[Convergence of afferent influences on neurons of the pigeon vestibular nuclei].
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Neurochemistry of the central vestibular pathways.
This review focuses on the neurochemistry of the central vestibular pathways. The main emphasis will be on the analysis of the central vestibular nuclei neurons, since several papers published in the past 5 years have provided important information on the role that neurotransmitter-dependent conductances play in the central processing of vestibular inputs. Indeed, increasing evidence suggests that both the non-linear intrinsic membrane properties of the neurons and the nature of the different neurotransmitters and neuromodulators involved in the vestibular network contribute to the various operations required for stabilising gaze and posture. It has also been demonstrated that the neurotransmitter-dependent conductances together with the ionic voltage-dependent conductances may determine the firing patterns of the medial vestibular neurons and interfere with their integrative properties. We hope that this review will show that by combining in vitro and in vivo electrophysiological approaches and the new powerful neuropharmacological techniques developed from the recent advances of molecular biology, the vestibular system can be used as a good model to elucidate some of the basic properties of the brain including learning, neural computation, network reconfiguration and post-lesional plasticity.
Acetylcholine↗
Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons.
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Animals↗
Evidence for glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus.
The localization and distribution of brain-stem afferent neurons to the cat abducens nucleus has been examined by high-affinity uptake and retrograde transport of 3H-glycine. Injections of 3H-glycine selectively labeled (by autoradiography) only neurons located predominantly in the ipsilateral medial vestibular and contralateral prepositus hypoglossi nuclei, and in the contralateral dorsomedial reticular formation, the latter corresponding to the location of inhibitory burst neurons. The specificity of uptake and retrograde transport of 3H-glycine was indicated by the absence of labeling of the dorsomedial medullary reticular neurons ipsilateral and in close proximity to the injection site, where local uptake by diffusion could have occurred. The selectivity of uptake and transport was demonstrated by the absence of retrograde labeling following injections of 3H-GABA or 3H-leucine into the abducens nucleus. The immunohistochemical localization of glycine and GABA revealed a differential distribution of the 2 inhibitory neurotransmitter candidates in the extraocular motor nuclei. Glycine-immunoreactive staining of synaptic endings in the abducens nucleus was dense with a widespread soma-dendritic distribution but was sparse in the trochlear and oculomotor nuclei. By contrast, GABA-immunoreactive staining within the oculomotor and trochlear nuclei was associated with synaptic endings that were particularly prominent on the somata of motoneurons. GABA-immunoreactive staining in the abducens nucleus, however, was sparse. These differences between glycine- and GABA-immunoreactive staining in the extraocular motor nuclei were correlated with differences in the immunoreactivity of axons in the descending (glycine) and ascending (GABA) limbs of the medial longitudinal fasciculus. Glycine-immunoreactive neurons, furthermore, were observed in the same locations as neurons that were labeled autoradiographically by retrograde transport of 3H-glycine from the abducens nucleus. Electrophysiological recordings from abducens motoneurons and internuclear neurons revealed a marked reduction in the slow positivity of the orthodromic extracellular potential elicited by ipsilateral vestibular nerve stimulation following systemic administration of strychnine, an antagonist of glycine. Intracellular recordings demonstrated that the vestibular-evoked disynaptic inhibitory postsynaptic potentials in abducens neurons were effectively blocked by strychnine but were unaffected by picrotoxin, an antagonist of GABA.(ABSTRACT TRUNCATED AT 400 WORDS)
Abducens Nerve↗
Organization of vestibular inputs to nucleus tractus solitarius and adjacent structures in cat brain stem.
The vestibular system is involved in maintaining stable blood pressure and respiration during changes in posture and is essential for eliciting motion sickness-related vomiting. Because the nucleus tractus solitarius (NTS) participates in the regulation of sympathetic and inspiratory outflow and the triggering of emesis, we tested the hypothesis that this region receives vestibular inputs in cats. In one set of experiments, microinjections of the tracer Phaseolus vulgaris leucoagglutinin into the medial and inferior vestibular nuclei labeled projections to the middle and lateral regions of the NTS. In electrophysiological experiments, electrical stimulation of the vestibular nerve modified the firing rates of neurons located in the same regions. Some neurons with vestibular inputs received convergent signals from the abdominal vagus nerve and could potentially mediate motion sickness-related vomiting. Others received convergent baroreceptor inputs and could act as a substrate for some components of vestibulosympathetic reflexes. In contrast, inspiratory neurons in the dorsal respiratory group received little vestibular input, suggesting that vestibulorespiratory reflexes are mediated by cells located elsewhere.
