Vestibular influences on the spontaneous activity of neurones in the lateral geniculate nucleus of the cat.
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Animals↗
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Microiontophoresis of acetylcholine, histamine and their antagonists on neurones in the medial and lateral vestibular nuclei of the cat.
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Acceleration↗
Efferent system degeneration in vestibular ganglionitis.
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Humans↗
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.
Acceleration↗
[Electrophysiologic effects of stimulating the vestibular nuclei on the sensomotor cortex of cats].
The evoked potentials in the anterior suprasylvian and posterior sigmoid gyri to the bulbar vestibular nuclei stimulation were recorded in relaxed anesthetized cats. Neuronal discharges of 70 units in the forelimb cortical zone in the posterior sigmoid gyrus were also recorded. 26 neurons responded to the vestibular nuclei stimulation, 6 of them were identified as cortico-rubral neurons. All of them were activated by the radial-nerve muscle branch stimulation. There was no neurons characterized by the muscle-vestibular convergence from the pyramidal tract neurons. The muscle-vestibular afferent system projection to the cortico-rubral neurons is supposed to play a major role in the tonic muscle coordination of the forelimbs.
Animals↗
Compensation of horizontal canal related activity in the medial vestibular nucleus following unilateral labyrinth ablation in the decerebrate gerbil. I. Type I neurons.
The spontaneous activity and dynamic responses to two frequencies (1.3 and 0.13 Hz) of sinusoidal angular horizontal head acceleration of type I neurons in the medial vestibular nucleus were recorded bilaterally in decerebrate Mongolian gerbils (Meriones unguiculatus) under three experimental conditions; normal labyrinth intact, acutely following unilateral labyrinthine lesion, and four to seven weeks following labyrinthine lesion. The mean spontaneous activity and number of detected type I neurons decreased immediately ipsilateral to the lesion but recovered significantly with time. In contrast, spontaneous activity on the contralateral side increased during compensation following hemilabyrinthectomy. The mean response gains at both frequencies of head oscillation were depressed bilaterally and asymmetrically acutely following the lesion such that the response gain of cells on the intact side exceeded that of the neurons recorded on the injured side. After compensation the number of detected type I neurons on the side ipsilateral to the injury increased but remained below normal levels. The mean gains remained depressed but became symmetric with compensation as a result of improvement in the response of ipsilateral neurons. The phase of responses were significantly advanced in the compensated animals. Although response gain is not fully restored, the linearity of the dynamic modulation in compensated animals is improved as evidenced by a continuous modulation of the increased spontaneous activity of neurons contralateral to the hemilabyrinthectomy. It is proposed that this effect is related to the concurrent improvement in the linearity of the horizontal vestibulo-ocular response. Electrical cathodal polarization of the vestibular nerve ipsilateral to the ablated labyrinth was utilized to investigate the relationship between recovery of spontaneous activity and dynamic function. Acutely following hemilabyrinthectomy, cathodal polarization restored activity in second-order type I neurons to near normal levels but their response gain to head rotation remained depressed. Similar galvanic stimulation in compensated animals also elevated ipsilateral spontaneous activity. As in the acute preparation, such stimulation did not modify the response gain or phase. Thus, the improvement in response of type I neurons in the compensated gerbil was not a direct consequence of restoration of spontaneous activity on the side of the injury.
Animals↗
Investigations into the cause of vertigo in sudden sensorineural hearing loss.
In this light microscopic study of the temporal bone, an attempt has been made to find a morphologic correlate of vertigo associated with idiopathic sudden sensori-neural hearing loss (ISSHL). Hair cell densities of the three cristae and both maculae, as well as vestibular ganglion cell (neuronal) count estimation, was done in nine ears that had documented histories of ISSHL. There were five ears with vertigo and four without. These quantitative data--i.e., hair cell densities and neuronal counts, of the vertiginous ears (group I) and nonvertiginous ears (group II)--was compared by histograms and statistically. Additionally, in each of the two groups, the data from three opposite normal hearing ears were taken as a control and used for comparison with the ISSHL ears. The differences between the vertiginous, nonvertiginous, and control ears were not significant at the 0.01 level, indicating that the vertigo was not caused by hair cell or neuronal degeneration. Gross morphologic alterations in the vestibular system, such as membrane ruptures, endolymphatic hydrops, etc., were also assessed, but no clear-cut pathology was identified in the vertiginous and nonvertiginous ears. The absence of a light microscopic morphologic correlate for vestibular disturbances associated with ISSHL suggests that the symptoms could result from ultrastructural changes in the hair cells and their synapses or from biochemical alterations in their environment.
Acute Disease↗
Eye position signals in the vestibular nuclei: consequences for models of integrator function.
