Primates (2007) 48:1–12
DOI 10.1007/s10329-006-0011-4
O R I G I N A L A RT I C L E
Visual search for orientation of faces by a chimpanzee
(Pan troglodytes): face-specific upright superiority
and the role of facial configural properties
Masaki Tomonaga
Received: 3 February 2006 / Accepted: 4 July 2006 / Published online: 13 September 2006
Japan Monkey Centre and Springer-Verlag 2006
Abstract A previous experiment showed that a
chimpanzee performed better in searching for a target
human face that differed in orientation from distractors when the target had an upright orientation than
when targets had inverted or horizontal orientation
[Tomonaga (1999a) Primate Res 15:215–229]. This
upright superiority effect was also seen when using
chimpanzee faces as targets but not when using photographs of a house. The present study sought to extend these results and explore factors affecting the
face-specific upright superiority effect. Upright superiority was shown in a visual search for orientation
when caricaturized human faces and dog faces were
used as stimuli for the chimpanzee but not when shapes
of a hand and chairs were presented. Thus, the configural properties of facial features, which cause an
inversion effect in face recognition in humans and
chimpanzees, were thought to be a source of the upright superiority effect in the visual search process. To
examine this possibility, various stimuli manipulations
were introduced in subsequent experiments. The results clearly show that the configuration of facial features plays a critical role in the upright superiority
effect, and strongly suggest similarity in face processing
in humans and chimpanzees.
M. Tomonaga (&)
Language and Intelligence Section,
Primate Research Institute, Kyoto University,
Inuyama, Kanrin 484-8506, Japan
e-mail: [email protected]
Introduction
Faces are quite important stimuli for primates,
including humans. We obtain a variety of information
from the face, including identity, expression, sex, age,
and attention. In humans, it is well known that face
processing is quite different from the processing of
other visual stimuli. One of the most striking phenomena in face perception is deteriorated recognition
when faces are presented in an inverted orientation
(Valentine 1988; Yin 1969). The inversion effect is
generally limited to facial stimuli (cf. Diamond and
Carey 1986) and is considered specific to faces because
we process the face as a whole (Diamond and Carey
1986; Farah et al. 1995; Tanaka and Farah 1991). Faces
consist of several features, such as the eyes, nose, and
mouth. We recognize facial identity not on the basis of
each feature separately but on the configural properties
of the features. Diamond and Carey (1986) also pointed out that the configural properties of objects can be
classified into two types: first-order relational information, which consists of the spatial relations of the
parts of an object with respect to one another, and
second-order relational information, which consists of
the spatial relations of the parts relative to the prototypical arrangement of the parts (see also Farah et al.
1995). Humans form face prototypes during prolonged
experience of a variety of faces, and as a result, they
can encode second-order relational information in faces (Diamond and Carey 1986).
Numerous past studies have explored face processing in nonhuman primates (Bruce 1982; Dittrich 1990;
Hamilton and Vermeire 1983, 1988; Kanazawa 1996;
Keating and Keating 1993; Martin-Malivel and Fagot
2001; Matsuzawa 1990; Overman and Doty 1982; Parr
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Primates (2007) 48:1–12
et al. 1998, 1999; Perrett and Mistlin 1990; Phelps and
Roberts 1994; Rosenfeld and Van Hoesen 1979; Tomonaga 1994, 1999a, b; Tomonaga et al. 1993; Wright
and Roberts 1996). Several decades ago, face inversion
effect studies were inconclusive in nonhuman primates
(Bruce 1982; Dittrich 1990; Rosenfeld and Van Hoesen
1979), but recent progress in this area has confirmed
that nonhuman primates perceive faces much as humans do (Hamilton and Vermeire 1988; Martin-Malivel and Fagot 2001; Overman and Doty 1982; Parr
et al. 1998; Phelps and Roberts 1994; Tomonaga 1994,
1999b; Wright and Roberts 1996). For example, Tomonaga (1999b), using a delayed matching paradigm,
reported that chimpanzees (Pan troglodytes) clearly
showed the inversion effect when human faces were
used as stimuli, but not when houses were used. Parr
et al. (1998) obtained similar results in chimpanzees
when using chimpanzee, capuchin, and human faces as
stimuli. Martin-Malivel and Fagot (2001) reported the
inversion effect in baboons (Papio papio) using the
priming paradigm. Several studies have also reported
the inversion effect in face perception by macaques
(e.g., Hamilton and Vermeire 1983, 1988; Overman
and Doty 1982; Phelps and Roberts 1994; Wright and
Roberts 1996).
Simple discrimination and matching tasks have been
commonly used to examine the inversion effect (Bruce
1982; Parr et al. 1998; Tomonaga 1999b; Yin 1969).
However, visual search tasks have also been increasingly employed to study face perception and recognition (Hansen and Hansen 1988; Levin 1996; Lewis and
Edmonds 2005; Montoute and Tiberghien 2001;
Nothdurft 1993; Öhman et al. 2001; Senju et al. 2005;
Suzuki and Cavanagh 1995; Tong and Nakayama 1999;
von Grünau and Anston 1995; Williams et al. 2005). In
a typical visual-search task, participants are required to
report the presence or absence of a predefined target
among distractors (Treisman and Gelade 1980). When
using animal subjects, the tasks are slightly modified,
and subjects are required to detect and respond to
123
TGT: Inv
Response Time (s)
Fig. 1 Upright superiority
effect for orientation during
visual search of faces
(Tomonaga 1999a). A
chimpanzee subject showed a
more efficient search for the
upright human face target
among disoriented faces.
From Visual search for
orientation of faces by a
chimpanzee (Pan troglodytes)
by Tomonaga (1999a)
(peck, point, or touch) a target (Blough 1979; Tomonaga 1993a, 2001a).
