Effect of gaze on postural responses to neck proprioceptive and vestibular stimulation in humans

Abstract

1. We studied the effect of gaze orientation on postural responses evoked by vibration of neck dorsal muscles or by galvanic stimulation of the vestibular system during quiet standing in healthy humans. Various gaze orientations were obtained by different combinations of horizontal head-on-feet (-90, -45, 0, 45, 90 deg) and eye-in-orbit (-30, 0, 30 deg) positions. The instantaneous centre of foot pressure was recorded with a force platform. 2. With a symmetrical position of the vibrator relative to the spine, neck muscle vibration elicited a body sway in the direction of the head naso-occipital axis when the eyes were aligned with it. The same result was obtained both during head rotations and when the head and trunk were rotated together. 3. For lateral eye deviations, the direction of the body sway was aligned with gaze orientation. The effect of gaze was present both with eyes open and eyes closed. After long-lasting (1 min) lateral fixation of the target the effect of gaze decreased significantly. 4. Postural responses to galvanic vestibular stimulation tended to occur orthogonal to the head naso-occipital axis (towards the anodal ear) but in eight of the 11 subjects the responses were also biased by the direction of gaze. 5. The prominent effect of gaze in reorienting automatic postural reactions indicates that both neck proprioceptive and vestibular stimuli are processed in the context of visual control of posture. The results point out the importance of a viewer-centred frame of reference for processing multisensory information.

Figure 1. Experimental set-up

A, location of markers placed on the body to measure head, shoulder and pelvis orientation in the horizontal plane. B, location of a vibrator in different head-on-trunk orientations (0 and 45 deg).

Figure 2. Samples of sagittal and frontal components of the sway response induced by vibration of the dorsal neck muscles with different eye-in-orbit (E), head-on-trunk (H) and trunk-on-feet (T) positions

In A, the head was turned 45 deg to the left; in B, the head and shoulders were turned together 45 deg to the left. In A and B, each test condition is indicated by a schematic drawing (top right in each panel). The bottom right diagrams in each panel represent X-Y plots of the CP displacement from the beginning of recording until the end of stimulation. Labels and calibrations in the bottom left panel in A also apply to all other panels. Abbreviations in this and other figures: sagit, sagittal; front, frontal; stim, stimulus; FW, forward; BW, backward; R, right; L, left; x R, x deg right; x L, x deg left; 0, 0 deg.

Figure 3. Vector representation of averaged postural responses to neck muscle vibration recorded with various head-on-feet and eye-in-orbit positions

Each head and shoulder orientation is indicated by a schematic drawing. Sectors represent ± s.d. values around the mean direction of sway response. Sector amplitude represents the mean amplitude of sway deviation.

Figure 4. Effect of history of head position and target fixation

A, sway response to 4 s neck vibration in the neutral head position while the subject fixated a target located 30 deg to the right with the head and feet aligned with each other. Several seconds after head right-left rotation, the subject tended to sway in the direction of gaze. After 1 min of continuous target fixation the body swayed in the direction of the head. B, sway response to 8 s neck vibration just after the head was turned 45 deg to the left and gaze 30 deg to the right and after 1 min of target fixation. In A and B, the bottom right diagrams in each panel represent X-Y plots of the CP displacement from the beginning to the end of the stimulus.

Figure 5. Effect of gaze direction on the body sway response to a 15 s neck vibration with eyes closed

The subject was asked to move his/her head, with eyes closed, 45 deg to the right, and the eyes towards an imagined target located −30, 0 and 30 deg relative to the head. The gaze signal was obtained by summing together eye-in-head (EOG) and head-in-space signals. The bottom right diagrams in each panel represent X-Y plots of the CP displacement during the 20 s period (covering the stimulus and a 5 s period before stimulation). Labels and calibrations given in the bottom panel also apply to the top and middle panels.

Figure 6. Two-dimensional spontaneous oscillations of the CP around the mean position during 20 s in all 15 combinations of head-on-feet and eye-in-orbit orientations

Each trace represents the pooled CP displacement data for all subjects. The shaded areas superimposed on the CP traces represent the 95 % tolerance ellipses of CP displacements.

Figure 7. Sway response induced by a 4 s galvanic stimulation while fixating on a target located 30 deg to the right

Results shown are the mean of 10 trials for each gaze direction from one subject. Dashed lines represent ± 1 s.d. Just before target fixation, the subject was asked to turn his/her head 45 deg to the right from the normal middle position. The bottom right diagrams in each panel represent X-Y plots of the CP displacement during the 8 s period (covering the stimulus and a 4 s period before stimulation). Labels and calibrations given in the bottom panel also apply to the top and middle panels.