Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder

Abstract

The amplitude of the auditory N1 component of the event‐related potential (ERP) is typically attenuated for self‐initiated sounds, compared to sounds with identical acoustic and temporal features that are triggered externally. This effect has been ascribed to internal forward models predicting the sensory consequences of one's own motor actions. The predictive coding account of autistic symptomatology states that individuals with autism spectrum disorder (ASD) have difficulties anticipating upcoming sensory stimulation due to a decreased ability to infer the probabilistic structure of their environment. Without precise internal forward prediction models to rely on, perception in ASD could be less affected by prior expectations and more driven by sensory input. Following this reasoning, one would expect diminished attenuation of the auditory N1 due to self‐initiation in individuals with ASD. Here, we tested this hypothesis by comparing the neural response to self‐ versus externally‐initiated tones between a group of individuals with ASD and a group of age matched neurotypical controls. ERPs evoked by tones initiated via button‐presses were compared with ERPs evoked by the same tones replayed at identical pace. Significant N1 attenuation effects were only found in the TD group. Self‐initiation of the tones did not attenuate the auditory N1 in the ASD group, indicating that they may be unable to anticipate the auditory sensory consequences of their own motor actions. These results show that individuals with ASD have alterations in sensory attenuation of self‐initiated sounds, and support the notion of impaired predictive coding as a core deficit underlying autistic symptomatology. Autism Res 2019, 12: 589–599 . © 2019 The Authors. Autism Research published by International Society for Autism Research published by Wiley Periodicals, Inc. Lay Summary Many individuals with ASD experience difficulties in processing sensory information (for example, increased sensitivity to sound). Here we show that these difficulties may be related to an inability to anticipate upcoming sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by individuals with ASD.

The effect of uncertainty on prediction error in the action perception loop

“…Here, we found no difference in accuracy of judgement of agency between healthy participants across a range of autism traits, consistent with previous research comparing autistic and healthy participants on similar measures ( David et al, 2008 ; Grainger et al, 2014 ; Russell & Hill, 2001 ; Williams & Happé, 2009 ; Zalla et al, 2015 ). As previously noted by Perrykkad and Hohwy (2020b) and Zalla and Sperduti (2015) , this is in contrast to sense of agency in autism being shown to be reduced under typical experimental paradigms ( Sperduti, Pieron, Leboyer, & Zalla, 2014 ; van Laarhoven, Stekelenburg, Eussen, & Vroomen, 2019 ). Our study also shows no main effects of AQ on other outcomes, except for a negative association with acceleration.…”

Prediction in Autism Spectrum Disorder: A Systematic Review of Empirical Evidence

“…van Laarhoven, Stekelenburg, Eussen, and Vroomen [2019] looked at predictions based on self‐action, as measured by evoked EEG response attenuation. The evoked responses of the ASD group were less attenuated by self‐generation than those of the NT group.…”

“…Ruiz‐Martínez et al [2020] and van Laarhoven et al [2019] used attenuation of the early component of EEG stimulus‐evoked activity as a measure of prediction. Both showed reduced modulation by prediction of the early ERP response to auditory stimuli in the ASD group compared to the control group.…”

Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions

“…Recent evidence has shown that self-initiation of tones does not attenuate the auditory N1 in autistic individuals, indicating that autistic individuals may have alterations in anticipating the auditory consequences of their own motor actions ( van Laarhoven et al, 2019 ). The current study extends these findings by demonstrating that the ability to anticipate the sensory consequences of others’ actions may be altered in ASD as well.…”

“…Recent evidence suggests that predictive coding might indeed be impaired in autistic individuals ( van Laarhoven et al, 2019 ). In this study, the neural response to self- versus externally initiated tones was examined in a group of autistic individuals and a group of age-matched individuals with typical development (TD).…”