visual representation of eye gaze is coded by a nonopponent multichannel system

Visual Representation of Eye Gaze Is Coded by a NonopponentMultichannel System

Andrew J. CalderMRC Cognition and Brain Sciences Unit, Cambridge

Rob JenkinsUniversity of Glasgow

Anneli CasselMRC Cognition and Brain Sciences Unit, Cambridge

Colin W. G. CliffordUniversity of Sydney

To date, there is no functional account of the visual perception of gaze in humans. Previous work hasdemonstrated that left gaze and right gaze are represented by separate mechanisms. However, these dataare consistent with either a multichannel system comprising separate channels for distinct gaze directions(e.g., left, direct, and right) or an opponent-coding system in which all gaze directions are coded by just2 pools of cells, one coding left gaze and the other right, with direct gaze represented as a neutral pointreflecting equal activation of both left and right pools. In 2 experiments, the authors used adaptationprocedures to investigate which of these models provides the optimal account. Both experimentssupported multichannel coding. Previous research has shown that facial identity is coded by anopponent-coding system; hence, these results also demonstrate that gaze is coded by a differentrepresentational system to facial identity.

Keywords: face perception, aftereffect, superior temporal sulcus, opponent coding

Accurate perception of others’ gaze direction is central to socialinteraction. Gaze signals a person’s focus of attention, providesinformation about the person’s cognitive and emotional state (Ad-ams & Kleck, 2003; Baron-Cohen, Campbell, Karmiloff-Smith,Grant, & Walker, 1995; Calder et al., 2002), and is used toestablish joint attention (Dunham & Moore, 1995) or exercisesocial control (Kleinke, 1986). These aspects of gaze processinghave been studied relatively extensively, but there is currently nofunctional account of human gaze perception. Two sources ofevidence provide important clues: single-cell recordings in nonhu-man primates and adaptation research in humans.

Electrophysiological Research

Seminal work by Perrett and colleagues identified cells tuned todifferent head orientations and gaze directions in the anteriorsuperior temporal sulcus (STS) of monkeys. Most of this work

addressed head orientation and found broadly tuned cells coding anumber of head orientations, with the majority tuned to a limitednumber of prototypical views (full face, left profile, right profile,up, and down; Perrett et al., 1985, 1989). Additional cells wereequally responsive to both horizontal profiles (i.e., left and rightprofiles) or both vertical orientations. Gaze received less extensiveinvestigation, and fewer distinct cell types were found. However,separate populations were maximally responsive to direct gaze(eye contact), upward gaze, and both averted directions in thehorizontal plane (i.e., equally responsive to left and right gaze).

The limited available data for gaze and, in particular, the lack ofevidence for distinct cell types tuned to each of left and right gazemake it difficult to draw firm conclusions regarding its visualrepresentation. One possibility is that the cells coding both hori-zontal gaze directions pool the output of as yet unidentified leftand right gaze-specific cells. Alternatively, the direct and horizon-tal gaze cells may code mental states relevant to detection of threatand other social interactions (Emery, 2000), such as “looking atme” and “not looking at me,” rather than visual representations ofgaze. The implications of the electrophysiological data for visualaccounts of human gaze representation are therefore unclear.

Adaptation

The second source of evidence comes from human adaptationresearch that has demonstrated separate mechanisms coding leftand right gaze (Calder et al., 2007; Jenkins, Beaver, & Calder,2006; Seyama & Nagayama, 2006). Adaptation has been primarilyassociated with low- or mid-level perceptual properties, such ascolor (Webster, 1996), orientation (Clifford, 2002), motion (Ans-tis, Verstraten, & Mather, 1998; Clifford, 2002), and aspect ratio(Regan & Hamstra, 1992). However, accumulating evidence

Andrew J. Calder and Anneli Cassel, MRC Cognition and Brain Sci-ences Unit, Cambridge, United Kingdom; Rob Jenkins, Department ofPsychology, University of Glasgow, Glasgow, United Kingdom; ColinW. G. Clifford, School of Psychology, University of Sydney, Sydney, NewSouth Wales, Australia.

The research was funded by the U.K. Medical Research Council(U.1055.02.001.00001.01). Colin W. G. Clifford is supported by an Aus-tralian Research Fellowship from the Australian Research Council. Thanksto Jill Keane for helpful comments on an earlier draft and to SimonStrangeways for preparing graphics.

Correspondence concerning this article should be addressed to AndrewJ. Calder, MRC Cognition and Brain Sciences Unit, 15 Chaucer Road,Cambridge CB2 7EF, United Kingdom. E-mail: [email protected]

Journal of Experimental Psychology: General Copyright 2008 by the American Psychological Association2008, Vol. 137, No. 2, 244–261 0096-3445/08/$12.00 DOI: 10.1037/0096-3445.137.2.244

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shows that complex visual representations, such as faces, are alsosusceptible to these effects (Fang & He, 2005; Jenkins et al., 2006;Jiang, Blanz, & O’Toole, 2006; Leopold, O’Toole, Vetter, &Blanz, 2001; Rhodes, Jeffery, Watson, Clifford, & Nakayama,2003; Webster & MacLin, 1999). For example, adaptation of facialidentity has been demonstrated whereby prolonged exposure to aparticular facial configuration (e.g., wide eyes and a thin nose)causes an average face to be mistaken for a person with a con-trasting configuration (i.e., narrow eyes and broad nose; Leopold etal., 2001; Rhodes & Jeffery, 2006). Similarly, adapting to a dis-torted face in which the features are contracted toward its centercauses an undistorted face to appear distorted in the oppositemanner (i.e., expanded; Rhodes et al., 2003; Watson & Clifford,2006; Webster & MacLin, 1999).

Adaptation of gaze demonstrates that a localized and highlyspecific facial cue (i.e., left or right gaze) can also be selectivelyadapted. Thus, adapting to a series of faces gazing 25° left (orright) increases participants’ tendency to perceive 5° and 10° gazein the adapted direction as direct (i.e., looking at them), whereasgaze in the opposite direction is unaffected or less likely to beperceived as direct (i.e., more likely to be categorized as right [orleft] following left [or right] gaze adaptation; Calder et al., 2007;Jenkins et al., 2006). These effects also persist over changes in theidentity, size, and head orientation of the adapting and probe faces(Jenkins et al., 2006), demonstrating that they do not reflectadaptation of low-level visual properties.

Using the gaze adaptation paradigm in an fMRI adaptationstudy, Calder et al. (2007) found evidence for separate pools ofcells in the human anterior STS tuned to left and right gaze. Thus,following adaptation to 25° leftward gaze, activation to 10° leftwas reduced relative to 10° right or direct gaze; similarly, theopposite pattern was observed following rightward gaze adaptation(i.e., 10° right ! 10° left or direct; see also Fang & He, 2005;Fang, Murray, & He, in press, for behavioral and fMRI adaptationinvestigations of viewer-centered representations of faces).

In summary, adaptation studies of eye gaze to date support afunctional and neural dissociation between the coding of left andright gaze in humans. However, this is compatible with either oftwo distinct perceptual frameworks, referred to as multichanneland opponent coding, and so, the visual representation of gazeremains undefined. The former framework has been applied to therepresentation (and adaptation) of orientation and spatial fre-quency (Suzuki, 2005), whereas the latter has been associatedmore with representation of color (e.g., red–green; Webster,1996), aspect ratio (Regan & Hamstra, 1992), and facial identity(Jiang et al., 2006; Leopold, Bondar, & Giese, 2006; Leopold etal., 2001; Rhodes et al., 2005). Here, we consider which frame-work provides the optimal account of the visual representation ofgaze.

Multichannel and Opponent-Coding Models of GazePerception

A multichannel model of gaze perception would consist ofseparate channels, each tuned to a particular gaze direction (seeFigure 1a). Gaze in the horizontal plane might be coded by left,direct, and right channels or by a larger number of channels withmore narrow tuning (e.g., 20° left, 10° left, etc.). As alreadydiscussed, relatively broad tuning of individual channels has a

basis in nonhuman primate research investigating cells sensitive todifferent head orientations (Perrett et al., 1985, 1991). Conse-quently, our predictions are illustrated in relation to a three-channel (left, direct, right) model.

In the alternative, opponent-coding framework (Regan & Ham-stra, 1992), all horizontal gaze directions are represented by twobroadly tuned channels, one maximally sensitive to left gaze, theother maximally sensitive to right, while direct gaze is representedas an equilibrium state with equal engagement of both left andright channels (see Figure 2a).

Two additional principles apply to both models. First, gazedirection is calculated by considering the output of all channels—the balance of both left and right channels for opponent coding orthe output of all channels for a multichannel system. Second,adaptation reduces any subsequent response of a channel in pro-portion to the firing rate evoked by the adapting stimulus.

