Human motor fatigability as evoked by repetitive movements results from a gradual breakdown of surround inhibition
- Neural Control of Movement Lab, Switzerland
- University of Zurich, Federal Institute of Technology Zurich, University and Balgrist Hospital Zurich, Switzerland
- Royal Holloway University of London, United Kingdom
Figures
Figure 1 with 1 supplement
Time and speed dependency of motor slowing.
(A) Time course of motor slowing. Participants tapped at maximum speed for 10 s (orange), 30 s (blue) or 50 s (pink) at their maximum speed. Slowing starts immediately with movement onset and …
Figure 1—figure supplement 1
Deviation from the target speed in the pacing experiment shown in Figure 1B.
During the first 10 s, participants slightly underpaced during the slow and ultraslow conditions whereas they overpaced during the fast condition. This error diminished for the two slower conditions …
Figure 2
Motor slowing of different movement effectors.
(A) General behavioural paradigm. Participants were asked to either perform long (≥30 s) or short (10 s) blocks of repetitive movements, followed by breaks of at least 30 s. Movement speed was …
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Figure 2—source data 1
Individual behavioural data (movement cycles per time bin) of the foot tapping experiment depicted in panel 2B.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.005
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Figure 2—source data 2
Individual behavioural data (movement cycles per time bin) of the eye movement experiment depicted in panel 2C.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.006
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Figure 2—source data 3
Individual behavioural data (movement cycles per time bin) of the finger tapping experiment depicted in panel 2D.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.007
Figure 3
Results of the recovery experiment (N = 17).
(A) Experimental paradigm to characterise the recovery process after motor slowing. Participants were instructed to tap with two fingers for 30 s (slowing condition) or 10 s (control condition) …
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Figure 3—source data 1
Individual behavioural data (movement cycles per time bin) after different break lengths depicted in panel 3B.
All values given in Hertz.
- https://doi.org/10.7554/eLife.46750.009
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Figure 3—source data 2
Individual behavioural data (movement cycles per time bin) before different break lengths depicted in panel 3C.
All values given in Hertz.
- https://doi.org/10.7554/eLife.46750.010
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Figure 3—source data 3
Individual data of recovery depicted in panel 3D.
- https://doi.org/10.7554/eLife.46750.011
Figure 4
Results of the functional magnetic resonance (fMRI) experiment (N = 25).
(A) Participants performed slowing (30 s) or control (10 s) two-finger tapping followed by a break of 30 s in the fMRI scanner. (B) A typical motor network was activated during tapping (pink, pFWE <0…
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Figure 4—source data 1
Individual behavioural data (movement cycles per time bin) of the fMRI experiment depicted in panel 4C.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.014
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Figure 4—source data 2
T-map of fMRI activation (motor network) depicted in panel 4B.
- https://doi.org/10.7554/eLife.46750.015
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Figure 4—source data 3
T-map of fMRI activation (slowing) depicted in panel 4B.
- https://doi.org/10.7554/eLife.46750.016
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Figure 4—source data 4
T-map of fMRI activation (recovery) depicted in panel 4B.
- https://doi.org/10.7554/eLife.46750.017
Figure 5
Results of the electroencephalography (EEG) experiment (N = 17).
(A) Participants performed slowing (30 s) or control (10 s) sequence tapping followed by a break of 30 s while EEG was measured. (B) Source localisation was performed using eLoreta and fluctuations …
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Figure 5—source data 1
Individual behavioural data (movement cycles per time bin) of the EEG experiment depicted in panel 5C.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.019
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Figure 5—source data 2
Individual alpha power data depicted in panel 5E.
- https://doi.org/10.7554/eLife.46750.020
Figure 6
Results of the short latency intracortical inhibition (SICI) experiment (N = 13).
(A) SICI was measured before (Pre) and after (Post), as well as during the break after either slowing (40 s) or control (10 s) tapping. (B) Motor slowing during the behavioural task (blue line) …
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Figure 6—source data 1
Individual behavioural data (movement cycles per time bin) of the SICI experiment depicted in panel 6B.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.022
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Figure 6—source data 2
Individual SICI data depicted in panel 6C.
- https://doi.org/10.7554/eLife.46750.023
Figure 7 with 1 supplement
Results of the surround inhibition experiment (N = 19).
