Brain System Abnormalities Associated with Reduced Control of Sustained and Repetitive Motor Behaviors

Background:  

A diverse set of sensorimotor impairments has been documented in autism spectrum disorder (ASD). We have found that patients show reduced control of manual motor behaviors when they attempt to maintain a constant level of force (sustained force), and when they produce rapid, repetitive action sequences (repetitive force). The severities of these two types of sensorimotor impairments are relatively independent across affected individuals. In the present study, we used functional MRI (fMRI) to identify brain systems contributing to sustained and repetitive motor impairments in ASD.

Objectives:

To identify the neural system abnormalities associated with dysmetria of sustained sensorimotor behaviors and repetitive sensorimotor behaviors in ASD.

Methods:

Twenty individuals with ASD and 15 healthy controls matched on age, IQ and handedness completed fMRI tests of precision grip force. During the sustained force test, participants pressed with their thumb and index finger on a force transducer while viewing a white FORCE bar on a screen that moved upwards with increased force toward a fixed green TARGET bar. Participants were instructed to maintain the FORCE bar at the level of the TARGET bar for 24 seconds. During the repetitive force test, participants completed 24 second blocks consisting of six repeated sequences in which they pressed on the transducer for 2 seconds and then relaxed for 2 seconds. Blocks for both tests were alternated with 24 sec rest blocks. Participants completed three blocks of each test at both 20 and 60% of their maximum force (12 force blocks total). The order of tasks and force level (20 and 60% of maximum force) were counterbalanced across participants.

Results:

Preliminary analyses were consistent with our published work (Mosconi et al., 2015; Wang et al., 2015) and indicated that individuals with ASD show increased force error relative to controls during the sustained force test, and less accurate initial force pulses compared to controls during the repetitive force test. During the sustained force test, individuals with ASD showed less activation in left superior temporal gyrus, bilateral posterior parietal cortex, supplementary motor cortex and bilateral cerebellum. During the repetitive force test, individuals with ASD showed less activation in supplementary motor cortex, contralateral primary motor cortex, right inferior parietal lobule and bilateral putamen.

Conclusions:

We report evidence that reduced accuracy of sustained motor behaviors in ASD is associated with reduced activation of parietal-cerebellar brain systems involved in transforming visual feedback into reactive motor adjustments. In contrast, reduced control of repetitive motor actions in ASD appears to reflect underactivity of frontal-striatal brain systems involved in initiating and terminating dynamic motor behaviors. These findings indicate that the diverse sensorimotor impairments that are evident in the majority of individuals with ASD reflect multiple distinct motor control and brain mechanisms. Our results also identify new brain targets for treatment development efforts aimed at reducing sustained sensorimotor dysmetria and repetitive behaviors in ASD. Further, this study shows that both cerebellar and striatal disruptions may represent significant components of the neurodevelopmental processes that cause ASD.