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Selective processing of vestibular reafference during self-generated head motion.
The vestibular sensory apparatus and associated vestibular nuclei are generally thought to encode head-in-space motion. Angular head-in-space velocity is detected by vestibular hair cells that are located within the semicircular canals of the inner ear. In turn, the afferent fibers of the vestibular nerve project to neurons in the vestibular nuclei, which, in head-restrained animals, similarly encode head-in-space velocity during passive whole-body rotation. However, during the active head-on-body movements made to generate orienting gaze shifts, neurons in the vestibular nuclei do not reliably encode head-in-space motion. The mechanism that underlies this differential processing of vestibular information is not known. To address this issue, we studied vestibular nuclei neural responses during passive head rotations and during a variety of tasks in which alert rhesus monkeys voluntarily moved their heads relative to space. Neurons similarly encoded head-in-space velocity during passive rotations of the head relative to the body and during passive rotations of the head and body together in space. During all movements that were generated by activation of the neck musculature (voluntary head-on-body movements), neurons were poorly modulated. In contrast, during a task in which each monkey actively "drove" its head and body together in space by rotating a steering wheel with its arm, neurons reliably encoded head-in-space motion. Our results suggest that, during active head-on-body motion, an efferent copy of the neck motor command, rather than the monkey's knowledge of its self-generated head-in-space motion or neck proprioceptive information, gates the differential processing of vestibular information at the level of the vestibular nuclei.
Action Potentials↗
[Reaction of cat vasomotor center neurons to stimulation of vestibular and somatic afferents].
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Animals↗
Vestibular afferent innervation in the vestibular efferent nucleus of rats.
To delineate the vestibular afferent innervation in the vestibular efferent nucleus in the brainstem, neurobiotin or biotinylated dextran amine was injected into the superior Scarpa's ganglion of Sprague-Dawley rats. The locations of vestibular efferent neurons in the brainstem were identified by neutral red or choline acetyltransferase staining. Of the three pairs of vestibular efferent nuclei, labeled fibers and bouton-like endings were found only within the dorsolateral vestibular efferent nucleus on the ipsilateral side. Labeled afferent terminals with bouton-like varicosities were observed in the vicinity of cell bodies or dendrites of these efferent neurons. Our findings suggest that vestibular primary afferents may exert direct influence on vestibular efferent neurons, constituting an ipsilateral close-loop arrangement in the central vestibular system.
Animals↗
Vestibular control of swimming in lamprey. III. Activity of vestibular afferents: convergence of vestibular inputs on reticulospinal neurons.
Experiments were carried out on the in vitro preparation of the lamprey brainstem isolated together with the labyrinths. The brain orientation in space could be changed in steps of 45 degrees by rotation (360 degrees) around the longitudinal axis (roll) or the transverse axis (pitch). Vestibular afferents in the VIII nerve, or reticulospinal (RS) neurons, were recorded extracellularly during roll and pitch. Two main types of afferents could be distinguished. Presumed otolith afferents responded both to a change of position and to a maintained new position. These afferents were classified in several groups according to the position of their zone of sensitivity. For roll, the largest group had their maximal sensitivity around 90 degrees tilt to the ipsilateral side, the next group in size responded at 180 degrees, and only a few afferents were activated by contralateral roll. For pitch, there are groups responding with maximal sensitivity at 90 degrees nose-up, 90 degrees nose-down and at 180 degrees. A minority of afferents were active when the brainstem was in a normal position, i.e. horizontal, with the dorsal side up. Another type of afferent responded only by a high-frequency burst to a change of brain orientation. They were classified as canal afferents in analogy with other species. All tested canal afferents responded to rotation towards ipsi-side down. Pitch tilt revealed two groups that responded to rotation towards either nose-up or nose-down. RS neurons from the anterior and middle rhombencephalic nuclei (ARRN and MRRN) were recorded before and after unilateral transection of the VIII nerve.(ABSTRACT TRUNCATED AT 250 WORDS)
Afferent Pathways↗
Light microscopical study of nitric oxide synthase I-positive neurons, including fibres in the vestibular nuclear complex of the cat.
