Increased Force Variability in Autism Reflects Reduced Modulation of Motor Neuron Pool Beta Oscillations

Background: Sensorimotor impairments are common in individuals with autism spectrum disorder (ASD). We recently demonstrated that patients exhibit amplified force variability during precision gripping. The neurophysiological mechanisms associated with these impairments are not well understood. Recording of activity of the motor neuron pool represents a promising approach for understanding brain mechanisms as motor unit activity represents the final pathway of the voluntary command from the brain to the muscle. Here, we used surface electromyography (EMG) and specialized surface electrodes to record multiple motor units during a test of manual force control.

Objectives: To determine the neuromuscular mechanisms that contribute to impaired force control in ASD during isometric index finger abduction.

Methods: Seventeen individuals with ASD and 13 healthy controls matched on age, gender, IQ and handedness performed an isometric index finger abduction task at 20, 40 and 60% of their maximum force. Participants pressed with their index finger against a precision load cell while viewing visual feedback on a monitor in front of them. As they increased force against the load cell, a force cursor on the monitor increased in height. They were instructed to press against the load cell so that the force cursor reached the height of a target line for 27 seconds. To determine individuals’ ability to modulate motor neuron pool activity, we used an EMG decomposition system To determine individuals’ ability to modulate motor neuron pool activity, we used an EMG decomposition system to identify and record action potentials from multiple motor units. A specialized electrode was placed along the fibers of the first dorsal interosseous muscle to record neuromuscular activity. Participants performed 2 trials at each force level interleaved with 1 min rest blocks.

Results:  Individuals with ASD exhibited greater force variability compared to healthy controls across force levels. Mean force was not different between groups at any force level. Mean discharge rate of the motor neuron pool decreased with increasing force levels. Individuals with ASD exhibited an increased mean discharge rate compared to healthy controls. Frequency analyzes showed that the majority of the modulation of motor neuron pool activity related to force control was in the beta range (10-35 Hz). Individuals with ASD showed reduced modulation of the motor neuron pool in the beta range compared to healthy controls.

Conclusions:  Our findings show that amplified force variability in individuals with ASD reflects altered activation of the motor neuron pool.  Increased firing rate of the motor neuron pool in ASD suggests that larger motor units recruited redundantly to produce force may impair force control in patients. We also found decreased motor neuron pool oscillations in the beta range (10-35 Hz) in ASD suggesting that neuromuscular activity associated with central commands involved in ensuring stable motor output are compromised in ASD. These results indicate that brain mechanisms involved in precisely stabilizing motor output are disrupted in ASD and may be promising targets for treatment and biomarker discovery research.