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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Feedback Adaptation to Unpredictable Force Fields in 250 ms

Frédéric Crevecoeur, James Mathew, Marie Bastin and Philippe Lefèvre
eNeuro 21 April 2020, 7 (2) ENEURO.0400-19.2020; DOI: https://doi.org/10.1523/ENEURO.0400-19.2020
Frédéric Crevecoeur
1Institute of Information and Communication Technologies, Electronics and Applied Mathematics (ICTEAM), University of Louvain, Louvain-la-Neuve, 1348, Belgium
2Institute of Neuroscience (IoNS), University of Louvain, Brussels, 1200, Belgium
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James Mathew
1Institute of Information and Communication Technologies, Electronics and Applied Mathematics (ICTEAM), University of Louvain, Louvain-la-Neuve, 1348, Belgium
2Institute of Neuroscience (IoNS), University of Louvain, Brussels, 1200, Belgium
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Marie Bastin
3DNAlytics, Louvain-la-Neuve, 1348, Belgium
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Philippe Lefèvre
1Institute of Information and Communication Technologies, Electronics and Applied Mathematics (ICTEAM), University of Louvain, Louvain-la-Neuve, 1348, Belgium
2Institute of Neuroscience (IoNS), University of Louvain, Brussels, 1200, Belgium
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  • Figure 1.
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    Figure 1.

    A, Illustration of the workspace and task. Participants were instructed to perform forward reaching movements toward a visual target. An open goal target was presented for a random delay uniformly distributed between 2 and 4 s before it was filled in. The cue to reach the target was given by filling in the goal in red. The goal was turned red if the time between the go signal and the stabilization in the target was comprised between 0.6 and 0.8 s. B, Hand paths from the first force field trials (top) and trial #25 selected for illustration (bottom) from each participant (n = 18). Counterclockwise and clockwise perturbations are depicted in blue and red, respectively. The black traces illustrate for each panel baseline trials selected randomly (one baseline trial per participant). Osh.: target overshoot; Max.: maximum displacement in the direction of the force field; Thresh.: the positional threshold used to align EMG data. C, Maximum displacement in the direction of the force field. The dashed trace illustrates that the exponential fit did not reveal any significant curvature across force field trials (p > 0.05). D, Maximum target overshoot in the direction opposite to the force field. Solid traces revealed strongly significant exponential decay across trials (p < 0.001).

  • Figure 2.
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    Figure 2.

    A, Activity of posterior deltoid (PD; agonist, solid), and pectoralis major (PM; antagonist, dashed) averaged across the first four (light blue) and last four counterclockwise (dark blue) perturbation trials. The vertical arrows illustrate the moment when a sliding paired comparison of the agonist activity averaged in a 30-m window dropped below p < 0.05. Traces were aligned to the position threshold corresponding to one-third of the reach path to reduce variability. B, Same as panel a for clockwise perturbation trials. The position threshold is also represented. C, Grand average of the difference between the agonist activities of the first four and last four force field trials, aligned to the position threshold and averaged across muscles and participants (n = 18). The gray area corresponds to the standard error of the mean. The dashed window is the first window that displays a significant difference from sliding paired comparison (*p < 0.05, width = 30 ms). The solid window is the window associated with the minimum p value (**p < 10−4). D, p value of the sliding paired comparison performed on the data from C. All EMG traces were smoothed with a 5-ms sliding window for illustration purposes. E, Cumulative individual distributions of the delay between movement onset, and the moment when the p value of panel d dropped below 0.05. This moment corresponds to the time of threshold crossing plus 122 ms. The median delay between movement onset, and this time was 237 ± 15 ms (mean ± SD across participants, n = 18). F, Average hand paths and standard dispersion ellipses for the first four and last four trials in each direction, Dispersion ellipses are displayed 50 ms (see Materials and Methods). The black dots represent the moment corresponding to the vertical arrows of A, B.

  • Figure 3.
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    Figure 3.