Recordings from neurons in the vestibular nuclei indicate that the cells that carry eye position signals encode the position of a single eye (either ipsilateral or contralateral) during both conjugate and vergence eye movements. The fact that the vestibular nuclei are aware of the positions of each eye is not surprising as the otolith-based linear vestibulo-ocular reflex is known to change its behaviour as a function of uniocular eye position. This result suggests that the signal coming from the oculomotor velocity-to-position integrator specifies the position of each eye during vergence movements and thus must receive a vergence velocity input along with its conjugate velocity inputs. As there is no vergence system in laterally eyed animals, we have proposed two possible models of integrator arrangement that could have developed from conjugate directional (rather than uniocular) integrators in lower animals without frontally mounted eyes. Both of these models explain the existence of near-response cells and produce the required bidirectional gaze paretic nystagmus following unilateral lesions of one integrator. The models also make specific and different predictions concerning the effects of unilateral integrator lesions on the behaviour of the vergence system and thus make suggestions for further experiments.
Animals↗
Nonuniformity in the linear network model of the oculomotor integrator produces approximately fractional-order dynamics and more realistic neuron behavior.
The oculomotor integrator is a network that is composed of neurons in the medial vestibular nuclei and nuclei prepositus hypoglossi in the brainstem. Those neurons act approximately as fractional integrators of various orders, converting eye velocity commands into signals that are intermediate between velocity and position. The oculomotor integrator has been modeled as a network of linear neural elements, the time constants of which are lengthened by positive feedback through reciprocal inhibition. In this model, in which each neuron reciprocally inhibits its neighbors with the same Gaussian profile, all model neurons behave as identical, first-order, low-pass filters with dynamics that do not match the variable, approximately fractional-order dynamics of the neurons that compose the actual oculomotor integrator. Fractional-order integrators can be approximated by weighted sums of first-order, low-pass filters with diverse, broadly distributed time constants. Dynamic systems analysis reveals that the model integrator indeed has many broadly distributed time constants. However, only one time constant is expressed in the model due to the uniformity of its network connections. If the model network is made nonuniform by removing the reciprocal connections to and from a small number of neurons, then many more time constants are expressed. The dynamics of the neurons in the nonuniform network model are variable, approximately fractional-order, and resemble those of the neurons that compose the actual oculomotor integrator. Completely removing the connections to and from a neuron is equivalent to eliminating it, an operation done previously to demonstrate the robustness of the integrator network model. Ironically, the resulting nonuniform network model, previously supposed to represent a pathological integrator, may in fact represent a healthy integrator containing neurons with realistically variable, approximately fractional-order dynamics.
Animals↗
Unbiased quantification of Scarpa's ganglion neurons in aminoglycoside ototoxicity.
While most studies have demonstrated damage to the cochlear and vestibular endorgan as the primary site of aminoglycoside toxicity, the effect on the primary afferent neurons of the vestibular ganglion remains to be determined. This study used the unbiased stereology-optical fractionator method to obtain estimates of the vestibular ganglion neuronal number. Archival temporal bone specimens from seven subjects with a history of gentamicin (n=3) and streptomycin (n=4) aminoglycoside ototoxicity were used. The post-ototoxicity survival time ranged from two months to 8 years, with an average of 2.2 years. Seven archival human temporal bone specimens from age-matched subjects with no history of audiovestibular symptoms or ototoxicity served as controls. Group means were compared using unpaired, two-tailed student's t test. The average vestibular ganglion neuronal number in the aminoglycoside ototoxicity group was 20, 733 neurons (CV=0.073), which was significantly lower (p<0.005) than the average number in the age-matched control group of 24, 902 neurons (CV=0.109). These findings may be consistent with either retrograde degeneration or a direct neurotoxic effect of the aminoglycosides on the vestibular ganglion neuron.
Adolescent↗
Neural correlates of compensation after hemilabyrinthectomy.
Vestibular brain stem neurons responsive to angular acceleration in the plane of the horizontal canal were examined in cats 30 to 52 days after contralateral labyrinthectomy and compared with similar units in cats with intact labyrinths and in other cats immediately after transection of the contralateral eighth nerve. In the compensated state, the mean spontaneous firing rate of type I neurons was 24 spikes/s, in contrast to the mean of 45/s observed immediately after contralateral labyrinthectomy. In intact cats, mean firing rate was 19 spikes/s. Sensitivity, as measured in spikes/s/deg/s2, was significantly lower immediately after labyrinthectomy than in intact controls and remained so in compensated cats. On the other hand, time constants and the ratio of adapting:nonadapting units was unchanged. Ablation of the midline cerebellum including vermis and fastigial nuclei did not materially affect these results. We concluded that (i) the main defects in static posture and nystagmus in the uncompensated state were due to the striking difference in resting firing rates between the ipsi- and contralateral vestibular nuclei; (ii) compensation in the static posture was the result of a tendency to equalize the resting firing rates in the two vestibular nuclei; and (iii) recovery in the dynamic, head-turning situation was due to partial recovery of sensitivity on the ipsilateral side, bringing it to the relatively constant, unchanging depressed sensitivity on the contralateral side.
