Social processing is a hallmark of human cognition and socially salient signals can be detected from greatly impoverished sensory information. A prime example is the highly specialized ability to detect diverse social information, such as emotion, mood, and gender from biological motion point light displays, in which body movements are represented through a small set of dots attached to the joints of humans as they perform common motions (1–4).
Remarkably, preference for upright biological motion over scrambled or inverted motion point light displays already appears to be present in children as young as two-days old (5, 6) and evolves rapidly over the first two years of life (7). This preference for upright motion suggests an innate predisposition to biological motion perception, with obvious implications for preferential detection of and responding to caretakers early in life (5). Furthermore, accuracy in recognizing human and non-human biological motion increases from ages three to five years, indicating that efficiency of biological motion processing continues to develop across early childhood in typical development (8). Given the obvious link between biological motion processing and the ability of an observer to decode the emotional state or intentions of another, it is not surprising that researchers have been interested in determining whether this capability is weakened in individuals with autism spectrum disorder (ASD) (9), a neurodevelopmental disorder characterized by difficulties in social interaction and communication (10).
Unfortunately, the literature has produced somewhat mixed results to date. The earliest behavioral findings from Moore and colleagues reported a significant impairment in children and adolescents with ASD in the inference of internal emotional and mental states from biological motion point light displays, but not in the categorization of overt biological actions (e.g. running, jumping, etc.), (11). This finding, which has been replicated in studies of high-functioning children with ASD as well as adolescents and young adults with ASD, is consistent with an emotion-processing dysfunction rather than a more fundamental sensory-perceptual biological motion-processing disorder (12, 13). Likewise, a lack of observed differences in biological motion identification and perception of specific biological motion features (i.e. kinematic profile, action discrimination in noise, direction discrimination in noise) provide further evidence for intact basic processing of biological motion in children, adolescents, and adults with ASD (14–19). Yet, other studies do report significant differences in recognition of biological motion, or discrimination of actions or direction of biological motion among those with ASD (20, 21). Atkinson and colleagues also describe a correlation between impaired emotion detection and motion coherence thresholds in adults with ASD, suggesting that emotion detection impairments may be partially explained by a lower level visual motion processing deficit (22). Furthermore, associations between reduced biological motion processing and clinical autism symptom severity, as measured by the Autism Diagnostic Observation Schedule and Childhood Autism Rating Scale or Autism Quotient, have been described (23, 24), affording some additional support for the notion that disruption of biological motion processing may be important in ASD. Three meta-analyses have attempted to integrate findings from these individual studies exploring the perception of biological motion in point light displays (25–27). These meta-analyses reveal an emerging pattern of overall small to moderate deficits in biological motion perception in ASD, but confirm high heterogeneity among studies. They also confirm that deficits in biological motion processing among autistic individuals tend to be more severe when inferring social implications including intentionality or emotion from biological motion, as opposed to lower-level detection of biological motion and discrimination of action or direction of biological motion in noise.
Likewise, neuroimaging studies in general suggest that individuals with ASD have biological motion task-related hypoactivation in brain regions previously implicated in biological motion processing. This includes the right superior temporal region (19, 28–31), an area that also appears highly linked to social cognition in ASD (32, 33), as well as altered activation in right middle and inferior temporal gyri, middle frontal gyrus, inferior parietal lobule, and supplementary motor area (26, 30, 34). Importantly, altered brain activation has been observed regardless of the presence of identifiable performance deficits, suggesting individuals with ASD may employ different brain networks to accomplish the same goal of biological motion processing (19, 30). Additionally, specific patterns of neural activation during biological motion processing have been linked with clinical symptoms in ASD. For example, hypoactivation of the superior temporal sulcus (STS), inferior frontal gyrus, and cerebellum during biological motion processing have been linked with higher ASD symptom severity (35, 36) and impaired gesture production (37), and pre-treatment STS activation selectivity to biological over scrambled motion predicts improvement in ASD symptoms with pivotal response therapy (38). Furthermore, STS activation during biological motion processing is one functional region that can distinguish aspects of familial risk for ASD (39, 40). While the STS has repeatedly been implicated in fMRI studies of biological motion processing in ASD, our understanding of associated temporal dynamics is somewhat more limited as fewer electrophysiologic studies have been conducted to date. Studies of oscillatory dynamics including mu suppression and beta activity during passive observation of biological motion have revealed no differences between individuals with ASD and controls (26, 41, 42). When examining evoked potentials to biological motion, Kroger and colleagues have found group differences in P1 amplitude along with atypical lateralization of visual evoked potentials during processing of both biological and scrambled motion in ASD. This suggests deficits in general visual motion processing or processing of complex stimuli rather than a biological motion-specific deficit (43). However, a trend toward decreased right hemisphere P1 in response to biological motion has been observed following social skills training in individuals with ASD, paralleling the findings of the neuroimaging literature by drawing a potential link between electrophysiologic mechanisms of biological motion processing and autism symptomatology (44).
