The question of whether and to what extent faces are processed differently when compared with non-face objects has been a major focus of research in humans. Converging evidence indicates that one key distinction is the holistic processing of faces. For example, parts presented in the context of a whole face are recognized better than when presented in isolation (Tanaka & Farah 1993
). Moreover, when faces are split into top and bottom halves, observers are influenced by the half that they were supposed to ignore, but only when the halves are aligned (Young et al. 1987
; Hole 1994
). The facilitation of performance for whole faces, as well as the relative inability to selectively attend to (or ignore) face parts, indicates that the face is normally processed as a single, indivisible entity, i.e. faces are processed holistically
Another distinguishing feature of face processing is the default, or entry point, level of categorization. Whereas most non-face objects are identified at the basic level, faces are identified subordinate to the basic level, at the level of the individual. For example, an image of a dog would be labelled ‘dog’ (basic) over ‘Rover’ (individual), yet a face is often labelled, for example, ‘Elvis’ over ‘face’ (Rosch et al. 1976
; Jolicoeur et al. 1984
; Tanaka 2001
). The subordinate-level entry point for objects of expertise, such as faces, has been observed in numerous studies using varied techniques (Tanaka & Taylor 1991
; Gauthier & Tarr 1997
; Johnson & Mervis 1997
; Tanaka 2001
; Tanaka et al. 2005
; but see Grill-Spector & Kanwisher 2005
). The processing mechanism(s) enabling a subordinate entry point for faces is not clearly specified—it could be the idiosyncratic features of an individual's face (featural), the unique spatial relationships of facial features (configural) or a unitary ‘template’ of the face of that individual (holistic). As such, the subordinate-level entry point marks a second, independent, aspect of face processing not typically seen for non-face objects.
These behavioural results have formed a foundation on which to explore the neural basis of face perception. Some of the most direct evidence for selective representation of faces in the brain arises from the electrophysiological studies of the temporal lobe of macaques (Gross et al. 1972
; Bruce et al. 1981
; Perrett et al. 1982
; Desimone et al. 1984
). Despite the numerous studies of face coding in the monkey brain, there has been relatively little research on the face processing abilities of the monkeys themselves, particularly in relation to the behavioural research in humans.
Our understanding of face perception in the monkey comes almost exclusively from the study of the face inversion effect, with mixed results. Macaques choose to look longer at upright than inverted images of conspecifics (Tomonaga 1994
; Guo et al. 2003
), though this does not necessarily indicate that they would show discrimination impairments for inverted compared with upright faces, i.e. a face inversion effect. Unfortunately, most of these studies used explicit reinforcement for some type of discrimination (Rosenfeld & Van Hoesen 1979
; Bruce 1982
; Overman & Doty 1982
; Perrett et al. 1988
; Keating & Keating 1993
; Wright & Roberts 1996
; Parr et al. 1999
). When tested, these protocols appeared to produce systematically altered or idiosyncratic response strategies, making it difficult to disentangle what monkeys are capable of learning from what they would do under natural circumstances (Perrett et al. 1988
; Keating & Keating 1993
). Moreover, the face inversion effect in humans may not be the result of holistic processing applied preferentially to upright faces; it may be merely the result of less experience discriminating upside down faces (Sekuler et al. 2004
). Thus, even if untrained macaques showed robust face inversion effects, it would not be clear that this was the result of the key attributes of face processing seen in humans.
Few studies have tried to address a second hallmark of face perception in monkeys, namely the entry point of categorization. Although macaques can discriminate the faces of other monkeys (Bruce 1982
; Pascalis & Bachevalier 1998
), it is not clear how this relates to their ability to discriminate faces at the basic level (compared with objects), nor to their discrimination of subordinate-level objects. One landmark study used an adaptation, or dishabituation, paradigm to reveal that the rebound in looking time following changes in a monkey's identity was as great as the rebound following a cross-species (or basic-level) change (Humphrey 1974
). In contrast, changes of identity within other domestic animal categories produced no significant rebound; only the basic-level, cross-species changes were significant. Thus, monkeys that had not been explicitly trained to differentiate images nevertheless displayed a subordinate-level entry point which was selective to conspecifics. Although hierarchical categorization has been observed in tamarins (Neiworth et al. 2004
) and Sulawesi macaques (Fujita et al. 1997
), these studies presented pictures of the entire monkey, thus it is not clear whether a subordinate-level entry point would be observed for faces presented in isolation.
Taken together, there have been indications that adult monkeys naturally individuate other monkeys (Humphrey 1974
), and that monkeys, like chimpanzees, are able
to process a configuration of facial features (Overman & Doty 1982
; Perrett et al. 1988
; Parr et al. 1999
), yet no evidence to date shows that monkeys' natural face processing abilities involve holistic processing or a subordinate-level entry point.
Here, we measure the untrained responses of macaques (Macaca mulatta) to address the following questions: (i) Do macaques differentiate conspecific faces better than other subordinate-level stimuli (e.g. dogs, birds or another monkey species)? (ii) Is their face perception characterized by holistic processing?
In experiment 1, the entry point of face categorization is measured using an adaptation task (a
) modelled after that described by Humphrey (1974)
.To the extent that monkeys individuate conspecific faces, greater rebound from adaptation is expected for trials of faces at the subordinate, relative to basic, level than for trials of other animals at the subordinate, relative to basic, level. In addition, configural information processing was investigated by manipulating the inter-ocular distance of monkey face images. If perceived similarity of faces is dependent on featural configuration, we should observe more rebound for faces that have undergone a configural manipulation and are rotated in plane than for the identical face merely rotated in plane (a
). Furthermore, as tested in experiment 2, if individuation of faces is species specific, then the relative subordinate-level rebound should be greater for macaque faces than for another species' faces (e.g. marmosets).
Figure 1 (a) Sample stimuli for experiment 1. Trial types included four monkey and three animal conditions, defined by differences between prior (adaptation) and present (novel) images. Trial types overlapped during the task; every novel trial served as an adaptation (more ...)
In experiment 3, holistic processing of faces was tested by adapting the test monkeys to composites of either vertically aligned or misaligned faces (c). If the aligned face is processed holistically, then presentation of a new bottom half should cause greater rebound in the aligned than in the misaligned condition, as though a face with a new bottom half is perceived as a whole new face. In this design, the tendency for gaze to be directed to novel parts of an image conflicts with monkeys' tendency to fixate the eye region, particularly when viewing new faces. Scan paths to the eye region during rebound periods will be compared in aligned and misaligned conditions, to determine whether scan patterns in the aligned condition also rebound, resembling those seen when viewing a new face.