Visual and Vestibular Integration Express Summative Eye Movement Responses and Reveal Higher Visual Acceleration Sensitivity than Previously Described

Abstract

Purpose Acceleration plays a great impact on the vestibular system, but is attributed little influence over vision. This study aims to explore how visual and vestibular acceleration affect roll-plane oculomotor responses, including their addiative effect. Methods Seated in a mechanical sled, 13 healthy volunteers (7 men, 6 women; mean age 25 years) were exposed to a series of visual (VIS) optokinetic, vestibular (VES) whole-body, and combined (VIS + VES) rotations. This was carried out at two acceleration intensities. Subjects wore a video-based eye tracker, enabling analysis of torsional and skewing eye movement responses, which were used to evaluate the individual response to each trial. The tracker also contained accelerometers allowing head tracking. Results Both ocular torsion and vertical skewing were sensitive to acceleration intensities for VES and VIS + VES. For VIS only, skewing exhibited such a response. An increased acceleration yielded a decreased torsion-skewing ratio for VIS, explained by the change in skewing, but remained unchanged for VES and VIS + VES. Torsion exhibited particularly reliable summative effect, yielding a relative contribution of 32% VIS and 75% VES during low acceleration, and 19% and 85%, respectively, during high acceleration. Conclusions The change in the skewing response to different intensities indicates that the visual system is more sensitive to visual accelerations than previously described. Eye movements showed reliable summative effects, indicating a robust visual-vestibular integration that indicates their integrative priorities for each acceleration, with the visual system being more involved during low accelerations. Such objective quantifications could hold clinical utility when assessing sensory mismatch in vertiginous patients.

Optokinetic stimulation induces vertical vergence, possibly through a non-visual pathway

“…Similarly, we know that vertical vergence adapts to visual accelerations while being generally unaffected by visual clutter, i.e. information density, while the inverse is true for the torsional response 3,6 . As such, one could suggest that the vertical vergence seen to visual rotations may be a reflexive manifestation of a visually induced activation of the vestibular nuclei.…”

“…This eye movement is also accompanied by ocular torsion in the same direction as the visual rotation 5 . While this torsional response seems insensitive to the acceleration of the visual rotation, vergence has proven comparably accommodating in showing decreased vergence to increased accelerations 6 .…”

Conserved subcortical processing in visuo-vestibular gaze control

“…The VOR and OKR act together to compensate for the disturbance generated by head movements, and contribute to robust eye movement control. As the velocity of the head movement increases the vestibular contribution becomes dominating 6 , 7 .…”

Visuo-vestibular gaze control – conserved subcortical processing

“…The vestibular stimulation noticeably produced a strong, long lasting eye movement as if the eye is compensating for the head displacement. It is therefore clear thatadditional visual input decidedly increases eye movement gain in lamprey as well as humans, providing further evidence that the underlying mechanisms are conserved 5,6,42 . Visual inputs from pretectum also potentiate vestibular responses controlling body posture in lampreys [43][44] , suggesting a key role of pretectum contributing to both gaze and posture stabilizing responses 45 .…”

“…The VOR and OKR act together to compensate for the disturbance generated by head movements, and contribute to robust eye movement control. As the velocity of the head movement increases the vestibular contribution becomes dominating [5][6] .…”