Researchers investigating adaptation of faces or, more specifi-cally, facial configurations have favored opponent coding (Jiang etal., 2006; Leopold et al., 2001; Rhodes & Jeffery, 2006; Rhodes etal., 2005; Robbins, McKone, & Edwards, 2007; Tsao & Freiwald,2006), whereby faces are coded in a multidimensional “facespace,” with each dimension constituting a distinct opponent-coded mechanism. Robbins et al. (2007) provided direct supportfor this view by testing the predictions of opponent and multichan-nel models of the representation of configural facial features.However, it is yet to be determined which model provides anappropriate framework for the visual representation of gaze direc-tion. To address this, we investigated predictions of the twoframeworks for gaze adaptation.

Central to the first of these predictions are the different ways inwhich each framework represents and adapts to direct gaze. In amultichannel (three-channel) system, direct gaze is represented asrelatively increased engagement of the direct channel together withlesser, equal engagement of both left and right channels (seeFigure 1a). Similarly, left (or right) gaze is represented as in-creased engagement of the left (or right) channel, with lesser or noengagement of the direct and right (or left) channels. In contrast, inan opponent-coding system, direct gaze is represented as an equi-librium state, with equal engagement of left and right channels,whereas left and right gaze are represented by increased engage-ment of their respective channels (see Figure 2a). Thus, direct gazehas a special status in opponent coding—it is not associated witha distinct channel but rather represents the null point or centraltendency of the system. Moreover, the position of the crossoverpoint between the left and right channels (see Figure 2) constitutesthe perceived position of direct gaze, relative to which all othergaze directions are estimated.

Since the two models represent direct gaze in different ways,they produce different predictions for adaptation to this gazedirection. In an opponent-coding system, adaptation to direct gazecauses both left and right channels to attenuate by an equivalentamount such that the position of the central tendency (i.e., cross-over between left and right channels) is unchanged, producing nochange of the perceived direction of any gaze angle (see Figure2d). In contrast, for a multichannel system, adapting to direct gazeproduces a disproportionate attenuation of the direct gaze channelrelative to the left and right channels, causing small angles of leftand right gaze to be perceived as more averted (see Figure 1d).

245EYE GAZE

The predictions for direct gaze adaptation were addressed in Ex-periment 1. In addition, we included two left and right gaze adaptationconditions, involving more and less extreme gaze adaptors (25° and10°). Again, the two systems make different predictions for these.Figures 1 and 2 illustrate the predictions for these conditions inrelation to adaptation to 25° left and 10° left. Figure 1b shows that amultichannel system predicts that adaptation to 25° leftward gazewould strongly attenuate the response of the left gaze channel andweakly attenuate or fail to attenuate the response of the direct gazechannel. However, adaptation to 10° left gaze (see Figure 1c) wouldattenuate the response of both left and direct gaze channels, with theleft channel showing a stronger attenuation than the direct channel.Thus, according to the multichannel model, adaptation to 25° leftwould produce a greater tendency to perceive averted gaze probes onthe left, adapted side as direct relative to 10° adaptation. In contrast,adaptation to 10° left would produce a reduced tendency to perceiveaverted gaze on the right, nonadapted side as direct relative to 25° leftadaptation. Similarly, the same predictions apply to adaptation to 25°and 10° rightward gaze.

In an opponent-coding system, the shift in the central tendencyfollowing adaptation is proportional to the degree of attenuation of theleft (or right) channel. Adaptation to 25° left (or right) would produceeither more or equal attenuation to 10° left (or right) adaptation; theformer is illustrated in Figure 2. In other words, opponent codingpredicts one of two outcomes for a comparison of adaptation to 25°and 10° leftward gaze: (a) that 25° will produce a more markedincrease in direct responses to left (adapted-side) gaze probes and amore marked reduction in direct responses to right (nonadapted-side)probes, or (b) that both adaptors will produce equivalent effects on theadapted- and nonadapted-side probes. Critically, opponent codingdoes not predict the pattern predicted by multichannel coding. InExperiment 2, we used simultaneous adaptation of left and right gazeas a second method of distinguishing between multichannel andopponent-coding systems. This involved adapting to sequences ofalternating left and right gaze faces. For an opponent-coding system,this would produce equivalent attenuation of both left and right gazechannels, resulting in no overall change in the position of the centraltendency and, hence, no change in the perceived direction of any ofthe gaze probes (see Figure 2e). For a multichannel system, both leftand right channels would be also attenuated by an equivalent amount;

however, the critical difference is that the additional direct channelwould be attenuated less, resulting in an increased tendency to per-ceive both left and right gaze probes as direct (see Figure 1e).

Experiment 1

Method

Participants. Twenty-four volunteers (11 female; M age "23.5 years, SD " 4.75; range, 18–35 years) with normal orcorrected-to-normal vision were recruited from the MRC Cogni-tion and Brain Sciences Unit (Cambridge, United Kingdom) vol-unteer panel and were paid for participating.

Materials. Color full-face photographs of 10 young-adultmodels were used as probe faces for the gaze acuity test. Eachmodel showed five different angles of gaze—10° left, 5° left, 0°direct (straight ahead), 5° right, and 10° right (50 images intotal)—by looking at fixed reference markers while keeping thehead straight. Photographs of the same 10 models gazing 25° leftand 25° right, 10° left and 10° right, and 0° direct were used asadaptation stimuli. All faces were presented in a black ellipticalmask (see Figure 3), and the adapting faces were 75% of the sizeof the probe faces.

Design and procedure. The adaptation experiment comprisedfive blocks—an initial baseline block (Baseline 1) to assess par-ticipants’ gaze discrimination prior to adaptation; three adaptationblocks in which participants adapted to 25° left (or right) gaze, 10°left (or right) gaze, and direct gaze in counterbalanced order; andfinally, a second baseline block that was identical to the first(Baseline 2). Each of the 25° and 10° adaptation blocks comprisedseparate left gaze adaptation and right gaze adaptation phases. Sothat the direct gaze adaptation block also contained two phases,participants adapted to the direct gaze faces twice, with one phasecontaining the original direct gaze adaptation images and thesecond phase the same images in mirror-image format. The orderin which participants completed the three adaptation blocks (25°,10°, and direct) and the order of the left and right gaze adaptationphases (in the 25° and 10° adaptation blocks) or direct and mirror-image direct (in the direct gaze adaptation block) were counter-balanced across participants. The format of the trials in the base-

Figure 1 (opposite). a: Schematic response of hypothetical channels preferring leftward (red), direct (black),and rightward (blue) gaze. The shaded grey region represents the range of gaze directions for which directresponses predominate, assuming that the most strongly responding channel determines the response. The barcharts at the top of the figure indicate the relative engagement of each channel for the five gaze directions usedas probe stimuli in Experiments 1 and 2 (10° left, 5° left, 0° [direct], 5° right, and 10° right). b–e: The effectof adaptation on channel responses, assuming that adaptation can be characterized by a divisive rescaling ofresponsiveness and that the degree of adaptation is proportional to the (unadapted) response to the adaptingstimulus. b: Adaptation to 25° leftward gaze (Adapt #25) predominantly affects the leftward channel, shiftingthe category boundary between leftward and direct gaze toward the adapting stimulus. c: Adaptation to 10°leftward gaze (Adapt #10) also affects the leftward channel the most (although to a lesser extent than 25°adaptation), shifting the category boundary between leftward and direct gaze toward the adapting stimulus.However, the direct gaze channel is also affected to a lesser extent, shifting the balance of responses betweendirect and rightward channels such that the category boundary between direct and rightward gaze shifts slightlytoward the adapting stimulus. d: Direct adaptation (Adapt Direct) affects all channels, with the direct gazechannel most strongly affected, resulting in a slight narrowing of the range of gaze directions classified as direct.e: Left–right adaptation (Adapt L/R) affects all channels, this time with the direct gaze channel least stronglyaffected, resulting in a broadening of the range of gaze directions classified as direct.

246 CALDER, JENKINS, CASSEL, AND CLIFFORD

247EYE GAZE

line block and an adaptation block (25° left adaptation) isillustrated in Figure 3 and described below. The 10° and directgaze adaptation blocks had the same basic format. To account forany slight asymmetries in the faces’ gaze (e.g., 5° left being moreaverted than 5° right), half of the participants (n " 12) completedan experiment identical to that described above but with all imagesmirror-reversed.

Baseline block. The experiment began with a baseline block(Baseline 1) that contained the 10 models posing each of five gazedirections (10° left, 5° left, 0°, 5° right, and 10° right; 50 stimuliin total). Trials consisted of a blank screen for 750 ms followed bya 750-ms fixation cross, then a probe face for 500 ms and a1,500-ms intertrial interval (ITI; see Figure 3). Presentation orderwas randomized, and participants pressed one of three keys withtheir right hand to categorize the probe face’s gaze direction as left,direct, or right. An identical baseline block (Baseline 2) waspresented at the end of the experiment, after the participants hadcompleted all adaptation blocks.