Using this visual-search task, I previously investigated the inversion effect with a chimpanzee as the
subject (Tomonaga 1999a). An adult chimpanzee was
trained for a visual-search task for photograph orientation. The subject was required to detect and touch
the target differing in orientation from the distractors.
Using human faces in three different orientations
(upright, horizontal, and inverted), the chimpanzee
showed better performance when the upright face appeared as the target against horizontal or inverted distracters than vice versa (Fig. 1; left and center
panels).In contrast, when horizontal and inverted faces
were paired, such visual search asymmetry was not
obtained (Fig. 1; right panel). Subsequent experiments
in which photographs of chimpanzee faces and houses
were used in addition to human faces further confirmed
and extended this upright superiority effect in visual
search. The chimpanzee showed the upright superiority
effect for chimpanzee faces but not for houses. These
results indicate that the upright superiority effect, defined as a more efficient search performance for upright stimuli than for other orientations, is specific to
facial stimuli, and that this effect seems to be closely
related to the inversion effect in face recognition by
humans and chimpanzees (Parr et al. 1998; Tomonaga
1999b; Valentine 1988; Yin 1969). Tomonaga (2001a)
replicated this upright superiority effect in visual
search using another chimpanzee as a subject. This
chimpanzee found the human face more quickly when
the target was upright than when the target was horizontal or inverted.
The present study aimed to extend the results of the
previous study (Tomonaga 1999a). In Experiments 1
and 4, the specificity of the upright superiority effect to
facial stimuli was further tested using various types of
facial stimuli (human caricaturized faces, dog faces,
and schematic faces) and non-face stimuli (human
hand shapes, chairs, and schematic faces with scram-
1.6
Up vs. Inv
Up vs. Hor
Hor vs. Inv
1.4
TGT: Hor
TGT: Inv
1.2
TGT: Hor
1.0
TGT: Up
0.8
TGT: Up
0.6
0.4
1 3
6
12
1 3
6
12
Number of Stimuli
1 3
6
12
Tomonaga (1999a)
Primates (2007) 48:1–12
bled features). To test the possibility that the facespecific upright superiority effect is caused by the
configural processing of faces by the chimpanzee, each
facial part (eyes, nose, and mouth) was presented alone
or in combination with the spatial configuration
(Experiments 2–4).
General methods
Subject
An adult female chimpanzee (Pan troglodytes), Chloe,
participated in the present experiments (see Fig. 2). At
the onset of the experiments, she was 17 years old. She
has experienced various types of computer-controlled
perceptual–cognitive tasks (Tomonaga 1993b, 1999c;
Tomonaga and Matsuzawa 1992), including visual
search tasks (Fagot and Tomonaga 1999; Tomonaga
1993a, 1995, 1997, 2001a, 2001b). She has also experienced face recognition tasks using a matching paradigm (Tomonaga 1999b). Immediately before the onset
of the present experiments, Chloe had been tested in
visual search for orientation of photographs including
human and chimpanzee faces and had exhibited the
face-specific upright superiority effect, as mentioned in
the introduction (Tomonaga 1999a). Chloe lives in a
social group of 11 individuals in an environmentally
enriched outdoor compound (770 m2; Ochiai and Matsuzawa 1998) connected to the experimental room by
a tunnel. No special food or water deprivation was
conducted during the present study. Care and use of
the chimpanzees adhered to the 2002 version of the
Guide for Care and Use of Laboratory Primates by the
3
Primate Research Institute, Kyoto University, Japan.
The research design was approved by the Animal
Welfare and Animal Care Committee of the Primate
Research Institute.
Apparatus
Sessions were conducted inside an experimental booth
for chimpanzees (1.8·2.15·1.75 m). A 21-inch color
CRT monitor (NEC PC-KH2021) with a capacitive
touchscreen device (Microtouch SM-T2) was installed
15 cm from the floor on one side of the booth.
Touching the monitor surface with a finger was defined
as a response. The screen was protected from deterioration by a transparent Plexiglas panel, fitted with an
armhole (10·47 cm) that allowed hand contact with
the CRT. The resolution of the monitor was 640·400
pixels. One hundred pixels corresponded to 55 mm.
The subject sat approximately 40 cm away from the
monitor surface, so 100 pixels corresponded to 8 of the
visual angle, and the length of 1 corresponded to
approximately 7 mm (13 pixels). A food tray was installed below the CRT. A universal feeder (Biomedica
BUF-310) delivered pieces of food (apples or raisins)
to this tray. The equipment was connected to a personal computer (NEC PC-9821 Xn) that controlled the
stimulus display, detected touches on the CRT, delivered rewards, and collected data.
Procedure
Figure 2 shows a typical visual search task trial. Each
trial began with presentation of the start key (blue
circle, 30 pixels in diameter) at the bottom center of
Fig. 2 A chimpanzee, Chloe,
performing a visual search for
orientation of faces
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4
the CRT monitor and an accompanying 0.5-s beep.
Immediately after the subject responded, the start key
disappeared, and the search display appeared on the
screen. The search display consisted of a 4·3 predefined stimulus presentation area and contained one
target stimulus and several uniform distractors different from the target but identical to each other (see
Fig. 2). Configurations of the search display randomly
changed from trial to trial. The target position was
counterbalanced. The task for the subject was to detect
the target and touch it on the screen. When the
chimpanzee touched the target, all the stimuli except
the target disappeared, a chime sounded, and a food
reward (small pieces of apple or raisins) was delivered
to the food tray followed by the termination of the
touched stimulus. When the chimpanzee made an error
(i.e., touched one of the distractors), a buzzer sounded,
and the identical search display was represented once
again; if a novel incorrect response was given, only the
target stimulus was represented on the screen in a
second correction trial. This correction procedure was
introduced because previous experiments have demonstrated that chimpanzees may stop working when
the rate of non-reinforced trials is too high (cf. Fagot
and Tomonaga 1999).
