Electrophysiological Study of Spatial Distribution of Vestibulospinal Neurons in the Frog Rana ridibunda

In experiments on a perfused brain preparation of the frog Rana ridibunda, the vestibulospinal neurons were identified, based on the excitatory postsynaptic potentials (EPSP) that appeared in response to an ipsilateral stimulation of the vestibular nerve and on the antidromic activity in response to stimulation of the cervical and lumbar enlargements of the spinal cord. The cells that could be antidromically activated only by stimulation of the cervical cord were designated as C-neurons. The cells that could be antidromically activated by stimulation of the lumbar cord were designated as L-neurons. The intracellular activity was recorded in 244 neurons of the vestibular nuclear complexes, out of which 127 cells (52%) were C-neurons and 117 (48%), L-neurons. The antidromic action potentials were recorded from the cells of lateral (143 neurons, 58.6%), descending (75 neurons, 30.7%), and medial (26 neurons, 10.6%) vestibular nuclei. The axon conduction velocity was determined to amount, on average, to 10.67 m/s for C-neurons and 15.84 m/s for L-neurons. In the vestibular nuclear complex, distribution of the fast and slow C- and L-neurons was studied. This study confirmed the previously made suggestion that C- and L-neurons of the frog, as sources of vestibular fibers, are distributed separately or, more often, as small groups, which leads to a patch-like somatotopy, rather than to formation of clearly separated fields.     

Morphological Study of Spatial Distribution of Vestibulospinal Neurons in the Frog Rana ridibunda

In the thew frog Rana ridibunda, local microphoretic injections of horseradish peroxidase into various parts of spinal cord were used for study of trajectory of retrograde enzyme-labeled fiber systems and topography of labeled neurons in vestibulospinal nuclei, the source of vestibulospinal fibers. The vestibulospinal tracts were shown to be formed by neurons of lateral vestibular nucleus, although descending vestibular nucleus also is partially involved, while medial vestibular nucleus contributes to even lesser degree. Besides, study of spatial distribution of C- and L-vestibulospinal neurons in the frog did not confirm the presence of the definite somatotopy that is characteristic of vestibular nuclei in mammals.     

Neuronal mechanisms of interaction of Deiters nucleus with the cerebral cortex.

The effects of stimulation of the vestibular nerve and five different cerebral cortex areas on the neuronal activity of the lateral vestibular nucleus of Deiters were studied. Stimulation of the cerebral cortex is shown to lead to antidromic and synaptic activation of Deiters neurons. The synaptic potentials of Deiters neurons evoked from the cerebral cortex were of mono- and polysynaptic origin. In particular, stimulation of the cerebral cortex evoked in Deiters neurons mono- and polysynaptic excitatory postsynaptic potentials. Collaterals of vestibulospinal neurons reaching different cortex fields as well as convergence of influences from these cortex fields on Deiters neurons were revealed. Inhibitory effects of the cerebral cortex on Deiters neurons were of polysynaptic origin and occurred rarely. The topical correlation between Deiters nucleus and different areas of the cerebral cortex was found. The peculiarities and functional significance of the effects obtained are discussed.     

Effect of vestibular,somatic, and autonomic afferent impulsation on vestibular nuclear unit activity in cats

Single unit responses in nuclei of the vestibular complex to stimulation of the labyrinths and of proprioceptive and autonomic afferents were investigated. Different types of unit responses were obtained to stimulation, including evoked activity consisting of a group of action potentials followed by inhibition of the spike discharge. Unit activity in the vestibular nuclei was shown to depend on extralabyrinthine stimulation. In response to adequate stimulation of the labyrinths by tilting the head, the role of receptors of muscles and joints in the neck was distinguished. The question of the somatotopic organization of the vestibular nuclei and convergence of various afferent flows on neurons giving rise to the vestibulospinal tract is discussed.Institute of Medico-Biological Problems, Ministry of Health of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 8, No. 5, pp. 507–513, September–October, 1976.     

Spatial organization of vestibulospinal neurons in the guinea pig

Quantitative characteristics of spatial organization of neuron populations of vestibular nuclei, forming projections into the spinal cord, were obtained in experiments on guinea pigs by the retrograde axonal transport of horseradish peroxidase, injected unilaterally into the upper cervical and lower thoracic segments of the spinal cord, method. Neurons accumulating the enzyme were found ipsilaterally in the lateral vestibular nucleus and bilaterally in the descending and medial vestibular nuclei. The distribution of vestibulospinal neurons along the length of the spinal cord was studied. Neuron populations of the medial and descending vestibular nuclei whose projection regions coincide with those of fibers of the corticospinal and rubrospinal systems were discovered. The role of vestibulospinal systems in the structure of supra-segmental control of the neuronal apparatus of the spinal cord is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 3, pp. 353–362, May–June, 1991.     

