Seeing it differently: visual processing in autism

Several recent behavioral and neuroimaging studies have documented an impairment in face processing in individuals with Autism Spectrum Disorder (ASD). It remains unknown, however, what underlying mechanism gives rise to this face processing difficulty. One theory suggests that the difficulty derives from a pervasive problem in social interaction and/or motivation. An alternative view proposes that the face-processing problem is not entirely social in nature and that a visual perceptual impairment might also contribute. The focus of this review is on this latter, perceptual perspective, documenting the psychological and neural alterations that might account for the face processing impairment. The available evidence suggests that perceptual alterations are present in ASD, independent of social function.

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).