Otolith-related Neurons Research Articles

Neural Interruption by Unilateral Labyrinthectomy Biases the Directional Preference of Otolith-Related Vestibular Neurons.

Background: The directional preference of otolith-related vestibular neurons elucidates the neuroanatomical link of labyrinths, but few direct experimental data have been provided. Methods: The directional preference of otolith-related vestibular neurons was measured in the vestibular nucleus using chemically induced unilateral labyrinthectomy (UL). For the model evaluation, static and dynamic behavioral tests as well as a histological test were performed. Extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation. Results: Seventy-seven neuronal activities were recorded, and the total population was divided into three groups: left UL (20), sham (35), and right UL (22). Based on directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-, 15/35, 43%; ipsi-, 20/35, 57%) in the sham (p = 0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p = 6.056 × 10−5), while left UL caused more contra-preferred neurons (13/20, 65%) (p = 0.058). In particular, the convergent neurons mainly led this biased difference (ipsi-, 100% after right UL and contra-, 89% after left UL) (p < 0.002). Conclusions: The directional preference of the neurons depended on the side of the lesion, and its dominance was mainly led by the convergent neurons.

Neuronal Responding Alteration Based on Directional Preference by Unilateral Labyrinthectomy

Dysfunction in the vestibular system caused unbalanced behavioral responses, but the experimental measurements often failed to elucidate their relations to its orientation in the vestibular neural information. To overcome these problems, the Directional Preference (DP) of canal- and otolith-related neurons was suggested, and its underlying neural mechanism was explained in this paper. To construct the vestibular imbalance, Unilateral Labyrinthectomy (UL) was given as a common model for the overall explanation. Based on the alteration in the DP, the ambiguity in the behavioral tests could be overcome, and expected to identify the neuronal characteristics to lead the alteration in the neural responses.

Topography of Inferior Olivary Neurons that Encode Canal and Otolith Inputs

Vestibular information arising from rotational head movement and that from translational head movement are detected respectively by the semicircular canal and otolith organ in the inner ear. Spatiotemporal cues are in turn processed by the vestibulo-olivo-cerebellar pathway for sensorimotor coordination, but the role of the inferior olive (IO) in this pathway remains unclear. To address whether rotational and translational movements are differentially represented in the IO, we studied the distribution pattern of IO neurons recruited into the circuitry following selective activation of receptor hair cells of the horizontal semicircular canal or the utricle in adult rats. Neurons in the beta nucleus of IO (IOβ) and dorso-medial cell column of IO were responsive to horizontal translation, but not rotation. Notably, otolith-related neurons were observable largely in the rostral IOβ. In contrast, the subnucleus A of IO (IOA), subnucleus C of IO (IOC), and dorsal cap of Kooy (IOK) were responsive to horizontal rotation, but not translation. In the IOA, these canal-related neurons were clustered in the medial portion of the subnucleus. In the IOC, canal-related neurons were skewed towards the rostral half. In the IOK, canal-related neurons were found throughout the subnucleus. These indicate that the distributions of canal- and otolith-related neurons encoding horizontal motions are clearly segregated in the IO. These discrete IO subnuclei therefore provide a topographic map for temporal and adaptive operations of sensorimotor coordination and spatial reference.

Developmental maturation of ionotropic glutamate receptor subunits in rat vestibular nuclear neurons responsive to vertical linear acceleration

We investigated the maturation profile of subunits of ionotropic glutamate receptors in vestibular nuclear neurons that were activated by sinusoidal linear acceleration along the vertical plane. The otolithic origin of Fos expression in these neurons was confirmed as a marker of functional activation when labyrinthectomized and/or stationary control rats contrasted by showing sporadically scattered Fos-labeled neurons in the vestibular nuclei. By double immunohistochemistry for Fos and one of the receptor subunits, otolith-related neurons that expressed either alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionate or N-methyl-d-aspartate subunits were first identified in the medial vestibular nucleus, spinal vestibular nucleus and Group x by postnatal day (P)7, and in the lateral vestibular nucleus and Group y by P9. No double-labeled neurons were found in the superior vestibular nucleus. Within each vestibular subnucleus, these double-labeled neurons constituted approximately 90% of the total Fos-labeled neurons. The percentage of Fos-labeled neurons expressing the GluR1 or NR2A subunit showed developmental invariance in all subnuclei. For Fos-labeled neurons expressing the NR1 subunit, similar invariance was observed except that, in Group y, these neurons decreased from P14 onwards. For Fos-labeled neurons expressing the GluR2, GluR2/3, GluR4 or NR2B subunit, a significant decrease was found by the adult stage. In particular, those expressing the GluR4 subunit showed a two- to threefold decrease in the medial vestibular nucleus, spinal vestibular nucleus and Group y. Also, those expressing the NR2B subunit showed a twofold decrease in Group y. Taken together, the postsynaptic expression of ionotropic glutamate receptor subunits in different vestibular subnuclei suggests that glutamatergic transmission within subregions plays differential developmental roles in the coding of gravity-related vertical spatial information.

Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity‐related horizontal orientations

We examined the expression profile of subunits of ionotropic glutamate receptors [N-methyl-D-aspartate (NMDA) and alpha-amino-3-hydroxy-5-methyl-4-isoxazole-proprionate (AMPA)] during postnatal development of connectivity in the rat vestibular nucleus. Vestibular nuclear neurons were functionally activated by constant velocity off-vertical axis rotation, a strategy to stimulate otolith organs in the inner ear. These neurons indicated Fos expression as a result. By immunodetection for Fos, otolith-related neurons that expressed NMDA/AMPA receptor subunits were identified as early as P7, and these neurons were found to increase progressively up to adulthood. Although there was developmental invariance in the percentage of Fos-immunoreactive neurons expressing the NR1, NR2A, GluR1, or GluR2/3 subunits, those expressing the NR2B subunit decreased from P14 onward, and those expressing the GluR4 subunit decreased in adults. These double-immunohistochemical data were corroborated by combined immuno-/hybridization histochemical data obtained from Fos-immunoreactive neurons expressing NR2B mRNA or GluR4 mRNA. The staining of both NR2B and GluR4 in the cytoplasm of these neurons decreased upon maturation. The percentage of Fos-immunoreactive neurons expressing the other ionotropic glutamate receptor subunits (viz. NR1, NR2A, GluR1, and GluR2/3) remained relatively constant throughout postnatal maturation. Triple immunofluorescence further demonstrated coexpression of NR1 and NR2 subunits in Fos-immunoreactive neurons. Coexpression of NR1 subunit with each of the GluR subunits was also observed among the Fos-immunoreactive neurons. Taken together, the different expression profiles of ionotropic glutamate receptor subunits constitute the histological basis for glutamatergic neurotransmission in the maturation of central vestibular connectivity for the coding of gravity-related horizontal head movements.

Spatial coding capacity of central otolith neurons

This review focuses on recent approaches to unravel the capacity of otolith-related brainstem neurons for coding head orientations. In the first section, the spatiotemporal features of central vestibular neurons in response to natural otolithic stimulation are reviewed. Experiments that reveal convergent inputs from bilateral vestibular end organs bear important implications on the processing of spatiotemporal signals and integration of head orientational signals within central otolith neurons. Another section covers the maturation profile of central otolith neurons in the recognition of spatial information. Postnatal changes in the distribution pattern of neuronal subpopulations that subserve the horizontal and vertical otolith systems are highlighted. Lastly, the expression pattern of glutamate receptor subunits and neurotrophin receptors in otolith-related neurons within the vestibular nuclear complex are reviewed in relation to the potential roles of these receptors in the development of vestibular function.

Maturation of otolith‐related brainstem neurons in the detection of vertical linear acceleration in rats

To investigate the critical maturation time of otolith-related neurons in processing vertical orientations, rats (postnatal day 4 to adults) were studied for functional activation of c-fos expression in brainstem neurons by immuno-/hybridization histochemistry. Conscious rats were subjected to sinusoidal linear acceleration along the vertical plane. Labyrinthectomized and/or stationary controls showed only sporadically scattered Fos-labeled neurons in the vestibular nuclei, confirming an otolithic origin of c-fos expression. Functionally activated Fos expression in neurons of the medial and spinal vestibular nuclei and group x were identifiable by P7 and those in group y by P9. A small number of Fos-labeled neurons characterized by small soma size were found in the ventral part of lateral vestibular nucleus by P9. Other vestibular-related areas such as prepostitus hypoglossal nucleus, gigantocellular reticular nucleus and locus coeruleus of normal experimental rats showed functionally activated c-fos expression at P7. Neurons in dorsal medial cell column and beta subnucleus of the inferior olive only showed functionally activated c-fos expression by the second postnatal week. These findings revealed a unique critical maturation time for each of the vestibular-related brainstem areas in the recognition of gravity-related vertical head orientations. By mapping the three-dimensional distribution of Fos-immunoreactive neurons, we found an even distribution of otolith-related neurons within the spinal vestibular nucleus in groups x and y but a clustered distribution in the middle-lateral-ventral part of the medial vestibular nucleus. Taken together, our findings reveal the developmental profile of neuronal subpopulations within the vertical otolith system, thereby providing an anatomical basis for postnatal coding of gravity-related vertical head movements.