Acceleration↗
Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau.
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)
Acoustic Stimulation↗
G-protein Golfalpha (GNAL) is expressed in the vestibular end organs and primary afferent neurons of Rattus norvegicus.
Guanine nucleotide binding proteins (G-proteins) play an important role in mediating signals transduced across the cell membrane by membrane-bound receptors. The precise role of these proteins and their coupled receptors in the physiology of the vestibular neuroepithelium is poorly understood. Although Golfalpha was originally discovered in the olfactory neuroepithelium and striatum, we recently identified this G-protein alpha subunit in a normalized cDNA library constructed from rat vestibular end organs and vestibular nerves including Scarpa's ganglia. In order to further characterize Golfalpha in the rat vestibular periphery, we used in situ hybridization and reverse transcription polymerase chain reaction to determine the anatomic context of this gene expression. Golfalpha was found in both the end organs and the ganglia and could serve unique roles in the physiology of the vestibular neuroepithelium.
Animals↗
Vestibular nucleus inputs to paramedian reticulospinal neurons in the cat.
Experiments were done in chloralose-anesthetized cats to identify single units in the paramedian reticular nucleus (PRN) that responded to stimulation of pressor sites in the vestibular nucleus complex (VNC) and that projected directly to the intermediate gray (IG) region of the upper thoracic cord. Forty-seven units responded orthodromically to stimulation of the ipsilateral VNC with a mean latency of 6.3 +/- 0.6 ms: 44 were excited and 3 were inhibited. Of these 47 units, 29 (62%) also were antidromically activated by stimulation of the ipsilateral IG at the level of T2. These data provide electrophysiological evidence for the existence of neurons in PRN that receive VNC inputs and project directly to spinal autonomic areas, and suggest that this pathway may be involved in mediating vestibulosympathetic reflex responses associated with postural adjustments.
Action Potentials↗
Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques.
1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the "marginal zone"). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral "on" directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
[Neuronal mechanisms of the horizontal canal system in the vestibular nuclei].
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Action Potentials↗
Changes in protein expression in the vestibular nuclei during vestibular compensation.
In the guinea pig, labyrinthectomy induces an immediate depression of the resting discharges in the neurons of the ipsilateral vestibular nuclei. Later on, in spite of the persistent deprivation of their ipsilateral labyrinthine input, a spontaneous restoration of activity, which is complete within 1 week, occurs in these neurons. Here, by using computer-assisted quantitative two-dimensional gel analysis, we have detected three proteins whose expressions were increased in the ipsilateral vestibular nuclei 1 week after unilateral labyrinthectomy. The spatio-temporal pattern of this phenomenon was compatible with a role for it in the restoration of activity in the vestibular neurons deprived of their ipsilateral labyrinthine input. Furthermore, the N-terminal amino acid sequences of two of these expressed proteins were obtained.
Animals↗
A realistic neural-network simulation of both slow and quick phase components of the guinea pig VOR.
A realistic neural-network model was constructed to simulate production of both the slow-phase and quick-phase components of vestibular nystagmus by incorporating a quick-phase pathway into a previous model of the slow phase. The neurons in the network were modelled by multicompartmental Hodgkin-Huxley-style spiking neurons based on known responses and projections of physiologically identified vestibular neurons. The modelling used the GENESIS software package. The slow-phase network consisted of ganglion and medial vestibular nucleus (MVN) neurons; the latter were constructed using biophysical models of MVN type A and B neurons. The quick-phase network contained several types of bursting cells which have been shown to have major roles in the generation of the quick phase: burster-driver neurons, long-lead burst neurons, pause neurons, excitatory burst neurons and inhibitory burst neurons. Comparison of the output neural responses from the model with guinea pig behavioural responses from the companion paper showed consistency between model and animal data for neuron firing patterns, maximal firing rates, and timing, duration and number of quick phases. Comparisons were made for stable head input and for sinusoidal angular stimuli at a range of frequencies from 0.1 to 2 Hz. Except for data at 0.1 Hz, where the simulation produced one more quick phase per half cycle than the animal data, the number of quick phases was consistent between the model and the animal data. The model was also used to simulate the effects both of unilateral vestibular deafferentation (UVD) and of vestibular compensation after UVD, and the responses in the modelled MVN neurons were affected in a way similar to those measured in guinea pig MVN neurons: the number of quick phases and their timing changed in a similar fashion to that observed in behavioural data.
Animals↗