Visual feedback and motor memory contributions to sustained motor control deficits in autism spectrum disorder across childhood and into adulthood

Abstract

Background: Autistic individuals show deficits in sustained fine motor control which are associated with an over-reliance on visual feedback. Motor memory deficits also have been reported during sustained fine motor control in autism spectrum disorders (ASD). The development of motor memory and visuomotor feedback processes contributing to sustained motor control issues in ASD are not known. The present study aimed to characterize age-related changes in visual feedback and motor memory processes contributing to sustained fine motor control issues in ASD.

Methods: Fifty-four autistic participants and 31 neurotypical (NT) controls ages 10-25 years completed visually guided and memory guided sustained precision gripping tests by pressing on force sensors with their dominant hand index finger and thumb. For visually guided trials, participants viewed a stationary target bar and a force bar that moved upwards with increased force for 15s. During memory guided trials, the force bar was visible for 3s, after which participants attempted to maintain their force output without visual feedback for another 12s. To assess visual feedback processing, force accuracy, variability (standard deviation), and regularity (sample entropy) were examined. To assess motor memory, force decay latency, slope, and magnitude were examined during epochs without visual feedback.

Results: Relative to NT controls, autistic individuals showed a greater magnitude and steeper slope of force decay during memory guided trials. Across conditions, the ASD group showed reduced force accuracy (β = .41, R² = 0.043, t_79.3=2.36, p = 0.021) and greater force variability (β=-2.16, R² = .143, t_77.1=-4.04, p = 0.0001) and regularity (β=-.52, R² = .021, t_77.4=-2.21, p = 0.030) relative to controls at younger ages, but these differences normalized by adolescence (age × group interactions). Lower force accuracy and greater force variability during visually guided trials and steeper decay slope during memory guided trials were associated with overall autism severity.

Conclusions: Our findings that autistic individuals show a greater rate and magnitude of force decay than NT individuals following the removal of visual feedback indicate that motor memory deficits contribute to fine motor control issues in ASD. Findings that sensorimotor differences in ASD were specific to younger ages suggest delayed development across multiple motor control processes.

Keywords: Visuomotor; autism spectrum disorders; entropy; fine motor control; grip force; motor memory; sensorimotor; sensory integration; visual feedback.

Figure 1. Task Design.

A) During visually guided trials, participants see a target bar that turns from yellow to green to indicate that they should start pressing. Participants also view feedback of their force output (white bar) for the entire trial. B) During memory guided trials, participants see visual feedback of their force output (white bar) and the green target bar for the first 3s of the trial, after which the white force bar disappears, and they are instructed to keep pressing at the same force level until the target turns red (12s later). C) Example force output (dark blue) for a visually guided trial. The grey line represents target force. D) Example force output (dark blue) for a memory guided trial with target force indicated by the grey line. The participants’ force usually begins to decay (black arrow) after the visual feedback disappears.

Figure 2. Force accuracy.

A) Age (log₁₀ scale) associations with force accuracy for the ASD (red circles) and NT (blue triangles) groups. B) Force accuracy during visually guided (filled points) and memory guided (empty points) precision gripping. Black diamonds represent condition means adjusted for random intercepts of subject in the LMER models. Error bands (A) and bars (B) represent the 95% confidence intervals from the MLM models after accounting for random intercepts of participant.

Figure 3. Force Variability in Newtons (N).

A) Age (log₁₀ scale) associations with force standard deviation (log₁₀ scale) for the ASD (red circles) and NT controls (blue triangles) groups. Effects did not vary by condition, so data were collapsed across the visually guided (filled points) and memory guided (empty points) conditions. Error bands represent the 95% confidence intervals from the MLM models after accounting for random intercepts of subject.

Figure 4. Force Regularity.

A) Age (log₁₀ scale) associations with force SampEn (log₁₀ scale) for the ASD (red circles) and NT controls (blue triangles) groups. Higher SampEn corresponds to lower regularity. B) Force SampEn for the ASD (red circles) and NT controls (blue triangles) groups during the visually guided feedback (Vis; solid points) and memory guided (Mem; open points) conditions. Error bands and bars represent the 95% confidence intervals from the MLM models after accounting for random intercepts of subject.

Figure 5. Decay Slope and Magnitude.

A) Slope of the force decay (square root scale) following the removal of visual feedback for the ASD (red circles) and NT controls (blue triangles) groups. B) Magnitude of the force decay (log₁₀ scale) following the removal of visual feedback for ASD (red circles) and NT controls (blue triangles). Large points represent group means adjusted for random intercepts of subject in the MLM models. Error bars represent the 95% confidence intervals from the MLM models after accounting for random intercepts of subject.

Figure 6. Relation of ASD Symptomatology to grip control.

Association between ADOS-CSS scores and A) force accuracy and B) force variability in Newtons (N; Standard deviation (log₁₀ scale)) during visually guided precision gripping. C) Association between ADOS-CSS scores and the slope of logarithmic force decay during memory guided precision gripping. Error bands represent standard error.