inversion effect in perception of human faces in a...

PRIMATES, 40(3): 417--438, July 1999 417

Inversion Effect in Perception of Human Faces in a Chimpanzee (Pan troglodytes)

MASAKI TOMONAGA Kyoto University

ABSTRACT. Three experiments investigated the inversion effect in lace perception by a chimpanzee (Pan troglodytes) under the matching-to-sample paradigm. The first two experiments addressed the inversion effect in the perception of human faces. In Experiment 1, the subject received identity matching using 104 photographs of faces and houses presented in four different orientations. The chimpanzee showed better accuracy when the faces were presented upright than when they were inverted. The inversion effect was not found for photographs of houses. In Experiment 2, the subject received rotational matching in which the sample and comparisons differed in orientation. The subject showed a clear inversion effect for faces but not for houses. Experiment 3 explored the hemispheric specialization of the face inversion effect with chimeric (artificially composed) faces. The subject showed no visual-field preference when the chimeric faces were presented as samples under nonreinforced probe testing, while the inversion effect was evident when the discrimination was based on the left part of the chimeric sample. The results suggested that the face-inversion was specific to the left visual field (i.e. right hemispheric processing). In general, these results were consistent with those found in humans in similar testing situations.

Key Words: Face perception; Inversion effect; Matching task; Chimpanzee (Pan troglodytes); Hemispheric specialization.

INTRODUCTION

For primates including humans, face perception and recognition are important for social life. For example, humans obtain various information from faces, such as identity, familiarity, race, sex, age, emotional state, attractiveness, and so on. As in humans, nonhuman primates have variations of their facial appearances and exhibit a variety of facial expressions in their social interactions (CHEVALIER-SKOLNIKOFF, 1973; HAUSER, 1996; VAN HOOFF, 1967). These facts imply that the face plays an important role in individual recognition and communication.

A large body of literature has examined various aspects of face perception and recognition in humans (e.g. BRUCE, 1988; BRUCE & HUMPHREYS, 1994; BRUYER, 1986; DAVIES et al., 1981). One of the most interesting phenomena in human face recognition is the inversion effect (KOHLER, 1940; VALENTINE, 1988; YIN, 1969). For humans, it is difficult to recognize faces and facial expressions when the faces are inverted. Although there are controversies among findings (e.g. DIAMOND & C;XREY, 1986; FARAH "et al., 1995), the inversion effect is shown to be specific to faces since this effect is not observed with photographs of houses, airplanes, and scenes which have complexity comparable to faces. Furthermore, patients with right hemispheric damages (YIN, 1970) or subjects who were presented faces tachistoscopically to their right visual field (HILLGER & KOENIG, 1991; LEEHEY et al., 1978) showed no evidence of the inversion effect. These results suggest that the face-inversion effect is specialized to the right hemisphere. This specialization may support the finding that the inversion effect is specific to faces.

Studies conducted from the developmental perspective have revealed that face recognition is

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not hampered by inversion in human children around 6 years old. The face-inversion effect is evident in 10-yr-old children (CAREY & DIAMOND, 1977, 1994). These results indicate that children around 6 yr old attend to specific facial features and do not process them as a whole. Face- inversion effect may occur when the processing of faces has changed from "piecemeal" to "configural" along with development. Some researchers have noted that this developmental change is accompanied by "practice" or "expertise." DIAMOND and CAREY (1986) found that expert dog breeders showed the inversion effect when recognizing photographs of dogs, but novice did not. Expertise may enhance configural processing of complex stimuli. This relationship between the expertise effect and the inversion effect was supported by neuropsychological studies which found that the right hemisphere is involved in holistic processing of spatial configurations whereas the left hemisphere is involved in processing of features of the stimuli (HmLGER & KOENIG, 1991).

Using nonhuman animals from birds to primates, there is an increasing number of studies of facial recognition in experimental psychology, neuroscience, and ethology (BRUCE, 1982; DASSER, 1988; DITTRICH, 1990; FUJITA, 1993; HAMILTON & VERMEIRE, 1983, 1988, 1991; HAUSER, 1993; ITAKURA, 1992; JITSUMOR1 & YOSHIHARA, 1997; KANAZAWA, 1996; KEATING & KEATING, 1993; MATSUZAWA, 1989, 1990; OVERMAN & DOTY, 1982; PARR et al., 1998; PERRETT & MISTUN, 1990; PHELPS & ROBERTS, 1994; ROSENFELD & VAN HOESEN, 1979; SANDS et al., 1982; SWARTZ, 1983; TOMONAGA, 1994; TOMONAGA et al., 1993; WRIGHT & ROBERTS, 1996). Pigeons showed no evidence of the inversion effect in human-face perception (PHELPS & ROBERTS, 1994). JITSUMOR1 and YOSHIHARA (1997) trained pigeons to discriminate between human facial expressions and found that they discriminated faces on the basis of additive inte- gration of features but not of configuration of features. Concerning the face-inversion effect in nonhuman primates, results are somewhat inconsistent. BRUCE (1982), for example, trained macaque monkeys on a simultaneous discrimination task using photographs of upright faces. After acquisition of the discrimination, the photographs were inverted. If a face-inversion effect would occur, the discrimination should deteriorate. BRUCE observed preservation of the original discrimination, suggesting that the face-inversion effect did not occur in this situation. There are additional reports of no face-inversion effect in nonhuman primates under simple and condi- tional discrimination and preferential looking procedures (DITTRICH, 1990; ROSENFELD • VAN HOESEN, 1979). In contrast, there are some reports which support the face-inversion effect (HAMILTON & VERMEIRE, 1983, 1988, 1991; OVERMAN & DOTY, 1982; PARR et al., 1998; PERRErr et al., 1988; SWARTZ, 1983; TOMONAGA, 1994; WRIGHT & ROBERTS, 1996). Among them, TOMONAGA (1994) examined the face-inversion effect in laboratory-raised Japanese macaques under a modified preferential looking task. The monkeys were allowed to look at photographs while they held down a lever. The monkeys showed a significant difference in looking time between upright photographs of rhesus and Japanese macaques (cf. FUJITA, 1990), but there was no difference when the same photographs were presented at 90 or 180 degrees. The strongest inversion effect was found for photographs showing clear, frontal views of faces. When the photographs did not show frontal faces but profiles, the inversion effect disappeared. KEATING and KEATING (1993) investigated the inversion effect in monkeys by using a face/non- face discrimination task. They argued that monkeys who showed an inversion effect might process the facial stimuli in the configural way, but those who did not show an inversion effect might process the local features of the stimuli (cf. JITSUMORI & YOSHIHARA, 1997).

