gaze direction modulates face recognition in a developmental study

Developmental Science 9:5 (2006), pp 465– 472

REPORT Blackwell Publishing Ltd

Eye remember you two: gaze direction modulates face recognition in a developmental study Alastair D. Smith, Bruce M. Hood and Karen Hector Department of Experimental Psychology, University of Bristol, UK

Abstract The effects of gaze direction on memory for faces were studied in children from three different age groups (6–7, 8–9, and 10– 11 years old) using a computerized version of a task devised by Hood, Macrae, Cole-Davies and Dias (2003). Participants were presented with a sequence of faces in an encoding phase, and were then required to judge which faces they had previously encountered in a surprise two-alternative forced-choice recognition test. In one condition, stimulus eye gaze was either direct or deviated at the viewing phase, and eyes were closed at the test phase. In another condition, stimulus eyes were closed at the viewing phase, with either direct or deviated gaze at the test phase. Modulation of gaze direction affected hit rates, with participants demonstrating greater accuracy for direct gaze targets compared to deviated gaze targets in both conditions. Reaction times (RT) to correctly recognized stimuli were faster for direct gaze stimuli at the viewing phase, but not at the test phase. The age group of participants differentially affected these measures: there was a greater hit rate advantage for direct gaze stimuli in older children, although RTs were less affected by age. These findings suggest that while the facilitation of face recognition by gaze direction is robust across encoding and recognition stages, the efficiency of the process is affected by the stage at which gaze is modulated.

Introduction The eyes are a powerful and informative source of interpersonal information (Argyle & Cook, 1976). Judging the direction and focus of the gaze of other people can allow us to interpret their attentional focus. Such information can be crucial to many aspects of human life: if the gaze of another alights upon an approaching tiger, then you would be best placed to pay attention yourself. Equally, if the gaze of another alights upon you, then (depending on the circumstances) your luck could be in. Given the importance of such signals it is no surprise that we are particularly sensitive to the eyes of conspecifics: from birth, humans prefer to look at faces with a direct gaze (Farroni, Csibra, Simion & Johnson, 2002), and adults are capable of detecting very slight deviations of gaze direction (Anstis, Mayhew & Morley, 1969). Baron-Cohen (1995) has suggested that specific functional architecture, an Eye Direction Detector (EDD), exists for the discrimination and interpretation of gaze. Subsequent imaging studies have supported this idea, with dedicated neural substrates for gaze perception

being identified with fMRI (Hoffman & Haxby, 2000), PET (Wicker, Michel, Henaff & Decety, 1998), and ERP (Puce, Allison, Bentin, Gore & McCarthy, 1998) techniques. Single cell electrophysiology has identified similar regions in monkey cortex, with populations of cells in the superior temporal sulcus coding the direction of seen gaze (Perrett & Mistlin, 1990). A result of our sensitivity to the eyes of others is that gaze direction can control the allocation of visuospatial attention. Infants will follow the direction of an adult’s gaze within the first year, providing a basis for joint attention (Scaife & Bruner, 1975). However, automatic gaze following also operates on low-level attentional orienting. Attentional cuing paradigms (see Posner, 1980) have demonstrated that valid and invalid gaze cues affect the processing of peripheral targets in adults (Driver, Davis, Ricciardelli, Kidd, Maxwell & Baron-Cohen, 1999; Friesen & Kingstone, 1998), and also in infants (Hood, Willen & Driver, 1998). Further research has examined the specificity of gaze cues, and while there are strong effects of other directional stimuli (e.g. such as arrows: Ristic, Friesen & Kingstone, 2002), attention seems to be

Address for correspondence: Alastair D. Smith, Department of Experimental Psychology, University of Bristol, 12a Priory Road, Bristol BS8 1TU, UK; e-mail: [email protected] © 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.

