 3/4-view thanfront-view heads and for cerebellar (CB) sites compared toparietal sites. A head by gaze interaction (F(1,15)=5.2, p<.05)was also found due to larger amplitudes for averted thanstraight gaze only when faces were in front-view (Fig. 2). Thiswas confirmed by follow-up analyses showing no effect ofgaze for 3/4-view faces (F(1,15)<1) but a main effect of gazefor front-view faces (F(1,15)=10.31, p<.01). Although theinteraction with hemisphere was not significant, the gazeeffect in the Head front conditions seemed larger on the leftthan on the right hemisphere. No effect of task was found.

Thus, the N170 was not affected by task demands, whetherthe attention was explicitly focused on the gaze direction(Gaze task) or on the head orientation (Head task). The N170was influenced by head orientation, with slightly longer andlarger N170s for 3/4-view than front-view faces. The effect ofgaze was significant, although it was very small in the actualmean values (Table 1) and present only for front-view faces.

Beside the classic peak analysis of the N170, we alsoanalyzed the data with Partial Least Square (PLS) analysis(see method for details). PLS allows for the analysis of thewhole epoch across all electrodes rather than focusing on a

Fig. 1 – Percent hits and mean reaction times (RTs) in the Gaze and Head tasks as a function of head orientation and gazedirection (vertical bars=standard errors).

81B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

few electrodes for a particular peak. A first global analysisincluding all 16 conditions (8 conditions×2 tasks) was run.As seen in Fig. 3, the significant latent variables (LV)obtained expressed complex interaction patterns betweentasks, gaze, head and side factors that justified the breakingdown into smaller and more defined analyses. We focusedon gaze and head orientation contrasts and their interac-tions with task.

2.2.2. Gaze direction contrastThe interaction contrast between gaze and tasks was notsignificant (p=.53). The gaze contrast was thus run across both

Fig. 2 – The N170 component (group mean) shown here at P7/8 sites as a function of head orientation and gaze direction(collapsed across both tasks). A slightly larger N170 for averted than straight gaze was found for front-view faces only (arrows)

tasks, comparing averted and straight gaze conditions. Thegaze direction contrast was significant (p=.016) (Fig. 4) andwas expressed maximally at centro-parietal and parietal sitesbetween 400 and 600 ms post-stimulus onset. Inspection ofgrand averages revealed significantly larger amplitudes forstraight than averted gaze between 420 and 580 ms at thesesites (bootstrap zN2.6), with the opposite effect at frontal andfronto-temporal electrodes.

2.2.3. Head orientation contrastThe interaction contrast between head orientation and taskwas significant (p<.05). The effect was mainly seen at centro-

.

Table 1 – Mean latencies and amplitudes of the N170across tasks and electrodes (standard errors inparenthesis)

3/4-viewheads

Front viewheads

N170 meanlatencies (ms)

Gaze averted 183.8 (2.8) 182.2 (3)Gaze straight 183 (2.9) 182.2 (2.9)

N170 meanamplitudes (μV)

Gaze averted −7.44 (0.89) −7.23 (0.83)Gaze straight −7.62 (0.86) −6.65 (0.86)

Fig. 3 – Design saliences of the first three Latent variables (LV)obtained from the first PLS analysis including all 16conditions. LV1, LV2, and LV3 were all significant but

82 B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

parietal and parieto-occipital sites from 200 to 800 ms (stableby bootstrap from 300–600 ms at Pz and POz) and reflectedlarger amplitudes for 3/4-view than front-view faces in theHead task while smaller or no differencewas seen for the Gazetask (Fig. 5).

The head orientation contrast was also run across bothtasks to detect the commonalities between the two tasks. Thecontrast was significant (p<.0001) and was expressed mainlyat bilateral occipital sites, between 100 and 180 ms, reaching amaximum around 136 ms at Oz electrode (Fig. 6). This effectencompassed the P1 which was larger for 3/4-view than front-view faces. The effect was also expressed between 180 and295 ms at lateral sites (P7/8, CB1/2), encompassing the N170and the P2, with amore negative N170 and a smaller P2 for 3/4-view than front-view faces. The effect was largest on the righthemisphere (Fig. 6). This head orientation effect on the N170confirms what was found in the peak analysis. These earlyeffectswere also seenwhen the two taskswere run separately.

As the early effects of head orientation on the P1 could bedue to low level visual effects, we measured the meanluminance and RMS (root mean square) contrast of eachpicture. An independent t-test was used to compare the meanluminance and RMS contrast of 3/4-view and front-view facepictures. There was no significant difference between the twogroups of pictures for the mean luminance (t(91.9)=1.25,p=.3)1 or the RMS contrast (t(94)=1.04, p=.3). Thus, theseearly head orientation effects on P1 were not due to adifference in contrast or luminance between front-view and3/4-view faces.

In summary, head orientation affected early componentssimilarly for both tasks but task differences were seen on laterlong-lasting amplitudes, with amplitude differences between3/4-view and front-view faces being more pronounced for theHead task where the focus was on head orientation.

