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. 2015 Jul 28;9:185.
doi: 10.3389/fnbeh.2015.00185. eCollection 2015.

Sensorimotor Organization of a Sustained Involuntary Movement

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Free PMC article

Sensorimotor Organization of a Sustained Involuntary Movement

Jack De Havas et al. Front Behav Neurosci. .
Free PMC article

Abstract

Involuntary movements share much of the motor control circuitry used for voluntary movement, yet the two can be easily distinguished. The Kohnstamm phenomenon (where a sustained, hard push produces subsequent involuntary arm raising) is a useful experimental model for exploring differences between voluntary and involuntary movement. Both central and peripheral accounts have been proposed, but little is known regarding how the putative Kohnstamm generator responds to afferent input. We addressed this by obstructing the involuntary upward movement of the arm. Obstruction prevented the rising EMG pattern that characterizes the Kohnstamm. Importantly, once the obstruction was removed, the EMG signal resumed its former increase, suggesting a generator that persists despite peripheral input. When only one arm was obstructed during bilateral involuntary movements, only the EMG signal from the obstructed arm showed the effect. Upon release of the obstacle, the obstructed arm reached the same position and EMG level as the unobstructed arm. Comparison to matched voluntary movements revealed a preserved stretch response when a Kohnstamm movement first contacts an obstacle, and also an overestimation of the perceived contact force. Our findings support a hybrid central and peripheral account of the Kohnstamm phenomenon. The strange subjective experience of this involuntary movement is consistent with the view that movement awareness depends strongly on efference copies, but that the Kohnstamm generator does not produces efference copies.

Keywords: efference copy; involuntary contraction; involuntary movement; motor control; sensory feedback.

Figures

Figure 1
Figure 1
A schematic of Experiment 1 showing the order in which the trials were experienced and the specific instructions given to the participants. Training was always completed first, followed by a Kohnstamm trial. The order of Kohnstamm trial types was randomized and counterbalanced across participants. Next were blocks of either Voluntary or Passive Movement trials, which were separately randomized and counterbalanced. Within each block of Voluntary or Passive trials there was always one trial at each force level. The specific order was randomized.
Figure 2
Figure 2
Schematic for Experiment 1 showing arm displacement and EMG from a representative no obstruction (A) and obstruction (B) trial. Note that only the last ~2 s of the 30 s isometric induction contraction are shown for both trials. This is followed by relaxation of the muscle which lasted ~1.5 s in this participant. The aftercontraction then began, accompanied by involuntary movement. In the no obstruction trial (A) the arm rose unimpeded. In the obstruction trial (B) an obstacle stopped the arm at ~20°.
Figure 3
Figure 3
The effect of obstruction on EMG during Kohnstamm. Dashed line indicates time of obstruction in obstruction condition and time when obstruction would have occurred in the no obstruction condition. Error bars show SEM.
Figure 4
Figure 4
Schematic for Experiment 2 showing EMG of obstructed left arm and unobstructed right arm from a single representative trial. Note that only the last ~3 s of the 30 s isometric induction contraction is shown.
Figure 5
Figure 5
Effects of introduction and removal of an obstacle on both the unobstructed and obstructed arm during bilateral Kohnstamm. Error bars show SEM.
Figure 6
Figure 6
Increase in EMG 60–160 ms post-contact with obstacle during Voluntary and Kohnstamm movements. Insert shows the mean increase in EMG relative to a trend line fitted to pre-contact EMG on every trial. Trend line is shown for illustrative purposes.
Figure 7
Figure 7
Rectified and smoothed EMG from both arms from a single representative trial (illustrates the signal oscillation during contact with obstacle).
Figure 8
Figure 8
Group average positive and negative AUC of first derivative of EMG for both Obstructed arm and Unobstructed arm. Resting muscle refers to 1000 ms window at the start of the trial, before the Kohnstamm induction. Before obstruction refers to a 500 ms window immediately prior to contact with obstacle. During obstruction refers to a window that includes the entire time in contact with the obstacle (~1750 ms), excluding the first 250 ms (stretch response). After release is a 500 ms window immediately after obstacle has been removed. All AUC calculations are adjusted for the number of samples in each window.
Figure 9
Figure 9
Force of initial Kohnstamm and Voluntary movements and subsequent Voluntary reproductions after 1 min. (A) In both conditions the movement generated a force and participant's had to remember the force and then reproduce it via a voluntary movement. (B) Force levels were defined based on the maximum amplitude of the first peak after contact with the stain gauge (shown is the initial force applied during a representative Kohnstamm trial). (C) There was significant interaction between force applied and the perception of that force across Kohnstamm and voluntary conditions [F(1, 11) = 5.72, p = 0.04].
Figure 10
Figure 10
A hybrid model of the Kohnstamm circuit. Note that afferent input has a suppressive effect on the motor commands output from the lower-level motor region, but there is no afferent feedback to the generator itself. See text for further details.

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