Adaptation block. Each adaptation block comprised twophases (see Figure 3). For example, the 25° averted block con-sisted of a 25° left adaptation phase and 25° right adaptation phase,each comprising two sections. Section 1 contained three presenta-tions of the 10 models gazing in the same direction (25° left or 25°right; 30 faces in total). Each face was presented for 4,000 ms andwas immediately followed by the next, such that the initial adap-tation phase lasted for 2 min. Participants were instructed to lookat each face, and no response was required. Section 2 contained thesame probe faces as the baseline block (10 models $ 5 gazedirections [10° left, 5° left, 0°, 5° right, and 10° right]; 50 stimuliin total); however, each probe was preceded by a top-up adaptationface gazing 25° in the same direction as the preceding Section 1(see Figure 3). Thus, for a leftward adaptation phase, each trial ofSection 2 comprised a 4,000-ms presentation of a top-up adapta-tion face gazing 25° to the left immediately followed by a 500-mspresentation of a probe face and then a 1,500-ms blank ITI. Theprobe was clearly identified with the label “RESPOND” printedabove and below the face, and participants were required to cate-gorize its gaze direction as left, direct, or right. The top-up adap-tation and probe faces never showed the same identity and weredifferent sizes. Hence, any adaptation effects cannot be attributedto facial identity adaptation or low-level aftereffects.

Results

Our previous research has shown that adaptation of left and rightgaze causes slightly averted gaze (5° and 10°) in the same directionto be mistaken as direct (Calder et al., 2007; Jenkins et al., 2006).Consequently, the data in Figure 4 are summarized as participants’mean number of direct responses, and any adaptation of left andright gaze probes (i.e., 5° and 10°) is measured as altered numbersof direct responses to these gaze angles; a full summary of left,direct, and right responses is shown in Table 1. The predictedeffects of adaptation in terms of direct gaze responses for themultichannel and opponent-coding models are as follows: For amultichannel system, adapting to direct gaze should produce adisproportionate attenuation of the direct gaze channel relative tothe left and right channels, causing a reduced tendency for smallangles of left and right gaze to be categorized as direct (see Figure1d). In contrast, for an opponent-coding system, adaptation todirect gaze causes both left and right channels to attenuate by anequivalent amount, such that the position of the central tendency(i.e., crossover between left and right channels) is unchanged,producing no change in the number of direct responses to thedifferent probe directions.

For all analyses, t-test comparisons were Bonferonni corrected,with uncorrected p values reported throughout. Prior to analysis,the data were arcsin-transformed to stabilize variance of the pro-portion measures, which showed a range of values includingvalues close to ceiling and floor. The patterns of results wereidentical to those found using nontransformed data, and all prin-cipal effects were also found using nonparametric Wilcoxonsigned ranks tests corrected for multiple comparisons.

Participants’ performance in the first and second baseline blocksfrom the beginning and end of the experiment are summarized inFigure 4a and Table 1. Performance on the two baselines wascompared with a three-factor analysis of variance (ANOVA) com-paring baseline (first and second; repeated measure), gaze direc-tion (10° left, 5° left, 0°, 5° right, and 10° right; repeated measure),and experiment version (original and mirror-reversed; between-subjects); Greenhouse-Geisser correction is used where appropri-ate in all ANOVAs reported. The results showed a main effect ofgaze direction, F(4, 88) " 225.84, p ! .0001, %p

2 " .91, reflectingmore direct responses to direct gaze probes, followed by 5° andthen 10° probes (see Figure 4a and Table 1). There was no maineffect of experiment version, F(1, 22) " 1.69, p & .2, or interac-

Figure 2 (opposite). a: Schematic response of hypothetical opponent-coded channels preferring leftward (red)and rightward (blue) gaze. The shaded grey region represents the range of gaze directions for which directresponses predominate. The bar charts at the top of the figure indicate the relative engagement of each channelfor the five gaze directions used as probe stimuli in Experiments 1 and 2 (10° left, 5° left, 0° [direct], 5° right,and 10° right). b–e: The effect of adaptation on channel responses, assuming that adaptation can be characterizedby a divisive rescaling of responsiveness and that the degree of adaptation is proportional to the (unadapted)response to the adapting stimulus. b: Adaptation to 25° leftward gaze (Adapt #25) affects the leftward channel,shifting the category boundary between leftward and rightward gaze toward the adapting stimulus. c: Adaptationto 10° leftward gaze (Adapt #10) also affects the leftward channel the most (although to a lesser extent than 25°adaptation), shifting the category boundary between leftward and rightward gaze toward the adapting stimulus.d: Direct adaptation (Adapt Direct) affects both left and right channels to an equal extent, resulting in no changein the range of gaze directions classified as direct. e: Left–right adaptation (Adapt L/R) also affects both left andright channels to an equal extent, again resulting in no change in the range of gaze directions classified as direct.

249EYE GAZE

Figure 3. Trial events and example stimuli from Experiment 1 for the baseline block and 25° adaptation block.Baseline gaze acuity was assessed at the beginning and end of the experiment, in which participants madekeypress judgments to indicate the gaze direction (left, right, or direct) of probe stimuli displaying one of fivegaze directions (10° left, 5° left, direct gaze, 5° right, and 10° right). Section 1 of the adaptation block compriseda series of faces with eyes averted in one consistent direction (left or right). In Section 2, the gaze acuity test wasrepeated, with each face preceded by a top-up adaptation face. Probe faces in Section 2 were identified with thelabel “RESPOND” printed above and below the face. Adapting faces were 75% of the size of the probe faces.ITI " intertrial interval; L " left; R " right.

tions with this factor (all ps & .1), and no main effect of baselineor Baseline $ Gaze interaction (Fs ! 1). Consequently, theseparate analyses of the 25°, 10°, and direct gaze adaptationconditions reported below compare adaptation with the average ofboth baseline conditions.

Data from the three adaptation conditions (25°, 10°, and directgaze) are summarized in Table 1 and Figure 4. It was not appro-priate to enter all three adaptation conditions into a single ANOVAbecause the direct gaze condition did not include adaptation direc-tion (left and right) as a repeated measures factor. Our first pre-diction related to the effects of direct gaze adaptation, so anANOVA comparing these data with the average baseline data ispresented first. This is followed by separate ANOVAs comparingthe performance of each of the 25° and 10° adaptation conditionswith the average baseline data and then a comparison of the 25°and 10° adaptation conditions to address the second prediction.

Direct gaze adaptation. To determine whether the two directgaze adaptation conditions produced statistically distinguishablepatterns, they were compared in a three-factor ANOVA comparingadaptation version (Direct Adaptation 1 [adaptation and probe

faces in same format] and Direct Adaptation 2 [adaptation facesmirror-reverse of probe faces]; repeated measure), gaze direction(10° left, 5° left, 0°, 5° right, and 10° right; repeated measure), andexperiment version (original and mirror-image probes; between-subjects). Results showed a small but statistically significant maineffect of adaptation version, F(1, 22) " 5.20, p " .033, %p

2 " .19,reflecting a slight overall increase in direct gaze responses whenthe adaptation and probe faces were shown in the same imageformat (i.e., both original or both mirror-reversed format; seeFigure 4d). There was no effect of experiment version (F ! 1) andno interactions with this factor ( ps & .2). As expected, there wasalso a significant main effect of gaze direction, F(3.0, 65.8) "287.57, p ! .0001, %p

2 " .93.Given the absence of any interaction with adaptation version

(Direct Adaptation 1 and Direct Adaptation 2), the two direct gazeconditions were pooled to give one direct gaze condition that wascompared with the average baseline in a three-factor ANOVAinvestigating adaptation (direct gaze adaptation and average base-line; repeated measure), gaze direction (10° left, 5° left, 0°, 5°right, and 10° right; repeated measure), and experiment version

Figure 4. From Experiment 1, participants’ mean number of direct responses with 95% confidence intervals.a: Data for the first and second baseline blocks. b: Discrimination of gaze probes following adaptation to 25° leftand 25° right gaze. c: Discrimination of gaze probes following adaptation to 10° left and 10° right gaze. d:Discrimination of gaze probes following adaptation to direct gaze in original (Direct 1) and mirror-image (Direct2) formats. Average baseline data are also shown in b, c, and d. L10 " 10° left; L05 " 5° left; S00 " directgaze; R05 " 5° right; R10 " 10° right.

251EYE GAZE

(original and mirror image; between-subjects). Results showedsignificant main effects of adaptation, F(1, 22) " 15.78, p ! .005,%p

2 " .42, and gaze direction, F(4, 88) " 347.23, p ! .0001, %p2 "

.94, qualified by an Adaptation $ Gaze Direction interaction, F(4,88) " 6.38, p ! .0001, %p

2 " .22. There was no main effect ofexperiment version (F ! 1) or significant interactions with thisfactor ( ps & .1). A breakdown of the Adaptation $ Gaze Directioninteraction with t-test comparisons (cutoff p ! .01) showed sig-nificantly fewer direct gaze responses for 5° left, t(23) " #3.70,p ! .001, and 5° right gaze, t(23) " #3.52, p ! .005, reflectingincreased correct categorization of these gaze directions (see Table1 and below). Similar effects or nonsignificant trends were ob-served for 10° left, t(23) " #3.45, p " .005, and 10° right gaze,t(23) " #1.88, p " .07, while direct gaze showed a nonsignificanttrend toward increased direct responses, t(23) " 1.76, p " .092.