Otolith and semicircular canal inputs to single vestibular neurons in cats.

Researchers studied the convergence of the vertical posterior semicircular canal (PC), saccular nerves (SAC), utricular nerves (UT), and horizontal semicircular canal nerves (HC) on single vestibular neurons. The vestibular neurons were categorized by their innervating targets. Vestibular neurons were classified as vestibulospinal proper neurons (VS), vestibulo-ocular proper neurons (VO), vestibulo-oculo-spinal neurons sending axon collaterals to the extraocular motoneuron pools and spinal cord (VOS), and vestibular nucleus neurons without axons to the oculomotor nuclei or the spinal cord (V). Results indicate that the percentage of convergence of VS neurons was higher that that of neurons sending axons to the oculomotor nuclei (VO and VOS). They conclude that the convergence of canal and otolith inputs likely contributes mainly to vestibulospinal reflexes by sending inputs to the neck and other muscles during head inclination, which creates the combined stimuli of angular and linear acceleration.     

Canal and otolith inputs to single vestibular neurons in cats

Convergence of both afferents from the PC and saccular macula, and those from the PC and utricular macula on single vestibular neurons was noted by use of intercellular recording from vestibular neurons. Vestibular neurons were classified VO neurons (vestibulo-ocular proper neurons), VOS (Vestibulo-oculo-spinal neurons sending axon collaterals both to the extraocular motoneuron pools and to the spinal cord), VS neurons (vestibulospinal proper neurons) and V neurons (vestibular neurons without axons to the oculomotor nuclei or the spinal cord) on the basis of whether or not they responded antidromically to stimulation of the oculomotor nuclei and the spinal cord. Of the total 143 vestibular neurons recorded in the series of experiments on convergence of the PC and saccular afferents, 47 neurons (33%) were received inputs from both the PC and saccular nerves. Twenty-six of the 47 convergent neurons were identified as having the nature of VS neurons. Half (13/26) of those were activated monosynaptically from both the PC and saccular nerves. Only one saccular-activated neuron without PC inputs sent an axon to the oculomotor nuclei. In the other series of experiments on the convergence of the PC and utricular afferents, 41 (37%) of 111 vestibular neurons were proved to converge on inputs from both nerves. The majority (35/41) of the neurons received monosynaptic inputs from the PC nerve and polysynaptic EPSP-IPSP sequences from the utricular nerve, or vice versa. The ratio of PC-otolith convergent neurons among utricular-activated neurons (41/54, 76%) was higher than that among saccular activated neurons (47/88, 53%). The percentage of utricular alone neurons without PC inputs (13/111, 12%) was less than that of the saccular alone without PC inputs (41/145, 28%). In conclusion, the convergence of canal and otolith inputs likely contribute mainly to vestibulospinal reflexes including the vestibulocollic reflex, by sending inputs to the neck and other muscles during head inclination which creates the combined stimuli of angular and linear acceleration.     

Comparative analysis of vestibulospinal neuron sizes in the guinea pig

A comparison was made between dimensions of vestibular neurons labeled with horseradish peroxidase projecting to the spinal cord and cells stained with neutral red not differentiated into vestibulospinal and not forming descending projections. The cells in nondifferentiated areas of descending, medial and lateral vestibular nuclei include neurons of all sizes. In the caudorostral direction of the vestibular complex, the number of small and average neurons decreased and the number of large and gigantic neurons increased. The vestibulospinal populations included cells of average, large and gigantic size, and large and gigantic neurons were dominant. In the caudorostral direction, neurons of various sizes were distributed relatively evenly without forming differentiated groups.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 5, pp. 616–624, September–October, 1991.     

Antidromic and synaptic potentials evoked in neurons of the lateral vestibular nucleus by stimulation of the interstitial nucleus of Cajal and Darkshevich's nucleus in cats

Effects of stimulation of the interstitial nucleus of Cajal and Darkshevich's nucleus on unit activity in the lateral vestibular nucleus of Dieters were investigated in cats anesthetized with pentobarbital. Stimulation of the above-mentioned structures was shown to lead to antidromic and orthodromic activation of Dieters neurons. Axon collateral of vestibular neurons, ascending to the above-mentioned brain-stem structures were discovered electrophysiologically. Stimulation of the nuclei of Cajal and Darkshevich was shown to evoke mono- and polysynaptic EPSPs and IPSPs in neurons of Deiters nucleus. Convergence of influences from both nuclei on the neurons studied was demonstrated. The particular features and functional role of the influences observed are discussed.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 822–829, November–December, 1984.     

