Autism is a neurodevelopmental disorder with a strong genetic component and a heterogeneous neurological substrate. Abnormalities have been reported in the limbic system (anterior cingulate, amygdala, hippocampus, and orbitofrontal cortex), cerebellum, frontal lobes, superior temporal gyrus, and subcortical structures including the thalamus and the basal ganglia (Lord, Cook, Leventhal, & Amaral, 2000). This broad range of neurological abnormalities is matched at the behavioral level by a broad phenotype that includes motor, linguistic, social, and emotional deficits (Joseph, 1999). Individuals with autism exhibit stereotypic and repetitive motor behavior, and their use of language is both delayed and disrupted. At its core, however, autism is a disorder of social interaction and communication.
Poor eye-gaze following is a specific marker of autism, and one of its earliest signs, evident in children as young as 18 months of age. Some children with autism even fail to use gaze as a cue to locate an object (Leekam & Moore, 2001). This is especially remarkable given that chimpanzees, who are incapable of joint attention, can nevertheless use gaze as an instrumental cue (Povinelli et al., 2000). In one study, schoolage children with autism were tested in a naturalistic environment for their ability to use eye gaze as an orienting cue. In the autistic group, children with high mental age performed normally, but those with low mental age were impaired relative to developmentally delayed children matched for mental age. Autistic children of low mental age were capable of following gaze when a target object was observable (a skill that emerges at 6 months of age in typically developing infants) but were impaired when the target was absent (a skill that normally develops at the age of 9 months and that indicates the emergence of joint attention; Leekam & Moore, 2001). Another study tested high-functioning 10-year-olds with autism in a computer-based paradigm and found normal cueing effects (Sweettenham, Condie, Campbell, Milne, & Coleman, 2003). Taken together, these two studies suggest that eye-gaze cueing deficits in autism vary according to the severity of impairment in general intelligence.
In contrast, joint attention deficits in autism occur independently of general intelligence and are an early marker of the disease. Children with autism show deviant patterns of reciprocal gaze behavior with their caregivers as well as deficits in the triadic coordination among themselves, adult, and object (Charman, 2003). Interestingly, joint attention in 3- and 4-year-old children with autism is positively correlated with orbitofrontal function, as measured by tasks that engage this region in normal subjects (Dawson et al., 2002). Orbitofrontal cortex is necessary for adding flexibility to stimulus-reward associations (Fellows & Farah, 2003; Rolls, 1999). An inability to assign stimulus-reward associations and flexibly modify them could be detrimental to the development of joint attention, as joint attention depends on social rewards, such as smiles, that are more variable than nonsocial rewards. Consistent with this hypothesis, autistic infants and toddlers prefer highly contingent, nonvariable feedback, while typically developing children instead prefer variable, imperfect feedback (Gergely & Watson, 1999). The contingency hypothesis illustrates the main problem of arguing for a module devoted exclusively to social stimuli. Even if certain brain regions do process social stimuli preferentially, it does not follow that such preferential processing is due to the "social" nature of the stimuli. In the aforementioned example, the driving force is the variability of the stimulus-reward association, which is typical of social stimuli but can be present in nonsocial stimuli as well.
Individuals with autism also show abnormalities in the processing of facial and emotional stimuli. Studies measuring event-related potentials (ERPs) reveal that children with autism are impaired in the discrimination of novel versus familiar faces, despite their normal discrimination of novel versus familiar objects. Relative to healthy adults, adults with autism have reduced response to facial emotions. This includes abnormal activity in the fusiform gyrus, amygdala, and the STS (Critchley et al., 2000). One possible interpretation of these data is that they provide evidence for a social perception module whose impairment in autism accounts for the social deficits exhibited by this group. Although this analysis captures much of what is wrong in autism, it makes the same mistake previously described in our analysis of stimulus-reward associations. Just because social stimuli such as faces happen to activate the fusiform face area, it does not follow that faces activate this area because they are stimuli of social relevance. Nonsocial stimuli such as cars and birds can similarly activate this region, provided that observers are experts in recognizing those objects and encode them globally. The critical factor, therefore, seems to be not the social nature of the stimulus but its holistic encoding. Of course, this is not to say that difficulties in face perception, emotion recognition, and gaze following do not have consequences for mental state inferences. On the contrary, such deficits may put children with autism at a severe disadvantage in their development of mental state understanding. Relative to typically developing children, children with autism have difficulties using the eyes as cues for attributing mental states (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, 2001) and in using faces to judge the approachability and trustworthiness of people (Adolphs, Sears, & Piven, 2001). There is also evidence that children with autism have difficulty understanding gaze in mental-istic terms (Baron-Cohen, 1995).