Nitric oxide is a gaseous neurotransmitter that is synthesized by the enzyme nitric oxide synthase I (NOS I). At present, little is known of NOS I-positive neurons in the vestibular nuclear complex of the cat (VNCc). The aim of the present study was to examine the morphology, distribution patterns and interconnections of NOS I-positive neurons, including fibres in the VNCc. Five adult cats were used as experimental animals. All cats were anaesthetized and perfused transcardially. Brains were removed, postfixed, cut on a freezing microtome and stained in three different ways. Every third section was treated with the Nissl method, other sections were stained either histochemically for NADPH diaphorase or immunohistochemically for NOS I. The atlas of Berman (1928) was used for orientation in the morphometric study. NOS I-positive neurons and fibres were found in all parts of VNCc: medial vestibular nucleus (MVN); lateral vestibular nucleus (LVN); superior vestibular nucleus (SVN); inferior vestibular nucleus (IVN); X, Y, Z groups and Cajal's nucleus. The NOS I-positive neurons were classified according to their size (small, medium-sized, large neurons type I and type II) and their shape (oval, fusiform, triangular, pear-shaped, multipolar and irregular). In every nucleus, a specific neuronal population was observed. In SVN, a large number of interconnections between NOS I-positive neurons were identified. In MVN, chain-like rolls of small neurons were found. Tiny interconnections between MVN and mesencephalic reticular formation were present. Our data provide information on the morphology, distribution patterns and interconnections of NOS I-positive neurons in the VNCc and can be extrapolated to other mammals.
Animals↗
[Response of the hypothalamic neurons to stimulation of the vestibular nerve and lateral vestibular nucleus in rabbits].
Effects of single, double, and rhythmic stimulation upon hypothalamic neurons responding to the 1st excitatory phase of lateral vestibular nucleus stimulation, were studied. The data obtained show that activation of some hypothalamic neurons following stimulation of the lateral vestibular nucleus has a monosynaptic character. The findings suggest that ascending afferents from the lateral vestibular nucleus to the hypothalamus pass via oligo- as well as polysynaptic pathways.
Afferent Pathways↗
[Activity of neurons of the guinea pig lateral vestibular nucleus evoked by tilting about a longitudinal axis during locomotion].
The activity of neurons of the lateral vestibular nucleus evoked by tilting about a longitudinal axis during spontaneous and mesencephalon stimulation-evoked locomotion have been investigated in the decerebrated guinea pig. In the vast majority of the investigated neurons the locomotor activity has led to changes in the responses to adequate vestibular stimulation. The enhancement of the responses is observed in almost all of the vestibulospinal neurons and in two thirds of neurons without descending projections. The diminishing of the responses is registered only in one quarter of neurons that do not projected to the spinal cord. Changes in responses are of the amplitude pattern. The angle lag value of these changes relative to acceleration that appears during the motion is quite constant. It is suggested that the observed enhancement of dynamic reactions of vestibular neurons provides the maintenance of the animal equilibrium during locomotion by different gaits and trajectories.
Animals↗
Vestibular nuclei activity and eye movements in the alert monkey during sinusoidal optokinetic stimulation.
In the alert monkey (Macaca fascicularis) vestibular nuclei neurons and eye movements were recorded during sinusoidal optokinetic stimulation in the horizontal plane at frequencies between 0.02-3.3 Hz. Maximal stimulus velocity was generally kept constant at 40 deg/s, except for frequencies above 1 Hz. Eye movements showed a nystagmus-like pattern up to 0.2 Hz with a gain (change in eye position/change in cylinder position) greater than 0.8; at frequencies above 1 Hz the gain dropped to 0.35 at 3.3 Hz. A decrease in gain was accompanied by an increasing phase lag. Recordings in the vestibular nuclei were obtained from 'vestibular only' and 'vestibular plus saccade' neurons. Neurons with a strong eye position signal ('vestibular plus position') were excluded. The vast majority (87%) of neurons were not modulated at 0.2 Hz or higher frequencies of sinusoidal optokinetic stimulation, and were classified as 'low-frequency' type neurons. Compared to the response at constant stimulus velocity, sensitivity (imp X s-1/deg X s-1) dropped to 72% at 0.03 Hz and 16% at 0.1 Hz. A few neurons (13%) responding at 0.2 Hz (sensitivity on average 65% of the constant velocity response) were classified as 'high-frequency' type neurons. They did not respond above 1.0 Hz and showed no modulation with individual eye movements. The results suggest that the activity in the groups of vestibular nuclei neurons tested here is insufficient to account for the eye movements in response to sinusoidal optokinetic stimulation at frequencies above 0.1 Hz.(ABSTRACT TRUNCATED AT 250 WORDS)
Animals↗
Effects of ethanol applied by electrosmosis on neurons in the lateral and medial vestibular nuclei.