Neurophysiological studies with macaques have reported evidence of "face" neurons in the temporal cortex (BAYLIS et al., 1985; BRUCE et al., 1981; HASSELMO et al., 1989a, b; PERRETT & MISTLIN, 1990; PERRETT et al., 1984, 1988). The inversion effect has been investigated in the response of face neurons, but the results are inconsistent. PERRFr et al. (1984) found the neu-

Face-inversion Effect in a Chimpanzee 419

runs that showed higher selectivity to upright faces than inverted faces. Other studies showed no evidence of the inversion effect in face neurons (HASSELMO et al., 1989b; PERRErr et al., 1988). Electroencepharographic (EEG) studies showed a larger latency to inverted faces both in humans (JEFFREYS, 1989) and macaques (PINEDA & NAVA, 1993).

Experimental factors may affect the inversion effect especially in animals, such as the number of stimuli, homogeneity among the stimuli, specific task requirements, and so on. TOMONAGA (1994) and PHELPS and ROBERTS (1994) suggested that variation in the number of stimuli used for training across studies is one of the critical variables that may be responsible of the inconsistent results. In concept-formation experiments in animals, it is necessary to use a large number of stimuli for the formation of a "concept" because a small number of stimuli usually establishes a discrimination based on specific stimuli (e.g. HERRNSTE1N et al., 1976; SANDS et al., 1982). Similarly, a small number of facial stimuli would facilitate attention to the local features resulting in no face-inversion effect. On the other hand, a large number of stimuli would induce the subjects to process the spatial configuration of the faces, resulting in an inversion effect. In fact, TOMONAGA (1994) used more than 20 different photographs and obtained clear evidence of the inversion effect in monkeys. TOMONAGA et al. (1993) tested the inversion effect for a chimpanzee in symbolic naming task. The subject was trained to select the correct "name" of familiar humans and apes when the photographs were presented as the sample. When the sample photographs were inverted, the subject responded as accurately and quickly to it as when it was upright. Thus, the subject did not show the inversion effect in facial recognition. However, when the sample photograph was rotated only 90 ~ , the subject increased the response times. The results were interpreted in terms of ecological constraints on visual perception because the residual arboreality of chimpanzees might bias their spatial cognition ability. However, alternative accounts may also be possible. In the naming task, the individuals used as stimuli were familiar (cagemates or trainers) to the subject. Thus, the number of available stimuli was limited: only three humans and three chimpanzees were used as stimuli. Furthermore, only four different photographs were prepared per each individual. The use of such a small number of stimuli might have caused the lack of an inversion effect in the TOMONAGA et al.'s (1993) experiment.

Studies with chimpanzees have investigated the various aspects of face perception, such as individual recognition (BAUER & PHILIP, 1983; MATSUZAWA, 1989, 1990; TOMONAGA et al., 1993), recognition of facial expressions (MORRIS & HOPKINS, 1993), sex discrimination (ITAKURA, 1992; HAYES & NISSEN, 1971), age discrimination (HAYES & NISSEN, 1971), preference for the facial stimuli in neonates (BARD et al., 1992), and the reconstruction of a face from its parts (PREMACK, 1975). Nevertheless, only few studies have addressed the inversion effect, and the results are again inconsistent; PARR et al. (1998) found the inversion effect under rotational matching, whereas TOMONAGA et al. (1993) failed to find it under the naming task, as mentioned above.

The inversion effect in face perception has been investigated in different experimental paradigms. In the recognition experiments with humans as subjects, this effect has been assessed in two ways. In some experiments the faces are presented in the same orientation between inspec- tion and recognition phases. The inversion effect is defined as the difference in performance between upright-upright and inverted-inverted conditions (DIAMOND & CAREY, 1986; HOCHBERG & GALPER, 1967; YIN, 1969; Experiment 1). The other experiments observed the inversion effect by comparing the performance between the upright-upright and upright-inverted conditions (HOCHBERG & GALPER, 1967; SCAPINELLO & YARMEY, 1970; Y1N, 1969; Experiment 2). In the matching experiments, there are also two ways of investigating the inversion effect. In some experiments, sample and comparison stimuli were both presented upright or else inverted (PHELPS & ROBERTS, 1994; WRIGHT & ROBERTS, 1996), while in other experiments the sample and comparison stimuli differed in their orientations (PARR et al., 1998; VALENTINE ~ BRUCE,

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1988). Y1N (1969) suggested that the face-inversion effect may involve two distinctive processes; one is memorization of inverted faces and the other is recognition of identical stimuli in different orientations. In the matching experiments, the former is assessed in the identity-matching task, and the latter is in the rotational-matching task.

Using a single chimpanzee, I explored these two processes of the inversion effect under the identity-matching (Experiment 1) and rotational-matching procedures (Experiment 2) by using 104 different photographs of faces of unfamiliar humans and 104 different photographs of houses as control stimuli. As noted before, face perception in humans is considered to lateralize to the right hemisphere. In Experiment 3, to check the hemispheric specialization of face perception in the chimpanzee and to develop a task for investigating hemispheric specialization, I gave the subject a matching task with chimeric stimuli similar to those used in comparable studies in humans (LEVY et al., 1983; cf. MORRIS & HOPKINS, 1993).

GENERAL METHODS

SUBJECT

A 13-yr-old female chimpanzee born in a zoological garden, Chloe, served as the subject in the present experiments. She came to the Primate Research Institute at an age of 4 yr and has served as a subject in various kinds of perceptual-cognitive experiments. In particular, she had been trained extensively in matching-to-sample tasks (TOMONAGA, 1993; TOMONAGA & MATSUZAWA, 1992). She lived in an outdoor enclosure (624m 2) with eight other chimpanzees. She was fed normally during the present study. She exclusively used her right hand to respond during the experimental period. It was reported that she showed very weak right-hand bias in a simple reaching task (laterality quotient was 6.4: TONOOKA & MATSUZAWA, 1995). The care and use of the chimpanzee adhered to the "Guide for the care and use of laboratory primates" of the Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

APPARATUS

Experimental sessions were conducted in a booth tbr chimpanzees (2.4•215 1.8m) in a room adjacent to the enclosure. A 21-inch cathode-ray-tube (CRT) display monitor (NEC Model PC-KH2021) with a capacitive touch screen (MicroTouch Systems Model 2012) was installed on one wall 15 cm above the floor. A transparent Plexiglas panel, fitted with a 10x47 cm arm hole at the level of the bottom of the screen, prevented deterioration of the setup. It was fixed 30 cm in front of and parallel to the monitor. The subject sat in front of the monitor about 50 cm away from the screen. A response was defined as the touch to the screen of the monitor. The apparatus also had a food tray which was installed below the CRT; a universal feeder (Davis Scientific Instruments Model UF-100) delivered pieces of food (apple or raisin) into the tray when correct responses were made. The equipment was connected to a personal computer (EPSON Model PC-386GS) that controlled the experimental events.

