Using identical stimuli and comparable testing methods, these data show clear species differences in holistic processing, assessed using the face inversion effect. Chimpanzees showed the inversion effect for conspecific’s faces only, not heterospecific’s faces (rhesus monkeys), houses, shoes, or clip art images. Therefore, for chimpanzees, the inversion effect appears to operate only on the most expert stimulus category, e.g., conspecific’s faces, not unfamiliar faces or nonface categories. This replicates previous findings in this species and, like humans, confirms the special status that conspecific faces have in eliciting holistic processing (Parr et al. 1998
; Parr and Heintz 2006
; Parr, 2011; Tomonaga 2007
). It is presumed that the special status of conspecifics’ faces comes from the extensive experience gained with this stimulus category throughout development and in daily interactions with other chimpanzees. Despite similar familiarity with conspecifics’ faces, rhesus monkeys showed significant inversion effects for all faces, conspecific and heterospecific (chimpanzee faces), as well as for houses. In addition, the cost for discriminating inverted shoes neared significance. No inversion effect was seen in either species for discriminations involving clip art images. These results support previous findings from our lab suggesting that the inversion effect in rhesus monkeys is not face-selective, occurring only for a special category of faces, e.g., conspecifics’ faces, nor is it face-specific, occurring only for faces compared to nonface images (Parr, 2011; Parr et al. 1999
; Parr and Heintz 2008
As a separate analysis of the inversion effect, we adjusted the difference scores between performance on upright and inverted trials based on the overall cost of inversion shown for the clip art trials. Changing the orientation of stimuli between the training and test trials is expected to produce a deficit in performance regardless of the identity of the stimulus categories. Our choice to adjust performance using the results from the clip art trials was based on previous data from numerous studies in our lab showing that clip art fail to reveal significant inversion costs. Therefore, general impairments on inverted clip art were used to compensate for the general costs of changing the quality (orientation) of stimuli between the training and test trials, and not differences in cognitive and/or perceptual processing strategies. However, it could also be argued that clip art does not reflect a stimulus category for which that are many within-category exemplars, like faces, and therefore may not be the most appropriate category. If, however, one were to utilize a different category, such as houses, the magnitude of inversion effects shown by the monkeys would be reduced, as houses revealed significant inversion effects. For example, for conspecific faces, the DI score adjusted for clip art was 10.78%, but when this was adjusted for houses, it dropped to 0.22%. The chimpanzees, however, showed slightly better performance discriminating inverted compared to upright houses, so the magnitude of their inversion effects would be increased if houses were chosen. For conspecific faces, the DI score adjusted for clip art was 16.39%, but when adjusted for houses this increased to 22.13%. These adjustments for the inversion effect in rhesus monkeys highlights the important finding; that the conspecific face lacks special status for the rhesus monkeys compared to the chimpanzee. Regardless of the approach taken, the results of these studies reveal significant species differences in the pattern of inversion effects and confirm the importance of holistic processing for conspecifics’ face in the chimpanzee, similar to humans.
Previous studies in monkeys have utilized the inversion effect as a marker for holistic processing and concluded that rhesus monkeys show face-selective holistic processing, just like humans (Dahl et al. 2009
; Adachi et al. 2009
). This requires that the inversion costs for conspecifics’ faces be compared to the results from both nonexpert face and nonface categories, but neither control was used in these studies. Without such comparisons, no conclusions can be made about the importance of holistic processing for conspecifics’ faces or its similarity to humans. Adachi and colleagues (2009)
reported similar face processing strategies between humans and monkeys using the Thatcher Illusion (Bartlett and Searcy 1993
; Thompson, 1980
). This is a test of holistic processing as it shows that information about the specific features of a face, e.g., orientation of the eyes and mouth, is hard to extract when the features are embedded in the context of a whole face (Tanaka & Farah, 1993
). Moreover, this effect is minimized when the faces are inverted, implicating its dependence on holistic processing. Using a viewing preference paradigm, monkeys looked longer at upright compared to inverted thatcherized faces, suggesting that they share similar face processing mechanisms as humans (Adachi et al. 2009
). This conclusion is premature, however, because the study failed to utilize any control stimuli, e.g., thatcherized faces of another species, or other manipulated nonface categories, to confirm that the effect was indeed selective for conspecifics’ faces. Problematically, what is often concluded from these and similar studies is that if monkeys show the inversion effect then, like humans, they must be sensitive to 2nd
order configural cues. This is an important comparative issue as the ability to utilize 2nd
order configural cues in humans requires a protracted period of development (Mondloch et al., 2003
) and is used to define adult-levels of face expertise (Crookes & McKone, 2009
). Moreover, whether monkeys are sensitive to the spacing of facial features has only been directly tested a few times with different results (Dahl et al. 2007
; Parr et al. 2008
; Sugita, 2008). Therefore, considerably more testing is needed before any conclusions can be drawn about species similarities or differences in sensitivity to both holistic processing and 2nd
order cues in faces.
There are some discrepancies in our published data from chimpanzees that should be discussed. Parr and colleagues (1998)
reported evidence of the inversion effect in chimpanzees for human faces, presumed to be an expert category, as subjects were raised in peer-groups by humans in the primate center nursery. However, a decade later, Parr and colleagues (2008)
failed to demonstrate holistic processing for human faces in the same chimpanzee subjects using the composite face task, another task of holistic processing (Young et al., 1987
). Although the exact cause of this discrepancy may never be known, it is very likely that a change in the chimpanzees’ expertise with human faces is responsible. Chimpanzees in both studies (4 of the same subjects were included in both studies) were all reared by humans in the Yerkes Primate Center nursery during the late 1980’s. After moving into the main colony at 4 years of age, the chimpanzees’ experience with humans was almost exclusively limited to caretakers and researchers wearing personal protective equipment (PPE), e.g., masks, face shields, hair covers, a procedure that was uncommon in the nursery. In the event that humans were seen without PPE, it was by regulation at a considerable distance from the subject and viewing distance is a critical factor in the ability to integrate facial features via holistic processing (McKone, 2009
). Therefore, the earlier expertise shown by chimpanzees for human faces appears to have diminished as their visual experience with human faces (not wearing PPE) became more restricted. It is because of this uncertain degree of expertise with human faces that they were not used in the present study.
There is no doubt that face processing is a complex and highly specialized skill in humans and the extent to which nonhuman primates share these skills, and to what degree, is a fascinating question in comparative social cognition. Researchers should be careful to design well-controlled experiments and be cautious in their interpretations so that this literature can move forward progressively. Moreover, discrepancies in the literature should not be ignored (Dahl et al., 2009
), or pushed aside as mere testing biases (Adachi et al., 2009
; Dahl et al., 2009
), as these discrepancies are a source of valuable information and addressing them directly is the only way to advance our understanding of the evolution of face processing skills in primates.