scholarly journals Efferent-Mediated Responses in Vestibular Nerve Afferents of the Alert Macaque

2009 ◽  
Vol 101 (2) ◽  
pp. 988-1001 ◽  
Author(s):  
Soroush G. Sadeghi ◽  
Jay M. Goldberg ◽  
Lloyd B. Minor ◽  
Kathleen E. Cullen
Keyword(s):  
Rotational Velocity ◽  
Semicircular Canals ◽  
Macaque Monkey ◽  
Nerve Fibers ◽  
Vestibular Nerve ◽  
Vestibular Afferents ◽  
Motion Responses ◽  
Unilateral Labyrinthectomy ◽  
Vestibular Nerve Afferents

The peripheral vestibular organs have long been known to receive a bilateral efferent innervation from the brain stem. However, the functional role of the efferent vestibular system has remained elusive. In this study, we investigated efferent-mediated responses in vestibular afferents of alert behaving primates (macaque monkey). We found that efferent-mediated rotational responses could be obtained from vestibular nerve fibers innervating the semicircular canals after conventional afferent responses were nulled by placing the corresponding canal plane orthogonal to the plane of motion. Responses were type III, i.e., excitatory for rotational velocity trapezoids (peak velocity, 320°/s) in both directions of rotation, consistent with those previously reported in the decerebrate chinchilla. Responses consisted of both fast and slow components and were larger in irregular (∼10 spikes/s) than in regular afferents (∼2 spikes/s). Following unilateral labyrinthectomy (UL) on the side opposite the recording site, similar responses were obtained. To confirm the vestibular source of the efferent-mediated responses, the ipsilateral horizontal and posterior canals were plugged following the UL. Responses to high-velocity rotations were drastically reduced when the superior canal (SC), the only intact canal, was in its null position, compared with when the SC was pitched 50° upward from the null position. Our findings show that vestibular afferents in alert primates show efferent-mediated responses that are related to the discharge regularity of the afferent, are of vestibular origin, and can be the result of both afferent excitation and inhibition.

Efferent Synaptic Transmission at the Vestibular Type II Hair Cell Synapse

2020 ◽  
Author(s):  
Zhou Yu ◽  
J. Michael McIntosh ◽  
Soroush Sadeghi ◽  
Elisabeth Glowatzki
Keyword(s):  
Hair Cells ◽  
Nerve Fibers ◽  
Repetitive Stimulation ◽  
Vestibular Nerve ◽  
Type I ◽  
Type Ii ◽  
Optogenetic Stimulation ◽  
Vestibular Afferents ◽  
Stimulation Of

ABSTRACTIn the vestibular peripheral organs, type I and type II hair cells (HCs) transmit incoming signals via glutamatergic quantal transmission onto afferent nerve fibers. Additionally, type I HCs transmit via ‘non-quantal’ transmission to calyx afferent fibers, by accumulation of glutamate and potassium in the synaptic cleft. Vestibular efferent inputs originating in the brainstem contact type II HCs and vestibular afferents. Here, we aimed at characterizing the synaptic efferent inputs to type II HCs using electrical and optogenetic stimulation of efferent fibers combined with in vitro whole-cell patch clamp recording from type II HCs in the rodent vestibular crista. Properties of efferent synaptic currents in type II HCs were similar to those found in cochlear hair cells and mediated by activation of α9/α10 nicotinic acetylcholine receptors (AChRs) and SK potassium channels. While efferents showed a low probability of release at low frequencies of stimulation, repetitive stimulation resulted in facilitation and increased probability of release. Notably, the membrane potential of type II HCs measured during optogenetic stimulation of efferents showed a strong hyperpolarization even in response to single pulses and was further enhanced by repetitive stimulation. Such efferent-mediated inhibition of type II HCs can provide a mechanism to adjust the contribution of signals from type I and type II HCs to vestibular nerve fibers. As a result, the relative input of type I hair cells to vestibular afferents will be strengthened, emphasizing the phasic properties of the incoming signal that are transmitted via fast non-quantal transmission.New and NoteworthyType II vestibular hair cells (HCs) receive inputs from efferent fibers originating in the brainstem. We used in vitro optogenetic and electrical stimulation of efferent fibers to study their synaptic inputs to type II HCs. Efferent inputs inhibited type II HCs, similar to cochlear efferent effects. We propose that efferent inputs adjust the contribution of signals from type I and type II HCs that report different components of the incoming signal to vestibular nerve fibers.