STIMULI

The stimuli were 256-step gray-scale digitized photographs collected from books and maga- zines. The human intact face set consisted of 104 Japanese male soccer players and the house set consisted of 104 pictures of houses. The photographs were equated in size and global bright-


ness and saved in four orientations; 0 ~ (upright), 90 ~ (horizontal), 180 ~ (inverted), and 270 ~ (horizontal). The chimeric faces used in Experiment 3 were made by combining the original and mirror images of right or left halves of the faces (see Methods of Experiment 3). These photographs were presented in the circle (8 cm in diameter) on a gray background. Examples of photographs are shown in the schematic diagrams for each experiment (see Figs. 1 & 3).

PROCEDURE

Matching Task

A zero-delay matching-to-sample task was employed in all experiments. Each trial began with a 1-s beep sound followed by the presentation of a 1.5-cm blue circle on a gray background in the central bottom position of the screen. When the subject responded to the circle, it disappeared, the sample stimulus was then presented for 0.5 s above the location of the previous blue circle. Immediately after the sample, two comparison stimuli were presented next to each other in the upper half of the screen. These stimuli were from the same stimulus set. The subject was required to touch the one that was identical to the sample or identical when rotated. The former was referred to as identity matching and the latter rotational matching. The correct comparison stimuli appeared equally often and randomly at the left and right positions within a session. A response time was defined as the time from the onset of comparisons to the subject's response. When the subject responded to the correct comparison, all stimuli disappeared and 1-s chime and food reward were presented. When she made an error, all stimuli disappeared and a 0.5-s buzzer was presented. The same trial appeared after an error trial (correction method). If the subject made two or three consecutive errors, only the correct comparison stimulus appeared after the sample in the next correction trial in order to prevent possible development of inappro- priate behaviors. The intertrial interval (ITI) was 3 s.

Preliminary Training

Although Chloe had been trained for a long time on various matching tasks before the present experiments, she had no experience in discriminating photographs. Before Experiment 1, I trained her on the identity-matching task with various photographs (birds, dogs, insects, and cars) as stimuli for 11 sessions of 80 trials each. Chloe showed 81.3% correct in the first session and 90.3% in average across the 11 sessions.

E X P E R I M E N T 1 : IDENTITY MATCHING WITH ROTATED PHOTOGRAPHS OF

FACES AND HOUSES

In Experiment 1, the subject was given the identity-matching task with photographs of human faces and houses. The difference in performance between upright and inverted photographs was used as measure of the inversion effect.

METHODS

In this experiment, the sample and correct comparison stimuli were the same both in identity and orientation, while correct and incorrect comparisons were the same in orientation but different in identity. Two types of sessions appeared alternately six times each. In face sessions, only

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Table 1. Mean percent errors and response times on correct trials for each stimulus set as a function of degree of rotation in Experiment 1.

Percent error Response time (s)

Set 0 +90 180 0 +90 180

Face 7. l 17.1 16.7 0.862 0.853 0.884

House 14.0 11.3 12.4 0.842 0.845 0.842

the faces were presented on all trials, whereas only the houses were presented in house sessions. Each session consisted of 100 trials, 25 trials for each orientation (0 ~ 90 ~ 180 ~ and 270~ Orientation and combination of correct and incorrect comparisons were randomly determined from trial to trial. In the data analyses, data from 90 ~ and 270 ~ were combined for each stimulus set and then used for statistical analyses. For convenience of exposition, these horizontal stimuli are designated as +90~ - 9 0 ~ being equal to 270 ~ .

RESULTS AND DISCUSSION

Table 1 shows the mean percent error and correct response time for each orientation of each stimulus set. Chloe was 86.4% correct for human faces and 87.4% correct for houses on average. A two-way ANOVA with session as repeated measure was conducted separately to the percent error and response time data, in which stimulus set (face, house) was a between-session factor and orientation (0 ~ +90 ~ 180 ~ was a within-session factor. For percent error, only the interaction was significant [F(2,20)--4.77, p<0.05] . Fisher's LSD test revealed that the percent error for upright human faces (0 ~ was significantly lower than the other orientations (ps<0.05). For response times, all main effects and their interaction were not significant.

The inversion effect was evident in the accuracy of the discrimination of human faces. The subject made fewer errors to the upright faces than to the rotated faces. In contrast, such an effect was not apparent with the houses. These results suggest that the subject perceives upright human faces in a different way from faces in other orientations. The results also indicated that faces may be perceived differently than houses. JITSUMORI and MATSUZAWA (1991) trained monkeys to discriminate the orientations (upright vs inverted) of a variety of full frontal view of humans. After establishing the discrimination, the monkeys showed a transfer to photographs of novel animals but not to artificial objects. The authors suggested that the uprightness of the natural stimuli facilitated the transfer across natural categories. The chimpanzee might recognize human faces, presented either upright or inverted, as meaningful. It is plausible that the meaningful patterns presented in unnatural orientations caused the difficulty in memorization of these patterns. This contrast might be responsible for the inversion effect.

EXPERIMENT 2: ROTATIONAL MATCHING WITH FACES AND HOUSES

Experiment 2 introduced a rotational matching paradigm instead of identity matching. In rotational matching, the subject was required to select the comparison stimulus that was identical to the sample regardless of its orientation.

METHODS

Experiment 2 started immediately after Experiment 1. Each session consisted of 96 trials, with all combinations of the sample and comparison orientations ( 4 x 4 = 1 6 ) appearing six


times. The order of photographs, combinations of orientations, and positions of correct comparisons were randomized in each session. Figure 1 illustrates examples of trials that were used in Experiment 2. As in Experiment 1, face sessions and house sessions appeared alternately for 16 sessions in total. The last eight sessions were used for data analyses.

