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The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex.

ABSTRACT: Although adult vertebrates sense changes in head position by using two classes of accelerometer, at larval stages zebrafish lack functional semicircular canals and rely exclusively on their otolithic organs to transduce vestibular information.Despite this limitation, we find that larval zebrafish perform an effective vestibulo-ocular reflex (VOR) that serves to stabilize gaze in response to pitch and roll tilts. By using single-cell electroporations and targeted laser ablations, we identified a specific class of central vestibular neurons, located in the tangential nucleus, that are essential for the utricle-dependent VOR. Tangential nucleus neurons project contralaterally to extraocular motoneurons and in addition to multiple sites within the reticulospinal complex.We propose that tangential neurons function as a broadband inertial accelerometer, processing utricular acceleration signals to control the activity of extraocular and postural neurons, thus completing a fundamental three-neuron circuit responsible for gaze stabilization.

SUBMITTER: Bianco IH

PROVIDER: S-EPMC3647252 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex.

Bianco Isaac H IH Ma Leung-Hang LH Schoppik David D Robson Drew N DN Orger Michael B MB Beck James C JC Li Jennifer M JM Schier Alexander F AF Engert Florian F Baker Robert R

Current biology : CB 20120614 14

<h4>Background</h4>Although adult vertebrates sense changes in head position by using two classes of accelerometer, at larval stages zebrafish lack functional semicircular canals and rely exclusively on their otolithic organs to transduce vestibular information.<h4>Results</h4>Despite this limitation, we find that larval zebrafish perform an effective vestibulo-ocular reflex (VOR) that serves to stabilize gaze in response to pitch and roll tilts. By using single-cell electroporations and targete ...[more]

PMID: 22704987

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Project description:The three-dimensional vestibulo-ocular reflex (3D VOR) ideally generates compensatory ocular rotations not only with a magnitude equal and opposite to the head rotation but also about an axis that is collinear with the head rotation axis. Vestibulo-ocular responses only partially fulfill this ideal behavior. Because animal studies have shown that vestibular stimulation about particular axes may lead to suboptimal compensatory responses, we investigated in healthy subjects the peaks and troughs in 3D VOR stabilization in terms of gain and alignment of the 3D vestibulo-ocular response. Six healthy upright sitting subjects underwent whole body small amplitude sinusoidal and constant acceleration transients delivered by a six-degree-of-freedom motion platform. Subjects were oscillated about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5 degrees in azimuth. Transients were delivered in yaw, roll, and pitch and in the vertical canal planes. Eye movements were recorded in with 3D search coils. Eye coil signals were converted to rotation vectors, from which we calculated gain and misalignment. During horizontal axis stimulation, systematic deviations were found. In the light, misalignment of the 3D VOR had a maximum misalignment at about 45 degrees . These deviations in misalignment can be explained by vector summation of the eye rotation components with a low gain for torsion and high gain for vertical. In the dark and in response to transients, gain of all components had lower values. Misalignment in darkness and for transients had different peaks and troughs than in the light: its minimum was during pitch axis stimulation and its maximum during roll axis stimulation. We show that the relatively large misalignment for roll in darkness is due to a horizontal eye movement component that is only present in darkness. In combination with the relatively low torsion gain, this horizontal component has a relative large effect on the alignment of the eye rotation axis with respect to the head rotation axis.

Project description:Superior semicircular canal dehiscence (SCD), which is characterized by a "third mobile window" in the inner ear, causes various vestibular and auditory symptoms and signs. Surgical plugging of the superior semicircular canal (SC) can eliminate the symptoms associated with increased perilymph mobility due to the presence of the third window. However, the natural course of vestibular function after surgical plugging remains unknown. Therefore, we explored longitudinal vestibular function after surgery in 11 subjects with SCD who underwent SC plugging using the middle cranial fossa approach. Changes in vestibulo-ocular reflex (VOR) gain in all planes were measured over 1 year with the video head impulse test. We also evaluated surgical outcomes, including changes in symptoms, audiometric results, and electrophysiological tests, to assess whether plugging eliminated third mobile window effects. The mean VOR gain for the plugged SC decreased from 0.81 ± 0.05 before surgery to 0.65 ± 0.08 on examinations performed within 1 week after surgery but normalized thereafter. Four of seven subjects who were able to perform both VOR tests before surgery and immediately after surgery had pathologic values (SC VOR gain < 0.70). Conversely, the mean VOR gain in the other canals remained unchanged over 1 year. The majority of symptoms and signs were absent or markedly decreased at the last follow-up evaluation, and no complications associated with the surgery were reported. Surgical plugging significantly attenuated the air-bone gap, in particular at low frequencies, because of increased bone conduction thresholds and deceased air conduction thresholds. Moreover, surgical plugging significantly increased vestibular-evoked myogenic potential thresholds and decreased the ratio of summating potential to action potential in plugged ears. Postoperative heavily T2-weighted images were available for two subjects and showed complete obliteration of the T2-bright signal intensity in the patent SC lumen in preoperative imaging based on filling defect at the site of plugging. Our results suggest that successful plugging of dehiscent SCs is closely associated with a transient, rather than persistent, disturbance of labyrinthine activity exclusively involved in plugged SCs, which may have clinical implications for timely and individualized vestibular rehabilitation.

Dataset Information

The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex.

Publications

The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex.

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