When seeing depends on knowing: Adults with Autism Spectrum Conditions show diminished top-down processes in the visual perception of degraded faces but not degraded objects
Introduction
Autism Spectrum Conditions (ASC, including autism, atypical autism, and Asperger Syndrome) are severe neuro-developmental conditions characterised by the co-occurrence of impairments in social interaction, communication, and restricted and repetitive behaviours. Despite considerable progress, the nature of the underlying abnormalities at the cognitive and neurobiological levels, is not fully understood.
One line of research suggests that deficits in social cognition and in an underlying ‘social brain network’ represent the core problem (Baron-Cohen, 2003, Baron-Cohen et al., 2000, Frith and Frith, 1999, Hobson, 2002, Klin et al., 2003, Mundy and Neal, 2001). Since many aspects of successful social interaction involve processing information from faces, over recent years abnormalities in face processing have become a key area of research in ASC (Dawson et al., 2005, Schultz, 2005). Behavioural studies have shown deficits and/or abnormalities in different aspects of face processing, including the ability to recognize social communicative cues (emotion expressions, eye gaze) from faces (Golan et al., 2006, Hobson, 1986, Katsyrie et al., 2008, Teunisse and de Gelder, 2003) and the ability to identify/remember individual face identities (Boucher and Lewis, 1992, Klin et al., 1999, Langdell, 1978, Joseph and Tanaka, 2003), though several negative findings also exist (see Jemel, Mottron, & Dawon, 2006, for a review).
Early neuroimaging studies found reduced activation in the lateral fusiform gyrus (a region also called “fusiform face area” [FFA] because it typically responds more strongly to faces than any other object class; Kanwisher, McDermott, & Chun, 1997) when viewers with ASC looked at faces, suggesting that abnormalities in the development or function of this brain region may be critical to the face processing abnormalities (Critchley et al., 2000, Pierce et al., 2001, Schultz et al., 2000). However, more recent studies showed relatively normal FFA activation in ASC (Bird et al., 2006, Dapretto et al., 2006, Hadjikhani et al., 2004, Hadjikhani et al., 2007) but a lack of the modulation of FFA activity by attention (fronto-parietal network, Bird et al., 2006) or emotional significance (notably the amygdala, Kleinhans et al., 2008, Pierce and Redcay, 2008), as is seen in typically developing volunteers (Vuilleumier et al., 2001). These findings are consistent with the proposal that diminished spontaneous attention to faces, perhaps because they do not convey the same significance or reward value as for other people, contributes to the face processing abnormalities in ASC (Klin et al., 2003).
A second approach to understanding ASC focuses on domain-general perceptual and cognitive abnormalities that may, in principle, play a role in the social impairments of ASC, but also in their non-social features, including exceptional perceptual abilities. In particular, a great deal of research has been inspired by the notion of weak central coherence, which refers to a cognitive style in which the normal tendency to integrate information in context and for meaning is diminished, with preferential focus on details and local information (Frith, 1989, Happé and Frith, 2006). In support of this, several studies have shown that people with ASC outperform comparison groups on tests where local processing and/or resistance to the overall gestalt, are advantageous; for example, the Embedded Figures and Block Design Tasks, and tests of visual illusions (Happé, 1996, Happé and Booth, 2008) and visual search (Plaisted, Swettenham, & Rees, 1999, but see, for example, Mottron et al., 1999, Ropar and Mitchell, 2001, for negative or conflicting findings).
Over recent years, the weak coherence hypothesis has evolved in two important directions: Some theorists have emphasised enhanced local processing abilities, distinct from global/contextual impairments (Mottron and Burack, 2001, Mottron et al., 2006, Plaisted, 2001). The study reported here is part of a second trend, which has revisited the notion of difficulties in ‘integrating information in context’. Earlier studies primarily focused on contextual processing in a Gestaltist sense, which requires the integration of different visual elements to form a coherent or meaningful whole, such as in the perception of Kanizka triangles (see, for example, Happé & Frith, 2006, for a review). However, “context” effects in visual perception also include the influence of one's past experience and prior knowledge of the world on the perception of an object, independent of or in addition to the intrinsic properties of the object itself. Indeed, over recent years there has been an increasing interest in abnormalities in the influence of prior knowledge in perception and cognition in ASC. (C. Frith, 2003, Frith and Frith, 2006, Greenaway and Plaisted, 2005, Loth, 2007, Loth et al., 2008, Ropar and Mitchell, 2002). This relates to processes commonly referred to as top-down processes, and they are reviewed next.
Section snippets
Top-down processes in visual perception
In cognitive science, the distinction between top-down vs. bottom up processes has a long-standing history. While bottom-up processes refer to stimulus-driven, passive, or reflexive processes, which proceed in a feed-forward manner, top-down processing refers to the recognition that perception and cognition are more active, adaptive and constructive—influenced by expectations based on prior knowledge, past experiences and “a dynamic searching for the best interpretation of the available data” (
Participants
14 individuals with ASC (11 male, 2 female, 12 with a diagnosis of Asperger Syndrome, 2 with a diagnosis of high-functioning autism, mean age 26 years) and 14 young TD adults (11 male, 2 female, mean age 23 years) took part in this experiment. Level of intellectual abilities was assessed using the Wechsler Abbreviated Scales of Intelligence (WASI, 1999). Participant details are shown in Table 1. A set of independent t-tests confirmed that the groups did not significantly differ on age, verbal
Behavioural results
Behavioural results from the Active Viewing Sequence are considered first.
Discussion
This study investigated whether high-functioning adults with ASC differ from typically developing adults in their spontaneous use of prior knowledge to perceive faces and objects from degraded images. Our findings from behavioural responses and gaze tracking were consistent: Both groups showed similarly large priming effects on the recognition of degraded objects when tested with explicit behavioural measures (naming the object when recognized) and with changes in their spontaneous scanning
Conclusion
Findings from eye-gaze measures and behavioural performance converged in showing that in the group with ASC top-down effects on the perception of degraded images were selectively reduced for faces, but not for objects. It is hoped that the current findings will inspire further research to specify the relative contribution of abnormalities in different cognitive processes (attention, mental imagery, feature-binding) and to test predictions regarding potential neurofunctional abnormalities.
Acknowledgements
This study was supported by an ESRC project grant (RES-000-22-1123) to EL and FH. Portions of this study were presented at the 7th International Meeting for Autism Research, London, 15-17 May 2008. We would like to thank three anonymous reviewers for their helpful comments on earlier versions of this manuscript. We also thank our participants, parents, and support groups for their help with this study, and Max Bimboese and Volker Loth for their help in creating some of the two-tone images.
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