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

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Inversion Effect in Perception of Human Faces in a Chimpanzee (Pan Troglodytes) 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 418 M. TOMONAGA 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 chil- dren 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 relation- ship 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 con- figurations 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 inconsis- tent 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 result- ing 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. TOMONAGAet 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,
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