Sensorimotor organization of a sustained involuntary movement

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.

Voluntary motor commands reveal awareness and control of involuntary movement

“…We found that during bilateral Kohnstamm, inhibition of one arm did not affect the EMG signal in the other arm. This suggests that there are separate Kohnstamm generators for each arm, potentially located in each contralateral hemisphere, and is consistent with earlier reports (De Havas et al, 2015; but see for evidence of interlimb coupling).…”

“…There is evidence for central (Duclos, Roll, Kavounoudias, & Roll, 2007;Solopova, Selionov, Zhvansky, Gurfinkel, & Ivanenko, 2016) and peripheral (Hagbarth & Nordin, 1998) contributions to the Kohnstamm phenomenon. Afferent input from the periphery can temporarily 'gate' motor output to the muscle (De Havas et al, 2015), while large changes in visual input have been shown to switch motor output from the muscle active during the induction to its antagonist (Ghafouri, Thullier, Gurfinkel, & Lestienne, 1998;Gilhodes, Gurfinkel, & Roll, 1992). Control processes for the Kohnstamm phenomenon may involve multiple regions of the central nervous system.…”

“…Control processes for the Kohnstamm phenomenon may involve multiple regions of the central nervous system. It is therefore convenient to speak of a 'Kohnstamm generator' when considering how a particular aftercontraction responds to input (De Havas et al, 2015;Ghosh, Rothwell, & Haggard, 2014;Moraitis & Ghosh, 2014). In this context the Kohnstamm generator is a functionally defined unit whose precise location within the central nervous system is not known.…”

Experimental investigations of control principles of involuntary movement: a comprehensive review of the Kohnstamm phenomenon

“…This was confirmed by a recent investigation (Fig. 3b), which found that obstructing the aftercontraction caused the increasing linear trend in agonist EMG to reach a plateau level (De Havas et al 2015). Thus, afferent signalling from the agonist muscle can affect the aftercontraction.…”

“…Complex interactions occur between muscle groups (Bellincioni 1926; Craske and Craske 1985), while sensory input can interact with the aftercontraction in surprising and divergent ways (Brun et al 2015; Brun and Guerraz 2015; De Havas et al 2015; Forbes et al 1926; Ghafouri et al 1998). As such, it may be necessary to consider hybrid models, combining both central and peripheral mechanisms, to explain the Kohnstamm phenomenon.…”