2.2.4. Gaze and head interaction contrastAlthough the Gaze direction and the Head orientationcontrasts yielded different effects, we tested their possibleoverlapping modulations by running an interaction contrastfor each task separately. For both tasks, the interactioncontrast was significant (p< .0001) but the effects weremainly seen after 600 ms, overlapping with motor-relatedERPs, paralleling the gaze by head interactions seen on RTs.When the same tests were run from 0 to 600 ms, theinteractions were no longer significant, suggesting that the

1 The degree of freedom has been adjusted for the luminancet-test as the variances were not equal (Levenes's test for equalityof variances).

above results of gaze and head processing were independentof each other.

3. Discussion

This paper investigated gaze processing and its interactionwith head orientation when attention was directed explicitlyto the gaze direction (Gaze task) or to the head orientation(Head task) of face stimuli. In both tasks congruent conditions(gaze and head in the same direction) elicited better accuracyand faster RTs than incongruent conditions with the head-front-gaze-straight condition eliciting the best accuracy andthe fastest RTs. These data replicate previous findings (Itieret al., 2007; Langton, 2000) and suggest that gaze wasprocessed implicitly in the head orientation judgment task,even though gaze was irrelevant.

expressed complex interaction patterns between tasks, headorientation, gaze direction, and side, justifying subsequentPLS analyses on more defined contrasts. GA: Gaze averted;GS: Gaze straight; HA: head averted (3/4-view); HF: head front;l: left side; r: right side.

Fig. 4 – Results of the gaze contrast tested with PLS across both tasks, shown here at Pz electrode. The difference betweenstraight and averted gaze was expressed at centro-parietal and parietal sites as seen on the topography of the ERP saliences,with the maximum reached around 500 ms at Pz electrode (salience peak). The green line represents the time period at whichthe contrast was stable by bootstrap test (zNNNN2.6, ~p<.01). At these timepoints and electrode locations, amplitudes werelarger for straight than averted gaze. The vertical dotted lines show the correspondence between the maximum ERP salienceand the expression of the contrast on ERPs.

83B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

The interaction between gaze and head orientation regard-less of task demands was also seen on the face sensitive N170component that was larger for averted than direct gaze onlywhen heads were in front-view. Previous ERP studies of theN170 have failed to find gaze effects for static stimuli (Grice etal., 2005; Klucharev and Sams, 2004; Schweinberger et al., 2007;Taylor et al., 2001c) except for one study (Watanabe et al., 2002)that reported a larger amplitude for averted than straight gazein the right hemisphere. Here we show that this amplitudemodulation is restricted to faces presented in front views.Faces turned by 30° to the right or to the left did not presentdifferences as a function of gaze direction. However, as thisamplitude difference was very small and given that the PLSinteraction contrast between face orientation and gazedirection was not significant before 600 ms, caution isrequired. Further investigation is needed to confirm such asmall effect of gaze on early ERP components.

Head orientation in contrast had clear effects on early ERPcomponents. This was seen in both tasks starting around 100ms on the P1 componentwhichwas larger and delayed for 3/4-view compared to front-view faces. Importantly this effect was

not due to luminance or contrast low level effects that did notdiffer between the front-view and 3/4-view faces. Largeramplitudes and delayed latencies for 3/4-view faces werealso seen on the N170 in both the PLS and the peak analysis,reinforcing the fact that this represents a reliable finding,obtained with two different analysis techniques, unlike whatwas seen for gaze direction. Finally, head orientation alsoinfluenced the P2 component, with smaller amplitudes seenfor 3/4-view faces.

The N170 is thought to reflect late structural encodingstages of faces, where representations of global configurationsare generated (Bentin et al., 1996; Carmel and Bentin, 2002;Eimer, 2000; George et al., 1996; Itier and Taylor, 2002; Rossionet al., 1999). Sensitivity to faces has also been reported for P1(Halit et al., 2000; Itier and Taylor, 2002, 2004b, 2004a;Linkenkaer-Hansen et al., 1998; Taylor et al., 2001a), althoughless consistently. Fewer studies have examined the P2 but it issensitive to some face manipulations (Itier and Taylor, 2002)and has been suggested to index stages of face recognition(Halit et al., 2000). P2 is also correlated with later long lastingamplitudes (George et al., 2005) that are implicated in

Fig. 5 – ERP saliences shown here at Pz and POz electrodes obtained in the head orientation×task interaction contrast. Thegrand averaged ERPs suggest that the difference between 3/4-view and front-view heads is larger in the Head task (headorientation judgment, implicit task) than in the Gaze task (gaze direction judgment, explicit task). The green line represents thetime period at which the contrast was stable by bootstrap test (zNNNN2.6, ~p<.01).

84 B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

familiarity and recognition stages (Itier and Taylor, 2004b;Schweinberger et al., 1995; Schweinberger et al., 2004;Schweinberger et al., 2002; Tanaka et al., 2006). Together,these studies suggest that global face detection starts as earlyas the P1 while the N170 reflects more refined encodingprocesses where the perceptual representation of a face isbeing created, and the P2 possibly reflects early face recogni-tion stages. The present data support this view and suggest aview-dependant representation of both early and late faceencoding stages, regardless of task demands.