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most strongly reflexive to eye gaze (Downing, Dodds & Bray, 2004; Friesen, Ristic & Kingstone, 2004). While deviated gaze can trigger a shift of attention away from the face, direct gaze seems to capture visuospatial attention (Senju & Hasegawa, 2005; von Grünau & Anston, 1995). Mutual gaze establishes social contact between people and is active from birth (Farroni et al., 2002). Furthermore, the same study showed that this preference confers a computational facilitation: 4month-old infants demonstrated increased neural activity for faces with direct gaze, which was taken to indicate enhanced facial processing. George, Driver and Dolan (2001) extended this enquiry in an fMRI study of adults, finding greater activation around the fusiform gyrus for faces with direct relative to averted gaze. Participants also performed more efficiently with direct gaze faces on a sex discrimination task. This demonstrates that increased cerebral activation associated with direct gaze is also accompanied by more efficient processing of facial features. The social significance of such a mechanism has been emphasized (e.g. Langton, Watt & Bruce, 2000) and studies have investigated eye gaze effects on factors such as person perception and memory for faces. Macrae, Hood, Milne, Rowe and Mason (2002) replicated the enhancement of sex discrimination for faces with a direct gaze, and also found that participants were more able to access social information for direct gaze faces. Furthermore, Mason, Hood and Macrae (2004) demonstrated that direct gaze also enhances person recognition, even when perceivers are not explicitly attempting to memorize the faces. While sensitivity to direct gaze emerges very early in the lifespan, there has been little research into whether it confers a similar enhancement of face recognition in young children as it does in adults. Gaze direction and person memory in childhood was directly addressed by Hood et al. (2003): participants were presented with a sequence of faces (direct or deviated gaze) to be studied, and then tested in a surprise recognition phase. Test items were arranged in pairs (target and foil) and all faces were presented with closed eyes; participants pointed to the previously encountered face. In order to test for any effects of gaze direction at the recognition phase, another condition had faces initially presented with eyes closed, and then appearing in the test phase with either direct or deviated gaze. Both children of 6 years and adults demonstrated a benefit for direct gaze: faces encountered with a direct gaze were better remembered than those with a deviated gaze. This advantage also appeared when gaze was manipulated in the test phase of the experiment. Not only does this support the modulation of person memory by gaze direction, but it also shows that children enjoy the same benefit as adults for direct © 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd.

gaze. While this finding indicates the operation of gaze sensitive mechanisms in face recognition for young children a number of questions remain unanswered. First, how robust is the effect and does it show any change over the course of middle childhood? Many studies of face recognition have concentrated on the age range of 6 to 10 years following reports that face processing undergoes qualitative shifts during this period (e.g. Carey, Diamond & Woods, 1980; Tanaka, Kay, Grinnell, Stansfield & Szechter, 1998). Furthermore, Hood et al. (2003) did not include a measure of response time, leaving out the possibility to investigate whether gaze information is differentially accessed at the encoding and/or retrieval stage. We aimed to address these issues in the present study by comparing children of three different age groups: 6–7 years, 8–9 years, and 10–11 years of age. Participants completed the same experiment as reported in Hood et al. (2003), but here the study was conducted on a computer rather than with cards (as used in the original study). The inclusion of such technology allowed us to measure the reaction time (RT) to make a recognition judgement.

Method Participants Three age groups were selected from schools, with 40 children in each group: Year 2 (6–7 years; 13 male, 27 female), Year 4 (8–9 years; 19 male, 21 female), and Year 6 (10–11 years; 18 male, 22 female). All participants had normal or corrected-to-normal vision and parental consent. Stimuli and apparatus Participants were presented with the same faces as appeared in the Hood et al. (2003) study. Stimuli consisted of 160 digitized monochrome images selected from a database of Caucasian student faces, presented on an Apple G4 laptop. Forty individuals (20 male, 20 female; aged 18–21 years) were photographed in an expressionless pose, with their eyes in four positions: staring ahead, closed, deviated left and deviated right. Lighting and background were identical for all photographs. Each image was modified using Adobe Photoshop software, cropping distinctive extraneous features (e.g. jewellery, clothing) and removing colour to produce monochrome tones. Sets were constructed so that stimuli were presented in a different order depending on the condition (i.e. eyes open at viewing and closed at the test phase, or vice versa). In order to control for any distinctiveness effects, additional sets were created for each condition