    A, Forward hand velocity (black) and measured lateral force (blue) normalized to the average maximum calculated on the first trial. Shaded areas represent one standard error across participants (n = 18). Panels display data from the trials with counterclockwise force field perturbation. B, Same as panel a for the last trial normalized to the average maximum of the first trial. C, Lateral force as a function of the forward velocity for CW and CCW perturbations (red and blue, respectively). D, Same as C for the last trial. For panels C, D, there was one trace per participant. Observe that the traces were smoother in the last trials. E, Mean ± SEM of the linear correlation (R2 statistics) across force field trials from experiment 1 (CCW and CW perturbations averaged). F, Difference between the correlations from experiment 1 as calculated in C, and the correlation between the lateral force of each trial with the forward hand velocity of a randomly picked surrogate trial with replacement. The surrogate correlations were calculated 100 times per trial and participants and averaged across. The shaded area is one SEM.

  • Figure 4.
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    Figure 4.

    Control experiment, data from Crevecoeur et al. (2020). A, Individual hand traces from the first and last perturbation trials in each direction from the control experiment (one traces per participant, n = 8). B, Commanded (black) and measured (red) force profiles for the first (left) and last (right) clockwise perturbations. The arrow highlights the increase in peak terminal force linked with the target overshoot. Observe that the traces become very similar, which increases the temporal correlation between them. C, Correlations between commanded force and measured force as in Figure 3 against trial indices. Correlations were averaged across directions and participants. Displays are mean ± SEM across participants.

  • Figure 5.
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    Figure 5.

    A, Hand paths from the first (light colors) and 25th (dark colors) trials with an orthogonal field chosen to illustrate changes in feedback responses. All data were taken from experiment 2, and each trace represents trials taken from each participant (n = 18). Blue and red traces represent counter clock-wise and clockwise perturbations. B, Same as panel a for the curl field. C, Path length across force field trials. D, Trial by trial correlations between the lateral commanded force (proportional to forward velocity) and the measured force. Correlations were averaged across counterclockwise and clockwise directions. The shaded areas represent one SEM across participants. The dashed traces (mean ± SEM) are the correlations between the measured lateral force and the commanded force corresponding to the velocity of randomly picked trials with replacement. The procedure was repeated 100 times for each participant, and the results were averaged across CCW and CW perturbations directions.

  • Figure 6.
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    Figure 6.

    A–D, Same as Figure 2 for the orthogonal force field data from experiment 2 (a distinct group of 18 participants). Traces are first and last four trials in the force field for pectoralis major (A, blue) and posterior deltoid (B, red) aligned to the position threshold. The activity during unperturbed trials was subtracted and the traces were smoothed with a 5-ms moving average for illustration. The vertical arrows show the moment with a sliding paired comparison of activity averaged in 30-ms bins became significant (p < 0.05). C, Difference between early and late feedback responses (mean ± SEM) averaged across participants and muscles. The results of the sliding paired comparisons are shown: one star, first 30 ms-bin with p < 0.05, two stars: minimum of p (p < 0.005; see Materials and Methods). D, Individual distributions of time elapsed between reach onset and the center of the first bin with p < 0.05. The cross is the median ± SD across participants. E–H, Same as A–D for the curl force field.

  • Figure 7.
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    Figure 7.

    A, Average activity of posterior deltoid in curl (thick) and orthogonal (thin) counterclockwise perturbations across the last 15 trials of each type of force field. B, Same as a for pectoralis major from clockwise perturbations. C, Difference between activities recorded during curl and orthogonal force fields averaged across participants and muscles. The onset of significant changes based on a 30-ms-wide sliding window is highlighted with one star (p < 0.05), followed by strongly significant differences (two stars, p < 0.005). D, Average hand paths during counterclockwise perturbations. Ellipses are two-dimensional standard dispersion across participants every 50 ms, and the impact of the force field is illustrated with the gray arrow (a common scaling for the two force fields was applied for illustration). The open dots are the moment when the activities started to differ across two types of perturbations.

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Feedback Adaptation to Unpredictable Force Fields in 250 ms
Frédéric Crevecoeur, James Mathew, Marie Bastin, Philippe Lefèvre
eNeuro 21 April 2020, 7 (2) ENEURO.0400-19.2020; DOI: 10.1523/ENEURO.0400-19.2020

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Feedback Adaptation to Unpredictable Force Fields in 250 ms
Frédéric Crevecoeur, James Mathew, Marie Bastin, Philippe Lefèvre
eNeuro 21 April 2020, 7 (2) ENEURO.0400-19.2020; DOI: 10.1523/ENEURO.0400-19.2020
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Keywords

  • adaptive control
  • feedback control
  • motor adaptation
  • reaching

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