Trends in Cognitive Sciences
Seeing it differently: visual processing in autism
Introduction
Autism is a neurodevelopmental disorder characterized by impairments in communication and social cognition, co-occurring with repetitive, stereotyped behaviors. Although not considered prosopagnosic per se, individuals with autism, also known as Autism Spectrum Disorder (ASD), often fail to recognize people. Indeed, the last decade has witnessed an explosion of data from behavioral and neuroimaging studies confirming that an impairment in face processing is widespread and present from an early age in ASD 1, 2. Questions about the cognitive and brain mechanisms involved in autism are the subject of intense debate in cognitive science and the issue addressed in this review concerns the underlying source of the face processing impairment. One explanation for the apparent difficulty with faces is that it derives from a pervasive problem in social interaction and the reward and motivational value of social stimuli. An alternative view is that the difficulty with faces is not entirely social in origin but that a visual perceptual impairment also contributes to this difficulty. The focus here is on this latter perspective and on the psychological and neural mechanisms that might give rise to the atypical face processing in ASD.
The face processing difficulty in ASD extends beyond face recognition, affecting the perceptual discrimination of faces too, as evident in same/different judgement tasks [3] (see Figure 1a and b). In addition, individuals with ASD do not always show the typical superiority for upright over inverted faces (4, 5 but see [6]) and perform atypically on tests of face memory but do well on tests of memory for buildings and leaves [7]. These face processing difficulties are more prevalent among children and cognitively less able individuals, although some studies report a reliable decrement in adults too 3, 8, 9.
The face processing impairment also extends beyond identity processing to affect processing of emotional expression 4, 10, 11, possibly independently of IQ. Interestingly, the difficulties in emotional expression processing seem to be exaggerated in the analysis of fear, perhaps because of reduced attention to core features of the face 10, 12, particularly the eyes (although see [13]), which are most informative for expressions like fear [11]. Difficulties in discriminating facial gender [14] and unusual patterns of eye gaze processing 15, 16, 17 have also been documented in ASD, with the latter perhaps reflecting the failure to track the intentions of the other individual [18].
The decrement in face processing ability is consistent with findings from recent functional imaging studies, documenting weak activation of the fusiform gyrus in ASD in response to faces 19, 20, 21, 22, 23, with concurrent activation of a host of other cortical regions not usually associated with face processing 19, 21, 22, 23, 24, 25. Other regions of the ‘social brain network’, including the superior temporal sulcus and amygdala, are also functionally atypical in ASD individuals 15, 26, 27, 28. The neuroimaging findings, however, are controversial: some studies do, in fact, report fusiform activation in ASD 29, 30 with greater signal for familiar than unfamiliar faces [30], as typically expected (see [31] for discussion of the discrepant results).
Abnormal neural responses are also observed in ASD in ERP studies: the N170 component, the best known ERP marker for faces 32, 33, 34, is reduced or less specific and its scalp topography is atypical, with more bilateral than unilateral (right) distribution (see also MEG study [35]). Also, atypically [1], the N170 in ASD is not delayed for inverted relative to upright faces [32] and later components (P400; Nc) do not differentiate between familiar and unfamiliar faces [1].
The hypoactivation of the face-selective cortical regions may not be attributable to a fundamental failure to engage the fusiform gyrus; fusiform activation was obtained in a child who was a Digimon expert when viewing Digimon (but not faces) in the scanner [23]. Rather, the hypoactivation may reflect the failure to attend to the eye region 16, 29, the failure to engage in configural processing and/or the failure to engage the fusiform region for face processing during the course of maturation and experience (see below).
Section snippets
Is the deficit in face processing perceptual in nature?
In spite of the data documenting atypical face processing in ASD, there is surprisingly little consensus concerning the source of this impairment. Several explanations, which are not necessarily mutually exclusive, have been offered. The first is that the difficulty with faces is secondary to a primary impairment in social motivation or affective tagging of socially relevant stimuli 1, 2: faces are not intrinsically emotionally salient (and may even be aversive) to individuals with ASD, perhaps
Is there a primary perceptual deficit in individuals with ASD?
The argument for a perceptual alteration, which may underlie the face processing impairment, is based on the observation that individuals with ASD are particularly attentive to local details or featural information and, concurrently, may fail to extract the gist or gestalt of the input. In fact, Kanner's original description of autism included ‘the inability to experience wholes without full attention to the constituent parts’, and ‘a persistent pre-occupation with parts of objects’ is one of
The perceptual deficit in relation to face processing
Although not all studies consistently uncover a perceptual deficit in ASD, there is growing consensus that perceptual alterations may well be characteristic of autism [39], independent of deficits in executive function, social behavior and ToM [41]. How might this perceptual bias towards local elements affect face processing? It has been suggested that because faces are perceptually similar, part or feature-based processing is not sufficient for identification, so face processing is
Does the perceptual deficit extend to other classes of visual stimuli?
One obvious prediction from the claim that there is a general perceptual deficit in ASD is that an impairment in processing stimuli other than faces should also be observed, although perhaps to a lesser extent given the undue reliance on relational processing for faces. Non-face processing is rather understudied in ASD and to the extent that it has, it is usually in the context of using non-face inputs as control stimuli for faces. Some studies of non-face processing claim that individuals with
Is there a more general underlying perceptual difficulty?
Before concluding that the face and non-face difficulty perceptual decrement results from the local bias (and holistic/configural difficulty) in ASD, we need to examine whether an even lower-level visual processing deficit may be ultimately responsible for the perceptual profiles in ASD. Global, holistic properties of a display are thought to be processed mainly by low spatial frequency channels, a property of the magnocellular system, and the local elements by higher-spatial frequency
Reconciliation?
This review has explored the possible contribution of altered perceptual function to the impairment in face processing abilities in individuals with ASD. The data, indicating a local bias and perhaps an even lower-level perceptual alteration, clearly indicate a difference in perceptual function in both children and adults with ASD. Taken together, these data suggest that the impairment in face processing need not necessarily arise solely from a social and/or motivational source but that a
Acknowledgements
The writing of this review was supported by grants from NICHD/NIDCD PO1/U19 (PI: Nancy Minshew), which is part of the NICHD/NIDCD Collaborative Programs for Excellence in ASD, The National Alliance for Autism Research and the Cure Autism Now foundation. We thank Drs N. Minshew, B. Luna and L. Mottron for their helpful comments.
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