Eye remember you two

where the target and foil faces were substituted. Thus each face was a target for half the participants and a foil for the remaining participants. Design The experiment was of a mixed design, with age group (Year 2, 4, or 6) and condition (eyes open at the viewing or test phase) as between-subjects factors, and gaze (direct or deviated) as a within-subject factor. Each experiment had 20 target faces in the viewing phase, and 40 faces (20 target and 20 foils) in the test phase. Presentation order was fully randomized for each participant. Dependent measures were hit rate (i.e. the proportion of target faces correctly recognized) and reaction time (RT) for each hit. Procedure Children were equally and randomly assigned to one of the two conditions. Participants completed both the viewing phase and the test phase of the task in one session. In the viewing phase 20 faces (10 male, 10 female) were sequentially presented for 5 sec each. The interstimulus interval was 1 sec, and images were positioned centrally on the screen. Children were asked to look

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quietly at each face. Following the viewing phase participants were instructed that the purpose of the experiment was to test their memory of the faces they had just seen. Forty faces comprising 20 target faces (previously presented in the viewing phase) and 20 foil faces were then presented in pairs. Each pair contained one target face and one foil of the same sex, and participants were asked to make a left/right decision, using a button box, depending on whether they recognized the face presented on the left- or the right-hand side of the screen. Target position was fully counterbalanced. The type of stimuli presented in each phase of the experiment differed depending on the condition. In the Encoding condition, faces were presented with either staring or deviated eyes in the viewing phase, and with the eyes closed in the test phase. In the Recognition condition, faces were presented with closed eyes in the viewing phase, and with the eyes staring or deviated in the test phase. Gaze direction (left, right) for deviated stimuli was fully counterbalanced (see Figure 1).

Results All participants completed the experiment. One Year 2 child was excluded from analysis for having a median

Figure 1 Examples of the stimuli presented in the experiment. In the Encoding Condition gaze direction is modulated in the viewing phase and eyes are closed in the test phase. In the Recognition Condition eyes are closed in the viewing phase and gaze direction is modulated in the test phase. © 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd.

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RT of 24,596 ms, over 16 standard deviations greater than the overall group median of 3026 ms (SD: 1188 ms). The remaining data (N = 119) were included in the analysis, with 75% of participants falling within one standard deviation of the median RT.

Table 1 Hit rate (proportion correct) for each age group. Standard deviations are in parentheses Condition

Gaze direction

Encoding

Direct Deviated Direct Deviated

Retrieval

Hit rate Hits were calculated as the proportion of targets correctly recognized in the test phase of the experiment, and summary data are contained in Table 1. There was a significant effect of gaze direction, with greater hit rates for targets with direct gaze compared to deviated gaze: F (1, 113) = 3.978, p < .05. There was also a significant effect of age: F(2, 113) = 8.00, p < .001. Post-hoc Tukey tests revealed that Year 6 children were significantly more accurate than Year 2 ( p < .0001), but there was no difference between Year 2 and Year 4 children, or between Year 4 and Year 6 children. There was no interaction between Gaze Direction and Age [F (2, 113) = 1.350, ns] and whilst a Gaze Direction × Condition interaction approached significance, implying a greater difference between deviated and direct gaze in the Encoding condition than in the Recognition condition [F (1, 113) = 3.633, p = .059], there was no overall effect of Condition [F (1, 113) < 1]. There was no interaction between Age and Condition: F (2, 113) = 1.155, ns. Lastly, there was no triple interaction between Gaze Direction, Age, and Condition: F (2, 113) < 1. Hit rates for Year 2 6-year-olds in the present study were comparable to those obtained for same age children in the original Hood et al. (2003) study, indicating a reliable comparison between the two paradigms. In order to ascertain any gender effects, the hit rates for male and female targets were entered into a repeated measures ANOVA, with participants’ Sex (male, female) and Condition (Encoding, Recognition) as betweensubjects factors. There was no difference in accuracy for male and female faces [F (1, 115) < 1], and no effect of participant Sex or of Condition [for both comparisons: F (1, 115) < 1]. Reaction time Mean RTs ranged between 1075 and 6499 ms in the Encoding condition and between 1552 and 9564 ms in the Recognition condition. Owing to the presence of outliers (Kolmogorov-Smirnoff: Encoding = .154; Recognition = .203) we calculated median reaction times as a more conservative measure of central tendency (see Driver et al., 1999; Langton & Bruce, 1999; Senju & Hasegawa, 2005). Median RTs to correct responses in the test phase (i.e. hits) are contained in Table 2. There © 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd.