Electrophysiological studies were performed to elucidate the effects of ethanol on neuron activities in the lateral vestibular nucleus (LVN) and medial vestibular nucleus (MVN) of cats using an electrosmotic and microiontophoretic method. The LVN and MVN neurons were classified into two types according to the firing pattern and latency of the first spike with vestibular nerve stimulation: monosynaptic and polysynaptic neurons. Electrosmotic application of ethanol up to 200 nA produced a dose-dependent inhibition of spikes of the LVN monosynaptic neurons with vestibular nerve stimulation and iontophoretically applied glutamate, but no significant alterations of the spikes of the LVN polysynaptic neurons. Acetylcholine-induced firing in the LVN monosynaptic neurons was also inhibited by ethanol. In the MVN, spike generation of the monosynaptic and polysynaptic neurons with vestibular nerve stimulation and iontophoretically applied glutamate remained unaltered with ethanol up to 200 nA. These results indicate that ethanol predominantly inhibits synaptic transmission of the LVN monosynaptic neurons, probably by acting on the postsynaptic cell bodies.
Acetylcholine↗
Betahistine, vestibular function and compensation: in vitro studies of vestibular function and plasticity.
Histamine has an excitatory action on rat medial vestibular nucleus neurones in vitro, an effect that is mediated by histamine H1 and H2 receptors. Betahistine, which is a weak agonist at the H1 receptor and a moderate antagonist at the presynaptic H3 autoreceptor, weakly excites medial vestibular nucleus cells but antagonizes their responses to histamine. Experiments were carried out on rat medial vestibular nucleus cells in vitro using slices prepared from animals that had undergone unilateral labyrinthectomy (UL). There was a significant increase in the intrinsic excitability of medial vestibular nucleus cells in the rostral region of the ipsi-lesional nucleus within 4 h post-UL, which was sustained for the following week. These changes in intrinsic excitability of the medial vestibular nucleus neurones were abolished in animals that were not exposed to the secretion of stress hormones that normally occurs following UL. Histamine is also released in response to the stress associated with vestibular dysfunction. It is possible that the beneficial effects of betahistine on vestibular compensation are related to an interaction between histaminergic receptors activated by the parallel release of histamine and the activation of glucocorticoid receptors through the activation of the stress axis. Further study of the interactions between histamine receptors and the activation of the stress axis may be useful in understanding the effects of betahistine on vestibular plasticity.
Adaptation, Physiological↗
Immunohistochemical localization of gamma-aminobutyric acid- and aspartate-containing neurons in the guinea pig vestibular nuclei.
The immunohistochemical distributions of gamma-aminobutyric acid (GABA)- and aspartate-containing neurons were studied in the guinea pig vestibular nuclei using purified antisera to GABA and aspartate, respectively. Most GABA-containing neurons had small cell bodies and were scattered throughout all regions of the vestibular nuclei. The largest number of these cells was found in the medial nucleus. Intraventricular injection of colchicine markedly increased GABA-like immunoreactivity in these cell bodies. GABA-containing terminals were distributed throughout all 4 subdivisions of the nuclei, with the richest localization found around the floor of the fourth ventricle. Various sized aspartate-containing neurons were noted in the vestibular nuclei and small cells were present in the superior, medial and lateral nucleus. Medium-sized cells were observed throughout the vestibular nuclei. Giant cells in the lateral nucleus also contained aspartate and were surrounded by GABA-like immunoreactive terminals, thereby suggesting the modulation of aspartate-containing neurons by GABAergic fibers from Purkinje cells.
Animals↗
Comments to: S.D. Newlands and A.A. Perachio: Neuronal activity in the medial vestibular nuclei following unilateral labyrinthectomy.
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Animals↗
Projection of thalamic neurons to cat primary vestibular cortical fields studied by means of retrograde axonal transport of horseradish peroxidase.
The two vestibular cortical projection areas in the anterior suprasylvian sulcus and post-cruciate dimple regions were defined by evoked potential technique in anaesthetized cats. The thalamic location of neurons with axon terminals in these fields was determined using the method of retrograde axonal transport of horseradish peroxidase. The ascending vestibular pathway appeared to be separated also at the thalamic level, where cells in the ventroposterolateral nucleus were found to project to the post cruciate dimple and cells in the posterior nuclear group to the anterior suprasylvian vestibular cortical fields.
Afferent Pathways↗