Experiment 1
In the first experiment, Chloe was tested with various
kinds of photographs including face and non-face
stimuli to extend the previous results by showing the
face-specific upright superiority effect in visual search
for a stimulus by orientation.
Methods
In Experiment 1, five types of 256-step grayscale photographs were used as stimuli (see Fig. 3): human faces,
human caricature faces, dog faces, human hand shapes,
and chairs. Each stimulus was 100·100 pixels in size.
For human faces, frontal views of 104 Japanese males
were used. These faces were identical to those used in
previous experiments (Tomonaga 1999a, b). For each
of the other categories, 36 different photographs were
prepared. Various types of hand signs were prepared
(such as a ‘‘V’’ sign) for the hand stimulus. For each
stimulus, global luminance was roughly equalized and
retouched onto the gray background using Paintshop
Pro 3.0. Each stimulus was prepared with three different orientations: upright (up), horizontal (hor), and
inverted (inv). By combining these orientations, six
target–distractor pairs of orientation were prepared.
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Primates (2007) 48:1–12
Each session consisted of 60 trials. In each session,
five types of stimuli and two numbers of stimuli (i.e.,
the numbers of a target and distractors in the search
display: 4 and 10) appeared equally and randomly, but
the target–distractor combination of orientation was
fixed. The subject received two sessions in a day; in
each session, the target and distractor orientations
were reversed. Each type of session was presented in a
random order and repeated more than 16 times. To
analyze the subject’s steady-state performance, the last
eight sessions for each condition were used for data
analyses.
Results and discussion
Table 1 shows the mean percentage of errors for each
condition. Chloe clearly made more errors for non-face
than for face stimuli and for horizontal versus inverted
(hor vs. inv) than for the other orientation combinations. A two-way analysis of variance (ANOVA) with
orientation (up vs. inv, up vs. hor, and hor vs. inv,
averaged across the target–distractor combination and
number of stimuli) as the between-session factor and
stimuli (five types) as the within-session factor, confirmed that both main effects [orientation,
F(2,21)=17.43, P<0.001; stimuli; F(4,84)=133.15,
P<0.001] and interaction [F(8,84)=6.56, P<0.001] were
significant. Post hoc multiple comparisons using Ryan’s
procedure indicated that errors for three types of facial
stimuli were significantly less than for the other nonfacial stimuli (P<0.001). Among the three types of facial stimuli, Chloe made more errors for dog faces than
for human and caricature faces (P<0.01). Furthermore,
there were significantly more errors for the hor vs. inv
condition than for the up vs. inv or up vs. hor conditions, when only the three types of facial stimuli were
presented (P<0.05).
Figure 3 shows the mean response times for each
condition. As shown in Table 1, the subject performed
very poorly under some conditions; the response times
from incorrect trials (correction trials were excluded)
were also used for analyses. Incorrect response times
were not used if the subject showed a ‘‘speed–accuracy
trade-off,’’ i.e., a faster (guessing) response in incorrect
trials than in correct trials. However, Chloe showed
longer response times on incorrect trials than on correct trials, so that response times averaged across
‘‘total’’ trials were a good measure in this study (cf.
Tomonaga and Matsuzawa 1992). Thus, subsequent
analyses used response times averaged across correct
and incorrect trials. Separate two-way (target orientation · number of stimuli) ANOVAs with sessions as
repeated measures were conducted for response-time
Primates (2007) 48:1–12
5
Fig. 3 Mean response times
for each condition in
Experiment 1. Examples of
each stimulus set are also
shown in each panel.
**P<0.01; ***P<0.001. TGT
Target, DST distractor, Up
upright, Hor horizontal, Inv
inverted
3.5
Human
Face
3.0
2.5
2.0
**
1.5
***
TGT/DST
1.0
Up/Inv
Inv/Up
Response Times (s)
0.5
3.5
Human
Caricature
Face
3.0
2.5
***
2.0
Up/Hor
Hor/Up
Hor/Inv
Inv/Hor
Human
Hand
p=0.061
***
1.5
1.0
0.5
Dog
Face
3.5
3.0
p=0.079
2.5
Chair
***
2.0
1.5
1.0
Up vs. Inv
Up vs. Hor
Hor vs. Inv
Up vs. Inv
Up vs. Hor
Hor vs. Inv
0.5
4
10
4
10
4
10
4
10
4
10
4
10
Number of Stimuli
Table 1 Mean percent errors for each condition in Experiment 1. Up Upright, Hor horizontal, Inv inverted
Stimulus set
Number of stimuli
Up vs. inv
Up/inv
Human face
Caricature face
Dog face
Human hand
Chair
a
4
10
Average
4
10
Average
4
10
Average
4
10
Average
4
10
Average
2.1
6.3
4.2
4.2
6.3
5.2
22.9
6.3
14.6
52.1
35.4
43.8
77.1
85.4
81.3
a
Up vs. hor
Hor vs. inv
Inv/up
Average
Up/hor
Hor/up
Average
Hor/inv
Inv/hor
Average
18.8
14.6
4.2
35.4
10.4
22.9
25.0
12.5
18.8
29.2
39.6
34.4
54.2
52.1
53.1
10.4
10.4
10.4
19.8
8.3
14.1
24.0
9.4
16.7
40.6
37.5
39.1
65.6
68.8
67.2
4.2
6.3
5.2
0.0
4.2
2.1
6.3
8.3
7.3
39.6
22.9
31.3
54.2
70.8
62.5
10.4
0.0
5.2
12.5
2.1
7.3
18.8
14.6
16.7
37.5
33.3
35.4
56.3
50.0
53.1
7.3
3.1
5.2
6.3
3.1
4.7
12.5
11.5
12.0
38.5
28.1
33.3
55.2
60.4
57.8
37.5
16.7
27.1
20.8
4.2
12.5
31.3
29.2
30.2
27.1
16.7
21.9
52.1
66.7
59.4
25.0
16.7
27.1
45.8
27.1
36.5
50.0
43.8
46.9
33.3
31.3
32.3
58.3
75.0
66.7
31.3
16.7
24.0
33.3
15.6
24.5
40.6
36.5
38.5
30.2
24.0
27.1
55.2
70.8
63.0
Target/distractor
data of each of the trials. Table 2 summarizes the
results of these ANOVAs. As shown in Fig. 3 and
Table 2, the subject showed longer response times
when the number of stimuli was larger. Furthermore,
the subject’s behavior was significantly affected by the
target orientation when the facial stimuli were used,
but this effect was seen only when the upright orientation and another orientation were paired. For all
123
6
Table 2 Summary of
ANOVAs (F-statistics)
conducted on the responsetime data from Experiment 1.
