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PubMed1998

Analysis and neural network modeling of the nonlinear correlates of habituation in the vestibulo-ocular reflex.

Through the process of habituation, continued exposure to low-frequency (0.01 Hz) rotation in the dark produced suppression of the low-frequency response of the vestibulo-ocular reflex (VOR) in goldfish. The response did not decay gradually, as might be expected from an error-driven learning process, but displayed several nonlinear and nonstationary features. They included asymmetrical response suppression, magnitude-dependent suppression for lower- but not higher-magnitude head rotations, and abrupt-onset suppressions suggestive of a switching mechanism. Microinjection of lidocaine into the vestibulocerebellum of habituated goldfish resulted in a temporary dishabituation. This suggests that the vestibulocerebellum mediates habituation, presumably through Purkinje cell inhibition of vestibular nuclei neurons. The habituated VOR data were simulated with a feed-forward, nonlinear neural network model of the VOR in which only Purkinje cell inhibition of vestibular nuclei neurons was varied. The model suggests that Purkinje cell inhibition may switch in to introduce nonstationarities, and cause asymmetry and magnitude-dependency in the VOR to emerge from the essential nonlinearity of vestibular nuclei neurons.

Animals↗
PubMed1982

The origin of efferent labyrinthine fibres: a comparative study in vertebrates.

Parent cells of efferent acoustic and efferent vestibular fibers were determined anatomically in all classes of vertebrates by use of retrograde axonal transport of horseradish peroxidase. These neurons were found in the brainstem, in particular in the reticular formation. In the goldfish, efferent labyrinthine neurons could be demonstrated in a medial position (lateral to the fasciculus longitudinalis medialis). In the frog, efferent neurons appeared more lateral, dorsomedial to the facial motor nucleus. In reptiles and birds, efferent acoustic neurons separate from efferent vestibular neurons. In mammals, efferent vestibular neurons are located more dorsally, lateral to the genu of the facial nerve. Efferent acoustic neurons take their origin from the superior olivary complex.

Alligators and Crocodiles↗
PubMed1999

Otolith processing in the deep cerebellar nuclei.

To investigate the otolith contribution to the responses of "vestibular only" neurons in the rostral fastigial nucleus (FN), single-unit activity was recorded in the alert monkey with the head fixed during static and dynamic stimulation (+/- 15 deg, 0.06-1.4 Hz) around an earth-fixed horizontal axis. Head orientation could be altered allowing for roll, pitch, and intermediate planes of orientation. For the vast majority of neurons a response vector orientation (RVO) with an optimal response and a null-response at a head orientation 90 deg apart could be determined. Presumably more than 30% of the vestibular only neurons had an otolith input, as indicated by responses to static tilt, head-position-related activity, large phase changes (> 100 deg) of neuronal activity between 0.06 and 1.4 Hz, changes of the RVO at different frequencies and complex responses (spatio-temporal convergence). Thus, neurons in FN reflecting an otolith or a combined canal-otolith input are much more common than up to now thought. Vestibular-only neurons are most likely involved in vestibulospinal mechanisms. Their precise functional role has yet to be determined.

Animals↗
PubMed2003

Vestibular input to brain monoamine neurons--a review.

Yates et al. reported that serotonergic RN neurons are associated with vestibulo-sympathetic responses and may control BP changes during body repositioning (Yates et al., 1992; 1993). Pompeiano et al. demonstrated that LC-NA neurons participate in the postural control and modify the vestibulo-spinal reflex (Pompeiano et al., 1990; 1991a; 2001). Nishiike et al. (1996a) examined the effects of caloric vestibular stimulation on the neuronal activity of LC-NA neurons in rats. The predominant effect of CA with both hot- and cold-water on the electrical activity of LC neurons is inhibitory and persists for several minutes. GABAA receptors located on the postsynaptic membrane of LC neurons are responsible for these inhibitory responses. The VLM may inhibit LC neuronal activity in response to the CA via GABAA receptors (Nishiike et al., 1997). It is suggested that LC-NA inhibition is involved in the development of motion sickness (Nishiike et al., 2001).

Animals↗
PubMed2004

Vestibulo-reticular projections in adult lamprey: their role in locomotion.

