New insights into vestibular-saccade interaction based on covert corrective saccades in patients with unilateral vestibular deficits

Abstract

In response to passive high-acceleration head impulses, patients with low vestibulo-ocular reflex (VOR) gains often produce covert (executed while the head is still moving) corrective saccades in the direction of deficient slow phases. Here we examined 23 patients using passive, and 9 also active, head impulses with acute (< 10 days from onset) unilateral vestibular neuritis and low VOR gains. We found that when corrective saccades are larger than 10°, the slow-phase component of the VOR is inhibited, even though inhibition increases further the time to reacquire the fixation target. We also found that ) saccades are faster and more accurate if the residual VOR gain is higher,) saccades also compensate for the head displacement that occurs during the saccade, and ) the amplitude-peak velocity relationship of the larger corrective saccades deviates from that of head-fixed saccades of the same size. We propose a mathematical model to account for these findings hypothesizing that covert saccades are driven by a desired gaze position signal based on a prediction of head displacement using vestibular and extravestibular signals, covert saccades are controlled by a gaze feedback loop, and the VOR command is modulated according to predicted saccade amplitude. A central and novel feature of the model is that the brain develops two separate estimates of head rotation, one for generating saccades while the head is moving and the other for generating slow phases. Furthermore, while the model was developed for gaze-stabilizing behavior during passively induced head impulses, it also simulates both active gaze-stabilizing and active gaze-shifting eye movements. During active or passive head impulses while fixating stationary targets, low vestibulo-ocular gain subjects produce corrective saccades when the head is still moving. The mechanisms driving these covert saccades are poorly understood. We propose a mathematical model showing that the brain develops two separate estimates of head rotation: a lower level one, presumably in the vestibular nuclei, used to generate the slow-phase component of the response, and a higher level one, within a gaze feedback loop, used to drive corrective saccades.

Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss

“…These saccade characteristics must change after vestibular loss to accomplish the goal to keep a stable gaze fixation, thereby proxy reflect the loss of VOR [4]. However, the negative effects of vision were significantly less in the earliest saccades to UVD ipsi compared to BVL, such that these most likely represent a form of saccadic motor learning to a vestibular stimulus [53]. Sensori-motor learning of both the VOR and saccades requires time and exposure to errors [63,64], suggesting that saccades characteristics could be of value in determining the age of a lesion e.g.…”

“…After the unilateral loss of the compensatory velocity response in UVD ipsi , we found subjects showed a new compensatory position response that depended on the velocity signal from the intact UVD contra ear. While a single intact ear (UVD ipsi ) was insufficient to generate a velocity change it was sufficient to generate a position change (Figs 1, 2 and 7), perhaps coordinated by separate velocity and position estimates [53]. After UVD the frequency and amplitude of the first saccade-often triggered during the head motion ('covert saccades') i.e.…”

“…After VOR loss short latency compensatory saccades can improve visual acuity [79][80][81][82], so the VOR and saccades provide complimentary and differential roles in gaze by generating compensatory velocity and position changes respectively [7,53]. The neuro-physiology of saccade modification after loss of the VOR could be explained by saccade motor learning paradigms, in man [83,84] and monkey [85,86], by which saccade characteristics are modulated over time by visual error feedback loops through the super colliculus and cerebellum [87][88][89][90][91][92].…”

Validation of the Italian Version of the Dizziness Handicap Inventory, the Situational Vertigo Questionnaire, and the Activity-Specific Balance Confidence Scale for Peripheral and Central Vestibular Symptoms

“…The diagnosis of the common vestibular pathologies as benign paroxysmal positional vertigo (BPPV), vestibular migraine ( 3 ), vertigo of central origin, vestibular neuritis or Meniere’s disease, is relatively simple during the acute phase based on the anamnesis and the clinical signs. Yet, after the acute phase or in the chronic patient, vestibular assessment becomes more difficult as the central nervous system activates very efficient adaptive and compensation mechanisms ( 4 – 9 ). Thus, a stabilized vestibular deficit can correspond either to a completely compensated condition, allowing the subject to perform even demanding tasks, or to a serious impairment, which may in turn improve with rehabilitation and still not change the neurophysiologic measurement.…”

A Novel Saccadic Strategy Revealed by Suppression Head Impulse Testing of Patients with Bilateral Vestibular Loss

“…While covert compensatory saccades are well known in patients with unilateral vestibular loss ( 11 – 14 ), their cause has not been established ( 15 ). The covert saccades in this group of BVL patients are of special interest, since they cannot be triggered by vestibular input, and the patients appear not to be able to suppress them in accordance with the instructions.…”