Data analyses were conducted on the basis of the relative orientations of the comparison stimuli, defined as the difference in orientation between the sample and the comparisons. Analyses were conducted separately for trials with 0 ~ and 180 ~ samples and 90 ~ and - 9 0 ~ samples. For '0 ~ and 180~ (upright and inverted sample) trials, data from horizontal (90 ~ and - 9 0 ~ comparisons were combined into one category, _+90 ~ For 90 ~ and -90~ (horizontal sample) trials, on the other hand, comparisons with 90 ~ and - 9 0 ~ relative orientations (0 ~ or 180 ~ in absolute orientation) were not combined because the results of Experiment 1 suggested that absolutely upright and inverted photographs might be processed in different ways. Data from two horizontal sample orientations (90 ~ and - 9 0 ~ ) were then combined for statistical analyses.

RESULTS

Chloe was 85.4% correct in the first face session and 88.5% correct in the first house session. Mean percent correct for the last eight sessions was 80.9% for face sessions and 87.2% for house sessions, respectively, and the mean response time on correct trials for the last eight sessions was 0.792s for face sessions and 0.730s for house sessions. Figure 2 represents the mean percent error (upper panels) and response time (lower panels) on correct trials for upright and inverted samples (left panels) and horizontal samples (right panels) for each stimulus set as a function of the relative orientation of the comparison stimuli. The horizontal axes indicate the orientation of the comparison stimuli relative to the sample orientation. Absolute orientations are also indicated in parentheses.

Unlike Experiment 1, the face-inversion effect based on identity matching was not evident either in percent error (20.8% for upright-upright and 16.7% inverted-inverted) or in response times (0.802s for upright-upright and 0.722s inverted-inverted). An inversion effect based on rotational matching was clearly indicated, however. For upright and inverted samples, there are increasing trends of response times as a function of relative orientations of comparisons for faces but not for houses. A three-way ANOVA with session as repeated measure was conducted separately on response time and percent error data, in which stimulus set (face, house) was the between-session factor, and sample orientation (0 ~ 180 ~ and comparison orientation (0 ~ +90 ~ 180 ~ ) were within-session factors. For response time, the effect of stimulus set was significant [F(1,14)= 10.11, p<0.01] . The interaction between stimulus set and sample orientation was marginal [F(1,14)=4.02, p=0.065] and that between stimulus set and comparison orientation was significant [F(2,28)=3.69, p<0.05]. Fisher's LSD test revealed that differences between 0 ~ and 180 ~ and between _+90 ~ and 180 ~ for faces were significant (ps<0.05). For percent error, the effect of stimulus set [F(I, 14)=7.49, p<0.05] and the interaction between stimulus set and sample orientation [F(1,14)=4.95, p<0.05] were significant.

Results from the horizontal (_+90 ~ ) samples were rather different for upright and inverted samples. For faces, percent errors and response times were worse for absolute upright comparisons than for the other orientations. Two-way ANOVAs with session as repeated measures were conducted separately for the response time and percent error data, in which stimulus set (face, house) was the between-session factor and comparison orientation (relative upright, absolute upright, relative inverted, absolute inverted) was the within-session factor. For response times, only the interaction was significant [F(3,42)=4.00, p<0.05]. Fisher's LSD test revealed that the response time for comparison faces at the absolute upright orientation was

424 M. TOMONAGA


Sample=0 ~ 40 (Upright)

Sample= 180 ~ ( I n v e r t e d )

30

LU "E 20 S

i = i

0 • 90 180 (0 • 90 180)

i i J _ _

0 • 90 180 (180 • 90 0)

40

30

20

10

0

Sample = :t: 90 ~ (Horizontal)

t i i i

0 90 180-90 Relative (--+90 0 ~90 180) Abso lu te

oj

I--

tY

0.9

0.8 Y

0,7 ~

i i i

0 • 90 180 (0 • 90 180)

0.9

o• 0.8

0.7

i i i

0 • 90 180 (180 -+ 90 O)

- -e - - F a c e

-o-- House

i i i i

0 90 180 -90 Relative (+--90 0 ~-90 180) Absolute

Relative and Absolute Orientation of Comparisons (Degree)

Fig. 2. Mean percent error (top panels) and response times on correct trials (bottom panels) for each stimulus type as a function of relative orientation of the comparison stimuli in Experiment 2. Left panels: upright and inverted samples. Right panels: horizontal samples.

significantly longer than that for the relative upright and absolute inverted comparison faces (ps<0.01). For percent error, the effects of stimulus set [F(1,14)= 19.94, p<0.001] and comparison orientation [F(3,42)=5.44, p<0.01] were both significant. Fisher's LSD test revealed that percent error for trials with absolute upright comparisons was significantly higher than the relative upright and relative inverted comparisons (ps<0.01). The difference between relative upright and inverted comparisons was also significant (p<0.05).

The analyses presented above were based mainly on the effect of comparison rotation. Another look at the data may reveal how the sample rotation influences choice and response times. Are there any differences between the data for the 0 ~ samples with various comparison orientations and the 0 ~ comparisons with various sample orientations? They might be equiva- lent in rotational matching. To answer this question, the mean percent error and correct response time for the 0 ~ sample orientation were averaged across 90 ~ 180 ~ and - 9 0 ~ comparison orientations for each stimulus set. Similarly, the mean percent error and correct response time for the 0 ~ comparison orientation were averaged across 90 ~ 180 ~ and - 9 0 ~ sample orientations for each stimulus set. Results are shown in Table 2. A separate two-way ANOVA with session as

Fig. 1. Schematic examples of trials that appeared in Experiment 2. COR: Correct comparison stimulus; 1NCOR: incorrect comparison stimulus; CMP: comparison stimuli; SMP: sample stimulus. Scales are different from the actual ones. Note that the sample and comparisons did not appear simultaneously in the actual experimental situations. Degree of sample rotation is indicated at the base of the columns, and degree of comparison rotations is indicated at the left side of the rows.

426 M. TOMONAGA

Table 2. Mean percent errors and response times on correct trials for each stimulus set when the sample or comparison was fixed at 0 ~ in Experiment 2.