Thus, although emerging evidence highlights possible differences in neural mechanisms of biological motion processing in ASD, as well as potential implications for social function, a high degree of inconsistency in findings makes it difficult to draw definitive conclusions. Variability in findings cannot be accounted for by within-subject unreliability as several studies have shown that behavioral and electrophysiologic responses to visual paradigms are highly consistent within individuals on repeated measures (45, 46). Instead, potential mediators of such study heterogeneity may include between-subjects developmental, cognitive and/or attentional factors. There are clear maturational changes in biological motion processing, and developmental trajectories appear to differ in ASD as compared to typical development. While NT children from ages 5-12 years steadily improve in their perceptual sensitivity to biological motion, children with ASD show a flat developmental trajectory, overlapping with NTs only at the youngest age, pointing to atypical development of biological motion perception in ASD (20). Although impaired recognition of biological motion has also been observed in adults with ASD (47), looking across studies, it appears that differences between ASD and NT participants decrease with age, as children with ASD show more substantial deficits than adolescents and adults (26), and the majority of studies of older adolescents and adults report no differences in behavioral performance on biological motion tasks.
The association between cognitive factors and biological motion processing has also been explored as a source of heterogeneity, but does not appear to be strongly influential in accounting for variability in study results. Individual studies have suggested that IQ may correlate with some aspects of biological motion processing ability only among those with ASD (15–18, 21). However, meta-analyses suggest minimal overall influence of IQ on biological motion processing (25, 26).
In contrast, attention remains a strong candidate mediator for some of the inconsistency in findings across studies and biological motion paradigms, since studies that have demonstrated correlation between differential fixations and task performance in biological motion paradigms suggest a modulatory role of attention (41, 48, 49). Additionally, a recent fMRI study showed that, unlike NT adults, adults with ASD did not have augmentation of STS functional activity in an explicit biological motion processing task compared to passive processing task (50), suggesting an inability to adapt to attentional task demands.
It is possible that this dysfunction results from very early attentional differences in children with ASD. There seems to be a fundamental difference in preferential attendance to biological motion in children with ASD in passive viewing paradigms as, unlike NT preschoolers, 2-3 year-olds with ASD did not show a preference for upright over inverted motion in point light displays or for motion of people over geometric shapes, and school-age children and adolescents with ASD likewise do not show a preference for biological over non-biological motion point light displays (51–54). In fact, patterns of fixation to biological over non-biological motion can even help distinguish children with ASD from NT children (55) or predict a future diagnosis of ASD in preschoolers (53). Even older adolescents and adults with ASD show a lower percentage of time fixating on movies of real people than on geometric shapes; however, they do not show a difference from NT controls in preferential fixation on upright vs. inverted motion point light displays (56). This may be due to developmental changes in biological motion processing, or may relate to the complexity of social stimuli (51, 52, 56, 57). It is important to note that large individual variability in biological motion preference (range = 11.6 - 90.2%) has also been reported in 3-year-old children with ASD, such that 8 out of 20 did show an intact biological motion preference (53). As biological motion preference also covaries with adaptive functioning and predicted reduction in symptom severity a year later, attendance to biological motion may well prove a sensitive measure of behavioral characteristics in children with ASD and have a cascading influence on developmental trajectory (53).
Therefore, in parsing the heterogeneity of findings in the biological motion literature it is reasonable to suggest that although individuals with ASD appear largely capable of discriminating basic non-emotional features of biological motion when explicitly directed to do so, they may differentially attend to biological motion which could impact detection of relevant social cues. As the modulatory role of attention on neural mechanisms of low-level biological motion processing in ASD remains incompletely understood, the current study takes advantage of a behavioral and electrophysiologic paradigm previously developed by our research group (58) to map spatiotemporal dynamics of unattended and explicitly attended processing of biological motion point light displays in typical development and ASD.