6 –7 years

8 –9 years

10 –11 years

0.72 0.62 0.70 0.67

0.80 0.69 0.72 0.73

0.83 0.82 0.74 0.76

(0.14) (0.20) (0.13) (0.23)

(0.12) (0.20) (0.16) (0.14)

(0.14) (0.11) (0.11) (0.16)

Table 2 Median RTs (ms) for hits. Standard deviations are in parentheses Condition

Gaze direction

Encoding

Direct Deviated Direct Deviated

Retrieval

6 –7 years 3042 3074 3100 3714

8 –9 years

(1165) 2856 (789) (1557) 2841 (799) (1766) 3205 (1248) (1438) 2998 (984)

10 –11 years 2697 2985 2393 2880

(879) (841) (1055) (2290)

was a significant effect of gaze direction, with faster RTs for targets with direct gaze compared to deviated gaze: F (1, 113) = 4.671, p < .05. There was no main effect of age [F (2, 113) = 1.554, ns] but there was a significant Gaze Direction × Age interaction [F (2, 113) = 3.556, p < .05], implying that older children demonstrated a greater RT advantage for direct gaze over deviated gaze than younger children. However, post-hoc Tukey tests revealed no significant differences between age groups. While there was no main effect of Condition, the result approached significance [F (1, 113) = 3.837, p = .053], which indicates that RTs were generally faster in the Encoding condition than in the Recognition condition. There was, however, no interaction between Condition and Gaze Direction [F (1, 113) < 1] or Condition and Age [F (2, 113) < 1]. Finally, there was no triple interaction between Gaze Direction, Age, and Condition: F (2, 113) < 1. The lack of a direct effect of Age on RT, despite the significant Gaze Direction × Age interaction, demonstrates that older children were not necessarily more accurate than younger children because they were taking a longer time to respond. A Pearson’s correlation between age and RT revealed a negative relationship that approaches significance [r = −.163, p = .077], suggesting that increasing age is associated with faster RTs (although the post-hoc tests above do not fully bear out this relationship). Analysis of RTs for incorrect trials (i.e. selection of the foil as a previously encountered stimulus) further suggests that there is no specific pattern to error data: there was no effect of gaze direction [F (1, 84) < 1], and no effect of Age [F (2, 100) < 1] or Condition [F (1, 100) < 1].

Eye remember you two

In order to ascertain any gender effects on reaction times, data for male and female targets were entered into a repeated measures ANOVA, with the participants’ Sex (male, female) and Condition (Encoding, Recognition) as between-subjects factors. There was a significant difference in RTs for male and female faces [F (1, 115) = 5.040, p < .05], with faster RTs for female targets. There was no effect of participant Sex [F (1, 115) < 1], although an effect of Condition approached significance [F(1, 115) = 3.674, p = .058], which implies a greater RT difference between male and female targets in the Encoding condition compared to the Recognition condition. There were no significant interactions between factors. The effect of target sex suggests one of two possibilities: first, children are generally faster to recognize female faces; or, second, some of the female targets were more distinctive than their male counterparts. This matter receives further attention in the analysis that follows. Efficiency While error analysis gave reason to doubt the existence of a speed–accuracy trade-off, a Pearson’s correlation between hit rate and RTs suggests that there is no clear relationship between the two variables: r = −.085, ns. As a result, we followed recommendations made by Christie and Klein (1995) and converted data into efficiency scores by dividing the RT by proportion correct for each participant. These are displayed in Table 3. There was a significant effect of gaze direction, with greater efficiency for targets with direct gaze compared to deviated gaze: F(1, 113) = 4.520, p < .05. There was also a main effect of age [F(2, 113) = 3.326, p < .05] with older children performing more efficiently. Post-hoc Tukey tests revealed that efficiency increased with age: Year 6 children were significantly more accurate than Year 2 children (p < .0001), but there was no difference between Year 2 and Year 4 children, or between Year 4 and Year 6 children. An effect of Condition approached significance [F (2, 113) = 3.175, p = .077], suggesting that participants were more efficient in the Encoding condition. There were no interactions between any of the factors. Efficiency scores for male and female targets were also analysed in a similar way. Here there was no effect of Table 3 Efficiency scores (median RTs divided by hit rate) for each age group. Standard deviations are in parentheses Condition Gaze direction Encoding Retrieval