Corticofugal postsynaptic influences on red nucleus neurons

The responses of red nucleus neurons to stimulation of the sensorimotor cortex was studied on nembutal-anesthetized cats. Most of the rubrospinal neurons were identified according to their antidromic activation. Stimulation of the sensorimotor cortex was shown to evoke in the red nucleus neurons monosynaptic excitatory potentials with a latency of 1.85 msec, polysynaptic excitatory potentials (EPSP), and inhibitory postsynaptic potentials (IPSP) with a latency of 9–24 msec. The EPSP often produced spikes. The probability of generation of spreading excitation is greater with motor cortex stimulation. The monosynaptic EPSP are assumed to arise under the influence of the impulses arriving over the corticorubral neurons as a result of excitation of axodendritic synapses. The radial type of branching of red nucleus neurons facilitates the transition from electrotonically spreading local depolarization to an action potential triggered by the initial axonal segment. Polysynaptic EPSP and IPSP seem to be a result of activation of fast pyramidal neurons whose axon collaterals are connected via interneurons with the soma of the red nucleus neurons.L. A. Orbeli Institute of Physiology of the Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 3, No. 1, pp. 43–51, January–February, 1971.     

Identification of Neural Networks That Contribute to Motion Sickness through Principal Components Analysis of Fos Labeling Induced by Galvanic Vestibular Stimulation

Motion sickness is a complex condition that includes both overt signs (e.g., vomiting) and more covert symptoms (e.g., anxiety and foreboding). The neural pathways that mediate these signs and symptoms are yet to identified. This study mapped the distribution of c-fos protein (Fos)-like immunoreactivity elicited during a galvanic vestibular stimulation paradigm that is known to induce motion sickness in felines. A principal components analysis was used to identify networks of neurons activated during this stimulus paradigm from functional correlations between Fos labeling in different nuclei. This analysis identified five principal components (neural networks) that accounted for greater than 95% of the variance in Fos labeling. Two of the components were correlated with the severity of motion sickness symptoms, and likely participated in generating the overt signs of the condition. One of these networks included neurons in locus coeruleus, medial, inferior and lateral vestibular nuclei, lateral nucleus tractus solitarius, medial parabrachial nucleus and periaqueductal gray. The second included neurons in the superior vestibular nucleus, precerebellar nuclei, periaqueductal gray, and parabrachial nuclei, with weaker associations of raphe nuclei. Three additional components (networks) were also identified that were not correlated with the severity of motion sickness symptoms. These networks likely mediated the covert aspects of motion sickness, such as affective components. The identification of five statistically independent component networks associated with the development of motion sickness provides an opportunity to consider, in network activation dimensions, the complex progression of signs and symptoms that are precipitated in provocative environments. Similar methodology can be used to parse the neural networks that mediate other complex responses to environmental stimuli.     

Neuronal responses of the reticular and anterior ventral thalamic nuclei to stimulation of the thalamic ventrolateral nucleus and motor cortex

Responses of 137 neurons of the rostral pole of the reticular and anterior ventral thalamic nuclei to electrical stimulation of the ventrolateral nucleus and motor cortex were studied in 17 cats immobilized with D-tubocurarine. The number of neurons responding antidromically to stimulation of the ventrolateral nucleus was 10.5% of all cells tested (latent period of response 0.7–3.0 msec), whereas to stimulation of the motor cortex it was 11.0% (latent period of response 0.4–4.0 msec). Neurons with a dividing axon, one branch of which terminated in the thalamic ventrolateral nuclei, the other in the motor cortex, were found. Orthodromic excitation was observed in 78.9% of neurons tested during stimulation of the ventrolateral nucleus and in 52.5% of neurons during stimulation of the motor cortex. Altogether 55.6% of cells responded to stimulation of the ventrolateral nucleus with a discharge of 3 to 20 action potentials with a frequency of 130–350 Hz. Similar discharges in response to stimulation of the motor cortex were observed in 30.5% of neurons tested. An inhibitory response was recorded in only 6.8% of cells. Convergence of influences from the thalamic ventrolateral nucleus and motor cortex was observed in 55.7% of neurons. The corticofugal influence of the motor cortex on responses arising in these cells to testing stimulation of the ventrolateral nucleus could be either inhibitory or facilitatory.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 10, No. 5, pp. 460–468, September–October, 1978.     

