Action perception is intact in autism spectrum disorder

Abstract

Autistic traits span a wide spectrum of behavioral departures from typical function. Despite the heterogeneous nature of autism spectrum disorder (ASD), there have been attempts at formulating unified theoretical accounts of the associated impairments in social cognition. A class of prominent theories capitalizes on the link between social interaction and visual perception: effective interaction with others often relies on discrimination of subtle nonverbal cues. It has been proposed that individuals with ASD may rely on poorer perceptual representations of other people's actions as returned by dysfunctional visual circuitry and that this, in turn, may lead to less effective interpretation of those actions for social behavior. It remains unclear whether such perceptual deficits exist in ASD: the evidence currently available is limited to specific aspects of action recognition, and the reported deficits are often attributable to cognitive factors that may not be strictly visual (e.g., attention). We present results from an exhaustive set of measurements spanning the entire action processing hierarchy, from motion detection to action interpretation, designed to factor out effects that are not selectively relevant to this function. Our results demonstrate that the ASD perceptual system returns functionally intact signals for interpreting other people's actions adequately; these signals can be accessed effectively when autistic individuals are prompted and motivated to do so under controlled conditions. However, they may fail to exploit them adequately during real-life social interactions.

Keywords: biological motion; enactive mind; human agency; inversion effect; mirror neuron; simulation theory.

Figure 1.

Autistic and control populations were matched in all respects except for autistic traits. A plots SRS scores on the y-axis versus IQ on the x-axis. B plots SRS against age. The ASD population (filled) clearly shows higher SRS scores but equivalent IQ and age relative to the TD population (open). Ovals in A are aligned with best linear fit, their radii matching 1×, 1.5×, and 2× (from thick to thin) the SD of the data projected onto the fit line and the line orthogonal to it. Solid lines in B show linear fits, and dashed lines mark 95% confidence intervals on the fit. Side histograms plot data distributions collapsed across corresponding axis.

Figure 2.

Selective scrambling of different stages along the action processing hierarchy. The original fighting sequence (A, B) was scrambled by randomly time shifting individual joints (C, D), limbs (E, F), or agents (G, H). The three manipulations are depicted by colored solid dots shifting away from their original trajectory (indicated by gray dots) in both first and second columns (the former in actual monitor coordinates, the latter in time coordinates) with respect to individual joints (indexed from 1 to 26 as labeled in A). Participants were asked to discriminate between intact (A) and scrambled (C, E, G) displays.

Figure 3.

The disruptive effect of inversion on sensitivity to BM is present in both ASD and TD groups. A–D demonstrate increasing levels of noise, plotted against E, to show corresponding variation in noise level. E–G show three example psychometric functions (percentage correct as a function of stimulus noise intensity) for ASD (F, G) and TD (E) participants in both upright (black) and inverted (gray) conditions. Dot size scales with number of trials. F and G show variation in measurement reliability found between participants within the ASD group, whereas E demonstrates a psychometric function typically found in TD participants. H plots perceptual thresholds for upright (y-axis) versus upside-down displays (inverted) across both ASD (filled) and TD (open) populations. Error bars show ±1 SEM (not visible when smaller than the symbol). H demonstrates an inversion effect in both groups (data points are shifted away from the diagonal equality line in the direction indicated by the magenta arrow). I, J, Show target displays of upright and inverted stimuli, respectively.

Figure 4.

We modified joint trajectories (A) to move in a robotic manner (B) and compared corresponding perceptual thresholds (x-axis in C) with those obtained from the original sequence (y-axis). Plotting conventions in C are similar to Figure 3H.

Figure 5.

We asked participants to discriminate fighting (A) from dancing (B) and measured corresponding perceptual thresholds (C). Plotting conventions in C are similar to Figure 3H.

Figure 6.

Inversion affects additional stages of action processing in both groups. E and F plot scrambling thresholds for both ASD (filled) and TD groups (open) in upright (y-axis) and inverted conditions. Icons in A–D depict varying levels of limb scrambling (increasing from left to right), and G–J show varying scrambling levels of inter-agent synchronization. Plotting conventions in E and F are similar to Figure 3H.

Figure 7.

We probed the potential role of generic attention by reducing the contrast of three joints for a brief period of time (indicated by Δt in B) during a relatively long presentation of the fighting sequence. Participants were asked to identify whether the target joints (green outline in A and B) were “dark gray” or “light gray” (the latter shown in A and B). C plots duration thresholds for judging the brightness of the modified joints (see Materials and Methods). Plotting conventions in C are similar to Figure 3H.

Figure 8.

ASD thresholds are slightly worse than control, but this effect is not specific to action processing. A plots the distribution of normalized sensitivity (larger for better performance) for ASD (filled) and TD (open) participants across four different experiments with upright displays. Thick arrow shows average shift from ASD (vertical solid line) to TD (vertical dotted line) across all four experiments; small arrows show shifts for different experiments (labeled numerically as 1 for joint scrambling, 2 for limb scrambling, 3 for agent scrambling, 4 for action recognition; no arrow is plotted when arrow length is shorter than the arrowhead). Smooth lines show Gaussian fits (solid for ASD, dashed for TD). B plots same for inverted displays. In both A and B, ASD sensitivity tends to be lower than TD (all small arrows point to the right). C plots upright/inverted sensitivity ratios from A and B using the same plotting conventions; when cognitive components not specific to action processing are factored out in this way, there is no longer any trend for a difference between ASD and TD populations.