Direct Deviated Direct Deviated

6 –7 years 3774 4391 5192 4645

(1605) (4580) (2383) (14627)

8 –9 years 3805 4411 4517 4509

(973) (2347) (2704) (1800)

10–11 years 2998 3826 3168 3300

(1242) (1297) (2296) (4814)

© 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd.

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target sex, or participant sex [for both comparisons: F(1, 115) < 1]. There was a main effect of Condition [F(1, 115) = 4.724, p < .05], again demonstrating greater efficiency in the Encoding condition, compared to the Recognition condition. There were no interactions between any of the factors. This suggests that once speed and accuracy are accounted for, there is no observable difference between male and female targets.

Discussion The present results support and extend previous findings on the effects of gaze direction on face recognition (Hood et al., 2003). The modulation of gaze direction affected hit rates, with participants demonstrating greater accuracy for direct gaze targets compared to deviated gaze targets. This was the case in both conditions, with increased hits for direct gaze stimuli in both the Encoding condition (i.e. stimulus eyes open in the viewing phase and closed in the test phase) and the Recognition condition (i.e. stimulus eyes closed in the viewing phase and open in the test phase). There was also an effect of age, as older children (Year 6) demonstrated a greater hit rate advantage for direct gaze stimuli than younger children (Year 2). The present study makes a further contribution to this issue by including reaction time measures of the recognition task. RTs to correctly recognized stimuli were faster for direct gaze stimuli compared to deviated gaze. However, unlike hit rate, this effect appeared to be modulated by condition, with a marginally greater benefit (approaching significance) for direct over deviated gaze in the Encoding condition, compared to the Recognition condition. There were no effects of age for RTs, with all age groups showing a similar profile. Efficiency scores (combining accuracy and RT measures) suggest that children were generally more efficient for direct gaze stimuli, although this was lessened in the Recognition condition. Like accuracy, efficiency was affected by age, with older children (Year 6) performing the task more efficiently than younger children (Year 2). Participants were more accurate at recognizing faces with a direct gaze than with a deviated gaze. This is consistent with other findings (George et al., 2001; Hood et al., 2003; Macrae et al., 2002; Mason et al., 2004) that demonstrate enhanced person perception and recognition memory for faces with direct gaze. The presence of the effect in both Encoding and Recognition conditions supports the findings of Hood et al. (2003) and is also consistent with accounts of enhanced neural processing of faces with direct gaze (Farroni et al., 2002; George et al., 2001). This may confer an advantage for faces at