TGT target orientation, N
number of stimuli
Primates (2007) 48:1–12
Stimulus set
Factor
Up vs. inv
Up vs. hor
Hor vs. inv
Human face
TGT
N
TGT
TGT
N
TGT
TGT
N
TGT
TGT
N
TGT
TGT
N
TGT
13.21**a
21.91**
3.48
30.09***
20.12**
1.49
4.21P = 0.079
94.21***
0.04
3.91
22.83**
0.47
0.65
23.48**
0.11
74.66***
37.37***
10.61*
81.16***
21.90**
4.88 P = 0.063
6.47*
18.41**
0.28
3.12
54.23***
0.20
3.69
59.63***
0.01
0.03
14.11**
1.59
4.96P = 0.061
53.78***
3.14
0.00
28.26**
2.00
0.74
19.77**
2.31
2.42
13.21**
2.56
Caricature face
Dog face
Human hand
a
Degree of freedom for each
F-value was 1,7
*P<0.05, **P<0.01,
***P<0.001
Chair
facial stimuli, Chloe showed faster response times for
upright targets than for other target orientations.
The results of Experiment 1 clearly replicated and
extended the results of the previous study (Tomonaga
1999a). The same subject as in Tomonaga (1999a)
demonstrated the upright superiority effect for orientation during visual search only when facial stimuli
were used. These results provide further evidence that
chimpanzees process facial stimuli using configural
properties of facial features. Furthermore, the ability
to recognize a stimulus as a ‘‘face’’ is not limited to
own-species or highly familiar types of stimuli (e.g.,
human and chimpanzee faces) but applicable broadly
to stimuli that contain facial configurations (e.g., caricature and dog faces). If this is correct, chimpanzees
should show similar results when the much simpler
‘‘facial’’ patterns that are frequently used in studies
with human adults and infants (e.g., Johnson and
Morton 1991; Nothdurft 1993; Öhman et al. 2001) are
used. Experiment 4 examined this possibility.
The subject’s more efficient detection of various
types of upright face in the present experiment is
inconsistent with some previous experiments. Parr
et al. (1998) reported that chimpanzees showed a clear
inversion effect for human and chimpanzee faces but
not for capuchin faces when using the rotational
matching paradigm. Wright and Roberts (1996) found
that rhesus macaques showed the inversion effect for
human faces but not for monkey faces. Phelps and
Roberts (1994) also reported that squirrel monkeys
showed the inversion effect only for human faces but
not for monkey faces. There was, however, quite a
large difference in the task demand between the
present study and these previous experiments. The
previous experiments required subjects to perform
individual recognition (or picture matching), while the
present experiment required the chimpanzee to
123
·N
·N
·N
·N
·N
discriminate the orientation of stimuli (cf. Ballaz et al.
2005; Jitsumori and Matsuzawa 1991). This critical
difference in task demand may have been responsible
for the different outcomes.
Experiment 2
Experiment 1 further indicated that the upright superiority in visual search for orientation in the chimpanzee was face-specific. As noted in the introduction, this
specificity may have reflected configural processing of
faces by the chimpanzee subject. In Experiment 2 the
facial stimuli were manipulated to examine this possibility directly.
Methods
In this experiment, facial features (eyes, nose, and
mouth) were presented alone or in combination while
maintaining the spatial configurations (see Fig. 4).
Sixty new Japanese male faces were prepared and
manipulated using Paintshop Pro 3.0. Among six types
of manipulated stimuli (test stimuli) presented on the
gray background, only single features were presented
for the three types in which each feature was mounted
at the center; two types of features were paired in the
other three types of stimuli. These stimuli were arranged in two orientations, upright and inverted.
Each session consisted of 72 trials. In half of the
trials, original (intact) faces were presented, while in
the other half of the trial’s test stimuli were presented.
Original and test stimuli appeared alternately in a
session. The order of original and test stimuli was
randomly counterbalanced. In this experiment, only
one number of stimuli (10) was used. As in Experiment
1, the chimpanzee received two successive sessions in a
Primates (2007) 48:1–12
4.0
*
Response Times (s)
Fig. 4 Mean response times
for each condition in
Experiment 2. *P<0.05;
**P<0.01; ***P<0.001
7
3.5
***
3.0
2.0
TGT/DST
*
2.5
Up/Inv
Inv/Up
**
1.5
1.0
0.5
Original
Nose
Eyes
(with
Eyebrows)
day. The target orientation was reversed between each
session. If the subject made an incorrect response, in
the next correction trial only the target was presented
to minimize the possibility of learning during sessions.
Chloe received eight sessions for each target-orientation condition.
Results and discussion
On average, the subject correctly detected a target in
96.2, 56.3, 18.8, 11.5, 86.5, 89.6, and 38.5% of original,
eyes, nose, mouth, eyes + nose, eyes + mouth, and
nose + mouth trials, respectively. The results of oneway ANOVA showed a significant main effect of
stimulus type [F(5,35) =75.39, P<0.001]. Post hoc
multiple comparisons (Ryan’s procedure) clearly
showed no significant difference between performances for nose and mouth and between eyes + nose
and eyes + mouth. Figure 4 shows the mean response
times (averaged for correct and incorrect trials) for
each condition. As shown in this figure, the upright
superiority effect was seen only when the eye region
was presented alone or combined with other features.
