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 a trend for a steeper slope of force decay during memory guided trials. Across conditions, the ASD group showed reduced force accuracy (β = 0.41, R² = 0.043, t_79.3=2.36, p = .021) and greater force variability (β=-2.16, R² = 0.143, t_77.1=-4.04, p = .0001) and regularity (β=-0.52, R² = 0.021, t_77.4=-2.21, p = .030) relative to NT controls at younger ages, but these differences normalized by adolescence (age x 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 magnitude and tendency for a greater rate 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: Autism spectrum disorders; Entropy; Fine motor control; Grip force; Motor memory; Sensorimotor; Sensory integration; Visual feedback; Visuomotor.

Fig. 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) in Newtons (N) for a neurotypical participant during a visually guided trial. The grey line represents target force. (D) Example force output (dark blue) in Newtons (N) for a neurotypical participant during 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. (E) Example force output (dark blue) in Newtons (N) for an autistic participant during a visually guided trial. (F) Example force output (dark blue) in Newtons (N) for an autistic participant during a memory guided trial

Fig. 2

Force accuracy. Age (years; log₁₀ scale) associations with force accuracy (proportion of mean force to target force) for (A) the autism (ASD; red circles) and (B) the neurotypical (NT; blue triangles) groups. The regression lines represent the significant group x age effects (across conditions), though data for visually guided (Vis; solid points) and memory guided (Mem; empty points) are also shown. (C) Force accuracy depicted as a function of group (NT: blue triangles; ASD: red circles) during visually guided (Vis; filled points) and memory guided (Mem; empty points) precision gripping. The large points represent group x condition marginal means adjusted for random intercepts of subject in the LMER models. The * represents the significant condition main effect. Error bands (A, B) and bars (C) represent the 95% confidence intervals from the MLM models after accounting for random intercepts of participant

Fig. 3

Force Variability in Newtons (N). Age (years; log₁₀ scale) associations with force standard deviation in Newtons (N; log₁₀ scale) for (A) the autism (ASD; red circles) and (B) neurotypical control (NT; blue triangles) groups. The regression lines represent the significant group x age effects (across conditions), though data for visually guided (Vis; solid points) and memory guided (Mem; empty points) are also shown. (C) Force variability depicted as a function of group (NT: blue triangles; ASD: red circles) during visually guided (Vis; filled points) and memory guided (Mem; empty points) precision gripping. The large points represent group x condition marginal means adjusted for random intercepts of subject in the LMER models. The * represents the significant group main effect. Error bands (A, B) and bars (C) represent the 95% confidence intervals from the MLM models after accounting for random intercepts of participant

Fig. 4

Force regularity. Age (years; log₁₀ scale) associations with force SampEn (unitless; log₁₀ scale) for (A) the autism (ASD; red circles) and (B) neurotypical control (NT; blue triangles) groups. Higher SampEn corresponds to lower regularity. The regression lines represent the significant group x age effects (across conditions), though data for visually guided (Vis; solid points) and memory guided (Mem; empty points) are also shown. (C) Force regularity depicted as a function of group (NT: blue triangles; ASD: red circles) during the visually guided feedback (Vis; solid points) and memory guided (Mem; empty points) conditions. The large points represent group x condition marginal means adjusted for random intercepts of subject in the LMER models. The * represents the significant effect of group in the visually guided condition (group x condition interaction). Error bands (A, B) and bars (C) represent the 95% confidence intervals from the MLM models after accounting for random intercepts of subject

Fig. 5

Decay slope and magnitude. (A) Slope of the force decay (square root scale) following the removal of visual feedback (memory guided condition) for the autism (ASD; red circles) and neurotypical control (NT; blue triangles) groups. (B) Magnitude of the force decay (log₁₀ scale) following the removal of visual feedback (memory guided condition) for the ASD (red circles) and NT control (blue triangles) groups. Large points represent group means adjusted for random intercepts of subject in the MLM models. The * represents a significant effect of group. Error bars represent the 95% confidence intervals from the MLM models after accounting for random intercepts of subject

Fig. 6

Relation of ASD Symptomatology to grip control. Association between Autism Diagnostic Observation Schedule – Composite Severity Scores (ADOS-CSS) for the autism group (ASD; red circles) and (A) force accuracy (proportion of mean force to target force) and (B) force variability (standard deviation; log₁₀ scale) in Newtons (N) during visually guided (Vis; solid points) precision gripping. (C) Association between ADOS-CSS scores for the ASD group (red circles) and the slope of logarithmic force decay (square root scale) during memory guided precision gripping (Mem; empty points). Error bands represent standard error