We conducted t-test comparisons of the right and left gazeresponses to verify that the reduction in direct responses for rightand left gaze probes reflected increased right and left responses,respectively. This was confirmed ( ps ! .005 unless stated)—rightresponses for 5° right, t(23) " 3.49, and 10° right, t(23) " 1.98,p " .06; left responses for 5° left, t(23) " 3.74, and 10° left, t(23)" 3.63.

In summary, consistent with the predictions of the multichannelmodel, the only effects that reached statistical significance fordirect gaze adaptation were a significant reduction in the number

of direct responses to both 5° and, to a lesser extent, 10° left andright gaze.

25° adaptation. Performance on the 25° adaptation and base-line conditions was compared in a three-factor ANOVA exploringadaptation (25° left adaptation, 25° right adaptation, and averagebaseline; repeated measure), gaze direction (10° left, 5° left, 0°, 5°right, and 10° right; repeated measure) and experiment version(original and mirror image; between-subjects). There were signif-icant main effects of adaptation, F(2, 44) " 327.06, p ! .0001,%p

2 " .55, and gaze direction, F(4, 88) " 219.71, p ! .0001, %p2 "

.91, qualified by an Adaptation $ Gaze Direction interaction,F(4.3, 94.8) " 96.82, p ! .0001, %p

2 " .82. There was no effect ofexperiment version, F(1, 22) " 1.99, p & .1, or significant inter-actions with this factor (Fs ! 1), excepting a borderline Adapta-tion $ Gaze $ Experiment Version interaction, F(4.3, 94.8) "2.16. p " .074.

To explore the Adaptation $ Gaze Direction interaction in moredetail, t-test comparisons ( p ! .01 cutoff) compared each gazedirection in the 25° left adaptation condition with the correspond-ing levels of the average baseline condition. Results showed asignificant increase in direct responses for 5° left, t(23) " 10.78,and 10° left gaze probes, t(23) " 6.67, ps ! .0001; a nonsignifi-cant trend toward decreased direct responses for 5° right, t(23) "#2.30, p " .03, and direct gaze, t(23) " #2.10, p " .046; and nosignificant effect for 10° right (t ! 1; see Table 1 and Figure 4b).

Table 1Experiment 1: Mean Proportion of Left, Direct, and Right Responses to the Five Probe Gaze Directions (10° Left, 5° Left, 0°,5° Right, and 10° Right) in the Baseline and Adaptation (25°, 10°, and Direct) Conditions

Response type bycondition

10° left 5° left 0° (direct) 5° right 10° right

M SE M SE M SE M SE M SE

Left responsesBaseline 1 0.95 0.01 0.63 0.04 0.08 0.02 0.00 0.00 0.00 0.00Baseline 2 0.94 0.02 0.60 0.05 0.08 0.02 0.00 0.00 0.00 0.00Average baseline 0.95 0.01 0.61 0.04 0.08 0.01 0.00 0.00 0.00 0.0025° left 0.50 0.07 0.07 0.02 0.00 0.00 0.00 0.00 0.00 0.0025° right 0.97 0.02 0.75 0.05 0.17 0.04 0.01 0.01 0.01 0.0110° left 0.93 0.02 0.28 0.03 0.00 0.00 0.01 0.01 0.00 0.0010° right 0.98 0.01 0.87 0.02 0.24 0.05 0.03 0.01 0.00 0.00Direct 1 1.00 0.00 0.72 0.04 0.03 0.01 0.00 0.00 0.00 0.00Direct 2 0.98 0.01 0.74 0.04 0.08 0.02 0.00 0.00 0.00 0.00

Direct responsesBaseline 1 0.04 0.01 0.38 0.04 0.90 0.02 0.52 0.06 0.10 0.03Baseline 2 0.05 0.02 0.40 0.05 0.89 0.02 0.53 0.05 0.07 0.02Average baseline 0.05 0.01 0.39 0.04 0.89 0.02 0.52 0.05 0.09 0.0225° left 0.50 0.07 0.93 0.02 0.91 0.03 0.40 0.06 0.08 0.0325° right 0.03 0.02 0.24 0.05 0.82 0.05 0.95 0.02 0.65 0.0510° left 0.08 0.02 0.71 0.03 0.87 0.03 0.24 0.04 0.02 0.0110° right 0.02 0.01 0.13 0.02 0.76 0.05 0.77 0.03 0.20 0.04Direct 1 0.00 0.00 0.28 0.04 0.95 0.01 0.39 0.05 0.06 0.03Direct 2 0.02 0.01 0.26 0.04 0.90 0.02 0.36 0.04 0.03 0.02

Right responsesBaseline 1 0.00 0.00 0.00 0.00 0.03 0.01 0.48 0.06 0.89 0.03Baseline 2 0.01 0.01 0.00 0.00 0.03 0.01 0.48 0.05 0.93 0.02Average baseline 0.01 0.00 0.00 0.00 0.03 0.01 0.48 0.05 0.91 0.0225° left 0.00 0.00 0.01 0.01 0.08 0.03 0.60 0.06 0.93 0.0325° right 0.00 0.00 0.01 0.01 0.01 0.01 0.04 0.02 0.34 0.0510° left 0.00 0.00 0.00 0.00 0.13 0.03 0.75 0.05 0.98 0.0110° right 0.00 0.00 0.00 0.00 0.00 0.00 0.20 0.03 0.80 0.04Direct 1 0.00 0.00 0.00 0.00 0.02 0.01 0.61 0.05 0.94 0.03Direct 2 0.00 0.00 0.00 0.00 0.02 0.01 0.63 0.04 0.97 0.02


For the 25° right adaptation condition, t-test comparisons showedthe corresponding opposite pattern, with significant increase indirect responses for 5° right, 5° t(23) " 10.80, and 10° right gaze,t(23) " 13.98, ps ! .0001; a decrease for 5° left, t(23) " #3.90,p ! .01; and no significant effect for 10° left, t(23) " #2.01, p ".057, or direct gaze (t ! 1).

Additional t tests of left and right responses were conducted todetermine whether the reduction in direct responses for 5° rightgaze following left gaze adaptation and 5° left following right gazeadaptation reflected increased correct categorization (i.e., in-creased right and left responses, respectively) as opposed to ran-dom response selection; t tests of left and right responses (seeTable 1) confirmed the former, showing significant or borderlineeffects that mirrored the patterns shown for direct responses—25°left adaptation, right responses for 5° right, t(23) " 2.31, p " .03;25° right adaptation, left responses for 5° left, t(23) " 3.66,p ! .01.

In summary, 25° adaptation produced a marked increase indirect responses to 5° and 10° gaze on the adapted side, togetherwith some evidence of decreased direct responses to 5° gaze on theopposite side, and no significant change in participants’ categori-zation of direct gaze.

10° adaptation. Performance on the 10° adaptation and base-line conditions was compared with a three-factor ANOVA identi-cal to that described for the 25° adaptation conditions. There wasa significant main effect of gaze direction, F(4, 88) " 423.85, p !.0001, %p

2 " .95, qualified by an Adaptation $ Gaze Directioninteraction, F(5.1, 112.1) " 56.49, p ! .0001, %p

2 " .72, but nomain effect of adaptation (F ! 1); experiment version, F(1, 22) "1.91, p & .1; or significant interactions with experiment version( ps & .1). Once again, t-test comparisons with Bonferonni correc-tion ( p ! .01 cutoff) were used to explore the Adaptation $ GazeDirection interaction. Comparing each gaze direction in the 10°left adaptation condition with its corresponding average baselineperformance showed a significant increase in direct responses for5° left, t(23) " 6.27, p ! .0001, but not 10° left gaze probes (t !1); a significant decrease in direct responses for 5° right, 5° t(23)" #8.49, and 10° right gaze, t(23) " #3.57, ps ! .005; and noeffect for direct gaze (t ! 1). The 10° right adaptation conditionshowed a corresponding opposite pattern, with a significant in-crease in direct responses for right gaze, 5° right, t(23) " 6.27, 10°right, t(23) " 3.75, ps ! .005; a decrease for left gaze, 5° left, t(23)" #6.88, 10° left, t(23) " #3.57, ps ! .01; and a similarnonsignificant trend for direct gaze, t(23) " #2.69, p " .013.

Additional t tests of left and right responses demonstrated thatthe reduction in direct responses for 5° and 10° right gaze follow-ing left gaze adaptation and for 5° and 10° left following right gazeadaptation reflected increased correct categorization (i.e., in-creased right and left responses, respectively) as opposed to ran-dom response selection—10° left adaptation, right responses for 5°right, t(23) " 7.71, 10° right, t(23) " 3.63; 10° right adaptation,left responses for 5° left, t(23) " 6.93, 10° left, t(23) " 3.60,ps ! .005.

In summary, adaptation to 10° gaze produced a marked signif-icant increase in direct responses to 5° gaze probes on the adaptedside and a similar nonsignificant trend for 10° probes. In addition,there was a significant decrease in direct responses to 5° probes onthe nonadapted side and a similar, although less marked, decreasefor nonadapted-side 10° probes. Right adaptation also produced a

significant decrease in direct responses to direct gaze probes (i.e.,increased tendency to categorize direct gaze as left; see Table 1),whereas there was no corresponding effect for left gaze adaptation.