(A) Surround inhibition was measured before (Pre) and after (Post), as well as during the break after either slowing (30 s) or control (10 s) tapping. The length of the break was increased to 60 s …
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Figure 7—source data 1
Individual behavioural data (movement cycles per time bin) of the surround inhibition experiment depicted in panel 7C.
All values normalised to control condition.
- https://doi.org/10.7554/eLife.46750.026
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Figure 7—source data 2
Individual coactivation data of the surround inhibition experiment depicted in panel 7D.
- https://doi.org/10.7554/eLife.46750.027
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Figure 7—source data 3
Individual surround inhibition data depicted in panel 7E.
- https://doi.org/10.7554/eLife.46750.028
Figure 7—figure supplement 1
Raw MEP Ratios from the surround inhibition experiment for FDI (A) and ADM (B).
Only the FDI muscle showed a condition specific effect for surround inhibition. ADM showed a general facilitation effect independent of tapping condition.
Figure 8
Potential mechanism of motor slowing.
Two populations of pyramidal neurons (P) control agonistic (PFlex) and antagonistic (PExt) movements. The tuning curve of those neurons is under control of inhibitory interneurons (I). At the …
Tables
Table 1
Comparison of movement speed (measured in movement cycles per 10 s) during the first 10 s of the first and last trials for different effectors, as well as movement speed within a 30 s trial (first vs. last 10 s).
The results show that movement speed at the beginning of each trial is stable, whereas movement speed decreased significantly within a trial. All values mean ± sem.
| Speed during first 10s | Speed within 30s | N Subjects | N Trials | |||
|---|---|---|---|---|---|---|
| First Trial | Last Trial | First 10s | Last 10s | |||
| 2-finger tapping | 39.48±1.61 | 37.00±1.24 | 37.89±1.12 | 31.82±1.04 | 25 | 16 |
| Foot tapping | 50.00±4.16 | 53.67±4.20 | 55.167±3.25 | 47.233±2.89 | 12 | 20 |
| Eye Movement | 14.33±0.83 | 16.83±0.95 | 15.817±0.77 | 12.933±0.67 | 12 | 20 |
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mean ± standard error of the mean, all values Movement Cycles per 10s.
Additional files
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Supplementary file 1
Table showing individual movement speeds for each condition of experiment 2, including the different target speeds of each participant.
- https://doi.org/10.7554/eLife.46750.030
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Supplementary file 2
Table showing peak fMRI activations during tapping.
- https://doi.org/10.7554/eLife.46750.031
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Supplementary file 3
Table showing rest motor threshold, conditioning stimulus and test stimulus intensities of SICI measures as % maximum stimulator output (%MSO), showing that stimulus intensities were comparable across sessions (all values mean ± standard deviation).
- https://doi.org/10.7554/eLife.46750.032
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Supplementary file 4
Table showing background EMG (mV) of SICI measures during the break.
Note that background EMG was very small and that potential differences were <0.001 mV and well below the observed standard deviation. Statistical tests revealed only non-significant effects of condition (F(1,12)=0.696, p=0.42), or time (F(2,12)=3.137, p=0.08). Most importantly, there was no significant condition x time (F(2,12) = 0.203, p=0.819) interaction for background EMG. All values mean ± std.
- https://doi.org/10.7554/eLife.46750.033
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Supplementary file 5
Table showing average motor evoked potentials of the control stimulus in mV for Pre and Post measurements, as well as during the break after 30 s and 10 s tapping showing that the control stimulus did not change during the surround inhibition experiment.
Further, the rest motor threshold (RMT, in percentage of maximum stimulator output) was comparable across both sessions.
- https://doi.org/10.7554/eLife.46750.034
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Supplementary file 6
Table showing background EMG of surround inhibition measures during the break.
Note that background EMG was very small and that potential differences were <0.002 mV and well below the observed standard deviation. Statistical tests revealed only non-significant effects of condition (F(1,18)=1.728, p=0.205) or time (F(2,18)=0.701, p=0.509). Most importantly, there was no significant condition x time (F(2,18) = 0.735, p=0.493) interaction for background EMG. All values mean ± std.
- https://doi.org/10.7554/eLife.46750.035
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Supplementary file 7
Data from previous studies used for sample size calculations as described in the transparent reporting form.
- https://doi.org/10.7554/eLife.46750.036
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Supplementary file 8
Summary table of the statistical tests performed in each experiment as described in the transparent reporting form.
- https://doi.org/10.7554/eLife.46750.037
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Transparent reporting form
- https://doi.org/10.7554/eLife.46750.038