Response of Vestibular-Nerve Afferents to Active and Passive Rotations Under Normal Conditions and After Unilateral Labyrinthectomy

2007 ◽  
Vol 97 (2) ◽  
pp. 1503-1514 ◽  
Author(s):  
Soroush G. Sadeghi ◽  
Lloyd B. Minor ◽  
Kathleen E. Cullen
Keyword(s):  
Discharge Rate ◽  
Vestibular Nerve ◽  
The Body ◽  
Head Movements ◽  
Whole Body ◽  
Before And After ◽  
Unilateral Labyrinthectomy ◽  
Vestibular Nerve Afferents ◽  
Head Rotations

We investigated the possible contribution of signals carried by vestibular-nerve afferents to long-term processes of vestibular compensation after unilateral labyrinthectomy. Semicircular canal afferents were recorded from the contralesional nerve in three macaque monkeys before [horizontal (HC) = 67, anterior (AC) = 66, posterior (PC) = 50] and 1–12 mo after (HC = 192, AC = 86, PC = 57) lesion. Vestibular responses were evaluated using passive sinusoidal rotations with frequencies of 0.5–15 Hz (20–80°/s) and fast whole-body rotations reaching velocities of 500°/s. Sensitivities to nonvestibular inputs were tested by: 1) comparing responses during active and passive head movements, 2) rotating the body with the head held stationary to activate neck proprioceptors, and 3) encouraging head-restrained animals to attempt to make head movements that resulted in the production of neck torques of ≤2 Nm. Mean resting discharge rate before and after the lesion did not differ for the regular, D (dimorphic)-irregular, or C (calyx)-irregular afferents. In response to passive rotations, afferents showed no change in sensitivity and phase, inhibitory cutoff, and excitatory saturation after unilateral labyrinthectomy. Moreover, head sensitivities were similar during voluntary and passive head rotations and responses were not altered by neck proprioceptive or efference copy signals before or after the lesion. The only significant change was an increase in the proportion of C-irregular units postlesion, accompanied by a decrease in the proportion of regular afferents. Taken together, our findings show that changes in response properties of the vestibular afferent population are not likely to play a major role in the long-term changes associated with compensation after unilateral labyrinthectomy.

Role of semicircular canals in positional alcohol nystagmus

1965 ◽  
Vol 208 (6) ◽  
pp. 1065-1070 ◽  
Author(s):  
K. E. Money ◽  
W. H. Johnson ◽  
B. M. A. Corlett
Keyword(s):  
Semicircular Canal ◽  
Semicircular Canals ◽  
The Other ◽  
Positional Nystagmus ◽  
Horizontal Semicircular Canal ◽  
Horizontal Canal ◽  
Unilateral Labyrinthectomy

Following unilateral labyrinthectomy or inactivation of one horizontal semicircular canal in cats, a horizontal positional nystagmus was observed when the cat, after ingesting alcohol, was held with the head up or with the head down. This nystagmus was toward the operated ear in the head-up position and away from the operated ear in the head-down position. It disappeared following inactivation of the horizontal canal of the other ear. In cats with both horizontal canals discretely inactivated, there was no horizontal alcohol nystagmus in any position, but the vertical and rotary components of positional alcohol nystagmus were still present. It was concluded that positional alcohol nystagmus is initiated by the action of gravity on receptors of the semicircular canals. No conclusion could be drawn concerning the site or mechanism of the action of alcohol.

scholarly journals Angular vestibuloocular reflex responses in Otop1 mice. II. Otolith sensor input improves compensation after unilateral labyrinthectomy

2019 ◽  
Vol 121 (6) ◽  
pp. 2300-2307 ◽  
Author(s):  
Serajul I. Khan ◽  
Charles C. Della Santina ◽  
Americo A. Migliaccio
Keyword(s):  
Semicircular Canals ◽  
Vertical Axis ◽  
Vestibuloocular Reflex ◽  
Peripheral Injury ◽  
Axis Parallel ◽  
Vor Adaptation ◽  
Unilateral Labyrinthectomy ◽  
Context Specific ◽  
Gain Loss