A comparison of 25° and 10° adaptation. To determinewhether adaptation to 25° and 10° gaze produced statisticallydifferent patterns, the data from these conditions were submitted toa four-factor ANOVA investigating adaptation angle (25° and 10°;repeated measure), adaptation direction (left and right; repeatedmeasure), gaze direction (10° left, 5° left, 0°, 5° right, and 10°right; repeated measure) and experiment version (original andmirror-image format; between-subjects). This showed a significantthree-way Adaptation Angle $ Adaptation Direction $ GazeDirection interaction, F(4, 88) " 25.81, p ! .0001, %p

2 " .54,confirming that the 25° and 10° conditions produced differentpatterns. For the five gaze levels of the 25° and 10° left adaptationconditions, t-test comparisons (cutoff p ! .01) showed that 25° leftproduced a greater increase in direct responses for 5° left, t(23) "8.04, and 10° left gaze probes, 10° left t(23) " 6.97, ps ! .0001,whereas 10° left adaptation produced a greater decrease in directresponses for 5° right, t(23) " 3.54, and 10° right gaze probes,t(23) " 2.82, ps ! .01. For direct gaze probes, 10° left adaptationshowed a trend toward fewer direct responses relative to 25° leftadaptation, t(23) " 2.26, p " .034.

A breakdown of adaptation to 25° and 10° rightward gazeshowed a similar but opposite pattern, such that 25° right produceda greater increase in direct responses for 5° right, t(23) " 7.56; and10° right gaze probes, t(23) " 10.88, ps ! .0001, whereas 10° rightadaptation produced a trend toward a greater decrease in directresponses for 5° left gaze probes, t(23) " 2.05, p " .052, but not 10°left probes (t ! 1); direct gaze showed a nonsignificant reduction indirect responses for 10° right adaptation, t(23) " 2.01, p " .052.

Consistent with the predictions of multichannel coding, thecomparison of adaptation with 25° and 10° showed that the formerproduced an increased tendency to perceive averted gaze on theadapted side (e.g., left side, following adaptation to left gaze) asdirect relative to 10° adaptation. In addition, and again consistentwith multichannel coding, adaptation to 10° gaze produced areduced tendency to perceive averted gaze on the nonadapted side(e.g., right side, following adaptation to left gaze) as direct relativeto 25° adaptation. This pattern cannot be accommodated by oppo-nent coding, and so, the comparison of the 25° and 10° adaptationconditions supports the multichannel model.

Asymmetry of gaze perception. Finally, exploration of the av-erage baseline data revealed an asymmetry in participants’ detec-tion of left and right gaze, with an increased tendency to mistake5° right gaze as direct compared with 5° left gaze, t(23) " 3.07.p ! .005, but no effect for the 10° angles (t ! 1; cutoff p ! .025,corrected for two comparisons). Consistent with the asymmetry,direct gaze was more likely to be misidentified as left than rightgaze, t(23) " 3.65, p ! .001, and showed increased susceptibilityto right than left gaze adaptation for the 10° adaptation condition(change in direct responses relative to baseline for right 10°adaptation vs. left 10° adaptation), t(23) " 2.23, p ! .05, and asimilar nonsignificant trend for 25° adaptation, t(23) " 2.03, p ".054. As there was no main effect of experiment version, thispattern could not reflect an asymmetry in the stimuli themselves.The significance of this finding is considered in the discussion.

253EYE GAZE

Discussion

As outlined earlier, opponent coding predicts no change inperceived gaze direction following direct gaze adaptation, whereasmultichannel coding predicts a decreased tendency to categorizesmall angles of left and right gaze as direct (i.e., increased correctcategorization of left and right gaze; see Figures 1 and 2). Thelatter pattern was confirmed for 5° left and right gaze probes, anda similar but less marked effect was found for the 10° probes. Ananalogous effect has been observed for adaptation of orientation,which is also thought to be coded by a multichannel system,whereby adaptation to a vertical stimulus causes left- and right-oriented stimuli on either side of vertical to appear more extreme(Clifford, Wyatt, Arnold, Smith, & Wenderoth, 2001; Kohler &Wallach, 1944; Regan & Beverley, 1985). In contrast, adaptationto the central tendency of opponent-coded dimensions, such ascolor (Webster, 1996), aspect ratio (Suzuki, 2005), and facialidentity (or facial configurations; Leopold et al., 2001; Webster &MacLin, 1999), has little or no effect on their perception.

The results of the two averted gaze adaptation conditions (i.e.,10° and 25°) were also in accord with a multichannel model, asillustrated in Figure 1. Thus, a comparison of adaptation to 25°relative to 10° gaze showed that the former produced a greaterincrease in direct responses to adapted-side gaze probes and asmaller reduction in direct responses to nonadapted-side probes. Incontrast, opponent coding predicts that 25° and 10° gaze wouldproduce equal adaptation effects or that 25° gaze adaptation shouldproduce a more marked reduction and more marked enhancementof adapted-side and nonadapted-side gaze, respectively.

An unexpected, but additional interesting finding was that partici-pants showed an asymmetry in their gaze discrimination, with moreaccurate categorization of left than right gaze for the average baselinedata (see Figure 4a). Consistent with this, direct gaze showed anincreased tendency to be incorrectly categorized as left rather thanright gaze and showed an increased susceptibility to right rather thanleft gaze adaptation. This could not be explained by any asymmetry inthe stimuli themselves because both original and mirror-reversedimages showed statistically indistinguishable patterns. We suggestthat the asymmetry reflects a small discrepancy between the actual(i.e., physical) and perceived gaze direction, such that participants’perception is shifted slightly to the left, with small angles of rightwardgaze being more likely to be perceived as direct than small angles ofleftward gaze and direct gaze showing an increased tendency to bemistaken for left rather than right gaze. This discrepancy is analogousto the small but significant leftward attentional bias observed inhealthy participants on line bisection and similar spatial tasks (Chok-ron, 2002; Failla, Sheppard, & Bradshaw, 2003; McCourt, Freeman,Tahmahkera-Stevens, & Chaussee, 2001). The observed counterpartof this attentional effect in gaze perception accords with the proposalthat attentional mechanisms comprise part of an extended systeminvolved in gaze perception (Haxby, Hoffman, & Gobbini, 2000).

Experiment 2

In Experiment 2, we sought further evidence for multichannelcoding using a simultaneous adaptation procedure in which par-ticipants adapted to an alternating sequence of 25° left and 25°gaze, resulting in equivalent attenuation of both left and rightchannels. A similar procedure has been used in previous adaptation

research to identify separate mechanisms (or opponent-codingsystems) representing different stimulus dimensions, includingupright and inverted faces (Rhodes et al., 2004) and Chinese andCaucasian faces (Jaquet, Rhodes, & Hayward, in press). In con-trast, if upright and inverted faces, for example, were coded by thesame opponent-coding system, then adaptation to each wouldcancel out, resulting in no overall effect of adaptation. Followinga similar logic, if left and right gaze are coded by independentchannels of a multichannel system, then simultaneous adaptationof 25° left and 25° right gaze should adapt both respective chan-nels but have a minimal or no effect on the direct gaze channel.This should result in an increased tendency to perceive both leftand right gaze probes as direct (see Figure 1e). However, if gazeis coded by a single (left–right) opponent-coding system, then thesimultaneous adaptation should adapt both left and right channelsby an equivalent amount, producing no overall change in thecrossover point between the two channels and, hence, no change inperception of any gaze angle (see Figure 2e). In short, the mul-tichannel system predicts an increased tendency to categorize leftand right gaze as direct (see Figure 1e), whereas the opponent-coded system predicts no change in the perceived direction of anygaze angle (see Figure 2e). On the basis of Experiment 1, weexpected that Experiment 2 would provide additional support formultichannel coding of gaze direction.

To further address the asymmetry in participants’ gaze percep-tion observed in Experiment 1, a set of images in which the leftgaze faces were mirror images of their right gaze counterparts wasused with all participants. The use of physically identical left andright gaze stimuli with every participant provided a stronger test ofany asymmetry.

Method

Participants. Eighteen volunteers (13 female; M age " 22.37years, SD " 2.34; range, 17–26 years) with normal or corrected-to-normal vision were recruited from the MRC Cognition and BrainSciences Unit volunteer panel and were paid for participating.

Materials. The probe faces were prepared from the 5° and 10°right and 0° gaze images used in Experiment 1. The 5° and 10°images were mirror-reversed to provide the left gaze probes.Similarly, the 25° right gaze adaptation faces from Experiment 1were mirror-reversed to produce 25° left gaze adaptation stimuli.As in Experiment 1, the adapting faces were 75% of the size ofprobe faces.

Design and procedure. The adaptation experiment comprisedthree blocks—an initial baseline to assess participants’ gaze discrim-ination prior to adaptation that was repeated at the end of the exper-iment and a single adaptation block in which participants adapted toan alternating sequence of 25° left and 25° right gaze. The format ofthe baseline block (i.e., number of trials and presentation duration)was identical to Experiment 1, hence, only the adaptation phase isdescribed and illustrated in Figure 5.

