Learning to stand with unexpected sensorimotor delays

  1. Brandon G Rasman
  2. Patrick A Forbes
  3. Ryan M Peters
  4. Oscar Ortiz
  5. Ian Franks
  6. J Timothy Inglis
  7. Romeo Chua
  8. Jean-Sébastien Blouin  Is a corresponding author
  1. School of Physical Education, Sport, and Exercise Sciences, University of Otago, New Zealand
  2. Department of Neuroscience, Erasmus MC, University Medical Center Rotterdam, Netherlands
  3. School of Kinesiology, University of British Columbia, Canada
  4. Faculty of Kinesiology, University of Calgary, Canada
  5. Hotchkiss Brain Institute, Canada
  6. Faculty of Kinesiology, University of New Brunswick, Canada
  7. Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Canada
  8. Institute for Computing, Information and Cognitive Systems, University of British Columbia, Canada
11 figures, 3 tables and 1 additional file

Figures

Experimental setup and block diagram of robotic simulation.

(A) The participant stood on a force plate mounted to an ankle-tilt platform and was securely strapped to a rigid backboard. The ankle-tilt platform and backboard were independently controlled by …

Standing balance behavior with delays.

(A) Experiment 1: raw traces of body position (black) and velocity (blue) for a single participant balancing on the robotic simulator for 60 s at different imposed delay conditions. Dashed lines …

Standing balance behavior during the training protocol.

(A) Whole-body position (°; black) and velocity (°/s; blue) traces of a representative participant when balancing in the first (left) and last (right) minute of training. During training trials, the …

Experiment 2 vestibular-evoked muscle responses.

Data are from pre-learning (n = 8), post-learning (n = 8), and retention (n = 7) conditions. (A) Coherence, gain, and cross-covariance between vestibular stimuli and rectified soleus EMG activity …

Experiment 2 perceptual testing and standing behavior results.

(A) A Bayesian estimation procedure was used to fit sigmoidal functions to perceptual responses. The proportion of correct responses (i.e., button pressed during delay period) was calculated for …

Experiment 3 sway velocity variance, time-varying electrical vestibular stimulus-electromyography (EVS-EMG) coherence and gain, and perceptual detection time during delay transitions.

Data are presented across transition periods where time zero represents the transition point from baseline (20 ms) to 200 ms delayed balance control, which lasted for 8 s (between grayed out areas) …

Author response image 1
Pooled non-normalized cross-covariance (left) and impulse response (right) estimates from pre-learning data set sampled at 2000 Hz.

Estimates were calculated by concatenating data from all eight participants.

Author response image 2
Pooled non-normalized cross-covariance (left) and impulse response (right) functions from pre-learning data, originally sampled at 2000Hz and then down-sampled offline to 50Hz.

Note that cross-covariance and impulse response functions now provide similar results after down-sampled to 50Hz. Both responses, however, have poor resolution when compared to the original …

Author response image 3
Pooled non-normalized cross-covariance (left) and impulse response (right) functions from pre-learning data, originally sampled at 2000Hz and then down-sampled offline to 100Hz.

Note that the impulse response functions already become noisy when the data are downsampled to 100Hz.

Author response image 4
Pooled cross-covariance estimates of vestibular-evoked muscle responses.

Normalized responses (left), non-normalized responses (center) and scaled non-normalized responses (right). All three approaches produce a similar outcome: vestibular-evoked response amplitudes …

Author response image 5
Experiment 3 time-varying EVS-EMG coherence, gain and sway velocity variability during detected (perceived) and missed (not perceived) delay transitions.

Data are presented across transition periods, where the simulation transitioned from baseline to 200 ms delayed balance control, which lasted for 8s (between dashed red vertical lines). Top panel, a …

Tables

Table 1
Summary of statistical results.
DelayLearningDelay × learning interaction
VariableFpFpFp
Sway velocity variance
Exp 1: standing balance trialsF(5,59.15) = 14.98< 0.001N/AN/AN/AN/A
Exp 2: vestibular testingF(5,111.26) = 33.89< 0.001F(2,113.19) = 46.65< 0.001F(10,111.25) = 5.72< 0.001
Exp 2: perceptual testingF(6,118.83) = 31.00< 0.001F(2,121.47) = 25.82< 0.001F(12,118.83) = 2.08= 0.023
Other variables
Exp 1: percent within limitsF(5,60) = 127.48< 0.001N/AN/AN/AN/A
Exp 2: cross-covarianceW(5) = 1158.86< 0.001W(2) = 70.57< 0.001W(7) = 90.89< 0.001
Exp 2: perceptual thresholdN/AN/AF(2,11.84) = 7.52= 0.008N/AN/A
  1. For Exp 2, vestibular cross-covariance responses (peak-to-peak amplitudes) were analyzed using an ordinal logistic regression after rank transforming the data.