Independent paired t-tests verified this inspection
[original, t(7)=5.166, P<0.01; eyes, t(7)=3.492, P<0.05;
eyes + nose, t(7)=7.851, P<0.001; eyes + mouth,
t(7)=3.063, P<0.05].
The results of Experiment 2 indicated that the upright
superiority effect was stronger when the facial features
were presented with their spatial configuration intact
than when the features were presented alone. These
results support the hypothesis that the upright superiority effect in the chimpanzee is based on the configural
processing of faces. Furthermore, the eye region was
necessary for the upright superiority effect to occur. The
Mouth
Eyes
+
Nose
Eyes
+
Mouth
Nose
+
Mouth
latter finding is quite interesting given that primates,
including humans, generally pay attention to the eyes
when viewing the face (Gothard et al. 2004; Hunnius
and Geuze 2004; Keating and Keating 1993; Luria et al.
1964; Nahm et al. 1998; Sato and Nakamura 1999; Yarbus 1967). It is plausible that chimpanzees may also pay
attention predominantly to the eye region of the facial
image given the finding that chimpanzee infants prefer
direct-gaze human faces to averted-gaze faces (MyowaYamakoshi et al. 2003). Chloe showed upright superiority when the eye region was presented alone. However, we should interpret these results with caution
because the eyes stimuli used in the present experiment
combined eyes and eyebrows. The spatial configuration
of the eyes and eyebrows may be sufficient to cause the
upright superiority effect. This possibility was further
tested in Experiment 4.
Experiment 3
Experiment 3 tested the effects of outer facial contours. In the previous experiments, the facial stimuli
included hair, ears, and facial contours, unlike those
commonly used for human experiments, in which
these features are removed by trimming with an
elliptic window (e.g., Senju et al. 2005; Yamaguchi
et al. 1995). Human adults recognize familiar faces
better by their internal parts than their external parts
(Ellis et al. 1979), but younger children show the
opposite tendency (Campbell et al. 1995). To rule out
the possibility that the chimpanzee predominantly
used external parts during the visual-search task,
external and internal parts were presented separately
in Experiment 3.
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Primates (2007) 48:1–12
Methods
Experiment 4
The 60 original faces were the same as those used in
Experiment 2. In the external parts stimuli, the inner
facial features were replaced by a gray ellipse. In the
internal parts stimuli, only the inner facial features
were presented in an elliptic contour on the gray
background (see Fig. 5). Each session consisted of 72
trials, of which half were the original face trials and the
other half were the test (external and internal stimuli,
six trials each) and catch trials (in which no target was
presented). The procedure was the same as in Experiment 2.
In the final experiment, two sets of stimuli were used
for additional testing. The first set was of schematic
faces (and those with features in scrambled patterns) to
extend the results of Experiment 1. The second set was
eyes + eyebrows (the same as in the eyes stimuli in
Experiment 2) and eyes-only stimuli, in which the
eyebrows had been removed from the eyes + eyebrows
stimuli. These were used to confirm the results of
Experiment 3.
Results and discussion
The original faces were the same as those in
Experiments 2 and 3. For schematic faces, three
different eye parts and two different mouthparts
were combined to yield six different schematic faces
(see Fig. 6). Each facial feature was randomly arranged to create six corresponding scrambled patterns. The eyes + eyebrows stimuli were the same as
the eyes stimuli used in Experiment 2. For the eyesonly stimuli, the eyebrow region was removed from
each of the eyes + eyebrows stimuli (see Fig. 6).
Each session consisted of 48 trials. In half of the
trials, original faces were presented and in the other
half, test stimuli were presented. The procedure was
the same as in Experiments 2 and 3.
Chloe correctly detected a target in 96.5, 52.1, and
88.5% of trials on average for the original, external,
and internal stimuli, respectively. She showed significantly better accuracy for internal than for external
stimuli [t(7)=6.999, P<0.001]. Figure 5 shows the mean
response times averaged across correct and incorrect
trials for each condition. The upright superiority effect
was significant only for internal stimuli [t(7) = 6.685,
P < 0.001], suggesting that the source of the upright
superiority effect was not the external but the internal
parts of the face.
Methods
Results and discussion
4.0
TGT/DST
Up/Inv
Inv/Up
Response Times (s)
3.5
***
3.0
2.5
2.0
**
1.5
1.0
0.5
Original
External
Parts
Internal
Parts
Fig. 5 Mean response times for each condition in Experiment 3.
**P<0.01; ***P<0.001
123
Chloe correctly performed in 94.8, 63.5, 36.5, 68.8,
and 31.3% of trials on average across target orientations for the original, schematic, schematic scrambled, eyes + eyebrows, and eyes only stimuli,
respectively. She showed higher accuracy for the
schematic face than for the schematic scrambled
stimuli [t(7)=4.202, P<0.01] and higher accuracy for
the eyes + eyebrows than for the eyes only stimuli
[t(7)=7.180, P<0.001].
Figure 6 shows the mean response times averaged
across the correct and incorrect trials for each condition. As in Experiment 1, the upright superiority effect
was also observed for the schematic face [t(7)=3.974,
P<0.01) but not for the scrambled patterns. These results further support the face specificity of the upright
superiority effect in visual search.
Chloe again showed a significant upright superiority
effect for eyes + eyebrows [t(7)=2.806, P<0.05] but not
for eyes only. These results were consistent with those
of Experiment 2, suggesting that the upright superiority effect is due to the configural processing of facial
stimuli.