Adaptation block. The adaptation block contained two sec-tions (see Figure 5). Section 1 comprised an alternating sequenceof 25° left and 25° right gazing faces (30 of each). Each face waspresented for 4,000 ms, followed by a 200-ms interstimulus inter-val (ISI). Consecutive faces never had the same identity, and the200-ms ISI was included to further ensure that each switch be-tween left and right gaze did not induce any apparent eye move-


ment. Participants were instructed to look at each face, and noresponse was required. Section 2 contained the same probe faces asthe baseline block (10 models $ 5 gaze directions [10° left, 5° left,0°, 5° right, and 10° right]; 50 stimuli in total); however, eachprobe was preceded by a top-up adaptation sequence of alternating25° left and 25° right gaze faces (three of each; see Figure 5). Onhalf of the trials, the top-up sequence ended with a 25° left gazeface (i.e., LRLRLRL) and, on the other half, with a 25° right gazeface (i.e., RLRLRLR). Each of the six top-up faces was presentedfor 1,333 ms, followed by a 200-ms blank ISI, and the final top-upface in each trial was followed by a 500-ms presentation of a probeface and then a 1,500-ms blank ITI. The probe was clearly iden-tified with the label “RESPOND” printed above and below the

face, and participants were required to categorize its gaze directionas left, direct, or right. On each trial, the top-up adaptation se-quence contained one male and one female identity selected fromthe 10 models (one displaying 25° left gaze, the other 25° right),and the probe face was always a different identity and a differentsize from the adaptation faces.

The adaptation block was followed by a second baseline blockthat was identical to the first.

Results

Data are summarized as participants’ mean number of directresponses; hence, any adaptation of left and right gaze (i.e., 5° and

Figure 5. Trial events and example stimuli from the adaptation blocks of Experiment 2. Section 1 of theadaptation block comprised a series of alternating face displaying 25° left and 25° right gaze. In Section 2, eachprobe stimulus was preceded by a top-up adaptation sequence of the same left and right gaze adapting stimuli.Probe faces in Section 2 were identified with the label “RESPOND” printed above and below the face. Thebaseline gaze acuity task at the beginning and end of the experiment was identical to that in Experiment 1 (seeFigure 3). ITI " intertrial interval; L " left; R " right.

255EYE GAZE

10°) is measured as increased direct responses for these gazeangles (see Figure 6). A full summary of left, direct, and rightresponses is shown in the Table 2. Prior to analysis the data werearcsin-transformed for the same reasons outlined in Experiment 1.The patterns of results were identical to those found using non-transformed, data and all principal effects were also found usingnonparametric Wilcoxon signed ranks tests corrected for multiplecomparisons. Participants’ performance in the first and secondbaseline blocks from the beginning and end of the experiment issummarized in Figure 6a. Performance on the two baselines wascompared with a two-factor repeated measures ANOVA compar-ing baseline (first and second) and gaze direction (10° left, 5° left,0°, 5° right, and 10° right). The results showed a main effect ofgaze direction, F(4, 68) " 119.27, p ! .0001, %p

2 " .88, reflectingmore accurate categorization of direct (88%) and 10° gaze (92%)than 5° gaze (56%). There was also a borderline main effect ofbaseline, F(1, 17) " 4.25, p " .055, %p

2 " .20, due to a smalloverall increase in direct responses for the second baseline block,suggesting that some residual adaptation carried over from theprevious adaptation block. As there was no Baseline $ GazeDirection interaction, F(4, 68) " 1.08, p & .3, the remaining

analyses compared adaptation with the average of both baselineconditions.

To test for an adaptation effect (indexed as increased directresponses), we compared performance on Section 2 of the left–right adaptation condition with performance on the average base-line condition using a two-way repeated-measures ANOVA inves-tigating adaptation (baseline and left–right adaptation) and gazedirection. The results showed a main effect of adaptation, F(1, 17)" 109.85, p ! .0001, %p

2 " .87, reflecting an overall increase indirect responses following adaptation, and a main effect of gazedirection, F(2.4, 40.7) " 133.00, p ! .0001, %p

2 " .89. These werequalified by an Adaptation $ Gaze Direction interaction, F(4, 68)" 4.26, p ! .01, %p

2 " .20. To investigate the interaction further,difference scores were calculated for each gaze angle by subtract-ing the number of direct responses in the average baseline condi-tion from those in the adaptation condition for each participant.Paired-sample t tests showed that difference scores for 10° left and10° right did not differ (t ! 1), nor did 5° left and 5° right (t ! 1);hence, the difference scores were pooled across left and right togive two averted gaze conditions (10° and 5°). A comparison ofthe difference scores for 10°, 5° and direct gaze (corrected for three

Figure 6. From Experiment 2, participants’ mean number of direct responses with 95% confidence intervals.a: Data for the first and second baseline blocks. b: Discrimination of gaze probes following adaptation toalternating 25° left and 25° right gaze faces; average baseline data are also shown. c: Data from selected trialsin which the final face of the top-up adaptation sequence showed leftward gaze (Final L) and rightward gaze(Final R); average baseline data are also shown. L10 " 10° left; L05 " 5° left; S00 " direct gaze; R05 " 5°right; R10 " 10° right.


comparisons; cutoff p ! .017) showed that 5° showed the greatestadaptation effect—that is, greatest increase in direct responses: 5°versus 10°, t(17) " 3.17; 5° versus direct, t(17) " 6.11, ps !.01—followed by 10°—10° versus direct, t(17) " 2.45, p " .026.Adaptation also produced an increase in direct responses for directgaze, one-sample t test, t(17) " 4.31, p ! .0001.

The top-up adaptation sequence ended with 25° left or 25° rightgaze on equal numbers of trials. Hence, it was important to excludethat the observed adaptation effects were driven by the finaltop-face alone. In other words, it is possible that only left adapta-tion or only right adaptation was found for the final left and finalright gaze top-up trials, respectively, but averaging across bothtrial types masked this selectivity. To investigate this, we split thedata into final left and final right trials (see Figure 6c) andcompared the proportion of direct responses for each with theproportion for the average baseline condition in the two-wayrepeated measures ANOVA investigating adaptation (baseline,final left adaptation, and final right adaptation) and gaze direction(10° left, 5° left, 0°, 5° right, and 10° right). The results showedsignificant main effects of adaptation, F(2, 34) " 70.84, p !.0001, %p

2 " .81, and gaze direction, F(2.7, 46.4) " 134.84, p !.0001, %p

2 " .88, qualified by a significant Adaptation $ GazeDirection interaction, F(8, 136) " 4.27, p ! .0001, %p

2 " .20.Critically, post hoc t tests (cutoff p ! .01) showed that both finalleft and final right trials showed significant adaptation for both leftand right gaze probes relative to baseline (all ps ! .005 unlessstated): final left—10° left, t(17) " 4.84; 5° left, t(17) " 6.22; 0°,t(17) " 3.90; 5° right, t(17) " 5.79; 10° right, t(17) " 3.60; finalright—10° left, t(17) " 2.59, p " .019; 5° left, t(17) " 4.71; 0°,t(17) " 4.09; 5° right, t(17) " 12.11; 10° right, t(17) " 2.70, p ".016.

Further inspection of the data showed that the final face in thetop-up sequence had some effect because the final right adaptation

trials produced increased direct responses for 5° right probesrelative to the final left adaptation trials, t(17) " #3.85, p ! .001(10° right, t ! 1), whereas the opposite, nonsignificant trend wasfound for the final left adaptation trials for left gaze, 5° left, t(17)" 1.71, p " .11; 10° left, t(17) " 2.30, p " .034.

As noted earlier, the participants showed a slight overall in-crease in direct responses in the second baseline relative to thefirst. Consequently, we also tested whether the adaptation effectsremained robust in relation to the second baseline. A two-wayANOVA showed the same pattern observed using the averagebaseline, with a significant effect of adaptation (baseline 2, left–right adaptation), F(1, 17) " 109.91, p ! .0001, %p

2 " .86, andgaze direction, F(2.4, 41.5) " 117.20, p ! .0001, %p

2 " .87, and anAdaptation $ Gaze Direction interaction, F(4, 68) " 2.82, p !.05, %p

2 " .14. For the four averted gaze conditions, t-test compar-isons (cutoff p ! .01) showed significant effects of adaptation (i.e.,increased direct responses), 10° left, t(17) " 5.23; 5° left, t(17) "5.42; 5° right, t(17) " 6.48; 10° right, t(17) " 4.57; all ps ! .0001,and a nonsignificant increase for direct gaze, t(17) " 2.29, p ".035.

Asymmetry of gaze perception. Consistent with Experiment 1,exploration of the average baseline data revealed an asymmetry inparticipants’ detection of left and right gaze, with an increasedtendency to mistake 5° right gaze as direct compared with 5° leftgaze, t(23) " 2.78. p " .013, and a similar nonsignificant trend forthe 10° angles, t(23) " 2.03. p " .058 (cutoff p ! .025, correctedfor two comparisons).