Somatotopic organization of the vestibulospinal tract in the toad

The origin of the vestibulospinal projection in the toad has been investigated by using the method of the retrograde axonal transport of HRP injected at various levels of the spinal cord. The vestibulospinal projection, in this species, was found to be somatotopically organized, since neurons projecting to the cervical segments of the spinal cord were located within the rostromedial part of the ventral vestibular nucleus and those neurons projecting to the lumbosacral segments of the spinal cord were located within the caudolateral part of that nucleus. This pattern of organization of the vestibulospinal projection in amphibia is similar to that described in mammals and birds.     

Bilateral otolith contribution to spatial coding in the vestibular system

Recent work on the coding of spatial information in central otolith neurons has significantly advanced our knowledge of signal transformation from head-fixed otolith coordinates to space-centered coordinates during motion. In this review, emphasis is placed on the neural mechanisms by which signals generated at the bilateral labyrinths are recognized as gravity-dependent spatial information and in turn as substrate for otolithic reflexes. We first focus on the spatiotemporal neuronal response patterns (i.e. one- and two-dimensional neurons) to pure otolith stimulation, as assessed by single unit recording from the vestibular nucleus in labyrinth-intact animals. These spatiotemporal features are also analyzed in association with other electrophysiological properties to evaluate their role in the central construction of a spatial frame of reference in the otolith system. Data derived from animals with elimination of inputs from one labyrinth then provide evidence that during vestibular stimulation signals arising from a single utricle are operative at the level of both the ipsilateral and contralateral vestibular nuclei. Hemilabyrinthectomy also revealed neural asymmetries in spontaneous activity, response dynamics and spatial coding behavior between neuronal subpopulations on the two sides and as a result suggested a segregation of otolith signals reaching the ipsilateral and contralateral vestibular nuclei. Recent studies have confirmed and extended previous observations that the recovery of resting activity within the vestibular nuclear complex during vestibular compensation is related to changes in both intrinsic membrane properties and capacities to respond to extracellular factors. The bilateral imbalance provides the basis for deranged spatial coding and motor deficits accompanying hemilabyrinthectomy. Taken together, these experimental findings indicate that in the normal state converging inputs from bilateral vestibular labyrinths are essential to spatiotemporal signal transformation at the central otolith neurons during low-frequency head movements.     

Single unit responses of the reticular and ventral anterior nuclei of the thalamus to electrical stimulation of the centrum medianum

In acute experiments on cats anesthetized with thiopental (30–40 mg/kg, intraperitoneally) and immobilized with D-tubocurarine (1 mg/kg) responses of 145 neurons of the reticular and 158 neurons of the ventral anterior nuclei of the thalamus to electrical stimulation of the centrum medianum were investigated. An antidromic action potential appeared after a latent period of 0.3–2.0 msec in 4.1% of cells of the reticular nucleus and 4.4% of neurons of the ventral anterior nucleus tested in response to stimulation. The conduction velocity of antidromic excitation along axons of these neurons was 1.7–7.6 m/sec. Neurons responding with an antidromic action potential to stimulation both of the centrum medianum and of other formations were discovered, electrophysiological evidence of the ramification of such an axon. Altogether 53.8% of neurons of the reticular nucleus and 46.9% of neurons of the ventral anterior nucleus responded to stimulation of the centrum medianum by orthodromic excitation. Among neurons excited orthodromically two groups of cells were distinguished: The first group generated a discharge consisting of 6–12 action potentials with a frequency of 130–640 Hz (the duration of discharge did not exceed 60 msec), whereas the second responded with a single action potential. Inhibitory responses were observed in only 0.7% of neurons of the reticular nucleus and 4.4% of the ventral anterior nucleus tested. Afferent influences from the relay nuclei of the thalamus, lateral posterior nucleus, and motor cortex were shown to converge on neurons responding to stimulation of the centrum medianum.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 12, No. 1, pp. 36–45, January–February, 1980.     

Neuronal activity of the lateral vestibular nucleus of the guinea pig evoked by tilting the animal about the longitudinal axis during locomotion

In experiments on decerebrate guinea pigs, the impulse activity of neurons of the lateral vestibular nucleus evoked by tilting the animal about the longitudinal axis was investigated under conditions of spontaneous and mesencephalon stimulation-evoked locomotor activity. In most investigated neurons, locomotor activity led to changes in their responses to adequate vestibular stimulation. The dominant reaction was intensification of such responses, which was observed in almost all vestibulospinal neurons and in 2/3 of cells not having descending projections. Responses were suppressed only in 1/4 of the neurons not projecting to the spinal cord. The changes in the evoked responses had an amplitude character; the lag of the changes in the discharge frequency relative to the acceleration that caused them was constant. It is suggested that intensification of dynamic reactions of vestibular neurons during locomotion provides maintenance of the animal's equilibrium during movements in space by various gaits and along different trajectories.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 5, pp. 541–549, September–October, 1991.     