Primates (2007) 48:1–12
9
Fig. 6 Mean response times
for each condition in
Experiment 4. *P<0.05;
**P<0.01
4.0
Up/Inv
Inv/Up
3.5
Response Times (s)
**
TGT/DST
*
3.0
2.5
2.0
1.5
**
1.0
0.5
Original
General discussion
The present experiments clearly replicated and extended the previous study in tests with the same subject
(Tomonaga 1999a). Chloe exhibited the upright superiority effect for orientation during visual search of
caricatures, dogs, and schematic faces, but not hand
shapes or chairs, indicating the face specificity of this
effect. Furthermore, if the normal spatial configuration
of the facial image could not be used, as in presentations of a single facial feature or due to rearrangements
of the spatial configuration of features, the upright
superiority effect was no longer observed. These results provide strong support for the hypotheses that
chimpanzees process facial images using configural
properties, as proven by the inversion effect under the
rotational matching paradigm (Parr et al. 1998; Tomonaga 1999b), and that the upright superiority effect
is caused by the configural processing of faces by the
chimpanzee (Tomonaga 1999a, 2001a).
There are no other reports of the same kind of effect
in primates, including humans, under identical experimental procedures. Thus, we should examine this effect both in humans and in other primates such as
macaques. Humans should show similar results if this
effect is closely related to configural processing of faces. Replicating the present results with macaque
monkeys would also be of interest because there have
been some confounding results concerning the facial
inversion effect in macaques.
Eyes
+
Eyebrows
Eyes
only
Schematic Schematic
Scrambled
Although the same effect has not been reported,
related phenomena have been observed in human
studies. One of these phenomena is called the ‘‘face
detection effect,’’ as reported by Purcell and Stewart
(1986, 1988). They found that detection of an upright
face in a brief time-frame is easier than detection of
inverted and scrambled faces. Recently Lewis and
Edmonds (2005) found a similar effect using visual
search tasks. They found that detection of an upright
face in scrambled scenes was easier than detection of
an inverted face. The difference between the present
experiments and those of Lewis and Edmonds is the
demand for discrimination; the present experiments
required the subject to detect a target face among
distractor faces, while Lewis and Edmonds had the
subject detect a target face among non-face distractors
(except in their second experiment). A visual search
for facial stimuli requiring discrimination among faces
is more difficult than discrimination between face and
non-face stimuli or among non-face stimuli (e.g.,
Hershler and Hochstein 2005; Lewis and Edmonds
2005; Nothdurft 1993). However, even though the task
demands were different, the present results are consistent with these human studies, and indicate better
detection of upright faces than inverted faces.
An upright face is also easier to find because it is
highly familiar to the subject compared with disoriented faces (Tomonaga 2001a). However, recent advances in the relationship between search asymmetries
and familiarity have provided opposite predictions.
123
10
When using familiar and unfamiliar items, human
observers have shown more efficient detection of
unfamiliar targets among familiar distractors than vice
versa (Malinowski and Hübner 2001; Shen and Reingold 2001; Wang et al. 1994; Wolfe 2001). Interestingly,
Wolfe (2001) reported that human observers found the
inverted silhouette of an elephant among upright elephants more efficiently than vice versa, which is
inconsistent with the present results. However, the
relationship between familiarity and search asymmetries has shown various results when using facial stimuli. Montoute and Tiberghien (2001) and Masuda
(2003) reported that famous faces can be more efficiently detected than unknown faces. Tong and Nakayama (1999) found that subjects searched for their
own face more efficiently than other faces. In contrast,
Levin (1996) reported that Caucasian subjects searched
for the faces of Africans among Caucasian faces more
efficiently than vice versa, even though Caucasian faces
are more familiar to Caucasian people. As Diamond
and Carey (1986) have suggested, increased familiarity
via prolonged exposure enhances configural processing
of stimuli. Although we should consider the different
levels of familiarity carefully, familiarity enhances
configural processing of upright faces and their efficient detection among disoriented faces or non-face
stimuli, as in the visual search for famous faces.
In conclusion, the present results provide further
support for the configural processing of faces in chimpanzees (Parr et al. 1998; Tomonaga 1999a, b, 2001a).
In humans, the development of face recognition has
been extensively investigated from very early infancy
to childhood (Carey and Diamond 1977, 1994; Johnson
and Morton 1991). Human children show a shift from
featural (or analytical) to configural processing of faces
during development. At present, comparative developmental studies on face recognition in chimpanzees
are relatively few (Kuwahata 2004; Kuwahata et al.
2003; Myowa-Yamakoshi et al. 2005; Tomonaga et al.
2004). Because of the relatively low task demand in
comparison to the matching paradigm (Tomonaga
1995), visual search for orientation of faces is an
effective means of investigating developmental changes in face processing in chimpanzees.
Acknowledgments This study and preparation of the manuscript were financially supported by Grants-in-Aid for Scientific
Research from the Japanese Ministry of Education, Culture,
Sports, Science and Technology (MEXT), Japan Society for the
Promotion of Science (JSPS; Grant # 04710053, 05206113,
05710050, 07102010, 09207105, 10CE2005, 12002009, 13610086,
16002001, 16300084) and MEXT Grants-in-Aid for the 21st
Century COE Program (A14 and D10). The author wishes to
thank Drs. Tetsuro Matsuzawa and Masayuki Tanaka for their
valuable comments on this study. Thanks are also due to Sumi-
123
Primates (2007) 48:1–12
haru Nagumo for his technical support and to Kiyonori Kumazaki, Norihiko Maeda, and the staff of the Center for Human
Evolution Modeling Research of the Primate Research Institute
(PRI) for their care of the chimpanzees.