Discussion

Simultaneous adaptation to 25° left and 25° right gaze produceincreased direct responses to both 5° and 10° left and right probesrelative to baseline performance. Once again, the results support

Table 2Experiment 2: Mean Proportion of Left, Direct, and Right Responses to the Five Probe Gaze Directions (10° Left, 5° Left, 0°,5° Right, and 10° Right) in the Baseline and Adaptation (25° Left, 25° Right) Conditions

Response type bycondition

10° left 5° left 0° (direct) 5° right 10° right

M SE M SE M SE M SE M SE

Left responsesBaseline 1 0.96 0.01 0.68 0.05 0.09 0.02 0.01 0.01 0.01 0.01Baseline 2 0.93 0.03 0.60 0.05 0.06 0.02 0.01 0.01 0.01 0.01Average baseline 0.95 0.02 0.64 0.04 0.07 0.02 0.01 0.01 0.01 0.00Adaptation: final right 0.41 0.03 0.18 0.03 0.01 0.01 0.00 0.00 0.00 0.00Adaptation: final left 0.37 0.03 0.13 0.03 0.02 0.01 0.00 0.00 0.00 0.00Adaptation: right-left 0.77 0.05 0.31 0.05 0.03 0.01 0.00 0.00 0.00 0.00

Direct responsesBaseline 1 0.04 0.01 0.31 0.05 0.86 0.03 0.43 0.05 0.07 0.03Baseline 2 0.07 0.03 0.39 0.05 0.89 0.02 0.58 0.05 0.15 0.05Average baseline 0.05 0.02 0.35 0.04 0.88 0.02 0.51 0.05 0.11 0.03Adaptation: final right 0.19 0.06 0.63 0.06 0.97 0.02 0.92 0.02 0.31 0.07Adaptation: final left 0.27 0.05 0.73 0.05 0.93 0.03 0.77 0.05 0.33 0.06Adaptation: right-left 0.23 0.05 0.68 0.05 0.95 0.01 0.84 0.03 0.32 0.05

Right responsesBaseline 1 0.00 0.00 0.01 0.01 0.05 0.02 0.56 0.05 0.92 0.02Baseline 2 0.00 0.00 0.01 0.01 0.06 0.02 0.41 0.05 0.84 0.05Average baseline 0.00 0.00 0.01 0.00 0.05 0.01 0.49 0.05 0.88 0.03Adaptation: final left 0.00 0.00 0.01 0.01 0.01 0.01 0.04 0.01 0.34 0.03Adaptation: final right 0.00 0.00 0.01 0.01 0.01 0.01 0.12 0.03 0.33 0.03Adaptation: left-right 0.00 0.00 0.01 0.01 0.02 0.01 0.16 0.03 0.68 0.05

257EYE GAZE

the predictions of a multichannel model rather than left–rightopponent coding, which would have predicted no change in par-ticipants’ perception of the probes. As we have also shown, thiseffect cannot be accounted for by adaptation from the final imagein each top-up sequence alone, although it did have a smallsignificant influence for the final right, but not final left, adaptationtrials. Again, this reflects an asymmetry in gaze perception, shownhere as increased susceptibility of right gaze probes to right gazeadaptation.

It is of interest that simultaneous adaptation also produced anincrease in direct responses to direct gaze probes. However, this isconsistent with the relative reduction in responsiveness of the leftand right gaze channels of a three-channel system following left–right adaptation. In other words, participants are less likely toreport direct gaze (correctly or falsely) as averted because thechannels signaling averted gaze have been attenuated. By contrast,opponent coding would predict no change in direct responses todirect gaze.

Finally, consistent with Experiment 1, Experiment 2 found anasymmetry in participants’ overall perception of gaze direction,with improved categorization of 5° left relative to 5° right probes.Given that the left and right gaze stimuli were physically identicalfor all participants, this provides a stronger demonstration of anasymmetry in gaze perception.

General Discussion

We investigated three distinct predictions of multichannel andopponent-coding models of gaze perception. In each case, the dataprovided clear support for a multichannel model. Our resultsprovide the first demonstration that the visual representation of eyegaze is coded by a distinct perceptual framework to facial identity,which is represented by an opponent-coding system (Leopold etal., 2001; Rhodes & Jeffery, 2006; Rhodes et al., 2005; Robbins etal., 2007; Tsao & Freiwald, 2006).

Our findings can be summarized as follows. First, adaptation todirect gaze produced a significant aftereffect, reflected as reducedtendency to categorize left and right gaze probes as direct (i.e.,increased tendency to categorize them as their respective gazedirections); opponent coding predicts no effect of adaptation. Sec-ond, adaptation to more and less extreme angles of averted gaze(i.e., 25° and 10° left or right) resulted in different effects, with 25°left (or right) producing more adaptation of adapted-side gazeprobes (reflected as a greater increase in direct responses) and lessadaptation of nonadapted-side gaze probes (reflected as a smallerdecrease in direct responses/smaller increase in correct left or rightresponses); opponent coding predicts either equal effects of theadapted and nonadapted sides for the 10° and 25° conditions orgreater effects on both sides for the 25° condition. Third, simul-taneous adaptation of both left and right gaze directions producedsignificant adaptation of gaze perception reflected as increaseddirect responses to both left and right gaze probes; no change ingaze perception is predicted by an opponent-coding system. Fi-nally, our data demonstrate an asymmetry in gaze perception, withleft gaze less often categorized as direct than right gaze. Wesuggest that this reflects a discrepancy between actual and per-ceived gaze direction, with participants’ perception of all gazeangles shifted slightly to the left.

Differences With Other Forms of Face Adaptation

Other facial cues showing adaptation have included facial iden-tity (Leopold et al., 2001; Rhodes et al., 2005), configural facialfeatures (e.g., relative eye positions; Robbins et al., 2007; Webster& MacLin, 1999), and sex (Webster, Kaping, Mizokami, & Du-hamel, 2004). These effects have been discussed in terms of anopponent-coding framework (Leopold et al., 2001; Rhodes &Jeffery, 2006; Rhodes et al., 2005; Robbins et al., 2007; Tsao &Freiwald, 2006) in which faces are coded in a multidimensionalspace, with each dimension constituting a separate opponent-codedmechanism. Indeed, some researchers have gone further to suggestthat the data provide support for an opponent-coding system inwhich the central tendency of the dimensions constitutes a norm oraverage face relative to which all faces are coded (Leopold et al.,2001; Rhodes & Jeffery, 2006; Rhodes et al., 2005; Robbins et al.,2007; Tsao & Freiwald, 2006). Thus, each face is coded as a vectorrepresenting its distance and direction of deviation from the norm.

Consistent with the idea of opponent coding, face adaptationstudies have shown that adaptation to the central tendency (anaverage or undistorted face) has minimal effect on face perception(Leopold et al., 2001; Webster & MacLin, 1999). In contrast andconsistent with a multichannel mode of representation, Experiment1 showed that adaptation to direct gaze, which could be regardedas the central tendency of different gaze directions, had a signifi-cant effect on gaze perception, producing a decreased tendency tocategorize small angles of leftward and rightward gaze as direct(i.e., increased tendency to categorize them as left and right,respectively). Moreover, this pattern was found in both levels ofthe experiment version condition in which the images were shownin their original and mirror-image format (see Figure 4d), provid-ing a replication of the effect across two conditions in the exper-iment. Similarly, the results of adaptation to 25° and 10° gaze werealso consistent with multichannel coding, in that 25° adaptorsproduced more adaptation of adapted-side gaze (i.e., a greaterincrease in direct responses) and less adaptation of nonadapted-side gaze (i.e., a smaller decrease in direct responses) relative tothe 10° adaptors. Opponent coding is unable to accommodate thesesorts of asymmetric effects. In other words, if 25° adaptors pro-duce more adaptation of adapted-side gaze than 10° adaptors, then,contrary to our current findings, opponent coding would predictthat the 25° condition must also produce a greater effect on thenonadapted side.

Experiment 2 used simultaneous adaptation of left and rightgaze as a second method of demonstrating multichannel coding ofgaze direction. A similar technique has been applied to adaptationof configural facial cues using distorted faces (i.e., faces in whichthe features are contracted toward, or expanded away from, thecenter of the face), but in these cases, it was used to demonstrateseparable coding of different facial categories, such as upright andinverted faces (Rhodes et al., 2004) or Chinese and Caucasianfaces (Jaquet et al., in press; see also Little, DeBruine, & Jones,2005). For example, simultaneous adaptation to expanded Cauca-sian faces and contracted Chinese faces caused subsequentlyviewed undistorted Caucasian and Chinese faces to appear con-tracted and expanded, respectively (Jaquet et al., in press). Thisdemonstrates separate mechanisms, or separate dimensions, cod-ing each race. In contrast, had the expanded and contracted facialstimuli been coded by the same opponent-coded system, then the


effects would cancel out, producing no significant aftereffect, asshown by Jeffery, Rhodes, and Busey (in press) for the adaptationof view-specific representations of faces.