Percent elTor Response time (s)

Set Sample fixed at 0 ~ Comparison fixed at 0 ~ Sample fixed at 0 ~ Comparison fixed at 0 ~

Face 13.9 28.5 0.860 0.857

House 16.7 13.2 0.708 0.714

repeated measure was conducted for each set of data. Stimulus set was the between-session factor and condition (sample at 0 ~ vs comparison at 0 ~ was the within-session factor. For percent error, the effects of condition [F(1,14)=4.69, p<0.05] and interaction [F(1,14)= 12.38, p<0.01] were significant. Subsequent analyses revealed that the effect of condition was only significant for faces (p<0.01). When the sample was at 0 ~ the subject made fewer errors than when the comparison was at 0 ~ but only for the face set. For response time, only the effect of stimulus set was significant IF(I,14)= 13.75, p<0.01].

DISCUSSION

Chloe showed a face-inversion effect based on rotational matching when the sample was upright or inverted, whereas she showed no evidence for an inversion effect for the house stimuli. These results indicate that the inversion effect in the chimpanzee was specific to face stimuli as in humans. Furthermore, for a horizontal face as the sample, the subject's performance was most impaired when the comparison was absolutely upright, not relatively inverted orientation predicted from inversion effect. The comparison faces in their natural orientation (upright) might have a detrimental effect when the samples were horizontal. It might be due to the dis- tinctiveness of upright faces.

Chloe showed better accuracy when the face sample was presented at 0 ~ than when the comparison was at 0 ~ This result is consistent with YIN'S (1969) study. He found that human subjects showed better recognition accuracy in an upright-inverted than in an inverted-upright condition. Regardless of the asymmetry of accuracy, Chloe's response time was the same between conditions. These analyses demonstrated the two different processes suggested by YIN (1969). Accuracy might reflect the inversion effect based on the difficulty in memorization of faces presented in unnatural orientations, whereas the response time might reflect the mental rotation processes to recognize the identity of disoriented faces.

E X P E R I M E N T 3: HEMIPHERIC SPECIALIZATION OF FACE PERCEPTION

ASSESSED WITH CHIMERIC FACES: A CASE STUDY

It is frequently reported that face perception in humans is lateralized to the right hemisphere (e.g. YIN, 1970). In assessing the functional specialization of face perception, chimeric faces made from original and mirror images of two vertical half parts of the face are often used as stimulus materials. By using such chimeric faces, visual inputs to each visual field can be controlled roughly under the assumption that the left half of a chimeric face is projected to the left visual field (LVF) and the right half to the right visual field (RVF). Under free viewing conditions, humans reported that chimeric faces made from the left half and a mirror image of the left half were more similar to the original face image than chimeric faces made up of the right half and a mirror rotation of the right half, indicating LVF (i.e. right hemispheric) dominance.


Monkeys did not show such an effect in the perception of chimeric faces of monkeys (OVERMAN & DOTY, 1982). Also in the perception of facial expression, humans show LVF dominance both under tachistoscopic and chimeric face studies (LEvy et al., 1983; LEY & BRYDEN, 1979; SUBERI & MCKEEVER, 1977). Chimpanzees also showed LVF dominance in the perception of facial expression using chimeric human faces (MORRIS & HOPKINS, 1993). Although no visual field dominance in perception of faces was seen in monkeys, they exhibited right hemispheric dominance (i.e. facial asymmetry) in the production of facial expression (HAUSER, 1993).

The inversion effect has also been related to the hemispheric specialization. Humans show the face-inversion effect when the faces are presented tachistoscopically to the LVF but not to the RVF (HILLGER & KOENIG, 1991; LEEHEY et al., 1978). YIN (1970) reported that subjects with damage to the right hemisphere showed a reduced inversion effect in face perception. If the chimpanzee showed a face-inversion effect, this effect might be lateralized to the right hemisphere as it is in humans.

In Experiment 3, I tried to investigate the hemispheric specialization of face perception in the chimpanzee focusing on the inversion effect using chimeric faces under a free viewing situation. Although I tested only one chimpanzee, the present experiment was conducted in an effort to improve the methodological development in the study of hemispheric specialization of face perception in nonhuman primates. In the first, preliminary, preference test, I presented chimeric faces in a nonreinforced procedure (OVERMAN & DOTY, 1982). In the second phase, the chimpanzee was tested under condition where the responses were differentially reinforced.

METHODS

Stimuli

In the present experiment, only faces were used as stimuli. Chimeric faces were used in addition to the original intact faces. The left half of each face was designated as A, B, C, -.-, and right half as a, b, c, -... Therefore, the original (intact) faces were designated as Aa, Bb, ..-. Similarly, chimeric faces made from the left half and the mirror image of the left half of the same person were AA, BB, ..., and those made from the right half and the mirror image of the right half of the same person were aa, bb, -... Chimeric faces made from the left and right half of faces from different persons were designated as Ab, Cd, ... (see Fig. 3).

Procedure

Preference test: The subject was given three types of baseline trials. In addition to the trials using original faces as in Experiments 1 and 2 [designated as Aa (sample)/Aa (correct comparison)-Bb (incorrect comparison)], trials using chimeric faces from different persons (Ab/Ab-Cd) and those using chimeric faces from the same persons (AA/AA-aa or aa/aa-AA) were given to the subject in order to investigate whether the subject could discriminate chimeric faces. Combinations of the two orientations (upright and inverted) yielded four different types (2• of rotational matching trials. Responses to the correct comparisons were reinforced in these baseline trials. To test the LVF preference, two types of probe trials were given. In Aa/AA-aa probe trials, the sample was an original face and the comparisons were chimeric faces made from one half of the original face. In Ab/Aa-Bb probe trials, the sample was the chimeric face consisting of the left and right half of different persons' faces and the comparisons were the original face of these two persons. If LVF (that is, the right hemisphere) is dominant for face perception, the subject should select AA in Aa/AA-aa trials and Aa in Ab/Aa-Bb trials.