References
Ballaz C, Boutsen L, Peyrin C, Humphreys GW, Marendaz C
(2005) Visual search for object orientation can be modulated by canonical orientation. J Exp Psychol Hum Percept
Perform 31:20–39
Blough DS (1979) Effects of the number and form of stimuli on
visual search in the pigeon. J Exp Psychol Anim Behav
Process 5:211–223
Bruce C (1982) Face recognition by monkeys: absence of an
inversion effect. Neurophsychologia 20:515–521
Campbell R, Walker J, Baron-Cohen S (1995) The development
of differential use of inner and outer face features in familiar
face identification. J Exp Child Psychol 59:196–210
Carey S, Diamond R (1977) From piecemeal to configurational
representation of faces. Science 195:312–314
Carey S, Diamond R (1994) Are faces perceived as configurations more by adults than by children? Visual Cogn 1:253–
274
Diamond R, Carey S (1986) Why faces are and are not special:
an effect of expertise. J Exp Psychol 115:107–117
Dittrich WH (1990) Representation of faces in longtailed macaques (Macaca fascicularis). Ethology 85:265–278
Ellis HD, Shepherd JW, Davies GM (1979) Identification of
familiar and unfamiliar faces from internal and external
features: some implications for theories of face recognition.
Perception 8:431–439
Fagot J, Tomonaga M (1999) Global-local processing in humans
(Homo sapiens) and chimpanzees (Pan troglodytes): use of a
visual search task with compound stimuli. J Comp Psychol
113:3–12
Farah MJ, Tanaka JW, Drain HM (1995) What causes the face
inversion effect? J Exp Psychol Hum Percept Perform
21:628–634
Gothard KM, Erickson CA, Amaral DG (2004) How do rhesus
monkeys (Macaca mulatta) scan faces in a visual paired
comparison task? Anim Cogn 7:25–36
von Grünau M, Anston C (1995) The detection of gaze direction:
a stare-in-the-crowd effect. Perception 24:1297–1313
Hamilton CR, Vermeire BA (1983) Discrimination of monkey
faces by split-brain monkeys. Behav Brain Res 9:263–275
Hamilton CR, Vermeire BA (1988) Complementary hemispheric specialization in monkeys. Science 242:1691–1694
Hansen C, Hansen R (1988) Finding the face in the crowd: an
anger superiority effect. J Pers Soc Psychol 54:917–924
Hershler O, Hochstein S (2005) At first sight: a high-level pop
out effect for faces. Vis Res 45:1707–1724
Hunnius S, Geuze RH (2004) Developmental changes in visual
scanning of dynamic faces and abstract stimuli in infants: a
longitudinal study. Infancy 6:231–255
Jitsumori M, Matsuzawa T (1991) Picture perception in monkeys
and pigeons: transfer of rightside-up versus upside-down
discrimination of photographic objects across conceptual
categories. Primates 32:473–482
Johnson MH, Morton J (1991) Biology and cognitive development the case of face recognition. Blackwell, Cambridge
Kanazawa S (1996) Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens).
Primates 37:25–38
Primates (2007) 48:1–12
Keating CF, Keating EG (1993) Monkeys and mug shots: cues
used by rhesus monkeys (Macaca mulatta) to recognize a
human face. J Comp Psychol 107:131–139
Kuwahata H (2004) Comparative–cognitive studies on face recognition in primates. PhD dissertation, Kyoto University,
Japan
Kuwahata H, Fujita K, Ishikawa S, Myowa-Yamakoshi M,
Tomonaga M, Tanaka M, Matsuzawa T (2003) Recognition
of facial patterns in infant chimpanzees (in Japanese). In:
Tomonaga M, Tanaka M, Matsuzawa (eds) Cognitive and
behavioral development in chimpanzees: a comparative
approach. Kyoto University Press, Kyoto pp 89–93
Levin DT (1996) Classifying faces by race: the structure of face
categories. J Exp Psychol Learn Mem Cogn 22:1364–1382
Lewis MB, Edmonds AJ (2005) Searching for faces in scrambled
scenes. Visual Cogn 12:1309–1336
Luria AR, Pravdina-Vinarskaya EN, Yarbus AL (1964) Eye
movement mechanisms in normal and pathological vision.
Sov Psychol Psychiatry 2:28–39
Malinowski P, Hübner R (2001) The effect of familiarity on visual-search performance: evidence for learned basic features. Percept Psychophys 63:458–463
Martin-Malivel J, Fagot J (2001) Perception of pictorial human
faces by baboons: effects of stimulus orientation on discrimination performance. Anim Learn Behav 29:10–20
Masuda S (2003) Effect of familiarity on visual search for faces
(in Japanese). In: Proceedings of the 67th annual convention
of the Japanese Psychological Association. Japanese Psychological Association, Tokyo, p 599
Matsuzawa T (1990) Form perception and visual acuity in a
chimpanzee. Folia Primatol 55:24–32
Montoute T, Tiberghien G (2001) Unconscious familiarity and
local context effects on low-level face processing: a reconstruction hypothesis. Conscious Cogn 10:503–523
Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T
(2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:B53–64
Myowa-Yamakoshi M, Yamaguchi M, Tomonaga M, Tanaka
M, Matsuzawa T (2005) Development of face recognition
in infant chimpanzees (Pan troglodytes). Cogn Dev 20:49–
63
Nahm FKD, Perrett A, Amaral DG, Albright TD (1998) How do
monkeys look at faces? J Cogn Neurosci 9:611–623
Nothdurft HC (1993) Faces and facial expressions do not pop
out. Perception 22:1287–1298
Ochiai T, Matsuzawa T (1998) Planting trees in an outdoor
compound of chimpanzees for an enriched environment. In:
Hare VJ, Worley E (eds) Proceedings of the third international conference on environmental enrichment. The Shape
of Enrichment, San Diego pp 355–364
Öhman A, Lundqvist D, Esteves F (2001) The face in the crowd
revisited: a threat advantage with schematic stimuli. J Pers
Soc Psychol 80:381–396
Overman WH, Doty RW (1982) Hemispheric specialization
displayed by man but not macaques for analysis of faces.