This early sensitivity to head orientation fits well withmonkey cell recordings showing that themajority (60%) of faceselective cells found in the monkey STS are view selective(Perrett et al., 1991). Some cells respond more to front views,others to profiles (Desimone et al., 1984; Perrett et al., 1985)and most cells sensitive to head views are also sensitive togaze direction (Perrett et al., 1985). This double sensitivity tohead orientation and gaze direction allows the cells to respondeven when one cue (e.g. gaze direction) is not available.Especially, head orientation is thought of as the “default cue”to process direction of others’ attention when the direction ofgaze is not available (Emery, 2000; Perrett et al., 1992). Thepresent data suggest that head orientation begins to beprocessed before gaze direction, as early as 100 ms.

In contrast to this early head orientation processing, areliable gaze direction effect was only seen between 420 and580 ms, with larger amplitudes for direct than averted gazeconditions seen regardless of head orientation. It has to beemphasized that the absence of strong earlier gaze effects

does not mean that gaze was not processed before 400 ms. Infact, at that late latency, the signal likely represents thecognitive outcome of gaze processing rather than gazeprocessing itself which very likely occurred earlier. A recentstudy reported no gaze effect on the N170 but a reliabledifference between left and right averted gaze (front-viewfaces) between 250 and 300 ms using an adaptation paradigm(Schweinberger et al., 2007). In contrast, later ERPs (300–600 ms) are affected by the social context of gaze (Carricket al., 2007) or the judgment of the mental state based on theeyes (Sabbagh et al., 2004). Thus gaze is likely processed earlierthan 400ms but the differencemay be too small to be recordedreliably on the scalp in our study. Again, although significant,the gaze effect found on theN170 for front-view faces onlywasreally small and needs to be replicated before we can concludethat gaze processing really occurs at that latency.

The processing of gaze, possibly occurring after the N170,could be seen as contrasting with the widespread view thatgaze cues elicit a fast and reflexive shift of spatial attention, asshown behaviorally (Driver et al., 1999; Friesen and Kingstone,1998; Friesen et al., 2005; Hietanen, 1999; Langton and Bruce,1999; Mansfield et al., 2003; Ricciardelli et al., 2002; Vuilleu-mier, 2002). These studies have shown that when an irrelevantdistractor face is presented centrally at fixation, responses to aperipheral target are faster when the gaze of the face isdirected toward the target location compared to when it isdirected toward the location opposite that of the target. Theidea here is that to be able to orient to a target in the periphery,one needs first to process the gaze cue. Gaze is thus believed to

Fig. 6 – Results of the head orientation contrast tested with PLS across both tasks. The difference between 3/4-view andfront-view faces is shown at Oz and CB2 where it was expressed maximally, encompassing the P1-N170-P2 complex.Topographies of the ERP saliences show that the effect was bilateral for the P1 but mostly right lateralized for the N170 and P2components. The green line represents the time period at which the contrast was stable by bootstrap test (zNNNN2.6, ~p<.01).The vertical dotted lines show the correspondence between the maximum ERP salience and the expression of the contrast onERPs.

85B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

be processed reflexively. The idea of a reflexive processing isdifficult to address with ERPs as there is no consensus on thedefinition: does a reflexive mechanism mean an effect onearly ERP components (P1, N170) or later on? This is all themore problematic since all these studies used reaction timesto assess their “reflexive” effect. Moreover, this effect oforienting to gaze cue is seen only with front-view faces andseems to be tight to the cueing paradigm itself, questioningthe pure reflexive nature of gaze processing which should beseen regardless of stimuli, paradigm and task demands. Nocueing effect was found when 3/4-view faces were used(Hietanen, 1999) which suggests an important influence ofhead orientation on gaze processing, as shown here andelsewhere (Emery, 2000; Hietanen, 1999; Langton, 2000;Langton et al., 2000).

Using the same tasks as the present ones in an eyemovement study, we recently showed that orienting to gaze,as reflected by the direction of the first saccade recorded afterstimulus onset, was found only in the Gaze task (Itier et al.,2007). In the Head task, eye movements were directed mostlyin the direction signaled by the head. This kind of taskmodulation was found for all the eye movements recorded,suggesting gaze orienting was not purely reflexive andexogenous but rather modulated by task demands. Thus, thereflexive nature of gaze processing seems apparent only whenusing a gaze cueing paradigm and front-view faces. Gaze may

thus not be processed reflexively, a notion in agreement withthe present ERP results.

However, although not necessarily reflexive, gaze proces-sing seems to occur implicitly evenwhen it is irrelevant for thetask such as in our Head task that required a head orientationjudgment. This could be the consequence of a strongattraction to the eye region which is seen in any face task(Althoff and Cohen, 1999; Henderson et al., 2005; Itier et al.,2007; Walker-Smith et al., 1977; Yarbus, 1967). Interestingly,amplitudes were larger for direct than averted gaze for bothtasks and could reflect a special role for straight gaze. Directgaze has been shown to influence many cognitive and brainprocesses. Faces with straight gaze are encoded and recog-nized better than faces with deviated gaze and this is seen inadults, children and even infants (Farroni et al., in press; Hoodet al., 2003; Vuilleumier et al., 2005). Infants prefer direct gazefaces because they engage in social contact (Farroni et al., inpress; Hains and Muir, 1996; Hood et al., 1998; Maurer, 1985)whereas clinical populations such as autistic and AspergerSyndrome subjects, as well as schizophrenics, avoid directgaze and fixate less on the eyes than control subjects(Andreasen, 1982; Dalton et al., 2005; Klin et al., 2002; Langdell,1978; Pelphrey et al., 2002). Direct gaze also modulatesactivation of the amygdala (Hooker et al., 2003; Kawashimaet al., 1999) which is implicated in social emotions such as fear(Adolphs, 2003) and increases the activation in the fusiform