So, is autism best characterized as a deficit in a social module or as a disorder of basic processes that apply to both social and nonsocial domains? Individuals with autism have deficits in joint attention and mental state attributions, but they also have motor deficits, visual attention deficits, and deficits in feedback processing, set switching, executive processing, and other nonsocial abilities (Joseph, 1999). Thus, although autism may present first and foremost as a problem of social cognition, it also manifests itself in nonsocial problems. This dual deficit poses a challenge to both the social module view (why should there be nonsocial deficits?) and the information-processing view (why should the deficit be mostly social?). Our proposal is that the solution to this paradox lies not in the brain itself but in the external stimuli that the brain processes. More specifically, we argue that attributes of social stimuli may correlate with basic information-processing computations. According to our framework, a deficit in the basic computation would affect primarily, but not exclusively, the processing of social information. We have already discussed the examples of variable stimulus-reward associations and holistic visual encoding. In both cases, there is a correlation between the type of stimulus (social/nonsocial) and a computational feature (variable/ nonvariable reward; holistic/feature-based encoding). We are not claiming that these two basic computations account for all deficits in autism; rather, we use these examples to illustrate the larger point that general computational deficits may account for what appear to be domain-specific deficits.
Stimulus category (social/nonsocial) may correlate with other basic computations, such as those involved in affective processing. Since social stimuli carry more affective valence than nonsocial stimuli, they should disproportionately tap limbic structures such as the amygdala and the orbitofrontal cortex. Limbic areas are activated by affective stimuli such as faces. These brain areas send feedback projections to regions of the temporal lobe including the fusiform gyrus. During normal development, this affective loop is likely to play a role in modulating the plasticity of the fusiform gyrus, which with experience becomes a dedicated system for face recognition (i.e., the FFA). To put it in psychological terms, faces are attractive stimuli that capture the child's attention, thus becoming the focus of preferred processing and, with the passage of time, a stimulus the child is expert with. But for children with autism, faces do not seem to carry their appropriate valence, and thus these children seem uninterested in faces. Within a social module framework, there is little one could do to rectify this problem. Within an information-processing framework, however, it should be possible to pair facial stimuli with nonsocial rewards that are valued by the autistic child and in this way engage the affective loop. Through extensive training in such a paradigm, it might be possible for children with autism to achieve the type of expertise with facial stimuli that typically developing children gain naturally (Carver & Dawson, 2002).
Also related to the affective dimension, type of stimulus (social/ nonsocial) may correlate with orienting effectiveness. For example, while the orienting deficit in autism is most severe for social stimuli, such as faces or being called by name, individuals with autism are also impaired in their orienting to nonsocial stimuli, such as a jack-in-the-box (Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998). Interestingly, deficits in joint attention correlate with deficits in orienting toward social stimuli but not with nonsocial orienting. This result is consistent with the idea raised earlier that the covariance of mental and nonmental levels (orienting to a location, finding a social stimulus at that location) may foster the mental state attribution process.
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Autism is a developmental disorder that manifests itself in early childhood and affects the functioning of the brain, primarily in the areas of social interaction and communication. Children with autism look like other children but do not play or behave like other children. They must struggle daily to cope and connect with the world around them.