Table 2
Vestibular response magnitude and sway behavior from vestibular stimulation trials in Experiment 2 vestibular testing.
Delay (ms)20100200300400500
Pre-learning (n = 8)
Cross-cov. (%EMG·mA)17.7/16.020.7/18.814.0/11.08.10/12.45.54/10.94.35/5.50
Sway velocity variance [°/s]20.18 ± 0.170.93 ± 0.586.52 ± 4.4011.35 ± 5.1016.79 ± 8.5111.80 ± 6.53
Post-learning (n = 8)
Cross-cov. (%EMG·mA)20.4/23.220.4/26.721.5/19.619.1/20.515.7/16.014.1/21.4
Sway velocity variance [°/s]20.05 ± 0.050.13 ± 0.090.54 ± 0.321.58 ± 0.744.20 ± 1.056.99 ± 2.61
Retention (n = 7)
Cross-cov. (%EMG·mA)18.8/20.015.3/17.619.3/20.116.4/12.511.8/9.1610.6/13.3
Sway velocity variance [°/s]20.09 ± 0.110.20 ± 0.120.90 ± 0.482.91 ± 1.255.51 ± 0.986.48 ± 3.51
Table 3
Perceptual detection rates and sway behavior from perceptual testing in Experiment 2.
Delay (ms)50100150200250300350
No learning (n = 10)*
 Used trials (out of 200)197194195196195198N/A
 Detections (% detected)8 (4%)60 (31%)128 (66%)172 (88%)186 (95%)198 (100%)N/A
 Sway velocity variance [°/s]20.12 ± 0.050.57 ± 0.481.69 ± 1.213.71 ± 2.524.87 ± 2.626.32 ± 1.95N/A
 Detection time (s)3.8 ± 2.04.7 ± 2.04.0 ± 1.93.5 ± 1.82.9 ± 1.52.6 ± 1.2N/A
Pre-learning (n = 8)
 Used trials (out of 160)148151147147150151152
 Detections (% detected)20 (14%)46 (30%)111 (76%)132 (90%)146 (97%)151 (100%)152 (100%)
 Sway velocity variance [°/s]20.24 ± 0.270.45 ± 0.331.84 ± 1.364.01 ± 2.334.18 ± 1.385.09 ± 1.464.70 ± 1.64
 Detection time (s)4.1 ± 2.13.7 ± 1.93.6 ± 1.83.2 ± 1.62.9 ± 1.62.4 ± 1.22.3 ± 1.1
Post-learning (n = 8)
 Used trials (out of 160)157156157156157157151
 Detections (% detected)16 (10%)23 (15%)52 (33%)101 (65%)136 (87%)153 (97%)151 (100%)
 Sway velocity variance [°/s]20.11 ± 0.100.16 ± 0.130.40 ± 0.261.34 ± 1.092.20 ± 1.613.02 ± 2.333.70 ± 2.37
 Detection time (s)4.2 ± 2.03.8 ± 2.44.1 ± 1.73.9 ± 1.73.4 ± 1.82.7 ± 1.32.2 ± 1.1
Retention (n = 5)
 Used trials (out of 100)96939898969892
 Detections (% detected)8 (8%)21 (23%)40 (41%)50 (51%)71 (74%)84 (86%)92 (100%)
 Sway velocity variance [°/s]20.05 ± 0.030.13 ± 0.060.27 ± 0.150.84 ± 0.511.51 ± 0.761.89 ± 1.092.60 ± 1.05
 Detection time (s)5.0 ± 1.74.2 ± 2.04.2 ± 2.23.8 ± 2.03.4 ± 1.83.1 ± 1.83.1 ± 1.4
  1. Sway velocity variance and detection time are presented as mean ± SD.

  2. *No learning group is an independent sample of participants that were not exposed to a 350 ms delay.

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