86 B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

gyrus (George et al., 2001; Pageler et al., 2003) implicated in faceprocessing (Haxby et al., 2000; Kanwisher et al., 1997;McCarthy et al., 1997). The larger amplitude for straight thanaverted gaze could reflect this modulation of various brainareas by direct gaze, due to the social impact of direct gaze,which would occur regardless of the task.

In conclusion, the present study suggests that the earlystages of face processing are view-dependant as early as100 ms. In contrast, the possible processing of gaze around170 ms remains equivocal although gaze is likely processedbefore 400 ms. The late gaze modulation around 420–580 ms,regardless of task demands or head orientation, likely reflectsthe outcome of gaze processing with a special role played bydirect gaze. Head orientation seems to interfere with gazeprocessing later on, at the decisionmaking level as reflected inreaction time measures. The direction of others' attentionseems first indicated by the orientation of the head and thenby the direction of gaze.

4. Experimental procedure

4.1. Participants

Nineteen young healthy volunteers from the Toronto areawere tested and paid for their participation. They all had nor-mal or corrected-to-normal vision and signed a written in-formed consent that was approved by the Ethics ResearchBoard of Baycrest. Three subjects were rejected because ofrecording problems or too noisy data, leaving 16 subjects forthe analyses (21–35 years; 10 females).

4.2. Stimuli and design

Grayscale face photographs of 12 individuals (half males;taken from George et al., 2001) displaying neutral expres-sion, were used. Each face was photographed in a frontview and with the face turned 30° to the right (3/4 view),with the eyes looking straight ahead at the camera or 30° tothe right. These four original pictures were then mirror-reversed using Photoshop to avoid any bias between theright and left sides, generating 8 conditions according to afull factorial design of Head orientation (3/4-view or front-view)×Gaze direction (straight or averted)×side (left orright). Scrambled faces of the front-view-gaze-straightpictures were used as fillers.

Subjects were comfortably seated in a dimly lit and sound-proof booth, 60cm in front of a computer monitor. Stimuliwere presented centrally on the screen (6.5°×8.5° visual angle)for 500mswith a random ISI between 2000 and 2500ms duringwhich a centered fixation cross appeared. Two tasks wereperformed with both hands using the left and right controlkeys of a keyboard. In the “Gaze task”, subjects discriminatedbetween straight and averted gaze regardless of head orien-tation (“Is the person looking at you or away?”). In the “Headtask”, they discriminated between front- and 3/4-view facesregardless of gaze direction. It was emphasized that theyshould ignore the gaze to focus on the head orientation.Subjects had to answer as quickly and accurately as possible toall except scrambled stimuli.

For each task, 2 blocks were presented with all conditionscounterbalanced across the twelve individual faces, for a totalof 84 trials per condition per task. Button keys were switchedbetween the two blocks of each task. The order of buttons,tasks, and blocks were counter-balanced across subjects.Within each block, the order of stimuli was semi-randomizedwith the constraint that the face of one individual in aparticular head orientation and gaze direction would never befollowed by the same face with a different gaze direction (e.g.head-averted-to-left-gaze-straight would never follow or pre-cede head-averted-to-left-gaze-averted for the same individ-ual face). This was to prevent the perception of gazemotion. Afew practice trials were given before each block. Breaks weregiven between blocks. Accuracy and reaction times wererecorded using the software Presentation that also controlledfor stimulus presentation.

4.3. Electrophysiological recording

The Electroencephalogram was recorded (NeuroScan 4.0)using 64-channel ElectroCaps (10/20 system) including twopairs of ocular sites monitoring vertical and horizontal eyemovements from the outer canthi and infra-orbital ridges.Electrode impedances were kept under 5 KΩ. Continuous EEGwas recorded at a 500 Hz sampling rate through a band-pass of0.01–100 Hz and amplified using two SynAmps amplifiers. Foreach subject, continuous files were first epoched into −1 to1.5 s trials which were concatenated. An IndependentComponent Analysis (ICA) was run on the concatenatedepochs and eye movements and other major artifacts pickedup as independent ICA components were removed. Trialswere then inspected visually and those contaminated withartifacts left over were removed. The artifact-free trials werethen re-epoched into −200–1200 ms trials and those for whicha correct response was recorded were averaged according tothe eight face conditions separately for each task, and digitallylow-pass filtered (20 Hz). Each average was made of 50–80trials.

