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 faceprocessing 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.</p

Probing the face-space of individuals with prosopagnosia

A useful framework for understanding the mental representation of facial identity is face-space (Valentine, 1991), a multi-dimensional cognitive map in which individual faces are coded relative to the average of previously encountered faces, and in which the distance among faces represents their perceived similarity. We examined whether individuals with prosopagnosia, a disorder characterized by an inability to recognize familiar faces despite normal visual acuity and intellectual abilities, evince behavior consistent with this underlying representational schema. To do so, we compared the performance of 6 individuals with congenital prosopagnosia (CP), with a group of age- and gender-matched control participants in a series of experiments involving judgments of facial identity. We used digital images of male and female faces and morphed them to varying degrees relative to an average face, to create caricatures, anti-caricatures, and anti-faces (i.e. faces of the opposite identity). Across 5 behavioral tasks, CP individuals’ performance was similar to that of the control group and consistent with the face-space framework. As a test of the sensitivity of our measures in revealing face processing abnormalities, we also tested a single acquired prosopagnosic (AP) individual, whose performance on the same tasks deviated significantly from the control and CP groups. The findings suggest that, despite an inability to recognize individual identities, CPs perceive faces in a manner consistent with norm-based coding of facial identity, although their representation is likely supported by a feature-based strategy. We suggest that the apparently normal posterior cortical regions, including the fusiform face area, serve as the neural substrate for at least a coarse, feature-based face-space map in CP and that their face recognition impairment arises from the disconnection between these regions and more anterior cortical sites.</p

Visual category-selectivity for faces, places and objects emerges along different developmental trajectories

The organization of category-selective regions in ventral visual cortex is well characterized in human adults. We investigated a crucial, previously unaddressed, question about how this organization emerges developmentally. We contrasted the developmental trajectories for face-, object-, and place-selective activation in the ventral visual cortex in children, adolescents, and adults. Although children demonstrated adult-like organization in object- and place-related cortex, as a group they failed to show consistent face-selective activation in classical face regions. The lack of a consistent neural signature for faces was attributable to (1) reduced face-selectivity and extent of activation within the regions that will become the FFA, OFA, and STS in adults, and (2) smaller volumes and considerable variability in the locus of face-selective activation in individual children. In contrast, adolescents showed an adult-like pattern of face-selective activation, although it was more right-lateralized. These findings reveal critical age-related differences in the emergence of category-specific functional organization in the visual cortex and support a model of brain development in which specialization emerges from interactions between experience-dependent learning and the maturing brain.</p

A fine-grained analysis of facial expression processing in high-functioning adults with autism

It is unclear whether individuals with autism are impaired at recognizing basic facial expressions, and whether, if any impairment exists, it applies to expression processing in general, or to certain expressions, in particular. To evaluate these alternatives, we adopted a fine-grained analysis of facial expression processing in autism. Specifically, we used the ‘facial expression megamix’ paradigm [Young, A. W., Rowland, D., Calder, A. J, Etcoff, N. L., Seth, A., & Perrett, D. I. (1997). Facial expression megamix: Tests of dimensional and category accounts of emotion recognition Cognition and Emotion, 14, 39–60] in which adults with autism and a typically developing comparison group performed a six alternative forced-choice response to morphs of all possible combinations of the six basic expressions identified by Ekman [Ekman, P. (1972). Universals and cultural differences in facial expressions of emotion. In J. K. Cole (Ed.), Nebraska symposium on motivation: vol. 1971, (pp. 207–283). Lincoln, Nebraska: University of Nebraska Press] (happiness, sadness, disgust, anger, fear and surprise). Clear differences were evident between the two groups, most obviously in the recognition of fear, but also in the recognition of disgust and happiness. A second experiment demonstrated that individuals with autism are able to discriminate between different emotional images and suggests that low-level perceptual difficulties do not underlie the difficulties with emotion recognition.</p

Cortical Patterns of Category-Selective Activation for Faces, Places and Objects in Adults with Autism

