Targeting head movements in humans: Compensation for disturbance from simultaneous body rotations

Abstract

Vestibular information plays an important role in spatially oriented motor control and perception. With regard to reorienting head movements, little is known of (1) how vestibular mechanisms compensate for disturbances from concurrent passive trunk rotations (e.g. in a veering vehicle), and (2) whether and how this disturbance compensation is related to the perception of body orientation in space. We here address these two questions in a single experiment.Six healthy subjects (Ss) seated on a turning chair in darkness performed two tasks. (1) Head pointing: Ss made swift head movements in darkness towards the angular position in space of a previously shown visual target. These movements were disturbed by concurrent rotations of the chair, and hence the trunk, which were driven by scaled down versions of the Ss’ own head-on-trunk rotations. Although unaware of the disturbance, Ss adjusted their head movements so as to attenuate its effect on head-in-space (HS) position by about 45%. (2) Visual straight ahead (VSA): Using a light pointer, Ss indicated their VSA before each head-pointing trial and tried to reproduce it after the trial. In all Ss, VSA accounted for the disturbing trunk rotation, although to individually varying degrees. No correlation could be detected between VSA reproduction and motor performance, neither within nor across subjects. A vestibular loss subject who performed the same two tasks made no compensatory movements during head pointing and did not account for the disturbance of his HS position during VSA reproduction.Three concepts of vestibular information processing for head movement control were explored with regard to their compatibility with the head-pointing results: (1) Conventional negative feedback, (2) Interaction with an efference copy, and (3) Interaction with neck proprioceptive information. Theoretical analyses and model simulations indicated that all three concepts can explain the observed disturbance compensation. However, they differ in terms of control stability in the presence of feedback time delays, with (3) being best and (1) worst. The different concepts might correspond to fast simple and slower complex compensation mechanisms, respectively, and possibly complement each other during natural behaviours. VSA reproduction may be based on analogous processing principles, but appears to involve different neural circuitries.