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Feedback responses to muscle vibration depend on task and reach direction

Johannes Keyser, Rob E. F. S. Ramakers, and Luc P. J. Selen

Radboud University Nijmegen, Donders Institute for Brain, Cognition and
Behaviour, Nijmegen, The Netherlands

Keywords: Sensorimotor, motor control, optimality
Support: EU FP7 604063 HealthPAC and NWO-VICI 453-11-001.

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A central prediction of optimal feedback control theory is that sensorimotor feedback gains are tuned to the specific constraints of a task (Todorov and Jordan 2002). In support, studies of goal-directed reaching have shown that on-line feedback corrections are down-regulated for task-irrelevant perturbations (e.g. Nashed et al. 2012). However, it remains an open question how the task-dependency of corrections is implemented throughout the nervous system. Specifically, for mechanical perturbations of the reaching limb, it is unclear which receptor channels enable task-dependent tuning of feedback gains. Muscle vibration provides a useful tool to perturb the feedback from selected muscle afferents, predominantly muscle spindles, thereby inducing illusory changes of limb position and velocity (reviewed in Proske and Gandevia 2012). Here, we investigated the task-dependency of vibration-evoked feedback corrections during goal-directed reaching.

Human subjects (N=8) made 20 cm reaching movements in the horizontal plane while holding the handle of a robotic manipulandum (Howard et al. 2009). The start and target locations were visually projected into the plane of movement by a mirror. During reaches subjects had no visual feedback of their hand. Per subject, a total of 600 trials were divided by 3 experimental factors (muscle vibration: biceps vs. triceps vs. no vibration, target width: narrow vs. wide, reach direction: away vs. toward the subject). Muscle vibration with a frequency of ~105 Hz and an amplitude of ~1-2 mm was applied by pneumatic vibrators over the distal tendons of m. biceps brachii or m. triceps brachii. Responses to muscle vibration were quantified by the force that subjects exerted against simulated force channels along a straight path from the initial hand location towards the target location. Reach directions alternated between away and toward the subject, along an axis rotated 35° counter-clockwise from straight-ahead, in an attempt to minimize the recruitment of biceps and triceps along the principal reach directions. To investigate task-dependency, subjects reached to targets with a depth of 2 cm along the reach direction, and either a narrow (1 cm) or a wide (>30 cm) dimension orthogonal to the reach direction, i.e. with demanding or relaxed accuracy requirements, respectively.
In 25% of trials, muscle vibration of biceps or triceps started about 150 ms after reach onset and lasted until the end of the reach. Another 25% of trials served as control trials without vibration but with activated force channels. In the remaining 50% of trials, movements were not restricted and feedback about reach accuracy was provided to reinforce the task requirements.

Results show that vibration-evoked corrections to either muscle depends on the reach direction and target width. Biceps vibration led to larger corrections during reaches away than toward the subject, while triceps vibration showed the opposite pattern. For both muscles, we also found corrections to be task-dependent, i.e. down-regulated for the wide compared to the narrow target, which again depended on the reach direction in an opposite manner. Corrections to biceps vibration were task-modulated in reaches away but not toward the subject, while corrections to triceps vibration were task-modulated only for reaches toward the subject. The dependency of reach direction may be explained by consideration whether the vibrated muscle is shortening or lengthening, since the effect of vibration is largely absent in a shortening muscle (Inglis and Frank 1990; Inglis et al. 1991). Since the reaches away from the subject stretched the biceps while shortening the triceps, this would explain the greater response and task-dependent modulation of the biceps in this case compared to the reaches toward the subject in which the biceps is shortening. Analogous reasoning explains the opposite direction effects of triceps vibration.

In conclusion, we show that signals from muscle afferents seems sufficient for task-dependent processing of feedback responses, provided the perturbation is not exclusively targeting a shortening muscle.


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