Time constants of vestibular nuclei neurons in the goldfish: A model with ocular proprioception

A simple model of the vestibular-ocular reflex with a proprioceptive eye velocity feedback loop is used to simulate recent data on the vestibular responses of neurons in the vestibular nuclei of spinal goldfish. The data support the hypothesis that a proprioceptive feedback loop elongates the vestibular nucleus time constant to equal that of the slow phase eye movements of vestibular nystagmus.     

Neuronal mechanisms of interaction between the red nucleus and other brain stem structures

Axon collaterals of rubrospinal neurons running to many brain stem structures were identified in acute experiments on cats by a technique of intracellular recording of antidromic action potentials in conjunction with collision testing. A systemic principle of organization of rubrospinal influences and also a tendency toward synchronous arrival of rubrospinal impulses at various brain stem centers were demonstrated. Most of these centers are relay nuclei, sending direct afferent projections to regions of the cerebellum which, in turn, control activity of the red nucleus. Besides such a loop, effecting dynamic cerebellar control over motor function, transmission of somatosensory information from nuclei of the dorsal columns of the spinal cord directly to the red nucleus was demonstrated. Special features of mono- and polysynaptic EPSPs evoked by stimulation of nuclei of the dorsal columns indicate that such PSPs arise in different regions of the soma-dendritic membrane of red nucleus neurons. The mechanisms of integration of descending motor volleys by the red nucleus are discussed.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 16, No. 5, pp. 665–678, September–October, 1984.     

Particle motion is broadly represented in the vestibular medulla of the bullfrog across larval development

In their shallow-water habitats, bullfrog (Rana catesbeiana) tadpoles are exposed to both underwater and airborne sources of acoustic stimulation. We probed the representation of underwater particle motion throughout the tadpole’s dorsal medulla to determine its spatial extent over larval life. Using neurobiotin-filled micropipettes, we recorded neural activity to z-axis particle motion (frequencies of 40–200 Hz) in the medial vestibular nucleus, lateral vestibular nucleus, dorsal medullary nucleus (DMN), and along the dorsal arcuate pathway. Sensitivity was comparable in the medial and lateral vestibular nuclei, with estimated thresholds between 0.016 and 12.5 μm displacement. Neither best responding frequency nor estimated threshold varied significantly over larval stage. Transport of neurobiotin from active recording sites was also stable over development. The DMN responded poorly to z-axis particle motion, but did respond to low-frequency pressure stimulation. These data suggest that particle motion is represented widely and stably in the tadpole’s vestibular medulla. This is in marked contrast to the representation of pressure stimulation in the auditory midbrain, where a transient “deaf period” of non-responsiveness and decreased connectivity occurs immediately prior to metamorphic climax. We suggest that, in bullfrogs, sensitivity to particle motion and to pressure follows different developmental trajectories.     

Effects of glutamate on the serotonin-induced responses of vestibular neurons

The aim of this work was to verify whether and how spontaneous or glutamate(GLU)-induced enhancements of the neuronal firing rate modified the responsiveness of the vestibular neurons to microiontophoretic application of serotonin (5-HT). During experiments performed on anaesthetized Wistar rats the responses to 5-HT applications were studied in neurons of the lateral vestibular nucleus identified by the antidromic activation upon stimulation of the vestibulospinal tract. The magnitude (in percent) of the 5-HT induced excitatory responses decreased (hyperbolic correlation, r = 0.91) when the background mean firing rate was enhanced spontaneously or by long-lasting application of GLU. Even in high-discharging units, the response never changed its sign. The trend to a depression of the response to 5-HT in function of the background discharge was observed when either the enhancement of firing occurred spontaneously and it was induced by an application of GLU, no significant difference (F-test) being found between the two cases. It is concluded that serotoninergic afferents can exert a strong control upon the vestibular neurons when the background activity is depressed, and only a weak influence when the neuronal firing is enhanced by other excitatory afferents. It remains to verify whether the type of interference observed between GLU and 5-HT is specific or can be also detected between 5-HT and other excitatory neuromediators.