Individual sensorimotor adaptation characteristics are independent across orofacial speech movements and limb reaching movements

Abstract

Sensorimotor adaptation is critical for human motor control but shows considerable interindividual variability. Efforts are underway to identify factors accounting for individual differences in specific adaptation tasks. However, a fundamental question has remained unaddressed: Is an individual's capability for adaptation effector system specific or does it reflect a generalized adaptation ability? We therefore tested the same participants in analogous adaptation paradigms focusing on distinct sensorimotor systems: speaking with perturbed auditory feedback and reaching with perturbed visual feedback. Each task was completed once with the perturbation introduced gradually (ramped up over 60 trials) and, on a different day, once with the perturbation introduced suddenly. Consistent with studies of each system separately, visuomotor reach adaptation was more complete than auditory-motor speech adaptation (80% vs. 29% of the perturbation). Adaptation was not significantly correlated between the speech and reach tasks. Moreover, considered within tasks, 1) adaptation extent was correlated between the gradual and sudden conditions for reaching but not for speaking, 2) adaptation extent was correlated with additional measures of performance (e.g., trial duration, within-trial corrections) only for reaching and not for speaking, and 3) fitting individual participant adaptation profiles with exponential rather than linear functions offered a larger benefit [lower root mean square error (RMSE)] for the reach task than for the speech task. Combined, results suggest that the ability for sensorimotor adaptation relies on neural plasticity mechanisms that are effector system specific rather than generalized. This finding has important implications for ongoing efforts seeking to identify cognitive, behavioral, and neurochemical predictors of individual sensorimotor adaptation.NEW & NOTEWORTHY This study provides the first detailed demonstration that individual sensorimotor adaptation characteristics are independent across articulatory speech movements and limb reaching movements. Thus, individual sensorimotor learning abilities are effector system specific rather than generalized. Findings regarding one effector system do not necessarily apply to other systems, different underlying mechanisms may be involved, and implications for clinical rehabilitation or performance training also cannot be generalized.

Keywords: auditory; reaching; sensorimotor adaptation; speech; vision.

Graphical abstract

Figure 1.

A: perturbation schedule for the gradual and sudden conditions, with the y-axis indicating the normalized extent of the perturbation and the x-axis indicating epochs of 3 trials (1 per reach target or word). B: equipment configuration for the speech auditory-motor adaptation task. Right: spectrogram for 1 trial of the word “tuck,” with solid turquoise tracking of the participant’s formants and the dashed purple tracks indicating the 250 cents upshift auditory feedback perturbation. C: experimental setup for the reach adaptation task. D, left: location of the 3 targets and central start position for the reach adaptation task. Right: unseen actual hand path (dashed red line) and projected visual feedback path (solid red line) for an early, full 30° counterclockwise perturbation trial.

Figure 2.

Group mean adaptation data (with shaded areas indicating ±1 SE) for gradual (pink) and sudden (blue) perturbation schedules (illustrated at top). Each participant’s data were first normalized to the median value of baseline trials 4–10. A: speech auditory-motor adaptation to a +250 cents shift of the vowel formant frequencies during monosyllabic word production (F1, F2: 1st and 2nd formant frequencies). B: reach visuomotor adaptation to a 30° counterclockwise rotation of fingertip cursor location during out-and-back movements. Data points correspond to epochs of 3 trials (cycles including 1 trial for each of 3 different target words or reach directions). The first 3 epochs of each condition (black symbols) were discarded to avoid initial familiarization effects on baseline normalization.

Figure 3.

A: boxplots of adaptation extent (as % of perturbation size) for the speech and reach tasks with sudden and gradual perturbation schedules. Adaptation was much more complete for reaching than for speaking (***P < 0.001). One outlier participant was identified in the sudden condition reach task. This individual’s data are marked with × in all conditions and were not included in the ANOVA. B: correlations between adaptation extent in the reach and speech tasks were not statistically significant for either the sudden (blue) or gradual (pink) condition. C: the correlation between adaptation extent in the gradual and sudden conditions was statistically significant for the reach task (gray diamonds) but not for the speech task (black circles). For B and C, lines and shaded regions represent linear regression fits with 95% confidence intervals; the asterisk indicates P_adj < 0.05; data points marked with × represent the participant with outlier data in the reach-sudden condition and were not included in the correlation analyses.

Figure 4.

Correlations between adaptation extent and perturbation phase measurements of within-trial corrections [reaching (A), speaking (B)] and trial duration [reaching (C), speaking (D)]. Gradual condition in pink; sudden condition in blue. In A and B, negative within-trial corrections indicate adjustments made in the opposite direction to the perturbation (gray shaded region). Outlier data points not included in the analyses are shown with × superimposed. Statistically significant correlations with adaptation extent occurred only for the reach task: for within-trial corrections in the gradual condition (A) and for trial duration in the sudden condition (C) (*P_adj < 0.05).

Figure 5.

Linear (Lin; green) and exponential (Exp; orange) model fitting for individual participant adaptation profiles in the sudden condition of the speech and reach tasks. Illustrations for a representative participant (A for speaking, C for reaching) show raw data and fitted functions together with root mean square error (RMSE) values for each fit (F1, F2: 1st and 2nd formant frequencies). Boxplots (B for speaking, D for reaching) show the RMSE values for exponential and linear fits for all participants. Two participants (1 in each task, both fitted functions) were found to have outlying data. These participants were not included in the final ANOVA and are marked with ×.