4.4. Data analysis

4.4.1. The N170 componentThe N170 ERP component was measured within a ±40 mswindow around the maximum of the grand-average mean foreach condition using an automated procedure, at the twoposterior sites on each hemisphere where it was largest (P7/P8and CB1/CB2). Peak latencies and amplitudes were measuredat each electrode. Repeated measures analyses of variance(ANOVA) were conducted using Greenhouse–Geisser adjusteddegrees of freedom, for the behavioral and N170 measures.Within-subject factors were task (Gaze or Head task), Headorientation (front-view or 3/4-view), Gaze direction (averted orstraight/direct), side (left/right), electrodes (parietal or cere-bellar) and hemisphere (left/right). Pair-wise compari-sons used t-tests with Bonferroni correction for multiplecomparisons.

4.4.2. PLS analysesThe data were also analyzed using the multivariate tech-nique Partial Least Square analysis (PLS, http://www.rotman-

87B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

baycrest.on.ca/pls). This technique has been validated foranalyses of PET (McIntosh et al., 1996), fMRI (McIntosh et al.,2004; McIntosh and Lobaugh, 2004), ERP, and MEG data (Hayet al., 2002; Itier et al., 2004; Lobaugh et al., 2001) and hasprovenuseful for face ERPs (Itier et al., 2004). It allows the studyof thewhole epoch simultaneously for all electrodes. PLS refersto the computation of the optimal least-squares fit to part of acovariance matrix. The part is the cross-block correlationbetween the experimental contrasts (conditions) and the ERPwaveforms recorded at all electrodes during a specific time(TaskPLS). The matrix for the TaskPLS is composed of electro-des as columns, and subjects and conditions as rows. Thematrix is subject to a Singular Value Decomposition (SVD) intoLatent Variables (LVs). Three outputs derived from the SVD areused to interpret the relationships between ERP amplitudesand task design. The first is a vector of singular values, whichrepresents the covariance of the experimental effect with theERP amplitude for each LV, and is also used to calculate theproportion of the cross-block covariancematrix attributable toeach LV. The second and third outputs contain the structureof the latent variables and are orthogonal pairs of vectors(saliences). One defines the contrasts among conditions(design saliences). The other identifies the electrodes andtimepoints at which these contrasts are expressed (electrodesaliences). The magnitude and sign of the electrode saliencesindicate the strength and direction of the contrasts at eachtimepoint. The significance of the singular values was deter-mined using permutation tests to provide an exact probabilityof observing the singular value by chance; the stability of theelectrode saliences at each timepoint and location in spacewas established through bootstrap resampling (Efron andTibshirani, 1985) to provide a standard error for each of thesaliences.

All PLS analyses were initially run from 0 to 800 ms andthen from 0 to 600 ms, using 500 replications for thepermutation tests and 200 replications for the Bootstraptests. The ratio of the salience to its bootstrapped standarderror is approximately equivalent to a z-score. Bootstrap ratiosgreater than 2.6 (roughly equivalent to p<.01) were taken toindicate stable saliences, or in other words, timepoints wherethe electrode saliences differed from zero. A first globalTaskPLS including all 16 conditions (8 conditions×2 tasks)was run. The significant LVs expressed complex interactionpatterns between tasks, gaze, head and side factors (Fig. 3) thatjustified the breaking down into smaller and more definedanalyses.

Because of the complexity of these interactions, non-rotated TaskPLS analyses (McIntosh and Lobaugh, 2004) wererun. In these analyses, the design contrast is defined a prioriby the experimenter (e.g. Gaze direction contrast) and theanalysis is constrained so that this contrast represents 100%of the cross-block covariance. The permutation tests assessthe significance of the gaze contrast and the electrodesaliences, and their boostrap ratio then identifies the time-points at which, for each electrode, there is a stable andreliable difference between averted and straight gaze acrossconditions. Several non-rotated analyses were run using apriori contrasts of Gaze direction (averted versus straight),Head orientation (front-view versus 3/4-view contrast), andtheir interactions with task.

Acknowledgments

We thank Dr. Nathalie George for the stimuli. Zainab Fatimaand Kate Sedore are warmly thanked for recruiting and testingsubjects. Thank you to Dr. Guillaume Rousselet for the matlabprograms on luminance and contrast calculation. This workwas supported by funding from CIHR, NSERC, and the Heartand Stroke Foundation.

R E F E R E N C E S

Adolphs, R., 2003. Is the human amygdala specialized forprocessing social information? Ann. N.Y. Acad. Sci. 985,326–340.

Allison, T., Puce, A., McCarthy, G., 2000. Social perception fromvisual cues: role of the STS region. Trends Cogn. Sci. 4,267–278.

Althoff, R.R., Cohen, N.J., 1999. Eye-movement-based memoryeffect: a reprocessing effect in face perception. J. Exp. Psychol.Learn Mem. Cogn. 25, 997–1010.

Andreasen, N.C., 1982. Negative symptoms in schizophrenia.Definition and reliability. Arch. Gen. Psychiatry 39,784–788.

Bentin, S., Allison, T., Puce, A., Perez, E., McCarthy, G., 1996.Electrophysiological studies of face perception in humans.J. Cogn. Neurosci. 8, 551–565.

Carmel, D., Bentin, S., 2002. Domain specificity versus expertise:factors influencing distinct processing of faces. Cognition 83,1–29.

Carrick, O.K., Thompson, J.C., Epling, J.A., Puce, A., 2007. It's all inthe eyes: neural responses to socially significant gaze shifts.Neuroreport 18, 763–766.