428 M. TOMONAGA

Responses to comparison stimuli on the probe trials were not reinforced (no food reward, no chime, and no buzzer). In these probe trials, there were four different combinations of the sample and comparison orientations, as it was the case in the baseline trials. Each session consisted of 64 baseline and 16 probe trials, in which 6 trials appeared for each orientation condition for Aa/Aa-Bb and Ab/Ab-Cd, 4 trials for AA/AA-aa (aa/aa-AA), and 2 trials for Aa/AA-aa and Ab/Aa-Bb. The subject was given six 2-session blocks. For probe trials, the percent LVF prefer-

Fig. 3. Schematic examples of baseline (aa/aa-bb and ab/ab-cd) and probe trials (ab/aa-cc and ab/bb-cc) that appeared in the discrimination test of Experiment 3. LVF: Left visual field; RVF: right visual field. Degree of sample and comparison rotations is indicated at the left side of the rows. See Figure 1 for captions.


ence was calculated. This index shows the proportion of trials in which the subject selected the comparison containing the left half of the sample face (AA and Aa).

Discrimination test: Figure 3 represents examples of trials in the second test series. Among 104 human face photographs, 68 (65.4%) showed a difference in brightness between the left and right halves: the right side was slightly brighter than the left due to the lighting condition. In total, the mean brightness was 129 (in 256 gray-scales) lbr the left half, while it was 146 for the right. This brightness asymmetry caused the distinctive difference in brightness between the chimeric stimuli that consisted of the same halves of a face such as AA and aa, depending on the side from which they were constructed. In the second phase, to avoid this biasing factor, chimeric faces were made from the right halves (i.e. brighter ones) of different persons (Aa and Bb), designated as "ab." These ab stimuli were presented as the sample during the probe trials. Comparison stimuli were aa (consisting of the left part of the sample ab) and cc (consisting of the right part of a different face Cc) for LVF probe trials, and bb (consisting of the right part of the sample) and cc for RVF probe trials. Thus, all chimeric stimuli were made from the right half of original faces in order to control the brightness difference. Responses to aa in the ab/aa- cc trials and to bb in the ab/bb-cc trials were reinforced. In addition to the two types of probe trials, two types of baseline trials (aa/aa-bb and ab/ab-cd) were presented. Each of these four types of trials was presented with 4 (2x2) different combinations of orientations, as in the preference test. The correspondence of left-right relationships between the sample and comparisons was based on the presented orientation of the sample but not on the absolute relationships (see Fig. 3). Each session consisted of 96 trials, in which 8 trials appeared for each baseline with 4 different orientation combinations and 4 trials for each probe with 4 different orientation combinations. As in the first test, six 2-session blocks were given to the subject.

RESULTS

Preference Test

The upper portion of Table 3 shows the mean percent error and response time for correct response for each baseline condition in the first test series as a function of sample and comparison orientations. Notice that the orientations of comparisons were relative values. A three-way

Table 3. Mean percent error and response time on correct trials for each of baseline and probe trials as a function of orientation combination in Experiment 4.

Percent error Response t ime (s)

0 ~ 180 ~ 0 ~ 180 ~

Sample comparisons relative 0 ~ 180 ~ 0 ~ 180 ~ 0 ~ 180 ~ 0 ~ 180 ~ Condition (absolute) (0 ~ (180 ~ (180 ~ (0 ~ (0 ~ (180 ~ (180 ~ (0 ~

Preference test Baseline Aa/Aa-Bb 6.9 13.9 11.1 19.4 0.704 0.835 0.674 0.708

Ab/Ab-Cd I 1.1 16.7 19.4 23.6 0.685 0.811 0.695 0.777 AA/AA-aa, aa/aa-AA 10.4 12.5 16.7 16.7 0.622 0.667 0.667 0.696

Discrimination test Baseline aa/aa-bb 11.5 6.3 14.6 10.4 0.649 0.737 0.653 0.737

ab/ab-cd 5.2 16.7 13.5 20.8 0.735 0.795 0.676 0.756

Probe ab/aa-cc (LVF) 31.3 29.2 20.8 31.3 0.679 0.810 0.696 0.738 ab/bb-cc (RVF) 22.9 33.3 20.8 37.5 0.693 0.767 0.788 0.772

430 M. TOMONAGA

ANOVA was conducted separately for the percent error and response time data, in which condition, sample orientation, and relative comparison orientation were within-session factors. For percent error, only the effect of sample orientation was significant [F(1,5)=8.69, p<0.05], while the effect of relative comparison orientation was marginal [F(1,5)=5.00, p=0.076]. For response time, the effects of condition [F(2,10)=6.01, p<0.05] and relative comparison orientation [F(1,5) = 12.71, p<0.05] were significant. These results indicated that the subject showed no difficulty in discriminating chimeric faces and showed a consistent inversion effect based on rotational matching for different types of faces. As in Experiment 1, inversion effect based on identity matching was evident in percent error (9.5% for upright-upright and 15.7% for inverted-Tinverted, averaged across baseline conditions) but not in response times (0.670s for upright-upright and 0.679s for inverted-inverted). On probe trials, however, the mean per- centage of LVF preference was 46.4% in total (range: 37.5-54.2), showing that the subject selected the comparison stimuli in a random manner.

Discrimination Test

The lower part of Table 3 shows the mean percent error and response time on correct trials for each type of baseline and probe trial as a function of orientation combination. The mean percent error for baseline trials (10.7% for aa/aa-bb and 14.1% for ab/ab-cd) was lower than that for probe trials (28.1% for ab/aa-cc and 28.7% for ab/bb-cc). An inversion effect based on iden, tity matching during baseline trials was evident in percent error (8.35% for upright-upright and 14.1% for inverted-inverted) but not in response times (0.692s for upright-upright and 0.665s for inverted-inverted). A three-way ANOVA with session blocks as repeated measures was conducted separately to the percent error and response time data, in which condition, sample orientation, and relative comparison orientation were within-session factors. For percent error, only the effect of condition was significant [F(3,15) = 8.02, p<0.01 ]. Fisher's LSD test revealed that each type of probe trials was significantly worse than each of the baseline trials (ps<0.05). For response time, the main effect of relative comparison orientation IF(1,5) = 19.03, p<0.01 ] and the interaction between sample and comparison orientations [F(1,5)---8.72, p<0.05] were significant. The interaction between condition and sample orientation was marginal [F(3,15)=3.10, p=0.059].

The inversion effect during probe trials based on identity matching was calculated by subtracting the data for the upright-upright condition from those for the inverted-inverted condition. Both for percent error and response time, there is no clear effect (percent error: -10.5% for LVF and -2 .1% for RVF trials; response times: 17ms for LVF and 95ms for RVF trials).