The role of the otoliths in mammals in the normal angular vestibuloocular reflex (VOR) was characterized in an accompanying study based on the Otopetrin1 (Otop1) mouse, which lacks functioning otoliths because of failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. That study showed that otoliths do not contribute to the normal horizontal (rotation about Earth-vertical axis parallel to dorso-ventral axis) and vertical (rotation about Earth-vertical axis parallel to interaural axis) angular VOR but do affect gravity context-specific VOR adaptation. By using these animals, we sought to determine whether the otoliths play a role in the angular VOR after unilateral labyrinthectomy when the total canal signal is reduced. In five Otop1 mice and five control littermates we measured horizontal and vertical left-ear-down and right-ear-down sinusoidal VOR (0.2–10 Hz, 20–100°/s) during the early (3–5 days) and plateau (28–32 days) phases of compensation after unilateral labyrinthectomy and compared these measurements with baseline preoperative responses from the accompanying study. From similar baselines, acute gain loss was ~25% less in control mice, and chronic gain recovery was ~40% more in control mice. The acute data suggest that the otoliths contribute to the angular VOR when there is a loss of canal function. The chronic data suggest that a unilateral otolith signal can significantly improve angular VOR compensation. These data have implications for vestibular rehabilitation of patients with both canal and otolith loss and the development of vestibular implants, which currently only mimic the canals on one side.NEW & NOTEWORTHY This is the first study examining the role of the otoliths (defined here as the utricle and saccule) on the acute and chronic angular vestibuloocular reflex (VOR) after unilateral labyrinthectomy in an animal model in which the otoliths are reliably inactivated and the semicircular canals preserved. This study shows that the otolith signal is used to augment the acute angular VOR and help boost VOR compensation after peripheral injury.

Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau

1985 ◽  
Vol 54 (2) ◽  
pp. 370-384 ◽  
Author(s):  
S. M. Highstein ◽  
R. Baker
Keyword(s):  
Semicircular Canal ◽  
Action Potentials ◽  
Behavioral Activation ◽  
Nerve Fibers ◽  
Primary Afferents ◽  
Vestibular Nerve ◽  
Behavioral Arousal ◽  
Vestibular Neurons ◽  
Vestibular Afferents ◽  
Single Spike

Spinalized toadfish were held in a lucite chamber and perfused through the mouth with running seawater. Primary vestibular afferents and vestibular efferent axons and somas were studied with glass microelectrodes. Vestibular semicircular canal afferent and efferent axons were visually identified and penetrated with glass microelectrodes. Afferents responded to pulses of injected current with trains of action potentials, whereas efferents responded with only a single spike. This differential response to injected current served to further distinguish these two classes of nerve fibers that share the same canal nerve for part of their course. When current pulses were injected into efferent somadendritic recording sites, cells responded with trains of action potentials similar to those seen in other central nervous system neurons. Semicircular canal afferents were spontaneously active and occupied the same spectrum of regularity as vestibular afferents recorded in other species. Behavioral arousal evoked by lightly touching the fish on the snout or over the eye resembled spontaneous arousal observed in the field and consisted of eye withdrawal, fin erection, and attempted swimming. Efferent vestibular neurons were spontaneously active and increased their frequency of discharge when the fish was behaviorally aroused. Most efferents were briskly activated by behavioral arousal, but the time constant of the decay of their responses was variable ranging from 100 to 600 ms. Not only touch, but multimodal stimuli were capable of increasing the level of spontaneous activity of efferent vestibular neurons. The shortest latency to behavioral activation was 160 ms. Vestibular primary afferents also manifested increase in neuronal activity with behavioral activation. Irregularly discharging afferents were much more responsive than regularly discharging afferents. One rare case of transient inhibition in a regularly discharging afferent is illustrated. Severing the efferent vestibular nerve blocked behavioral activation in vestibular primary afferents. Electrical stimulation of the efferent vestibular nerve produced excitatory postsynaptic potentials (EPSPs) at latencies within the monosynaptic range in vestibular primary afferents. These monosynaptic EPSPs could produce action potentials in primary afferents or could sum with subthreshold depolarizations produced by current passed through the microelectrode to initiate impulses.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Effects of Canal Plugging on the Vestibuloocular Reflex and Vestibular Nerve Discharge During Passive and Active Head Rotations

2009 ◽  
Vol 102 (5) ◽  
pp. 2693-2703 ◽  
Author(s):  
Soroush G. Sadeghi ◽  
Jay M. Goldberg ◽  
Lloyd B. Minor ◽  
Kathleen E. Cullen
Keyword(s):  
Semicircular Canals ◽  
Vestibular Nerve ◽  
Head Movements ◽  
Vestibuloocular Reflex ◽  
Phase Lead ◽  
Afferent Discharge ◽  
Vestibular Nerve Afferents ◽  
Head Rotations ◽  
Central Adaptation ◽  
Nerve Discharge

