Transformation of vestibular signals for the decisions of hand choice during whole body motion

Abstract

In daily life, we frequently reach toward objects while our body is in motion. We have recently shown that body accelerations influence the decision of which hand to use for the reach, possibly by modulating the body-centered computations of the expected reach costs. However, head orientation relative to the body was not manipulated, and hence it remains unclear whether vestibular signals contribute in their head-based sensory frame or in a transformed body-centered reference frame to these cost calculations. To test this, subjects performed a preferential reaching task to targets at various directions while they were sinusoidally translated along the lateral body axis, with their head either aligned with the body (straight ahead) or rotated 18° to the left. As a measure of hand preference, we determined the target direction that resulted in equiprobable right/left-hand choices. Results show that head orientation affects this balanced target angle when the body is stationary but does not further modulate hand preference when the body is in motion. Furthermore, reaction and movement times were larger for reaches to the balanced target angle, resembling a competitive selection process, and were modulated by head orientation when the body was stationary. During body translation, reaction and movement times depended on the phase of the motion, but this phase-dependent modulation had no interaction with head orientation. We conclude that the brain transforms vestibular signals to body-centered coordinates at the early stage of reach planning, when the decision of hand choice is computed. NEW & NOTEWORTHY The brain takes inertial acceleration into account in computing the anticipated biomechanical costs that guide hand selection during whole body motion. Whereas these costs are defined in a body-centered, muscle-based reference frame, the otoliths detect the inertial acceleration in head-centered coordinates. By systematically manipulating head position relative to the body, we show that the brain transforms otolith signals into body-centered coordinates at an early stage of reach planning, i.e., before the decision of hand choice is computed.

Corticospinal correlates of hand preference for reaching during whole-body motion

“…This again confirms that hand choice is modulated by sinusoidal body motion in a sinusoidal fashion. The modulation is thought to reflect the influence of bottom-up acceleration signals on hand choice (Bakker et al 2017(Bakker et al , 2019.…”

“…Specifically, the target for which both hands are equally likely to be selected shifts maximally to the left (indicating a preference for using the right hand) at maximum leftward body acceleration ( Figure 2B), and maximally to the right at maximum rightward body acceleration (Bakker et al 2017(Bakker et al , 2019. Corticospinal excitability also modulates sinusoidally with body motion.…”

“…Full-body acceleration differentially modulates the biomechanical costs of left and righthand movements and consequently hand preferences are modulated by the current dynamic situation (Bakker et al 2017(Bakker et al , 2019. The physiological basis of this motion related modulation of hand preference is unknown.…”

“…Recently, Bakker et al (2017Bakker et al ( , 2019 studied hand choice when participants are in motion. In such a dynamic situation, not only vision and proprioception provide information about the state of the body and the environment, also information about whole body motion is registered by the vestibular organ (Angelaki and Cullen 2008).…”

The RT-Chair: a Novel Motion Simulator to Measure Vestibular Perception

“…In the case of translation, motorized sleds are used to deliver linear translations either on the inter-aural (IA), that is to the left or right, and the naso-occipital (NO) axis, that is forward or backward (e.g. [6]). A combination of rotatory and linear movements can be achieved with more complex systems that allow 6 Degrees Of Freedom (DOF) (e.g.…”