Dalton, K.M., Nacewicz, B.M., Johnstone, T., Schaefer, H.S.,Gernsbacher, M.A., Goldsmith, H.H., Alexander, A.L., Davidson,R.J., 2005. Gaze fixation and the neural circuitry of faceprocessing in autism. Nat. Neurosci. 8, 519–526.

Desimone, R., Albright, T.D., Gross, C.G., Bruce, C., 1984. Stimulusselective properties of inferior temporal neurons in themacaque. J. Neurosci. 4, 2051–2062.

Driver, J., Davis, G., Ricciardelli, P., Kidd, P., Maxwell, E.,Baron-Cohen, S., 1999. Gaze perception triggers reflexivevisuospatial orienting. Vis. Cogn. 6, 509–540.

Efron, B., Tibshirani, R., 1985. The Bootstrap Method for AssessingStatistical Accuracy. Technical Report Series, University ofToronto, Department of Statistics, vol. 4. University of Toronto,Toronto, pp. 1–53.

Eimer, M., 2000. The face-specific N170 component reflects latestages in the structural encoding of faces. Neuroreport 11,2319–2324.

Emery, N.J., 2000. The eyes have it: the neuroethology, functionand evolution of social gaze. Neurosci. Biobehav. Rev. 24,581–604.

Farroni, T., Csibra, G., Simion, G., Johnson, M.H., 2002. Eye contactdetection in humans from birth. Proc. Natl. Acad. Sci. U. S. A.99, 9602–9605.

Farroni, T., Massaccesi, S., Menon, E., Johnson, M.H., in press.Direct gaze modulates face recognition in young infants.Cognition.

Friesen, C.K., Kingstone, A., 1998. The eyes have it! Reflexiveorienting is triggered by nonpredictive gaze. Psychon. Bull. Rev.5, 490–495.

Friesen, C.K., Moore, C., Kingstone, A., 2005. Does gaze directionreally trigger a reflexive shift of spatial attention? Brain Cogn.57, 66–69.

88 B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

George, N., Evans, J., Fiori, N., Davidoff, J., Renault, B., 1996. Brainevents related to normal and moderately scrambled faces.Cogn. Brain Res. 4, 65–76.

George, N., Driver, J., Dolan, R.J., 2001. Seen gaze-directionmodulates fusiform activity and its coupling with other brainareas during face processing. Neuroimage 13, 1102–1112.

George, N., Jemel, B., Fiori, N., Chaby, L., Renault, B., 2005.Electrophysiological correlates of facial decision: insights fromupright and upside-down Mooney-face perception. Brain Res.Cogn. Brain Res. 24, 663–673.

Grice, S.J., Halit, H., Farroni, T., Baron-Cohen, S., Bolton, P.,Johnson, M.H., 2005. Neural correlates of eye-gaze detection inyoung children with autism. Cortex 41, 342–353.

Hains, S.M., Muir, D.W., 1996. Infant sensitivity to adult eyedirection. Child Dev. 67, 1940–1951.

Halgren, E., Raij, T., Marinkovic, K., Jousmaki, V., Hari, R., 2000.Cognitive response profile of the human fusiform face area asdetermined by MEG. Cereb. Cortex 10, 69–81.

Halit, H., de Haan, M., Johnson, M.H., 2000. Modulation ofevent-related potentials by prototypical and atypical faces.Neuroreport 11, 1871–1875.

Haxby, J.V., Hoffman, E.A., Gobbini, M.I., 2000. The distributedhuman neural system for face perception. Trends Cogn.Neurosci. 4, 223–233.

Hay, J.F., Kane, K.A., West, R., Alain, C., 2002. Event-related neuralactivity associated with habit and recollection.Neuropsychologia 40, 260–270.

Henderson, J.M., Williams, C.C., Falk, R.J., 2005. Eyemovements arefunctional during face learning. Mem. Cogn. 33, 98–106.

Hietanen, J.K., 1999. Does your gaze direction and head orientationshift my visual attention? Neuroreport 10, 3443–3447.

Hood, B.M., Willen, J.D., Driver, J., 1998. Adults' eyes triggershifts of visual attention in human infants. Psychol. Sci. 9,131–134.

Hood, B.M., Macrae, C.N., Cole-Davies, V., Dias, M., 2003. Eyeremember you: the effects of gaze direction on face recognitionin children and adults. Dev. Sci. 6, 67–71.

Hooker, C.I., Paller, K.A., Gitelman, D.R., Parrish, T.B., Mesulam,M.M., Reber, P.J., 2003. Brain networks for analyzing eye gaze.Brain Res. Cogn. Brain Res. 17, 406–418.

Itier, R.J., Taylor, M.J., 2002. Inversion and contrast polarityreversal affect both encoding and recognition processes ofunfamiliar faces: a repetition study using ERPs. Neuroimage15, 353–372.

Itier, R.J., Taylor, M.J., 2004a. N170 or N1? Spatiotemporaldifferences between object and face processing using ERPs.Cereb. Cortex 14, 132–142.

Itier, R.J., Taylor, M.J., 2004b. Effects of repetition learning onupright, inverted and contrast-reversed face processing usingERPs. Neuroimage 21, 1518–1532.