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any point in the recognition process that mutual gaze is established. In the Encoding condition this might take the form of superior coding and storage of a face. In comparison, direct gaze targets in the Recognition condition may induce a more efficient identification process in order to correctly decide whether a face had previously been encountered. While hit rates were affected by gaze direction in both conditions, the speed at which these correct judgements were made did appear to be affected by the stage at which gaze direction was modulated. Participants were generally fastest at correctly recognizing faces with a direct gaze, but this was more pronounced in the Encoding condition, and less clear in the Recognition condition. Therefore it seems that while accuracy for direct over deviated gaze is robust, the speed of that judgement is affected by the stage at which gaze is modulated. Along with being generally more accurate, older children demonstrated a greater hit rate advantage for direct gaze stimuli than did the younger children. However, RT was unrelated to age group. This suggests that sensitivity to gaze direction increases as children get older, while the speed of recognition judgements does not. The similarity of RT across age groups tallies with previous findings, such as those of Ellis, Ellis and Hosie (1993) who found that RTs for familiarity judgements (in a priming paradigm) were similar for children of 5 years and adults. In contrast, De Sonneville, Verschoor, Njiokikjien, Op het Veld, Toorenaar and Vranken (2002) report a facilitation of RTs in a face-processing task between the ages of 7 and 10 years. This disparity highlights the fact that different tasks confer their own developmental profiles. In the present study we see that different measures within the same task are separately related to age. However, when accuracy and RTs are combined we find that children become more efficient at performing the task as they get older. Hood et al. (2003) suggested that the benefit for direct gaze stimuli might be based on arousal. Mutual eye contact is known to increase autonomic arousal (Nichols & Champness, 1971) and also enhances amygdala activation (Kawashima, Sugiura, Kato, Nakamura, Hatano, Ito, Fukuda, Kojima & Nakamura, 1999), an area identified with emotional reinforcement. Increased arousal levels may therefore lead to a greater evaluation of socially relevant stimuli. In this case, arousal might enhance the accuracy of evaluation, regardless of whether it occurs at encoding or retrieval. However, it appears only to enhance the speed of that evaluation at the stage that faces are initially encoded. Once faces were committed to memory, the speed of their retrieval was no longer affected by gaze direction in the same way. This suggests that arousal does not necessarily © 2006 The Authors. Journal compilation © 2006 Blackwell Publishing Ltd.

affect all aspects of task performance in a proportional manner. An alternative account is that visual properties of the stimuli favour more efficient encoding in certain circumstances. For example, faces with a direct gaze might be considered a canonical form and are therefore more efficiently and accurately stored than those in a non-canonical form (i.e. in this case, face-on but with deviated gaze; cf Vuilleumier, George, Lister, Armony & Driver, 2005). In a similar manner, information that supports efficient face recognition and engenders robust configural processing may be more accurately coded for direct gaze stimuli. For instance, we may be better able to calculate inter-ocular distance when eyes are staring forward rather than to the side (we thank Bruno Rossion for this suggestion). Evidence from functional imaging supports a dissociation between the encoding and recognition stages of face memory that might also account for the current findings. Haxby, Ungerleider, Howitz, Maisog, Rapoport and Grady (1996) report the activation of distinct and separate brain areas depending on the different types of task, and suggest that the processes supporting recognition are not based on the same processes by which a given face was initially encoded. They argue that certain areas (within ventral occipitotemporal cortex) are active during all forms of face perception, independent of the memorial elements of the task, which themselves activate separate and additional areas. Our findings suggest that a direct gaze benefit is present in both conditions as the perceptual element of the task is equal (i.e. both conditions involve the perceptual coding of face stimuli). This approach separates the recognition element of face memory from the perceptual process of coding features, and supports the independent modulation of hit rate and RT. So, while the accuracy of judgements was not affected by the stage at which gaze was modulated, the speed of the recognition judgement (and the overall ‘efficiency’) was lessened when gaze was modulated at the test phase. This may reflect a slightly longer latency needed to access and evaluate faces initially encoded with closed eyes. Further study is required in this area of face recognition. In particular, the finding that gaze direction seems to affect recognition accuracy even when modulated at the test phase (replicating the results Hood et al., 2003) needs to be considered further as it may not be easily accounted for by existing models of face recognition (e.g. Burton, Bruce & Hancock, 1999; Haxby, Hoffman & Gobbini, 2000). The relationship between arousal and person perception also needs to be more specifically addressed, and we hope to gain insight with recent experiments that have employed measures of pupil dilation (Porter, Hood, Troscianko & Macrae, in press).

Eye remember you two

Making eye contact with other individuals facilitates social interaction. The current study shows that this key aspect of social cognition it not only present in young children, but also becomes more efficient as they get older.

Acknowledgements This study was supported by a Biotechnology and Biological Sciences Research Council grant (S16726) awarded to BMH. We are particularly grateful for the assistance of Samantha Bracey. We also thank Bruno Rossion and an anonymous reviewer for helpful comments on a previous draft of this paper.

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