1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of the medial vestibular nucleus (MVN) in the alert guinea pig after a unilateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared with the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit activity and for eye movement recording (scleral search coil technique). To enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibular nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on the vestibular nerve. Of the 589 recorded neurons, 424, defined as second-order vestibular neurons, were recruited at monosynaptic latencies (0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hundred three second-order vestibular neurons were recorded in the control group, 173 in the just-postoperative group, and 148 in the 1-wk-postoperative group. 4. The activity of the electrically recruited neurons was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-intercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensitivity of the neuron-to-head velocity. 5. In the absence of statistically significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of these cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control state, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and completely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spikes/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperative group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, which was 0.69 +/- 0.48 (SD) spikes.s-1/deg.s-1 in the control state and which fell to 0.03 +/- 0.11 spikes.s-1/deg.s-1 just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 spikes.s-1/deg.s-1). Moreover, the slight recovery of sensitivity to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neurons (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in the control g...
There is considerable evidence from studies on cats and monkeys that several cortical areas such as area 2v at the tip of the intraparietal sulcus, area 3av in the sulcus centralis, the parietoinsular vestibular cortex adjacent to the posterior insula (PIVC) and area 7 in the inferior parietal lobule are involved in the processing of vestibular information. Microelectrode recordings from these areas have shown that: (1) most of these cortical neurons are connected trisynaptically to the labyrinthine endorgans and (2) they receive converging vestibular, visual and somatosensory inputs. These data suggest that a multimodal cortical system is involved in postural and gaze control. In humans, recent positron emission tomography (PET) scans and functional magnetic resonance imaging (fMRI) studies have largely confirmed these data. However, because of the limited temporal resolution of these two methods, the minimum time of arrival of labyrinthine inputs from the vestibular hair cells to these cortical areas has not yet been determined. In this study, we used the evoked potential method to attempt to answer this question. Due to its excellent temporal resolution, this method is ideal for the investigation of the tri- or polysynaptic nature of the vestibulocortical pathways. Eleven volunteer patients, who underwent a vestibular neurectomy due to intractable Meniere's disease (MD) or acoustic neurinoma resection, were included in this experiment. Patients were anesthetized and the vestibular nerve was electrically stimulated. The evoked potentials were recorded by 30 subcutaneous active electrodes located on the scalp. The brain electrical source imaging (BESA) program (version 2.0, 1995) was used to calculate dipole sources. The latency period for the activation of five distinct cortical zones, including the prefrontal and/or the frontal lobe, the ipsilateral temporoparietal cortex, the anterior portion of the supplementary motor area (SMA) and the contralateral parietal cortex, was 6 ms. The short latency period recorded for each of these areas indicates that several trisynaptic pathways, passing through the vestibular nuclei and the thalamic neurons, link the primary vestibular afferents to the cortex. We suggest that all these areas, including the prefrontal area, process egomotion information and may be involved in planning motor synergies to counteract loss of equilibrium.
Otolithic afferents with regular resting discharge respond to gravity or low-frequency linear accelerations, and we term these the static or sustained otolithic system. However, in the otolithic sense organs, there is anatomical differentiation across the maculae and corresponding physiological differentiation. A specialized band of receptors called the striola consists of mainly type I receptors whose hair bundles are weakly tethered to the overlying otolithic membrane. The afferent neurons, which form calyx synapses on type I striolar receptors, have irregular resting discharge and have low thresholds to high frequency (e.g., 500 Hz) bone-conducted vibration and air-conducted sound. High-frequency sound and vibration likely causes fluid displacement which deflects the weakly tethered hair bundles of the very fast type I receptors. Irregular vestibular afferents show phase locking, similar to cochlear afferents, up to stimulus frequencies of kilohertz. We term these irregular afferents the transient system signaling dynamic otolithic stimulation. A 500-Hz vibration preferentially activates the otolith irregular afferents, since regular afferents are not activated at intensities used in clinical testing, whereas irregular afferents have low thresholds. We show how this sustained and transient distinction applies at the vestibular nuclei. The two systems have differential responses to vibration and sound, to ototoxic antibiotics, to galvanic stimulation, and to natural linear acceleration, and such differential sensitivity allows probing of the two systems. A 500-Hz vibration that selectively activates irregular otolithic afferents results in stimulus-locked eye movements in animals and humans. The preparatory myogenic potentials for these eye movements are measured in the new clinical test of otolith function—ocular vestibular-evoked myogenic potentials. We suggest 500-Hz vibration may identify the contribution of the transient system to vestibular controlled responses, such as vestibulo-ocular, vestibulo-spinal, and vestibulo-sympathetic responses. The prospect of particular treatments targeting one or the other of the transient or sustained systems is now being realized in the clinic by the use of intratympanic gentamicin which preferentially attacks type I receptors. We suggest that it is valuable to view vestibular responses by this sustained-transient distinction.
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