Itier, R.J., Taylor, M.J., Lobaugh, N.J., 2004. Spatiotemporal analysisof event-related potentials to upright, inverted, andcontrast-reversed faces: effects on encoding and recognition.Psychophysiol. 41, 643–653.

Itier, R.J., Latinus, M., Taylor, M.J., 2006. Face, eye and object earlyprocessing: what is the face specificity? Neuroimage 29,667–676.

Itier, R.J., Villate, C., Ryan, J.D., 2007. Eyes always attract attentionbut gaze orienting is task-dependent: evidence from eyemovement monitoring. Neuropsychologia 45,1019–1028.

Jemel, B., George, N., Chaby, L., Fiori, N., Renault, B., 1999.Differential processing of part-to-whole and part-to-part facepriming: an ERP study. Neuroreport 10, 1069–1075.

Kanwisher, N., McDermott, J., Chun, M.M., 1997. The fusiform facearea: a module in human extrastriate cortex specialized forface perception. J. Neurosci. 17, 4302–4311.

Kawashima, R., Sugiura, M., Kato, T., Nakamura, A., Hatano, K.,Ito, K., Fukuda, H., Kojima, S., Nakamura, K., 1999. The human

amygdala plays an important role in gaze monitoring. A PETstudy. Brain 122 (Pt 4), 779–783.

Klin, A., Jones, W., Schultz, R., Volkmar, F., Cohen, D., 2002. Visualfixation patterns during viewing of naturalistic socialsituations as predictors of social competence in individualswith autism. Arch. Gen. Psychiatry 59, 809–816.

Klucharev, V., Sams, M., 2004. Interaction of gaze direction andfacial expressions processing: ERP study. Neuroreport 15,621–625.

Langdell, T., 1978. Recognition of faces: an approach to the study ofautism. J. Child Psychol. Psychiatry 19, 255–268.

Langton, S.R., 2000. The mutual influence of gaze and headorientation in the analysis of social attention direction.Q. J. Exp. Psychol., A. 53, 825–845.

Langton, S.R., Bruce, V., 1999. Reflexive visual orienting inresponse to the social attention of others. Vis. Cogn. 6,541–567.

Langton, S.R., Watt, R.J., Bruce, I.I., 2000. Do the eyes have it? Cuesto the direction of social attention. Trends Cogn. Sci. 4,50–59.

Linkenkaer-Hansen, K., Palva, J.M., Sams, M., Hietanen, J.K.,Aronen, H.J., Ilmoniemi, R.J., 1998. Face-selective processing inhuman extrastriate cortex around 120 ms after stimulus onsetrevealed by magneto- and electroencephalography.Neurosci. Lett. 253, 147–150.

Lobaugh, N.J., West, R., McIntosh, A.R., 2001. Spatiotemporalanalysis of experimental differences in event-related potentialdata with partial least squares. Psychophysiol. 38,517–530.

Lu, S.T., Hamalainen, M.S., Hari, R., Ilmoniemi, R.J., Lounasmaa,O.V., Sams, M., Vilkman, V., 1991. Seeing faces activates threeseparate areas outside the occipital visual cortex in man.Neurosci. 43, 287–290.

Macrae, C.N., Hood, B.M., Milne, A.B., Rowe, A.C., Mason, M.F., 2002.Are you looking at me? Eye gaze and person perception.Psychol. Sci. 13, 460–464.

Mansfield, E.M., Farroni, T., Johnson, M.H., 2003. Does gazeperception facilitate overt orienting? Vis. Cogn. 10, 7–14.

Maurer, D., 1985. Infants' perception of facedness. In: Field, T., Fox,N. (Eds.), Social Perception in Infants. Ablex, Norwood, NJ, pp.73–100.

McCarthy, G., Puce, A., Gore, J.C., Allison, T., 1997. Face-specificprocessing in the human fusiform gyrus. J. Cogn. Neurosci. 9,605–610.

McIntosh, A.R., Lobaugh, N.J., 2004. Partial least squares analysis ofneuroimaging data: applications and advances. Neuroimage 23(Suppl 1), S250–S263.

McIntosh, A.R., Bookstein, F.L., Haxby, J.V., Grady, C.L., 1996.Spatial pattern analysis of functional brain images usingPartial Least Squares. Neuroimage 3, 143–157.

McIntosh, A.R., Chau, W.K., Protzner, A.B., 2004. Spatiotemporalanalysis of event-related fMRI data using partial least squares.Neuroimage 23, 764–775.

Pageler, N.M., Menon, V., Merin, N.M., Eliez, S., Brown, W.E., Reiss,A.L., 2003. Effect of head orientation on gaze processing infusiform gyrus and superior temporal sulcus. Neuroimage 20,318–329.

Pelphrey, K.A., Sasson, N.J., Reznick, J.S., Paul, G., Goldman, B.D.,Piven, J., 2002. Visual scanning of faces in autism. J. Autism.Dev. Disord. 32, 249–261.

Perrett, D.I., Smith, P.A., Potter, D.D., Mistlin, A.J., Head, A.S.,Milner, A.D., Jeeves, M.A., 1985. Visual cells in the temporalcortex sensitive to face view and gaze direction. Proc. R. Soc.Lond., B Biol. Sci. 223, 293–317.

