Task-dependent vestibular feedback responses in reaching

Abstract

When reaching for an earth-fixed object during self-rotation, the motor system should appropriately integrate vestibular signals and sensory predictions to compensate for the intervening motion and its induced inertial forces. While it is well established that this integration occurs rapidly, it is unknown whether vestibular feedback is specifically processed dependent on the behavioral goal. Here, we studied whether vestibular signals evoke fixed responses with the aim to preserve the hand trajectory in space or are processed more flexibly, correcting trajectories only in task-relevant spatial dimensions. We used galvanic vestibular stimulation to perturb reaching movements toward a narrow or a wide target. Results show that the same vestibular stimulation led to smaller trajectory corrections to the wide than the narrow target. We interpret this reduced compensation as a task-dependent modulation of vestibular feedback responses, tuned to minimally intervene with the task-irrelevant dimension of the reach. These task-dependent vestibular feedback corrections are in accordance with a central prediction of optimal feedback control theory and mirror the sophistication seen in feedback responses to mechanical and visual perturbations of the upper limb. Correcting limb movements for external perturbations is a hallmark of flexible sensorimotor behavior. While visual and mechanical perturbations are corrected in a task-dependent manner, it is unclear whether a vestibular perturbation, naturally arising when the body moves, is selectively processed in reach control. We show, using galvanic vestibular stimulation, that reach corrections to vestibular perturbations are task dependent, consistent with a prediction of optimal feedback control theory.

Task‐dependent responses to muscle vibration during reaching

“…There was neither a significant effect of reach direction on lateral spread ( F 1,8 = 0.1, p = 0.8), nor an interaction of reach direction and target width ( F 1,8 = 0.9, p = 0.4). The increased spread of reach endpoints in the wide condition was seen in all participants, consistent with previous observations (Keyser et al., ; Nashed et al., ). We conclude that subjects were able to adapt their control policy in a task‐appropriate manner on a trial‐by‐trial basis.…”

“…Vibration‐evoked corrections were down‐regulated for reaches to the wide compared to the narrow target, for conditions in which vibration induced an illusory lengthening, that is, for biceps vibration in away reaches and triceps vibration in reaches toward the subject. The observed reduction in magnitude of the corrections by 34%–37% in the wide condition is similar to the 40% and 33% reduction found for visual and vestibular perturbations, respectively (Keyser et al., ; Knill et al., ). One might wonder why the corrections to the wide target were not abolished entirely.…”

“…With different task constraints, such as different target shapes, the same perturbation elicits different corrective responses, which supposedly reflects the minimal intervention principle. In addition to mechanical perturbations, also corrections to visual (e.g., Franklin & Wolpert, 2008;Knill, Bondada, & Chhabra, 2011) and vestibular perturbations (Keyser, Medendorp, & Selen, 2017) have been shown to conform to the minimal intervention principle. Unlike mechanical perturbations, the latter two are purely sensory perturbations, changing only the estimated state of the arm without directly affecting the actual arm trajectory.…”

Ascending vestibular pathways to parietal areas MIP and LIPv and efference copy inputs from the medial reticular formation: Functional frameworks for body representations updating and online movement guidance

“…Indeed, there is evidence that the brain uses vestibular signals to generate the appropriate reaching command required to maintain accuracy during self-motion (Blouin, Bresciani, Guillaud, & Simoneau, 2015;Moreau-Debord, Martin, Landry, & Green, 2014). Reach corrections to vestibular perturbations are task-dependent, consistent with online integration of self-motion signals into an internal model for reach control (Keyser, Medendorp, & Selen, 2017). TMS studies point to a key role of an intermediate portion of the human medial IPS for online adjustments of goal-directed arm movements based on vestibular and proprioceptive feedback (Reichenbach, Thielscher, Peer, Bülthoff, & Bresciani, 2014;Reichenbach et al, 2016).…”

Hierarchical integration of communicative and visuospatial perspective-taking demands in sensorimotor control of referential pointing

“…Trajectory displacement is determined by a combination of initial amplitude of a desired movement and movement correction. In turn, the initial amplitude of a desired movement (forward kinematics) is computed with internal anticipatory inputs, such as target location estimation (Körding & Wolpert, 2004;Taylor et al, 2014;Cluff & Scott, 2015;Keyser et al, 2017) and distal goals of the movement, e.g. its instrumental or communicative purpose (Sartori et al, 2009;Sacheli et al, 2013;Vesper et al, 2017).…”