Atypical development of face and greeble recognition in autism.

Impairments in face processing are a relatively recent discovery in autism, but have quickly become a widely accepted aspect of the behavioral profile. The impairment goes beyond face recognition and involves difficulty in remembering faces (Boucher & Lewis, 1992), processing facial expressions (Ashwin, Baron-Cohen, Weelwright, O’Riordan, & Bullmore, 2006), and knowing which components of faces convey especially important communicative information (Joseph & Tanaka, 2003). Not surprisingly, these deficits contribute significantly to social dysfunction in autism. Despite the growing empirical evidence, the origin of the face processing deficits in autism remains unknown. One view suggests that individuals with autism have a decreased motivation to attend to social stimuli, which limits the ability to gain expertise in face processing (Dawson, et al., 2002; Grelotti, Gauthier, & Schultz, 2002). This social motivation impairment should not affect the recognition of non-social objects. Another view proposes that face-processing deficits result from atypical perceptual processing (e.g. enhanced processing of local features; Happe & Frith, 2006; Mottron, Dawson, Soulieres, Hubert, & Burack, 2006), which limits the ability to develop expertise with any class of visual objects (Behrmann, et al., 2006a; Behrmann, Thomas, & Humphreys, 2006b;). This failure to develop expertise disproportionately impacts processing of perceptually homogenous objects since fine-grained discrimination and representation of the subtle metric variations between the constituent features, also called the configural properties of these stimuli (Diamond & Carey, 1986), is required to differentiate these similar objects. Faces are a paradigmatic class of such objects and the bias to focus on local features may impede the processing of the relational properties needed for individuating faces and other perceptually similar non-face objects. To distinguish between these two potential origins of the face-processing deficit in autism, we evaluated whether individuals with autism have difficulty developing perceptual expertise and whether any such decrement is specific to faces or extends to other objects. We employed two empirical definitions of visuoperceptual expertise. First, we evaluated children’s and adult’s sensitivity to face inversion: typically-developing (TD) children and adults are slower and less accurate to recognize an inverted face (Valentine, 1988; Yin, 1969). Sensitivity to inversion is considered a measure of visuoperceptual expertise (Carey & Diamond, 1977) because: 1) the magnitude of the face inversion effect (FIE) increases with age, resulting from increasing knowledge about the spatial-relational properties of faces (see Carey 1981; Flin 1983); 2) it is evident in experts recognizing other objects of expertise (e.g., dogs for dog experts; Diamond & Carey, 1986) and in adults trained to recognize a novel class of objects (Gauthier & Tarr, 1996), and 3) it is less evident for other classes of objects that are not typically recognized at the individual level (Diamond & Carey, 1986; Yin, 1969). However, there are disparate findings about whether individuals with autism show an intact FIE. Several studies have reported the absence of a FIE and superior performance on inverted face recognition in children and adolescents with autism compared to TD individuals (Hobson, Ouston, & Lee, 1988; Langdell, 1978; McPartland, et al., 2004; Tantam, Monagham, Nicholson, & Stirling, 1989). Other studies have found evidence for a spared FIE in children and adolescents with autism (Joseph & Tanaka, 2003; Lahaie, et al., 2006; Teunisse & de Gelder, 2003). Part of the discrepancy in these findings may be related to the inclusion of broad age ranges, which may have masked the ability to observe developmental changes in the FIE, heterogeneity of the sample (Barton et al., 2007) and/or the use of stimuli in which simultaneous changes in orientation and facial expression are present. To circumvent these potential confounds, we used naturalistic faces with neutral expressions to evaluate the FIE from childhood (ages 8–13) to adulthood in relatively high-functioning individuals with autism (HFA) and age-matched typically-developing participants (TD). Our second measure of face expertise, previously used to evaluate deficits in expert face and object recognition in adults with acquired visual agnosia (Gauthier, Behrmann, & Tarr, 1999), involved manipulating the level of categorization at which faces are recognized. Most objects are recognized at the “basic” level of abstraction (e.g., dog versus chair) and can be distinguished by unique features or configurations of features (Rosch 1978; Tanaka & Taylor, 1991). However, all objects can be recognized at more “subordinate” levels (e.g., cocker spaniel vs poodle), where all exemplars share similar parts in a similar basic configuration but differ in the spatial relations within this basic configuration. It is at this level that sensitivity to configural information is critical for making subordinate-level discriminations between exemplars (Diamond & Carey, 1986). Expertise with any particular object class is indicated by the ability to recognize objects equally fast at the individual level (e.g., Joey’s face), where featural differences are less diagnostic than configural properties for recognition, and at the basic level, where featural differences are very discriminating (Gauthier et al., 1999). Recent studies of adults with autism suggest that the ability to recognize faces at the individual level is disproportionately slower than at the basic level, indicating a lack of expertise (Behrmann, et al., 2006a). Interestingly, this difficulty was not limited to faces; in fact, adults with autism showed similar difficulties in discriminating common and novel objects at the individual levels, indicating that atypical face processing may be related to a more general abnormality in visuoperceptual processing. In the current study, we evaluated the developmental trajectory of the ability to discriminate faces, homogeneous novel objects known as Greebles, and common objects at the individual level in HFA and TD children and adults.