When viewing naturalistic social situations, individuals with autism demonstrate abnormal patterns of social visual pursuit consistent with reduced salience of eyes and increased salience of mouths, bodies, and objects. Fixation times on mouths and objects but not on eyes are strong predictors of degree of social competence.
Deficits in eye contact have been a hallmark of autism1,2 since the condition’s initial description3. They are cited widely as a diagnostic feature4 and figure prominently in clinical instruments5; however, the early onset of these deficits has not been known. Here we show in a prospective longitudinal study that infants later diagnosed with autism spectrum disorders (ASD) exhibit mean decline in eye fixation within the first 2 to 6 months of life, a pattern not observed in infants who do not develop ASD. These observations mark the earliest known indicators of social disability in infancy, but also falsify a prior hypothesis: in the first months of life, this basic mechanism of social adaptive action—eye looking—is not immediately diminished in infants later diagnosed with ASD; instead, eye looking appears to begin at normative levels prior to decline. The timing of decline highlights a narrow developmental window and reveals the early derailment of processes that would otherwise play a key role in canalizing typical social development. Finally, the observation of this decline in eye fixation—rather than outright absence—offers a promising opportunity for early intervention, one that could build on the apparent preservation of mechanisms subserving reflexive initial orientation towards the eyes.
Typically-developing human infants preferentially attend to biological motion within the first days of life1. This ability is highly conserved across species2,3 and is believed to be critical for filial attachment and for detection of predators4. The neural underpinnings of biological motion perception are overlapping with brain regions involved in perception of basic social signals such as facial expression and gaze direction5, and preferential attention to biological motion is seen as a precursor to the capacity for attributing intentions to others6. However, in a serendipitous observation7, we recently found that an infant with autism failed to recognize point-light displays of biological motion but was instead highly sensitive to the presence of a non-social, physical contingency that occurred within the stimuli by chance. This observation raised the hypothesis that perception of biological motion may be altered in children with autism from a very early age, with cascading consequences for both social development and for the lifelong impairments in social interaction that are a hallmark of autism spectrum disorders8. Here we show that two-year-olds with autism fail to orient towards point-light displays of biological motion, and that their viewing behavior when watching these point-light displays can be explained instead as a response to non-social, physical contingencies physical contingencies that are disregarded by control children. This observation has far-reaching implications for understanding the altered neurodevelopmental trajectory of brain specialization in autism9.
Looking at the eyes of others is important in early social development and in social adaptation throughout one's life span. Our results indicate that in 2-year-old children with autism, this behavior is already derailed, suggesting critical consequences for development but also offering a potential biomarker for quantifying syndrome manifestation at this early age.
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