Perrett, D.I., Oram, M.W., Harries, M.H., Bevan, R., Hietanen, J.K.,Benson, P.J., Thomas, S., 1991. Viewer-centred andobject-centred coding of heads in the macaque temporalcortex. Exp. Brain Res. 86, 159–173.

Perrett, D.I., Hietanen, J.K., Oram, M.W., Benson, P.J., 1992.

89B R A I N R E S E A R C H 1 1 7 7 ( 2 0 0 7 ) 7 9 – 8 9

Organization and functions of cells responsive to faces in thetemporal cortex. Philos. Trans. R. Soc. Lond., B Biol. Sci. 335,23–30.

Puce, A., Allison, T., Bentin, S., Gore, J.C., McCarthy, G., 1998.Temporal cortex activation in humans viewing eye and mouthmovements. J. Neurosci. 18, 2188–2199.

Puce, A., Smith, A., Allison, T., 2000. ERPs evoked by viewing facialmovements. Cogn. Neuropsychol. 17, 221–239.

Ricciardelli, P., Bricolo, E., Aglioti, S.M., Chelazzi, L., 2002. My eyeswant to look where your eyes are looking: exploring thetendency to imitate another individual's gaze. Neuroreport 13,2259–2264.

Rossion, B., Campanella, S., Gomez, C.M., Delinte, A., Debatisse, D.,Liard, L., Dubois, S., Bruyer, R., Crommelinck, M., Guerit, J.-M.,1999. Task modulation of brain activity related to familiar andunfamiliar face processing: an ERP study. Clin. Neurophysiol.110, 449–462.

Sabbagh, M.A., Moulson, M.C., Harkness, K.L., 2004. Neuralcorrelates of mental state decoding in human adults:an event-related potential study. J. Cogn. Neurosci. 16, 415–426.

Sams, M., Hietanen, J.K., Hari, R., Ilmoniemi, R.J., Lounasmaa, O.V.,1997. Face- specific responses from the human inferioroccipito-temporal cortex. Neurosci. 77, 49–55.

Schweinberger, S., Pfütze, E.-M., Sommer, W., 1995. Repetitionpriming and associative priming of face recognition: evidencefrom event-related potentials. J. Exper. Psychol., Learn., Mem.,Cogn. 21, 722–736.

Schweinberger, S.R., Pickering, E.C., Jentzsch, I., Burton, A.M.,Kaufmann, J.M., 2002. Event-related brain potential evidencefor a response of inferior temporal cortex to familiar facerepetitions. Brain Res. Cogn. Brain Res. 14, 398–409.

Schweinberger, S.R., Huddy, V., Burton, A.M., 2004. N250r:a face-selective brain response to stimulus repetitions.Neuroreport 15, 1501–1505.

Schweinberger, S.R., Kloth, N., Jenkins, R., 2007. Are you looking at

me? Neural correlates of gaze adaptation. Neuroreport 18,693–696.

Senju, A., Hasegawa, T., 2005. Direct gaze captures visuospatialattention. Vis. Cogn. 12, 127–144.

Tanaka, J.W., Curran, T., Porterfield, A.L., Collins, D., 2006.Activation of preexisting and acquired face representations:the N250 event-related potential as an index of face familiarity.J. Cogn. Neurosci. 18, 1488–1497.

Taylor, M.J., Edmonds, G.E., McCarthy, G., Allison, T., 2001a. Eyesfirst! Eye processing develops before face processing inchildren. Neuroreport 12, 1671–1676.

Taylor, M.J., George, N., Ducorps, A., 2001b.Magnetoencephalographic evidence of early processing ofdirection of gaze in humans. Neurosci. Lett. 316, 173–177.

Taylor, M.J., Itier, R.J., Allison, T., Edmonds, G.E., 2001c. Direction ofgaze effects on early face processing: eyes-only versus fullfaces. Brain Res. Cogn. Brain Res. 10, 333–340.

Vuilleumier, P., 2002. Perceived gaze direction in faces and spatialattention: a study in patients with parietal damage andunilateral neglect. Neuropsychologia 40, 1013–1026.

Vuilleumier, P., George, N., Lister, V., Armony, J., Driver, J., 2005.Effects of perceivedmutual gaze and gender on face processingand recognition memory. Vis. Cogn. 12, 85–101.

Walker-Smith, G.J., Gale, A.G., Findlay, J.M., 1977. Eyemovement strategies involved in face perception. Perception6, 313–326.

Watanabe, S., Kakigi, R., Puce, A., 2001. Occipitotemporal activityelicited by viewing eye movements:a magnetoencephalographic study. Neuroimage 13, 351–363.

Watanabe, S., Miki, K., Kakigi, R., 2002. Gaze direction affects faceperception in humans. Neurosci. Lett. 325, 163–166.

Watanabe, S., Kakigi, R., Miki, K., Puce, A., 2006. Human MT/V5activity on viewing eye gaze changes in others:a magnetoencephalographic study. Brain Res. 1092, 152–160.

Yarbus, A., 1967. Eye Movements and Vision. Plenum, New York.