The inversion effect based on rotational matching for each probe trial for each sample orientation was again calculated by subtracting the data for relative orientation 0 ~ from 180 ~ Each effect was statistically tested with separate paired t tests. For percent error, there are no significant effects ( -4 .7% averaged across conditions). Figure 4 shows the inversion effect in response times. The effect for ab/aa-cc at sample orientation 0 ~ was significant [132ms, t(5)=5.88, p<0.01, two-tailed], but the others were not.

DISCUSSION

In the first phase, the subject showed no LVF (or RVF) preference for chimeric faces. This result can not simply be attributed to her inability to discriminate chimeric laces because she showed good performance on chimeric baseline trials (in total, she was 84.1% correct), which was comparable to the intact-face baseline trials (87.2% correct). In probe trials, both comparisons


Fig. 4. Inversion effect based on rotational matching for each probe-trial type and sample orientation in Experiment 3. The inversion effect was calculated by subtracting mean response times on "upright" trials from those on "inverted" trials. LVF: Left visual field; RVF: right visual field.

contained the left or right halves of the sample. For the chimpanzee both comparisons might be "correct." This ambiguity might disrupt the subject's probe performance. The other possibility is a disruptive effect of nonreinforcement. When using nonreinforcement on probe trials, the chimpanzee's performance may easily decline to random in the course of testing (e.g. TOMONAGA et al., 1991). It may be due to the dominance of position or stimulus biases, or to win-stay-lose-shift strategy with respect to the positions of the comparison stimuli.

Unlike the first test, the subject showed a difference in the inversion effect based on rotational matching among probe trials in the discrimination test. For upright samples, the inversion effect based on response time was significant when the correct comparison was made from the left part (ab/aa-cc) but not when it was of the right part (ab/bb-cc). For inverted samples, she showed no significant inversion effect in both types of probe trials. For the present chimpanzee subject, upright faces might be processed dominantly in the right hemisphere. As noted before, the present results were derived from only one subject. One should be cautious to draw the conclusion that all chimpanzees show LVF (i.e. right hemispheric) dominance in the inversion effect in face perception. In nonhuman primates, as in humans, many aspects of visual processing are functionally specialized in each hemisphere, especially face perception, spatial cognition, recognition of shapes, processing modes such as global or local, semantic processes, and so on. Again, we should be careful in discussing the present results in terms of special processing for faces in chimpanzees. The present results might possibly be due to the specialization for complex forms in general (cf. HELUGE, 1993). We should further examine the relationship between each of perceptual and cognitive specializations. If we can clarify these relations among specific hemispheric specializations, single-subject research, as in the present case, will be much more fruitful.

GENERAL DISCUSSION

The present study investigated the inversion effect on face perception in a chimpanzee. As described in the introduction, the inversion effect can be tested in two ways: identity matching between the same stimuli in the same orientations and rotational matching between the same stimuli in different orientations. In the present experiments these two aspects were examined in the chimpanzee. In Experiment 1, the chimpanzee was tested under the identity-matching para-

432 M. TOMONAGA

Fig. 5. Inversion effect assessed with identity matching with rotated faces. Each point shows the data from each of the seven identity-matching conditions in Experiments 1-3. Each bar shows the average across these conditions.

digms, and showed better accuracy for the upright-upright condition than for the inverted- inverted condition when the photographs were faces but not when they were houses. In Experiment 2, the subject was given rotational matching, and she showed a clear inversion effect specific to the photographs of laces. The same pattern of results was also seen in the baseline trials of Experiment 3.

In Experiments 2 and 3, the subject was also given identity-matching conditions. Figure 5 shows the percent error and response times for correct responses for each of the seven identity- matching conditions with rotated faces that were used in Experiments 1 -3 (Experiment l, Experiment 2, Aa/Aa-Bb, Ab/Ab-Cd, and AA/AA-aa in the baseline for the preference test in Experiment 3, aa/aa-bb and ab/ab-cd in the baseline for the discrimination test in Experiment 3) as well as the mean values. The mean percent error was 10.5% for upright-upright and 15.5% for inverted-inverted matching [paired t test, t(6)=2.86, p<0.05, two-tailed], while the response time was 0.713s for upright-upright and 0.709s for inverted-inverted matching [t(6)=0.14, p>0.05]. On the other hand, data from the two identity-matching conditions with photographs of houses (Experiments 1 and 2) did not show such an effect; the mean percent error was 15.3% for upright-upright matching and 9.3% for inverted-inverted matching (not available for statistical testing). The mean response time was 0.775s for upright-upright matching and 0.782s for inverted-inverted matching. This analysis clearly indicates that the chimpanzee showed an inversion effect in identity matching with rotated faces but not with rotated houses.

Experiment 2 also provided additional evidence of the inversion effect. The chimpanzee showed better accuracy when the sample was presented at 0 ~ than when the comparison was at 0 ~ This result clearly indicated the difficulty in memorization of well-configured patterns with unnatural orientations (CAREY & DIAMOND, !977); this difficulty might be one source of the inversion effect. This difference in performance between upright and inverted face samples was replicated well in the baseline trials of Experiment 3. In the average across five baseline conditions, Chloe showed 13.2% errors in upright-inverted matching and 18.2% in inverted-upright matching It(4) = 8.972, p<0.001 ].


The present finding is inconsistent with our previous study (TOMONAGA et al., 1993) which showed the lack of or a reduced inversion effect in another chimpanzee's perception of faces under a naming task. It should be noted again that the present experimental setting was difl'erent from the previous one in the size of the stimulus set, familiarity of the stimulus faces, and the basic task requirement. As noted in the introduction, a small number of stimuli may enhance the subject's use of featural processing of the faces (BRucE, 1982). Furthermore, many studies with humans as subjects have indicated that familiarity could modulate the processing of faces. For example, VALENTINE and BRUCE (1986) showed that human subjects showed a stronger inversion effect with faces of other races than with own-race faces. ELLIS et al. (1979) found that for recognizing familiar faces humans mainly used local (inner) features of the faces, suggesting a difference in processing between familiar and unfamiliar faces. BRUCE (1983) pointed out that "naming" also enhances the familiarity of faces. Taken together, the results from the present experiments and related studies, the previous finding with one chimpanzee (TOMONAGA et al., 1993) might have resulted from the use of the small number of stimuli and the use of faces highly familiar to the subject. Familiarity may modulate the processing of faces also in nonhuman primates. TOMONAGA (1998) and TOMONAGA et al. (1993) discussed the possibility of an effect of ecological constraints on spatial perception, including face perception. To address this issue, we need further investigations with various primate species adapted to either arboreal or terrestrial environments.