In Experiment 2, simultaneous adaptation was used to demon-strate separate mechanisms, or channels, coding left, direct, andright gaze. Following the logic outlined above, if different gazedirections are coded by a single opponent-coded system with twochannels for left and right gaze, then simultaneous adaptation ofleft and right gaze would cancel out, leaving no significant after-effect (see Figure 2). However, consistent with multichannel cod-ing, we found that the simultaneous adaptation procedure produceda symmetric aftereffect for left and right gaze probes, with eachshowing an increased tendency to be categorized as direct gaze.

One of the reviewers suggested that an alternative interpretationof the direct gaze adaptation is that the direct gaze adaptors serveto remind participants of what direct gaze looks like and so reducethe likelihood of categorizing small angles of left and right gaze asdirect. In which case, the reviewer suggested that the results of thismanipulation might not be inconsistent with opponent coding. Weagree that it is difficult to exclude that this may contribute to thedirect gaze adaptation effect. However, similar effects are notobserved when participants adapt to the central tendency of otheropponent-coded dimensions, such as aspect ratio (Suzuki, 2005)and color (Webster, 1996). More crucially, the comparison ofadaptation to 10° and 25° gaze (Experiment 1) and the simulta-neous adaptation of left and right gaze (Experiment 2) cannot beaccommodated within an opponent-coding system. Taken to-gether, then, the results of both experiments clearly support mul-tichannel coding of gaze direction.

Comparisons With Single-Cell Recordings

In the introduction, we discussed how the limited data availablefrom single-cell recording studies of gaze perception in monkeysprovide little indication of whether gaze is multichannel or oppo-nent coded. Thus, our study provides the first demonstration ofmultichannel coding of gaze direction in both human and nonhu-man primates.

Head orientation has been investigated more extensively thangaze, and the existence of separate cell populations coding differ-ent head directions (Hasselmo, Rolls, Baylis, & Nalwa, 1989;Perrett et al., 1989, 1991; Perrett et al., 1985) suggests that it is alsomultichannel coded. However, before drawing analogies betweenthese different areas, it is important to note that different types ofhead-orientation cells have been identified. Some are maximallyresponsive to a particular view of one or a limited number ofidentities. These cells are thought to code view-centered represen-tations of a particular facial configuration and to contribute to faceidentification rather than discrimination of head orientation (Per-rett et al., 1989), so it is important to make this distinction. Notealso that while some cells are responsive to gaze or head orienta-tion alone, a large proportion respond to the same direction sig-naled by either gaze, heads, or even body orientation (Perrett,Hietanen, Oram, & Benson, 1992). In addition, the response ofthese cells is attenuated when the gaze is incongruent with thepreferred head direction (Perrett et al., 1985, 1992). If the adap-tation effects we have found operate at the level of cells sensitiveto gaze and head oriented in the same direction, then we wouldexpect that gaze discrimination should be affected to an equivalent

extent by adapting to either gaze or heads (with the gaze masked)oriented in the same direction. However, in as yet unpublishedwork (Jenkins, Keane, & Calder, 2007), we have not found thispattern, and gaze adaptation effects appear to occur at a gaze-specific level of coding (i.e., cells coding gaze alone). This sug-gests that our current results reflect adaptation of cells sensitive tothe visual representation of gaze alone.

Are Three Channels Sufficient?

Our predictions for a multichannel system have been illustratedin the context of a three-channel system, with a single channel foreach of left, direct, and right gaze. This form of broad tuning hasa basis in single-cell recording studies in monkeys investigatingthe coding of head orientation (Perrett et al., 1985, 1991). For themajority of cells, a discrepancy of 45° to 60° from the angle ofpreferred view is required to reduce the firing rate to half thedifference between the response to the most and least preferredviews, although for some cells, this extends up to 125° (Perrett etal., 1991).

The breadth of tuning of gaze cells has not been addressed andis difficult to extrapolate from the head-orientation data, not leastbecause gaze has a more restricted range than head orientations,which include both front and back views of the head. Although ourpresent study did not specifically address the number of channelscoding gaze direction, our results are compatible with a three-channel system coding left, direct, and right gaze. This followsbecause, despite the 25° gaze adaptors being close to the maximumpossible averted angle, adapting to this stimulus produced a greaterchange in the perception of 5° and 10° gaze probes on the adaptedside than adapting to 10° gaze (Experiment 1). This suggests oneof two possibilities: (a) There is only one channel for each of leftand right gaze, and 25° gaze engages each channel more than 10°gaze (see Figure 1), an interpretation that accords with the generalprinciple that neurons are usually (though not always) moststrongly adapted by the stimuli to which they most strongly re-spond (Crowder et al., 2006). (b) Alternatively, there are multiplechannels for left and right gaze, but a discrepancy of approxi-mately 15° to 20° between the adapting and probe stimuli (thedistance between 25° adaptors and 10°/5° probes on the adaptedside) produces enhanced adaptation. However, the latter is lesslikely when we consider that although a 15° discrepancy applied tothe 10° adaptors and 5° nonadapted-side probes, the 10° adaptorsaltered the perception of 5° probes on the adapted and nonadaptedsides by the same amount (t ! 1), although in different directions.To this extent, our data are consistent with the proposal that thereis one left and one right channel coding gaze averted by up to 25°,although more detailed studies would be required to confirm this,and we do not wish to argue for a three-channel system on thebasis of these data alone.

It is interesting to compare our results with Fang and He’s(2005) investigation of adaptation of different head orientations.Although these authors did not explicitly address whether headorientation is opponent or multichannel coded, their data favor thelatter because small angles of head-orientation probes (3° and 6°)were adapted by 30° but not 60° head adaptors. This suggests thatleft and right head orientations are each coded by more than onechannel because otherwise, the 60° stimuli would have producedsome adaptation. Intuitively, this makes good sense because, un-

259EYE GAZE

like gaze, heads can rotate by 360°, and so, a three-channel systemwould require each channel to be very broadly tuned, makingdiscrimination of differences in head orientation correspondinglypoor. However, it is important to add that Fang and He (2005)were investigating adaptation of view-specific representations offacial identity (i.e., the representation of different views of thesame identity) and consequently used the same facial identity astheir adapting and probe stimuli. Hence, it remains to be deter-mined whether the neural coding of identity-invariant head-orientation representations shows similar effects. This would re-quire additional experiments using different identities as theadapting and probe faces.

Asymmetry in Gaze Perception

Both studies observed an asymmetry in gaze perception,whereby participants showed less accurate categorization of rightrelative to left gaze and an increased tendency to categorize directgaze as left than right. In addition, both experiments showedevidence of increased susceptibility to right gaze adaptation ratherthan left gaze adaptation. The data suggest a discrepancy betweenactual and perceived gaze direction, with participants’ perceptionshifted slightly to the left. As discussed, a similar leftward bias orpseudoneglect has been observed for spatial attention tasks (Chok-ron, 2002; Failla et al., 2003; McCourt et al., 2001), where healthyvolunteers demonstrate a slight tendency to neglect the right halfof space. An interesting question is whether the gaze bias iscorrelated with its spatial counterpart. Alternatively, given evi-dence suggesting that spatial cuing by gaze and other directionalcues tap different attentional mechanisms (Kingstone, Friesen, &Gazzaniga, 2000; Vuilleumier, 2002), the leftward bias for gazeand nongaze cues may be independent.

In conclusion, our study provides the first demonstration that thevisual representation of gaze direction is coded by a multichannelsystem with separate channels coding left, direct, and right gaze.Although we have not explicitly tested the number of left and rightchannels, our results are compatible with the existence of onechannel for each of left, direct, and right gaze. Our study alsoemphasizes the functional dissociation between different compo-nents of face perception, specifically, eye gaze and facial identity(Haxby et al., 2000). Previous studies have argued that facialidentity is opponent coded, whereas the present experiments dem-onstrate that gaze direction is coded by a multichannel system.Finally, we have also demonstrated an asymmetry in gaze discrim-ination, such that participants’ perception of gaze direction isshifted slightly to the left of its actual (physical) position. A similarleftward bias has been demonstrated in healthy volunteers onspatial attention tasks, and this accords with the proposal thatattentional mechanisms form part of an extended system support-ing visual discrimination of gaze direction (Haxby et al., 2000).Together with other recent research, our study demonstrates theutility of adaptation techniques for investigating the functionalbasis of different aspects of face perception.

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Received May 29, 2007Revision received August 17, 2007

Accepted August 20, 2007 !

Correction to Duncan et al. (2008)

In the article, “Goal Neglect and Spearman’s g: Competing Parts of a Complex Task,” by JohnDuncan, Alice Parr, Alexandra Woolgar, Russell Thompson, Peter Bright, Sally Cox, Sonia Bishop,and Ian Nimmo-Smith (Journal of Experimental Psychology: General, 2008, Vol. 137, No. 1, p.131), the DOI for the supplemental materials was printed incorrectly. The correct DOI is as follows:http://dx.doi.org/10.1037/0096-3445.137.1.131.supp

DOI: 10.1037/0096-3445.137.2.261

261EYE GAZE

visual representation of eye gaze is coded by a nonopponent multichannel system

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