This study describes the anatomical projections from vestibular secondary neurons to reticulospinal neurons in the adult lamprey and the modulation of vestibular inputs during fictive locomotion. Anatomical tracers were applied in the posterior (PRRN) and middle rhombencephalic reticular nuclei as well as to the proximal stumps of cut vestibular nerve branches to identify the neurons projecting to the reticular nuclei that were in close proximity with vestibular primary afferents. Labeled neurons were found in the intermediate (ION) and posterior (PON) octavomotor nuclei, and were more numerous on the side of the injection (around 56-87 and 101-107 for the ION and the PON, respectively). Morphologies varied but cells were mostly round or oval. Axonal projections from the PON formed a dense bundle, whereas those from the ION were less densely packed. Based on their morphology and the distribution of their projections, most vestibulo-reticular neurons were presumed to be vestibulospinal cells. Reticulospinal cells from the PRRN were recorded intracellularly in the in vitro brainstem-spinal cord preparation and large excitatory post-synaptic potentials (EPSPs) were evoked following stimulation of the ipsilateral anterior and the contralateral posterior branches of the vestibular nerves, whereas inhibitory post-synaptic potentials (IPSPs) or smaller EPSPs were elicited by stimulation of the ipsilateral posterior or of the contralateral anterior branches. During fictive locomotion, both the excitatory and the inhibitory responses displayed phasic changes in amplitude such that the amplitude of the EPSPs was minimal when the spinal cord activity switched from the ipsilateral to the contralateral side of the recorded reticulospinal cell. The IPSPs were then of maximal amplitude. We propose that this modulation could serve to reduce the influence of vestibular inputs in response to head movements during locomotion.

Animals↗
PubMed1993

Electrophysiological and pharmacological characterization of vestibular inputs to identified frog abducens motoneurons and internuclear neurons in vitro.

Synaptic vestibular inputs of antidromically identified motoneurons and internuclear neurons in the abducens nucleus were studied electrophysiologically and pharmacologically in the isolated brain of grass frogs (Rana temporaria). The prevailing response pattern of abducens motoneurons (AbMOT) following stimulation of the VIIIth nerve was crossed disynaptic excitation and uncrossed disynaptic inhibition. A few AbMOT (five of 46), however, exhibited uncrossed excitation instead of inhibition. Abducens internuclear neurons (AbINT), identified by antidromic activation following stimulation of the contralateral medial longitudinal fascicle, exhibited disynaptic response patterns to stimulation of the VIIIth nerve that were very similar in latency and rise time to those of AbMOT except for the absence of uncrossed disynaptic inhibition. Bath application of strychnine (50 microM), a glycine antagonist, blocked the uncrossed inhibitory vestibular input to AbMOT and AbINT completely and reversibly, whereas picrotoxin (100 microM), a GABA (gamma-aminobutyric acid) antagonist, had no detectable effect on these disynaptic potentials. These results suggest glycine as the transmitter of inhibitory vestibular projections onto AbMOT and AbINT. The pharmacology of the excitatory vestibular input of these neurons was studied by electrical stimulation of the vestibular nuclear complex. Crossed monosynaptic excitatory inputs in AbMOT and AbINT were blocked completely by CNQX (6-cyano-7-nitroquinoxaline-2,3-dione) (10 microM), an antagonist of AMPA (alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) receptors, indicating glutamatergic excitation. Comparison of these results with those in the cat suggests the presence of a basic horizontal vestibulo-ocular reflex that is very similarly organized, and corroborates the hypothesis that major behavioural differences in the performance of compensatory eye movements between species result from the properties of supplementary networks and not from differences in a common 'three-neuron' vestibulo-ocular arc.

Abducens Nerve↗
PubMed1996

Transneuronal pathways to the vestibulocerebellum.