Mechanical occlusion (plugging) of the slender ducts of semicircular canals has been used in the clinic as well as in basic vestibular research. Here, we investigated the effect of canal plugging in two macaque monkeys on the horizontal vestibuloocular reflex (VOR) and the responses of vestibular-nerve afferents during passive head rotations. Afferent responses to active head movements were also studied. The horizontal VOR gain decreased after plugging to <0.1 for frequencies <2 Hz but rose to about 0.6 as frequency was increased to 15 Hz. Afferents innervating plugged horizontal canals had response sensitivities that increased with the frequency of passive rotations from <0.01 (spikes/s)/(°/s) at 0.5 Hz to values of about 0.2 and 0.5 (spikes/s)/(°/s) at 8 Hz for regular and irregular afferents, respectively (<50% of responses in controls). An increase in phase lead was also noted following plugging in afferent discharge, but not in the VOR. Because the phase discrepancy between the VOR and afferent discharge is much larger than that seen in control animals, this suggests that central adaptation shapes VOR dynamics following plugging. The effect of canal plugging on afferent responses can be modeled as an increase in stiffness and a reduction in the dominant time constant and gain in the transfer function describing canal dynamics. Responses were also evident during active head rotations, consistent with the frequency content of these movements. We conclude that canal plugging in macaques is effective only at frequencies <2 Hz. At higher frequencies, afferents show significant responses, with a nearly 90° phase lead, such that they encode near-rotational acceleration. Our results demonstrate that afferents innervating plugged canals respond robustly during voluntary movements, a finding that has implications for understanding the effects of canal plugging in clinical practice.

Relationship of Semicircular Canal Size to Vestibular-Nerve Afferent Sensitivity in Mammals

2007 ◽  
Vol 98 (6) ◽  
pp. 3197-3205 ◽  
Author(s):  
Aizhen Yang ◽  
Timothy E. Hullar
Keyword(s):  
Semicircular Canal ◽  
High Frequency ◽  
High Gain ◽  
Vestibular Nerve ◽  
Radius Of Curvature ◽  
Horizontal Canal ◽  
Vestibular Nerve Afferents ◽  
The Relationship ◽  
Irregular Afferents ◽  
Anterior Canal

The relationship between semicircular canal radius of curvature and afferent sensitivity has not been experimentally determined. We characterized mouse semicircular canal afferent responses to sinusoidal head rotations to facilitate interspecies and intraspecies comparisons of canal size to sensitivity. The interspecies experiment compared the horizontal canal afferent responses among animals ranging in size from mouse to rhesus monkey. The intraspecies experiment compared afferent responses from the larger anterior canal to those from the smaller horizontal canal of mice. The responses of mouse vestibular-nerve afferents showed a low- and high-frequency phase lead and high-frequency gain enhancement. Regular horizontal-canal afferents showed a sensitivity to 0.5-Hz sinusoidal rotations of 0.10 ± 0.03 (SD) spike · s−1/deg · s−1 and high-gain irregular afferents showed a sensitivity of 0.25 ± 0.11 spike · s−1/deg · s−1. The interspecies comparison showed that the sensitivity of regular afferents was related to the radius of curvature R according to the formula Gr = 0.23R − 0.09 ( r2 = 0.86) and the sensitivity of irregular afferents was related to radius according to the formula Gi = 0.32R + 0.01 ( r2 = 0.67). The intraspecies comparison showed that regularly firing anterior canal afferents were significantly more sensitive than those from the relatively smaller horizontal canal, with Gr = 0.25R. This suggests that canal radius of curvature is closely related to afferent sensitivity both among and within species. If the relationship in humans is similar to that demonstrated here, the sensitivity of their regular vestibular-nerve afferents to 0.5-Hz rotations is likely to be about 0.67 spike · s−1/deg · s−1 and of their high-gain irregular afferents about 1.06 spikes · s−1/deg · s−1.

The role of C-tactile nerve fibers in human social development

2022 ◽  
Vol 43 ◽  
pp. 20-26
Author(s):  
Ilona Croy ◽  
Merle T Fairhurst ◽  
Francis McGlone
Keyword(s):  
Social Development ◽  
Nerve Fibers
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