Neuropsychologia 20:113–128
Parr LA, Dove T, Hopkins WD (1998) Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn
Neurosci 10:615–622
Parr LA, Winslow IT, Hopkins WD (1999) Is the inversion effect
in rhesus monkey face-specific? Anim Cogn 2:123–129
Perrett DI, Mistlin AJ (1990) Perception of facial characteristics by monkeys. In: Stebbins WC, Berkley MA (eds)
Comparative perception vol 2, Wiley, New York, pp 178–
215
11
Phelps MT, Roberts WA (1994) Memory for pictures of upright
and inverted primate faces in humans (Homo sapiens),
squirrel monkeys (Saimiri sciureus), and pigeons (Columbia
livia). J Comp Psychol 108:114–125
Purcell DG, Stewart AL (1986) The face-detection effect. Bull
Psychon Soc 24:118–120
Purcell DG, Stewart AL (1988) The face-detection effect: configuration enhances detection. Percept Psychophys 43:355–
366
Rosenfeld SA, Van Hoesen GW (1979) Face recognition in the
rhesus monkey. Neuropsychologia 175:503–509
Sato N, Nakamura K (1999) Detection of directed gaze in rhesus
monkeys (Macaca mulatta). J Comp Psychol 115:115–121
Senju A, Hasegawa T, Tojo Y (2005) Does perceived direct gaze
boost detection in adults and children with and without
autism? The stare-in-the-crowd effect revisited. Visual Cogn
12:1474–1496
Shen J, Reingold EM (2001) Visual search asymmetry: the
influence of stimulus familiarity and low-level features.
Percept Psychophys 63:464–475
Suzuki S, Cavanagh P (1995) Facial organization blocks access to
low-level features: an object inferiority effect. J Exp Psychol
Hum Percept Perform 21:901–913
Tanaka JW, Farah MJ (1991) Second-order relational properties
and the inversion effect: testing a theory of face perception.
Percept Psychophys 50:367–372
Tomonaga M (1993a) Use of multiple-alternative matching-tosample in the study of visual search in a chimpanzee (Pan
troglodytes). J Comp Psychol 107:75–83
Tomonaga M (1993b) Tests for control by exclusion and negative
stimulus relations of arbitrary matching to sample in a
‘‘symmetry-emergent’’ chimpanzee. J Exp Anal Behav
59:215–229
Tomonaga M (1994) How laboratory-raised Japanese monkeys
(Macaca fuscata) perceive rotated photographs of monkeys:
evidence for an inversion effect in face perception. Primates
35:155–165
Tomonaga M (1995) Visual search by chimpanzees (Pan):
assessment of controlling relations. J Exp Anal Behav
63:175–186
Tomonaga M (1997) Precuing the target location in visual
searching by a chimpanzee (Pan troglodytes): effects of
precue validity. Jpn Psychol Res 39:200–211
Tomonaga M (1999a) Visual search for orientation of faces by a
chimpanzee (Pan troglodytes) (in Japanese with English
abstract). Primate Res 15: 215–229
Tomonaga M (1999b) Inversion effect in perception of human
faces in a chimpanzee (Pan troglodytes). Primates 40:417–
438
Tomonaga M (1999c) Establishing functional classes in a chimpanzee (Pan troglodytes) with a 2-item sequential-responding procedure. J Exp Anal Behav 72:57–79
Tomonaga M (2001a) Investigating visual perception and cognition in chimpanzees (Pan troglodytes) through visual
search and related tasks: from basic to complex processes.
In: Matsuzawa T (eds) Primate origin of human cognition
and behavior. Springer, Tokyo, pp 55–86
Tomonaga M (2001b) Visual search for biological motion patterns in chimpanzees (Pan troglodytes). Psychologia 44:46–
59
Tomonaga M, Matsuzawa T (1992) Perception of complex
geometric figures in chimpanzees (Pan troglodytes) and
humans (Homo sapiens): analyses of visual similarity on
the basis of choice reaction time. J Comp Psychol 106:43–
52
123
12
Tomonaga M, Itakura S, Matsuzawa T (1993) Superiority of
conspecific faces and reduced inversion effect in face perception by a chimpanzee. Folia Primatol 61:110–114
Tomonaga M, Myowa-Yamakoshi M, Mizuno Y, Yamaguchi
MK, Kosugi D, Bard KA, Tanaka M, Matsuzawa T (2004)
Development of social cognition in infant chimpanzees (Pan troglodytes): face recognition, smiling, gaze
and the lack of triadic interactions. Jpn Psychol Res
46:227–235
Tong F, Nakayama K (1999) Robust representations for faces:
evidence from visual search. J Exp Psychol Hum Percept
Perform 25:1016–1035
Treisman A, Gelade G (1980) A feature-integration theory of
attention. Cogn Psychol 12:97–136
Valentine T (1988) Upside-down faces: a review of the effects of
inversion upon face recognition. Br J Psychol 79:471–491
123
Primates (2007) 48:1–12
Wang Q, Cavanagh P, Green M (1994) Familiarity and pop-out
in visual search. Percept Psychophys 56:495–500
Williams M, Moss SA, Bradshaw JL, Mattingley JB (2005) Look
at me, I’m smiling: visual search for threatening and nonthreatening facial expressions. Visual Cogn 12:29–50
Wolfe JM (2001) Asymmetries in visual search: an introduction.
Percept Psychophys 63:381–389
Wright AA, Roberts WA (1996) Monkey and human face perception: inversion effects for human but not for monkey
faces or scenes. J Cogn Neurosci 8:278–290
Yamaguchi MK, Hirukawa T, Kanazawa S (1995) Judgment of
gender through facial parts. Perception 24:563–575
Yarbus AL (1967) Eye movements and vision. Plenum, New
York
Yin RK (1969) Looking at upside-down faces. J Exp Psychol
81:141–145