The alpha-herpes virus (pseudorabies, PRV) was used to observe central nervous system (CNS) pathways associated with the vestibulocerebellar system. Retrograde transneuronal migration of alpha-herpes virions from specific lobules of the gerbil and rat vestibulo-cerebellar cortex was detected immunohistochemically. Using a time series analysis, progression of infection along polyneuronal cerebellar afferent pathways was examined. Pressure injections of > 20 nanoliters of a 10(8) plaque forming units (pfu) per ml solution of virus were sufficient to initiate an infectious locus which resulted in labeled neurons in the inferior olivary subnuclei, vestibular nuclei, and their afferent cell groups in a progressive temporal fashion and in growing complexity with increasing incubation time. We show that climbing fibers and some other cerebellar afferent fibers transported the virus retrogradely from the cerebellum within 24 hours. One to three days after cerebellar infection discrete cell groups were labeled and appropriate laterality within crossed projections was preserved. Subsequent nuclei labeled with PRV after infection of the flocculus/paraflocculus, or nodulus/uvula, included the following: vestibular (e.g., z) and inferior olivary nuclei (e.g., dorsal cap), accessory oculomotor (e.g., Darkschewitsch n.) and accessory optic related nuclei, (e.g., the nucleus of the optic tract, and the medial terminal nucleus); noradrenergic, raphe, and reticular cell groups (e.g., locus coeruleus, dorsal raphe, raphe pontis, and the lateral reticular tract); other vestibulocerebellum sites, the periaqueductal gray, substantia nigra, hippocampus, thalamus and hypothalamus, amygdala, septal nuclei, and the frontal, cingulate, entorhinal, perirhinal, and insular cortices. However, there were differences in the resulting labeling between infection in either region. Double-labeling experiments revealed that vestibular efferent neurons are located adjacent to, but are not included among, flocculus-projecting supragenual neurons. PRV transport from the vestibular labyrinth and cervical muscles also resulted in CNS infections. Virus propagation in situ provides specific connectivity information based on the functional transport across synapses. The findings support and extend anatomical data regarding vestibulo-olivo-cerebellar pathways.

Animals↗
PubMed1996

Visual potentiation of vestibular responses in lamprey reticulospinal neurons.

The lamprey normally swims with the dorsal side up. Illumination of one eye shifts the set-point of the vestibular roll control system, however, so that the animal swims with a roll tilt towards the source of light (the dorsal light response). A tilted orientation is often maintained for up to 1 min after the stimulation. In present study, the basis for this behaviour was investigated at the neuronal level. The middle rhombencephalic reticular nucleus (MRRN) is considered a main nucleus for the control of roll orientation in lampreys. Practically all MRRN neurons receive vestibular and visual input and project to the spinal cord. Earlier extracellular experiments had shown that optic nerve stimulation potentiates the response to vestibular stimulation in the ipsilateral MRRN. This most likely represents a neural correlate of the dorsal light response. Experiments were carried out in vitro on the isolated brainstem of the silver lamprey (Ichthyomyzon unicuspis). MRRN cells were recorded intracellularly, and the overall activity of descending systems was monitored with bilateral extracellular electrodes. The responses to 10 Hz optic nerve stimulation and 1 Hz vestibular nerve stimulation, and the influence of optic nerve stimulation on the vestibular responses, were investigated. In most preparations, optic nerve stimulation excited practically all ipsilateral MRRN cells. After stimulation, the cell was typically depolarized and showed an increased level of synaptic noise for up to 80 s. In contralateral MRRN neurons, optic nerve stimulation usually evoked hyperpolarization or no response. Vestibular nerve stimulation evoked compound excitatory postsynaptic potentials (EPSPs) or spikes in approximately 90% of the cells, both ipsilaterally and contralaterally. A smaller subpopulation of MRRN cells (approximately 10%) received vestibular inhibition. In 26 of 48 recorded MRRN cells, the response to vestibular stimulation was potentiated after ipsilateral optic nerve stimulation. The potentiation was seen in cells receiving either excitatory or inhibitory vestibular input as an increase in EPSP amplitude/spiking (85%) and a decrease in inhibitory postsynaptic potential amplitude (15%) respectively. In most cases the vestibular responses did not return to control levels during the testing period (10-30 min), and thus the visual stimulation most likely induced long-lasting changes in the functional connectivity of the role control network, in addition to the short-lasting afteractivity. In four of the 11 cells recorded contralateral to the stimulated optic nerve, a depression of the vestibular response could be seen. In potentiated cells, single vestibular pulses often evoked longer episodes of large synaptic noise and sometimes spiking. In the latter case, the action potentials appeared with highly variable latency after each stimulation pulse. This indicates that an important mechanism underlying the potentiation may be a long-lasting increase in excitability in a pool of unidentified interneurons located either upstream of the MRRN cells, relaying vestibular and visual inputs, or downstream, providing positive feedback.

