Feedforward and Feedback Motor Control Abnormalities Implicate Cerebellar Dysfunctions in Autism Spectrum Disorder

Abstract

Sensorimotor abnormalities are common in autism spectrum disorder (ASD) and among the earliest manifestations of the disorder. They have been studied far less than the social-communication and cognitive deficits that define ASD, but a mechanistic understanding of sensorimotor abnormalities in ASD may provide key insights into the neural underpinnings of the disorder. In this human study, we examined rapid, precision grip force contractions to determine whether feedforward mechanisms supporting initial motor output before sensory feedback can be processed are disrupted in ASD. Sustained force contractions also were examined to determine whether reactive adjustments to ongoing motor behavior based on visual feedback are altered. Sustained force was studied across multiple force levels and visual gains to assess motor and visuomotor mechanisms, respectively. Primary force contractions of individuals with ASD showed greater peak rate of force increases and large transient overshoots. Individuals with ASD also showed increased sustained force variability that scaled with force level and was more severe when visual gain was highly amplified or highly degraded. When sustaining a constant force level, their reactive adjustments were more periodic than controls, and they showed increased reliance on slower feedback mechanisms. Feedforward and feedback mechanism alterations each were associated with more severe social-communication impairments in ASD. These findings implicate anterior cerebellar circuits involved in feedforward motor control and posterior cerebellar circuits involved in transforming visual feedback into precise motor adjustments in ASD.

Impaired Communication Between the Motor and Somatosensory Homunculus Is Associated With Poor Manual Dexterity in Autism Spectrum Disorder

“…Abnormality of these regions may have a distinct influence on motor impairment in ASD. For example, although the S1-M1 connections likely play a role in sensory feedback after contact with an object, anterior cerebellar abnormalities may be associated with deficits in the feedforward planning, which occurs before object contact (58). A more comprehensive assessment of the tracts involved in motor planning and execution, which may also include, for example, the superior cerebellar peduncle and the superior longitudinal fasciculus system, will be necessary to understand the specific role of each tract to fine motor skills in ASD.…”

Memory-guided force output is associated with self-reported ADHD symptoms in young adults

“…The precision grip task studied here has been employed in previous investigations to understand how the neural control of voluntary movement is impaired in Autism Spectrum Disorders (ASD) (Mosconi et al 2015; Wang et al 2015), Parkinson’s disease (Vaillancourt et al 2001) and atypical parkinsonian disorders (Neely et al 2013b), and essential tremor (Neely et al 2015; Poon et al 2011). Visual stimuli were presented on a 102 cm (40-inch) Samsung television screen with resolution 1920 × 1080 and a 120 Hz refresh rate.…”

Motor Memory Deficits Contribute to Motor Impairments in Autism Spectrum Disorder

“…In a pair of studies examining precision gripping, we reported that individuals with ASD make less accurate initial force contractions and show increased variability of sustained force output despite similar levels of overall force relative to controls (Mosconi et al 2015; Wang et al 2015). These findings suggest that the internal action representation used for feedforward control (i.e., the initial contraction) may not be accurate in individuals with ASD.…”

“…Further, the finding that individuals with ASD produce greater variability during sustained force implicates the online visuomotor mechanisms involved in translating visual feedback into corrective motor commands. Importantly, the variability in sustained force increased further when visual feedback was reduced (Mosconi et al 2015). Taken together, these findings demonstrate that individuals with ASD may have inaccurate internal representations to plan force output and may also be more reliant on visual feedback to make adjustments during sustained force output.…”

“…The removal of visual feedback required that participants initially utilize proprioceptive and somatosensory feedback mechanisms to maintain a constant level of force, and subsequently rely on stored internal representations to guide force output. Participants completed a precision gripping task similar to that previously used by our group to document alterations in visually guided force control in ASD (Mosconi et al 2015; Wang et al 2015). They initially gripped opposing load cells with their thumb and index finger and attempted to maintain a constant level of force while viewing online visual feedback on a monitor in front of them.…”