Autism is associated with widespread atypicalities in perception, cognition and social behavior. A crucial question concerns how these atypicalities are reflected in the underlying brain activation. One way to examine possible perturbations of cortical organization in autism is to analyze the activation of category-selective ventral visual cortex, already clearly delineated in typical populations. We mapped out the neural correlates of face, place and common object processing, using functional magnetic resonance imaging (fMRI), in a group of high-functioning adults with autism and a typical comparison group, under both controlled and more naturalistic, viewing conditions. There were no consistent group differences in place-related regions. Although there were no significant differences in the extent of the object-related regions, there was more variability for these regions in the autism group. The most marked group differences were in face-selective cortex, with individuals with autism evincing reduced activation, not only in fusiform face area but also in superior temporal sulcus and occipital face area. Ventral visual cortex appears to be organized differently in high-functioning adults with autism, at least for face-selective regions, although subtle differences may also exist for other categories. We propose that cascading developmental effects of low-level differences in neuronal connectivity result in a much more pronounced effect on later developing cortical systems, such as that for face-processing, than earlier maturing systems (those for objects and places).</p

Normal Movement Selectivity in Autism

It has been proposed that individuals with autism have difficulties understanding the goals and intentions of others because of a fundamental dysfunction in the mirror neuron system. Here, however, we show that individuals with autism exhibited not only normal fMRI responses in mirror system areas during observation and execution of hand movements but also exhibited typical movement-selective adaptation (repetition suppression) when observing or executing the same movement repeatedly. Movement selectivity is a defining characteristic of neurons involved in movement perception, including mirror neurons, and, as such, these findings argue against a mirror system dysfunction in autism.</p

Reduced Structural Connectivity in Ventral Visual Cortex in Congenital Prosopagnosia

Using diffusion tensor imaging and tractography, we found that a disruption in structural connectivity in ventral occipitotemporal cortex may be the neurobiological basis for the lifelong impairment in face recognition that is experienced by individuals who suffer from congenital prosopagnosia. Our findings suggest that white-matter fibers in ventral occipitotemporal cortex support the integrated function of a distributed cortical network that subserves normal face processing

Configural Processing in Autism and its Relationship to Face Processing

Studies of the perceptual performance of individuals with autism have focused, to a large extent, on two domains of visual behavior, one associated with face processing and the other associated with global or holistic processing. Whether autistic individuals differ from neurotypical individuals in these domains is debatable and, moreover, the relationship between the behaviors in these two domains remains unclear. We first compared the face processing ability of 14 adult individuals with autism with that of neurotypical controls and showed that the autistic individuals were slowed in their speed of face discrimination.We then showed that the two groups differed in their ability to derive the global whole in two different tasks, one using hierarchical compound letters and the other using a microgenetic primed matching task with geometric shapes, with the autistic group showing a bias in favor of local information. A significant correlation was also observed between performance on the face task and the configural tasks. We then confirmed the prediction that the ability to derive the global whole is not only critical for faces but also for other objects as well, as the autistic individuals performed more slowly than the control group in discriminating between objects. Taken together, the results suggest that the bias for local processing seen in autistic individuals might have an adverse impact on their ability to process faces and objects

Reduction in White Matter Connectivity, Revealed by Diffusion Tensor Imaging, May Account for Age-related Changes in Face Perception

An age-related decline in face processing, even under conditions in which learning and memory are not implicated, has been well documented, but the mechanism underlying this perceptual alteration remains unknown. Here, we examine whether this behavioral change may be accounted for by a reduction in white matter connectivity with age. To this end, we acquired diffusion tensor imaging data from 28 individuals aged 18 to 86 years and quantified the number of fibers, voxels, and fractional anisotropy of the two major tracts that pass through the fusiform gyrus, the pre-eminent face processing region in the ventral temporal cortex. We also measured the ability of a subset of these individuals to make fine-grained discriminations between pairs of faces and between pairs of cars. There was a significant reduction in the structural integrity of the inferior fronto-occipital fasciculus (IFOF) in the right hemisphere as a function of age on all dependent measures and there were also some changes in the left hemisphere, albeit to a lesser extent. There was also a clear age-related decrement in accuracy of perceptual discrimination, especially for more challenging perceptual discriminations, and this held to a greater degree for faces than for cars. Of greatest relevance, there was a robust association between the reduction of IFOF integrity in the right hemisphere and the decline in face perception, suggesting that the alteration in structural connectivity between the right ventral temporal and frontal cortices may account for the age-related difficulties in face processing.</p