Animals↗
PubMed1993

Immunocytochemical localization of substance P and neurofilament proteins in the guinea pig vestibular ganglion.

To examine the cytochemical features of primary vestibular afferent neurons, we examined the immunocytochemical distribution of substance P(SP) and neurofilament proteins (NFP) in the guinea pig vestibular endorgans and ganglion. 84.9% of vestibular ganglion cells showed SP-like immunoreactivity. SP immunoreactive cells were small in diameter (25.4 microns), and randomly distributed in the ganglia. NFP immunoreactive cells (34.2%) were relatively large in diameter (31.1 microns). By double-staining immunocytochemistry it was possible to distinguish three different cell types: SP-positive/NFP-negative, SP-negative/NFP-positive, and SP/NFP-positive vestibular ganglion cells. Vestibular ganglion cells can thus be classified on the basis of size and immunocytochemical characteristics. These chemically distinct subpopulations of vestibular ganglion cells may be an indication of functional differences within vestibular afferent neurons.

Animals↗
PubMed2004

Signal processing in the vestibular system during active versus passive head movements.

In everyday life, vestibular receptors are activated by both self-generated and externally applied head movements. Traditionally, it has been assumed that the vestibular system reliably encodes head-in-space motion throughout our daily activities and that subsequent processing by upstream cerebellar and cortical pathways is required to transform this information into the reference frames required for voluntary behaviors. However, recent studies have radically changed the way we view the vestibular system. In particular, the results of recent single-unit studies in head-unrestrained monkeys have shown that the vestibular system provides the CNS with more than an estimate of head motion. This review first considers how head-in-space velocity is processed at the level of the vestibular afferents and vestibular nuclei during active versus passive head movements. While vestibular information appears to be similarly processed by vestibular afferents during passive and active motion, it is differentially processed at the level of the vestibular nuclei. For example, one class of neurons in vestibular nuclei, which receives direct inputs from semicircular canal afferents, is substantially less responsive to active head movements than to passively applied head rotations. The projection patterns of these neurons strongly suggest that they are involved in generating head-stabilization responses as well as shaping vestibular information for the computation of spatial orientation. In contrast, a second class of neurons in the vestibular nuclei that mediate the vestibuloocular reflex process vestibular information in a manner that depends principally on the subject's current gaze strategy rather than whether the head movement was self-generated or externally applied. The implications of these results are then discussed in relation to the status of vestibular reflexes (i.e., the vestibuloocular, vestibulocollic, and cervicoocular reflexes) and implications for higher-level processing of vestibular information during active head movements.

Afferent Pathways↗
PubMed1975

Physiologic characteristics of vestibular first-order canal neurons in the cat. II. Response to constant angular acceleration.

The physiologic response of first-order vestibular canal neurons, recorded within the internal auditory canal with glass microelectrodes, was studied in anesthetized cats. Neurons from all three canals were subjected to velocity trapezoidal rotations about the canal axis, and about different axes extending up to 90 degrees on either side of the canal axis in "roll" and 30 degrees on either side of "pitch." Each cell examined exhibited a spontaneous discharge and responded to constant angular acceleration in a fashion predictable from the direction of the in-plane acceleration vector and the known receptor hair cell polarization. Under conditions of prolonged constant acceleration, (5 degrees/s2 for 40 s) about 30% of the units which could be classified showed adaptation, 55% did not, and 14%, termed reverse adapting cells, demonstrated a fast rise followed by a slower, continual increase during stimulation. Secondary responses (undershoot or overshoot) were noted in most adapting neurons, but were absent in the reverse adapting group. Adapting neurons were distinguished from the nonadapting group by significantly lower resting rates, more irregular interspike-interval distributions, and greater sensitivity to acceleration. When compared with nonadapting neurons, reverse adapting cells had higher spontaneous rates, less irregular spike intervals, and higher sensitivities. The mean canal sensitivity to angular acceleration for all cells was 2 spikes . s-1/deg . s-2 (range 0.3-7.4 spikes . s-1/deg . s-2). Significant differences in mean sensitivity values between canal neurons were demonstrated, with those from the anterior being the most sensitive, followed by the posterior and horizontal canals, respectively. Time constants for all canals governing the transitory rise (or fall) in rate with constant acceleration averaged 3.8 s. Small differences in mean values were noted between canals but these were not significant. Incremental time constants were found to be slightly but significantly longer (mean = 3.9 s) than decremental time constants (mean = 3.6 s). Some cells showed different tine constants to many trials of one stimulus as well as to different levels of stimulus. Most canal unitary responses were approximately linearly related to stimulus magnitudes over the range of 2-18 degrees/s2. This being the case, the angle between the canal plane and plane of stimulus become the main determinant in the first-order neural response. Here, a linear cosine relationship descriged the three-dimentionsal unitary response curve: maximum canal response was elicited with rotation about the canal axis, while no response was evoked with rotation about an axis approximately 90 degrees to canal axis. Between these two extremes, the response of a cell was determined by the cosine of the angle between the canala axis and the axis of rotation.