Expression of Trk receptors in otolith-related neurons in the vestibular nucleus of rats

The expression of the three Trk receptors (TrkA, TrkB, and TrkC) in otolith-related neurons within the vestibular nuclei of adult Sprague–Dawley rats was examined immunohistochemically. Conscious animals were subjected to sinusoidal linear acceleration along either the anterior-posterior (AP) or interaural (IA) axis on the horizontal plane. Neuronal activation was defined by Fos expression in cell nuclei. Control animals, viz labyrinthectomized rats subjected to stimulation and normal rats that remained stationary, showed only a few sporadically scattered Fos-labeled neurons. Among experimental rats, the number of Fos-labeled neurons and their distribution pattern in each vestibular subnucleus in animals stimulated along the antero-posterior axis were similar to those along the interaural axis. No apparent topography was observed among neurons activated along these two directions. Only about one-third of the Trk-immunoreactive neurons in the vestibular nucleus expressed Fos. Double-labeled Fos/TrkA, Fos/TrkB and Fos/TrkC neurons constituted 85–98% of the total number of Fos-labeled neurons in vestibular nuclear complex and its subgroups x and y. Our findings suggest that Trk receptors and their cognate neurotrophins in central otolith neurons may contribute to the modulation of gravity-related spatial information during horizontal head movements.

Rostral Fastigial Nucleus Activity in the Alert Monkey During Three-Dimensional Passive Head Movements

The fastigial nucleus (FN) receives vestibular information predominantly from Purkinje cells of the vermis. FN in the monkey can be divided in a rostral part, related to spinal mechanisms, and a caudal part with oculomotor functions. To understand the role of FN during movements in space, single-unit activity in alert monkeys was recorded during passive three-dimensional head movements from rostral FN. Seated monkeys were rotated sinusoidally around a horizontal earth-fixed axis (vertical stimulation) at different orientations 15 degrees apart (including roll, pitch, vertical canal plane and intermediate planes). In addition, sinusoidal rotations around an earth-vertical axis (yaw stimulus) included different roll and pitch positions (+/-10 degrees, +/-20 degrees). The latter positions were also used for static stimulation. One hundred fifty-eight neurons in two monkeys were modulated during the sinusoidal vertical search stimulation. The vast majority showed a uniform response pattern: a maximum at a specific head orientation (response vector orientation) and a null response 90 degrees apart. Detailed analysis was obtained from 111 neurons. On the basis of their phase relation during dynamic stimulation and their response to static tilt, these neurons were classified as vertical semicircular canal related (n = 79, 71.2%) or otolith related (n = 25; 22.5%). Only seven neurons did not follow the usual response pattern and were classified as complex neurons. For the vertical canal-related neurons (n = 79) all eight major response vector orientations (ipsilateral or contralateral anterior canal, posterior canal, roll, and nose-down and nose-up pitch) were found in Fn on one side. Neurons with ipsilateral orientations were more numerous and on average more sensitive than those with contralateral orientations. Twenty-eight percent of the vertical canal-related neurons also responded to horizontal canal stimulation. None of the vertical canal-related neurons responded to static tilt. Otolith-related neurons (n = 25) had a phase relation close to head position and were considerably less numerous than canal-related neurons. Except for pitch, all other response vector orientations were found. Seventy percent of these neurons responding during dynamic stimulation also responded during static tilt. The sensitivity during dynamic stimulation was always higher than during static stimulation. Sixty-one percent of the otolith-related neurons responded also to horizontal canal stimulation. These results show that in FN, robust vestibular signals are abundant. Canal-related responses are much more common than otolith-related responses. Although for many canal neurons the responses can be related to single canal planes, convergence between vertical canals but also with horizontal canals is common.

Response of otolith-related neurons in bilateral vestibular nucleus of acute hemilabyrinthectomized cats to off-vertical axis rotations.

Annals of the New York Academy of SciencesVolume 656, Issue 1 p. 755-765 Response of Otolith-Related Neurons in Bilateral Vestibular Nucleus of Acute Hemilabyrinthectomized Cats to Off-Vertical Axis Rotationsa Y. S. CHAN, Y. S. CHAN Department of Physiology Faculty of Medicine University of Hong Kong 5 Sassoon Road Hong KongSearch for more papers by this authorY. M. CHEUNG, Y. M. CHEUNG Department of Physiology Faculty of Medicine University of Hong Kong 5 Sassoon Road Hong KongSearch for more papers by this author Y. S. CHAN, Y. S. CHAN Department of Physiology Faculty of Medicine University of Hong Kong 5 Sassoon Road Hong KongSearch for more papers by this authorY. M. CHEUNG, Y. M. CHEUNG Department of Physiology Faculty of Medicine University of Hong Kong 5 Sassoon Road Hong KongSearch for more papers by this author First published: May 1992 https://doi.org/10.1111/j.1749-6632.1992.tb25254.xCitations: 10 a This study was supported by research grants from the Lee Wing Tat Medical Research Fund, Sun Yat Sen Foundation Fund for Medical Research, Research Grants Committee of the University of Hong Kong, and University and Polytechnic Grants Committee (UPGC). AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Citing Literature Volume656, Issue1Sensing and Controlling Motion: Vestibular and Sensorimotor FunctionMay 1992Pages 755-765 RelatedInformation