Catch-Up Saccades in Vestibulo-Ocular Reflex Deficit: Contribution of Visual Information?

Objectives: Catch-up saccades help to compensate for loss of gaze stabilization during rapid head rotation in case of vestibular deficit. While overt saccades observed after head rotation are obviously visually guided, some of these catch-up saccades occur with shorter latency while the head is still moving, anticipating the needed final eye position. These covert saccades seem to be generated based on the integration of multisensory inputs. Vision could be one of these inputs, but the known delay for triggering visually guided saccades questions this possibility. The main objective of this study is to evaluate the potential role of visual information for controlling (triggering and guiding) the first catch-up saccades in patients suffering from bilateral vestibulopathy. To investigate this, we used head impulse test in a virtual reality setting allowing to create different visuo-vestibular mismatch conditions. Design: Twelve patients with bilateral vestibulopathy were recruited. We assessed in our patient group the validity of our virtual reality head impulse testing approach by comparing recorded eye and head movement to classical video head impulse test. Then, using the virtual reality system, we tested head impulse test under both normal and three visuo-vestibular mismatch conditions. In these mismatch conditions, the movement of the visual scene relative to the head movement was altered: decreased in amplitude by 50% (half), nullified (freeze), or inverted in direction (inverse). Recorded eye and head movements during these different conditions were then analyzed, more specifically the characteristics of the first catch-up saccade. Results: Impaired vestibulo-ocular reflex required subjects to systematically perform catch-up saccades, which could be covert or overt. The latency of the first catch-up saccade increased along with the amount of visuo-vestibular mismatch between the four conditions (i.e., from normal to half to freeze to inverse) and, consequently, the mean percentage of covert saccades decreased with increasing visual feedback error. However, the freeze and inverse conditions allowed us to reveal the existence of many saccades performed in the wrong direction relative to visual feedback. These visually discordant saccades were present in over half of the trials, they were mainly covert and their percentage was inversely correlated with residual vestibulo-ocular reflex gain. Conclusions: Visual information significantly impacts catch-up saccade latency and the relative number of covert saccades during head impulse testing in vestibular deficit. However, in more than 50% of trials involving a visuo-vestibular mismatch, catch-up saccades remained directed in the compensatory direction relative to head movement, that is, they were visually discordant. Therefore, contrary to previously published proposals, visual information does not appear to be the primary component of the multisensory inputs required for the production of catch-up covert saccades in vestibular deficit. Finally, we discuss a new nomenclature of catch-up saccades in case of vestibular deficit introducing the terms of open and closed loop saccades.