title: 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 that1) saccades are faster and more accurate if the residual VOR gain is higher,2) saccades also compensate for the head displacement that occurs during the saccade, and3) 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.NEW & NOTEWORTHYDuring 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.
authors.affiliation: Department of Electrical, Computer and Biomedical Engineering, University of Pavia, Pavia, Italy.
authors.forename: Paolo
authors.initials: P
authors.lastname: Colagiorgio
authors.affiliation: Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.|Laboratory of Neuro-otology and Neuro-ophthalmology, C. Mondino National Neurological Institute, Pavia, Italy.
authors.forename: Maurizio
authors.initials: M
authors.lastname: Versino
authors.affiliation: Department of Public Health, Experimental and Forensic Medicine, University of Pavia, Pavia, Italy.|Inter-Department Multiple Sclerosis Research Centre, C. Mondino National Neurological Institute, Pavia, Italy.
authors.forename: Silvia
authors.initials: S
authors.lastname: Colnaghi
authors.affiliation: UOC Otorinolaringoiatria, Fondazione IRCCS San Matteo and University of Pavia, Pavia, Italy.
authors.forename: Silvia
authors.initials: S
authors.lastname: Quaglieri
authors.affiliation: UOC Otorinolaringoiatria, Fondazione IRCCS San Matteo and University of Pavia, Pavia, Italy.
authors.forename: Marco
authors.initials: M
authors.lastname: Manfrin
authors.affiliation: Department of Otorhinolaryngology, Head and Neck Surgery, lnselspital, Bern University Hospital, University of Bern, Bern, Switzerland; and.
authors.forename: Ewa
authors.initials: E
authors.lastname: Zamaro
authors.affiliation: Department of Otorhinolaryngology, Head and Neck Surgery, lnselspital, Bern University Hospital, University of Bern, Bern, Switzerland; and.
authors.forename: Georgios
authors.initials: G
authors.lastname: Mantokoudis
authors.affiliation: Department of Neurology, Otolaryngology-Head and Neck Surgery, Neuroscience, Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland.
authors.forename: David S
authors.initials: DS
authors.lastname: Zee
authors.affiliation: Department of Electrical, Computer and Biomedical Engineering, University of Pavia, Pavia, Italy; stefano.ramat@unipv.it.
authors.forename: Stefano
authors.initials: S
authors.lastname: Ramat
mesh_terms: D000328:Adult; D000368:Aged; D025461:Feedback, Physiological; D005260:Female; D006801:Humans; D008297:Male; D008875:Middle Aged; D008959:Models, Neurological; D012027:Reflex, Vestibulo-Ocular; D012438:Saccades; D015837:Vestibular Diseases / Q000503:physiopathology*
keywords: VOR; covert saccades; gaze feedback loop; mathematical model; vestibular neuritis