Initial action output and feedback-guided motor behaviors in autism spectrum disorder

Kathryn E Unruh,John A Sweeney,Walker S Mckinney,Kandace K Fleming,Erin K Bojanek,Matthew W Mosconi

doi:10.1186/s13229-021-00452-8

Abstract

BackgroundSensorimotor issues are common in autism spectrum disorder (ASD), related to core symptoms, and predictive of worse functional outcomes. Deficits in rapid behaviors supported primarily by feedforward mechanisms, and continuous, feedback-guided motor behaviors each have been reported, but the degrees to which they are distinct or co-segregate within individuals and across development are not well understood.MethodsWe characterized behaviors that varied in their involvement of feedforward control relative to feedback control across skeletomotor (precision grip force) and oculomotor (saccades) control systems in 109 individuals with ASD and 101 age-matched typically developing controls (range: 5–29 years) including 58 individuals with ASD and 57 controls who completed both grip and saccade tests. Grip force was examined across multiple force (15, 45, and 85% MVC) and visual gain levels (low, medium, high). Maximum grip force also was examined. During grip force tests, reaction time, initial force output accuracy, variability, and entropy were examined. For the saccade test, latency, accuracy, and trial-wise variability of latency and accuracy were examined.ResultsRelative to controls, individuals with ASD showed similar accuracy of initial grip force but reduced accuracy of saccadic eye movements specific to older ages of our sample. Force variability was greater in ASD relative to controls, but saccade gain variability (across trials) was not different between groups. Force entropy was reduced in ASD, especially at older ages. We also find reduced grip strength in ASD that was more severe in dominant compared to non-dominant hands.LimitationsOur age-related findings rely on cross-sectional data. Longitudinal studies of sensorimotor behaviors and their associations with ASD symptoms are needed.ConclusionsWe identify reduced accuracy of initial motor output in ASD that was specific to the oculomotor system implicating deficient feedforward control that may be mitigated during slower occurring behaviors executed in the periphery. Individuals with ASD showed increased continuous force variability but similar levels of trial-to-trial saccade accuracy variability suggesting that feedback-guided refinement of motor commands is deficient specifically when adjustments occur rapidly during continuous behavior. We also document reduced lateralization of grip strength in ASD implicating atypical hemispheric specialization.

Highlights

Sensorimotor deficits are common in autism spectrum disorder (ASD), emerge within the first years of life, often prior to social-communication issues [3, 10] and are predictive of worse functional outcomes [9, 68].Unruh et al Molecular Autism (2021) 12:52While sensorimotor issues repeatedly have been demonstrated in ASD, the majority of existing studies either have approached sensorimotor behaviors as a unitary construct or interrogated component motor processes in isolation
We identify reduced accuracy of initial motor output in ASD that was specific to the oculomotor system implicating deficient feedforward control that may be mitigated during slower occurring behaviors executed in the periphery
Maximum voluntary contraction Individuals with ASD showed reduced maximum voluntary contraction (MVC) compared to typically developing (TD) controls, and the severity of these differences varied as a function of hand tested (Fig. 2; group x hand tested: F1,2103 = 54.00, p < .001)

Summary

Introduction

Sensorimotor deficits are common in autism spectrum disorder (ASD), emerge within the first years of life, often prior to social-communication issues [3, 10] and are predictive of worse functional outcomes [9, 68].Unruh et al Molecular Autism (2021) 12:52While sensorimotor issues repeatedly have been demonstrated in ASD, the majority of existing studies either have approached sensorimotor behaviors as a unitary construct or interrogated component motor processes in isolation. Sensorimotor deficits are common in autism spectrum disorder (ASD), emerge within the first years of life, often prior to social-communication issues [3, 10] and are predictive of worse functional outcomes [9, 68]. In addition to showing reduced coordination of complex lower (e.g., gait; [41]) and upper body movements (e.g., reaching; [16, 17]), and higher rates of dyspraxia [8, 9, 48], individuals with ASD show deficits in sensorimotor behavior that implicate dysfunction of both feedforward motor control mechanisms and sensory feedback processes. Reduced entropy of individuals’ force time series during sustained precision gripping has been documented repeatedly in ASD suggesting the ability to integrate the multiple feedback and feedforward processes involved in dynamically adjusting ongoing behavior is compromised. Deficits in rapid behaviors supported primarily by feedforward mechanisms, and continuous, feedback-guided motor behaviors each have been reported, but the degrees to which they are distinct or co-segregate within individuals and across development are not well understood

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