Perception of horizontal head and trunk rotation: modification of neck input following loss of vestibular function

Chronic loss of vestibular function modifies the role of neck afferents in human perception of self-motion. We characterized this change by comparing the self-motion perception of patients with chronic vestibular loss (Ps) to that of normal subjects (Ns). Stimuli consisted of sinusoidal horizontal rotations (0.025–0.4 Hz) of the trunk relative to the head (neck stimulation) and/or of the head in space (vestibular stimulation). Perception of head rotation relative to the trunk, of trunk rotation in space, or of head rotation in space was assessed in terms of gain and phase (veridical perception, G=1 and =0°) as well as detection threshold using a pointing procedure. (1) Perception of head rotation relative to the trunk (neck proprioception). Ps' detection threshold of head-to-trunk rotation was normal (i.e. similar to that of Ns) across all frequencies tested. Also, with peak angular velocities above 5°/s, the gain of their perception was approximately normal. When peak velocity was decreased below this value, however, either by lowering stimulus frequency with peak displacement kept constant (±8°) or by decreasing peak displacement at constant frequency (0.05 Hz), the gain increased above unity, unlike in Ns. In contrast, the phase remained normal (approximately 0°). (2) Perception of trunk rotation in space. Ps perceived their trunks as stationary during neck stimulation and all vestibular-neck combinations at medium to low frequencies. At 0.4 Hz, however, Ps consistently perceived the trunk rotation, conceivably due to somatosensory selfmotion cues arising from high body acceleration. In contrast, Ns perceive a trunk-in-space rotation with the neck stimulation and most of the stimulus combinations across the whole frequency range tested. Ns perceived their trunks as stationary only during head rotation on the stationary trunk (presumed to reflect a mutual cancellation of neck and vestibular signals). (3) Perception of head rotation in space. In Ps, unlike Ns, this perception always resembled that of head rotation relative to the trunk. (4) When Ps were presented with a visual or somatosensory space reference (not motion cues), their perception of trunk and head rotation in space became approximately normal. (5) We suggest that there are basically two changes in the neck induced self motion perception associated with chronic vestibular loss. First, neck proprioception shows a non linear gain that overemphasizes low stimulus velocities, for unknown reasons. Second, the neck signal which normally is used for the perception of trunk rotation in space is suppressed (Ps in the dark, deprived of any space reference, resort to the notion that their trunks are stationary). The change in Ps' perception of head rotation in space is attributed to the former two changes (assuming that they superimposed their notion of head on trunk rotation on that of a stationary trunk).