Acceleration↗
PubMed2002

Modifications of vestibular responses of individual reticulospinal neurons in lamprey caused by unilateral labyrinthectomy.

A postural control system in the lamprey is driven by vestibular input and maintains the dorsal-side-up orientation of the animal during swimming. After a unilateral labyrinthectomy (UL), the lamprey continuously rolls toward the damaged side. Normally, a recovery of postural equilibrium ("vestibular compensation") takes about 1 mo. However, illumination of the eye contralateral to UL results in an immediate and reversible restoration of equilibrium. Here we used eye illumination as a tool to examine a functional recovery of the postural network. Important elements of this network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections to the spinal cord. In this study, we characterized modifications of the vestibular responses in individual RS neurons caused by UL and the effect exerted on these responses by eye illumination. The activity of RS neurons was recorded from their axons in the spinal cord by chronically implanted electrodes, and spikes in individual axons were extracted from the population activity signals. The same neurons were recorded both before and after UL. Vestibular stimulation (rotation in the roll plane through 360 degrees ) and eye illumination were performed in quiescent animals. It was found that the vestibular responses on the UL-side changed only slightly, whereas the responses on the opposite side disappeared almost completely. This asymmetry in the bilateral activity of RS neurons is the most likely cause for the loss of equilibrium in UL animals. Illumination of the eye contralateral to UL resulted, first, in a restoration of vestibular responses in the neurons inactivated by UL and in an appearance of vestibular responses in some other neurons that did not respond to vestibular input before UL. These responses had directional sensitivity and zones of spatial sensitivity similar to those observed before UL. However, their magnitude was smaller than before UL. Second, the eye illumination caused a reduction of the magnitude of vestibular responses on the UL side. These two factors tend to restore symmetry in bilateral activity of RS neurons, which is the most likely cause for the recovery of equilibrium in the swimming UL lamprey. Results of this study are discussed in relation to the model of the roll control system proposed in our previous studies as well as in relation to the vestibular compensation.

Action Potentials↗
PubMed2003

Vestibular signals of posterior parietal cortex neurons during active and passive head movements in macaque monkeys.

The posterior parietal cortex may function as an interface between sensory and motor cortices and thus could be involved in the formation of motor plans as well as abstract representations of space. We have recorded from neurons in the intraparietal sulcus, namely, the ventral and medial intraparietal areas (VIP and MIP, respectively), and analyzed their head-movement-related signals in relation to passive and active movements. To generate active head movements, we made the animals track a moving fixation spot in the horizontal plane under head-free conditions. When under certain circumstances the animals were tracking the fixation spot almost exclusively via head movements, a clear correlation between neuronal firing rate and head movement could be established. Furthermore, a newly employed paradigm, the "replay method," made available direct comparison of neuronal firing behavior under active and passive movement conditions. In such case, the animals were allowed to make spontaneous head movements in darkness. Subsequently, the heads were fixed and the previously recorded active head-movement profile was reproduced by a turntable as passive stimulation. Neuronal responses ranged from total extinction of the vestibular signal during active movement to presence of activity only during active movement. Furthermore, in approximately one-third of the neurons, a change of vestibular on-direction depending on active versus passive movement mode was observed, that is, type I neurons became type II neurons, etc. We suggest that the role of parietal vestibular neurons has to be sought in sensory space representation rather than reflex behavior and motor control contexts.

Animals↗