Self-motion perception in autism is compromised by visual noise but integrated optimally across multiple senses

Abstract

Perceptual processing in autism spectrum disorder (ASD) is marked by superior low-level task performance and inferior complex-task performance. This observation has led to theories of defective integration in ASD of local parts into a global percept. Despite mixed experimental results, this notion maintains widespread influence and has also motivated recent theories of defective multisensory integration in ASD. Impaired ASD performance in tasks involving classic random dot visual motion stimuli, corrupted by noise as a means to manipulate task difficulty, is frequently interpreted to support this notion of global integration deficits. By manipulating task difficulty independently of visual stimulus noise, here we test the hypothesis that heightened sensitivity to noise, rather than integration deficits, may characterize ASD. We found that although perception of visual motion through a cloud of dots was unimpaired without noise, the addition of stimulus noise significantly affected adolescents with ASD, more than controls. Strikingly, individuals with ASD demonstrated intact multisensory (visual-vestibular) integration, even in the presence of noise. Additionally, when vestibular motion was paired with pure visual noise, individuals with ASD demonstrated a different strategy than controls, marked by reduced flexibility. This result could be simulated by using attenuated (less reliable) and inflexible (not experiencedependent) Bayesian priors in ASD. These findings question widespread theories of impaired global and multisensory integration in ASD. Rather, they implicate increased sensitivity to sensory noise and less use of prior knowledge in ASD, suggesting increased reliance on incoming sensory information.autism | multisensory integration | noise | coherence | Bayesian

A computational perspective on autism

“…To the extent that a Bayesian prior accurately reflects the statistics of the world, it will improve task performance by reducing the number of probable stimuli. As such, an attenuated prior in autism could potentially increase behavioral sensitivity to sensory noise, as well as increase variability in stimulus-driven neural activity, both of which are consistent with recent findings on the disorder (47,48). We next simulate how Bayesian priors can be implemented through divisive normalization, establishing a link between alterations in neural computation and high-level hypotheses about how autism affects the ability to perform statistical inference.…”

“…However, it is unclear whether these results reflect differences in earlier unisensory representations or in the process of multisensory integration itself. The possibility of intact multisensory processing is supported by a recent study reporting near-optimal integration of visual and vestibular cues in self-motion perception in both controls and subjects with autism (48). Importantly, this finding is not inconsistent with the hypothesis of altered divisive normalization in autism since cue integration does not theoretically require divisive normalization (42).…”

Disentangling signal and noise in autism spectrum disorder

“…Remarkably, converging evidence was recently provided by Zaidel et al (2015), using a paradigm in which participants had to discern the direction of simulated self-motion through random dot clouds (optic flow). Specifically, adolescents with ASD were slightly better for the condition in which 100% of dots moved in a coherent way, while their performance was disproportionately negatively affected when a proportion of dots moved randomly (noise), producing higher thresholds than controls.…”

“…It follows that we should be careful in stating that individuals with ASD cannot form informative priors (only ''weak" or low precision priors), as several authors seem to suggest (Manning, Tibber, Charman, Dakin, & Pellicano, 2015;Pellicano & Burr, 2012;Sinha et al, 2014;Zaidel, Goin-Kochel, & Angelaki, 2015). Surely, in lots of cases individuals with ASD can detect and learn to use regularities (in the form of informative priors).…”

The vestibular system

“…I propose that there is a very promising line of research to develop in order to better understand the bidirectional links between emotion, social processing, and vestibular disorders. Future studies should determine why visuo-vestibular integration differs in patients with anxiety, vestibular migraine [124], and impaired social functioning [125].…”