Recently, the global precedence effect (NAVON, 1977) on the processing of hierarchical visual patterns in primates were extensively investigated (FAGOT & TOMONAGA, 1999; DERUELLE & FAGOT, 1998; HOPKINS, 1997). The global-local distinction is closely related to the mode of processing (holistic or local) of faces (CAREY & DIAMOND, 1977; HELLIGE et al., 1984). The global properties of hierarchical stimuli correspond to second-order relational properties, while local properties correspond to features. In human perception global properties dominate over local properties (NAVON, 1977). This tendency is weakened in chimpanzees (FAGOT & TOMONAGA, 1999), and local processing is dominant in baboons (DERUELLE & FAGOT, 1998). The relationship between perception of faces and hierarchical stimuli in nonhuman animals is still unclear. There might be a species difference related to these processes.

The face-inversion efl'ect as assessed with rotational matching is closely related to mental rotation (YIN, 1969; ROCK, 1974; VALENTINE & BRUCE, 1988). Humans show "mental rotation," that is, a linear increase of response times as a function of degree of rotation between sample and comparison stimuli during mirror-image discrimination of complex patterns (SHEPARD & METZLER, 1971). With non mirror-image pairs, humans showed no evidence of mental rotation (DELIUS & HOLLARD, 1995). Furthermore, VALENTINE and BRUCE (1988) found mental rotation of faces by using a successive matching procedure, similar to the one used in the present experiments. On the other hand, nonhuman animals such as pigeons failed to show a mental rotation effect (DELIUS & HOLLARD, 1995; HOLLARD & DELIUS, 1982; but see HAMM et al., 1997). Baboons also showed less clear-cut evidence of mental rotation (HOPKINS et al., 1993; VAUCLAIR et al., 1993). Nonhuman animals showed a strong rotational invariance even for mirror-image patterns, while humans only show invariance for non mirror-image patterns. This fact implies that there might be a substantial difference in processing rotated stimuli between humans (and the chimpanzee) and other nonhuman animals. In the present experiments, the photographs of houses were used as control stimuli. Faces were highly homogeneous to each other, while the houses were not as similar (see Fig. 1). As DIAMOND and CAREY (1986) noted, the inversion effect occurs when members of a class can be difl'erentiated on the basis of distinctive relations among the elements that define the common configuration. These relations are called second- order relational properties. The photographs of houses used in the present experiments had no

434 M. TOMONAGA

common configuration as seen in Figure 1. They could be distinguished on the basis of the difference of features (roofs, windows, doors, and so on). For the house stimuli, this difference between these stimulus classes may have prevented an inversion effect based on both identity and rotational matching for houses. We might have obtained an inversion effect for houses if we had used the set of photographs that met the criterion DIAMOND and CAREY (1986) indicated: houses with common configuration but different relations among features.

By using faces, however, pigeons showed no inversion effect (PHELPS & ROBERTS, 1994). They might use specific features such as eyes or mouths to discriminate faces (cf. JITSUMORI & YOSHIHARA, 1997). These results suggest the possibility that nonhuman animals would not show an inversion effect for highly configural stimuli if they do not have the expertise (highly over- learned skill) to make use of the distinctive relational properties of these stimuli. In the present experiments, I did not use photographs of chimpanzees but of humans. The present subject was born in a zoological garden and has been raised by humans, so she might have an expertise for human faces. If so, the present results in a chimpanzee with human photographs might offer another strong evidence for the effects of "expertise" on the inversion effect (DIAMOND & CAREY, 1986). There is, however, another possibility. Human faces might be similar enough in their morphological structure to the chimpanzee faces to cause an inversion effect without special experience or expertise (PARR et al., 1998). This possibility is related to the issue of the "face schema" (GOLDSTEIN & CHANCE, 1980). To address this issue, we need to test the inversion effect with conspecific faces (that is, chimpanzees; e.g. PARR et al., 1998; PHELPS & ROBERTS, 1994; WRIGHT & ROBERTS, 1996) and other species faces such as dogs which are unfamiliar to the subject (e.g. DIAMOND & CAREY, 1986). If the chimpanzees have a generalized face schema, the inversion effect should be observed for various types of faces. If they have only the limited schema specific to their own species faces, they should show no inversion effect for quite different species such as dogs, and the present results can be explained by the expertise effect.

In Experiment 3, I tried to explore the possibility of hemispheric specialization in the inversion effect. The results are limited but show the possibility of right hemispheric dominance for this effect. The limited evidence might be due to the free-viewing condition in which the present experiment was conducted. If the subject moved her eyes during the presentation of the chimeric sample, each half of the face would be projected to both visual fields. One way to prevent this is to reduce the presentation time of the sample from 0.5 s to shorter (such as 150 ms, shorter than a single saccade) and to control the subject's eye movement. There are several tech- niques available that can keep the subject's eye fixation such as the use of the joystick (MORRIS &HOPKINS, 1993; WILDE et al., 1994). The chimeric face test is a convenient way to test hemispheric specialization, but need to be developed further for application in nonhuman primates.

In conclusion, the chimpanzee clearly showed an inversion effect specific to laces both under identity- and rotational-matching paradigms. However, some questions still remain, such as the effect of familiarity, the expertise effect, the generality of this effect to the faces of other species, and the relationship to hemispheric specialization between face perception and other visual processing. These questions should be addressed in future research.

Acknowledgments. I would like to thank the staff of the Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University. In particular, I thank Mr. SUMIHARU NAGUMO for his techni- cal advice, l also thank Dr. M. JITSUMOm and 1. H. IVERSEN for their critical comments on the manuscript. A part of this research was presented at the 14th annual meeting of the Primate Society of Japan, at lnuyama, Aichi, Japan, June 1995. This research was supported financially by a Grant-in-Aid for Scientific Research to the author from the Ministry of Education, Science, Sports, and Culture, Japan (Grant No. 04710051, No. 05710050).


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- - Received: December 15, 1997; Accepted: February 23, 1999

Author's Name and Address: MASAKI TOMONAGA, Department ~/ Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, lnuyama, Aichi 484-8506, Japan. e-mail: [email protected]

inversion effect in perception of human faces in a...

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