Sensitivity to Motor Error in Children with Autism

When making a movement, the brain receives sensory feedback about the consequences of that action. If sensory feedback differs from predicted, the brain experiences an error, driving adaptation and improving subsequent movements. How much the brain adapts to error is governed by its sensitivity. Computationally, sensitivity is a scaling factor, specifying the relative amount of adaptation that occurs, while theoretically it is a quantification of the error’s value. In children with autism spectrum disorder (ASD), the response to sensory feedback appears abnormal. In particular, they are hyperresponsive to proprioceptive feedback and hyporesponsive to visual feedback. Here, we hypothesized that these sensory abnormalities would be manifested as an increased sensitivity to proprioceptive error and a decreased sensitivity to visual error. Further, we hypothesized that this pattern of error sensitivity would be related to anatomical abnormalities in the cerebellum, known to be a neural substrate of motor learning. Typical models of adaptation assume sensitivity to error to be a constant; however several studies contradict this, reporting a non-linear relationship between adaptation and error. Therefore, we first characterized sensitivity in healthy adults with a reach adaptation task, in which we perturbed their movements both proprioceptively and visually. By normalizing the trial-to-trial change in motor commands by the error size, we isolated sensitivity to error. We found that, for both visual and proprioceptive errors, sensitivity declined with increasing error size. Interestingly, the probability of a complex spike in cerebellar Purkinje cells, previously believed to be a neural representation of an error, declined with increasing error as well. We therefore posited that complex spikes represent sensitivity to error during cerebellar adaptation. We then repeated our paradigm on children with ASD. As hypothesized, we found increased sensitivity to proprioceptive error and decreased sensitivity to visual error, relative to healthy control children. In these same subjects, we used anatomical MRI to measure the volume of the senosorimotor region of the cerebellum. We found this region was significantly smaller in children with ASD, and that sensitivity was a predictor of volume, identifying a potential neural substrate for the sensorimotor abnormalities seen in ASD