Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse

2007 ◽  
Vol 98 (3) ◽  
pp. 1549-1565 ◽  
Author(s):  
M. Beraneck ◽  
K. E. Cullen

As a result of the availability of genetic mutant strains and development of noninvasive eye movements recording techniques, the mouse stands as a very interesting model for bridging the gap among behavioral responses, neuronal response dynamics studied in vivo, and cellular mechanisms investigated in vitro. Here we characterized the responses of individual neurons in the mouse vestibular nuclei during vestibular (horizontal whole body rotations) and full field visual stimulation. The majority of neurons (∼2/3) were sensitive to vestibular stimulation but not to eye movements. During the vestibular-ocular reflex (VOR), these neurons discharged in a manner comparable to the “vestibular only” (VO) neurons that have been previously described in primates. The remaining neurons [eye-movement-sensitive (ES) neurons] encoded both head-velocity and eye-position information during the VOR. When vestibular and visual stimulation were applied so that there was sensory conflict, the behavioral gain of the VOR was reduced. In turn, the modulation of sensitivity of VO neurons remained unaffected, whereas that of ES neurons was reduced. ES neurons were also modulated in response to full field visual stimulation that evoked the optokinetic reflex (OKR). Mouse VO neurons, however, unlike their primate counterpart, were not modulated during OKR. Taken together, our results show that the integration of visual and vestibular information in the mouse vestibular nucleus is limited to a subpopulation of neurons which likely supports gaze stabilization for both VOR and OKR.

2002 ◽  
Vol 88 (1) ◽  
pp. 13-28 ◽  
Author(s):  
Marko Huterer ◽  
Kathleen E. Cullen

For frequencies >10 Hz, the vestibuloocular reflex (VOR) has been primarily investigated during passive rotations of the head on the body in humans. These prior studies suggest that eye movements lag head movements, as predicted by a 7-ms delay in the VOR reflex pathways. However, Minor and colleagues recently applied whole-body rotations of frequencies ≤15 Hz in monkeys and found that eye movements were nearly in phase with head motion across all frequencies. The goal of the present study was to determine whether VOR response dynamics actually differ significantly for whole-body versus head-on-body rotations. To address this question, we evaluated the gain and phase of the VOR induced by high-frequency oscillations of the head on the body in monkeys by directly measuring both head and eye movements using the magnetic search coil technique. A torque motor was used to rotate the heads of three Rhesus monkeys over the frequency range 5–25 Hz. Peak head velocity was held constant, first at ±50°/s and then ±100°/s. The VOR was found to be essentially compensatory across all frequencies; gains were near unity (1.1 at 5 Hz vs. 1.2 at 25 Hz), and phase lag increased only slightly with frequency (from 2° at 5 Hz to 11° at 25 Hz, a marked contrast to the 63° lag at 25 Hz predicted by a 7-ms VOR latency). Furthermore, VOR response dynamics were comparable in darkness and when viewing a target and did not vary with peak velocity. Although monkeys offered less resistance to the initial cycles of applied head motion, the gain and phase of the VOR did not vary for early versus late cycles, suggesting that an efference copy of the motor command to the neck musculature did not alter VOR response dynamics. In addition, VOR dynamics were also probed by applying transient head perturbations with much greater accelerations (peak acceleration >15,000°/s2) than have been previously employed. The VOR latency was between 5 and 6 ms, and mean gain was close to unity for two of the three animals tested. A simple linear model well described the VOR responses elicited by sinusoidal and transient head on body rotations. We conclude that the VOR is compensatory over a wide frequency range in monkeys and has similar response dynamics during passive rotation of the head on body as during passive rotation of the whole body in space.


2003 ◽  
Vol 90 (2) ◽  
pp. 739-754 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Julia T. L. Choi ◽  
Kathleen E. Cullen

Burst-tonic (BT) neurons in the prepositus hypoglossi and adjacent medial vestibular nuclei are important elements of the neural integrator for horizontal eye movements. While the metrics of their discharges have been studied during conjugate saccades (where the eyes rotate with similar dynamics), their role during disjunctive saccades (where the eyes rotate with markedly different dynamics to account for differences in depths between saccadic targets) remains completely unexplored. In this report, we provide the first detailed quantification of the discharge dynamics of BT neurons during conjugate saccades, disjunctive saccades, and disjunctive fixation. We show that these neurons carry both significant eye position and eye velocity-related signals during conjugate saccades as well as smaller, yet important, “slide” and eye acceleration terms. Further, we demonstrate that a majority of BT neurons, during disjunctive fixation and disjunctive saccades, preferentially encode the position and the velocity of a single eye; only few BT neurons equally encode the movements of both eyes (i.e., have conjugate sensitivities). We argue that BT neurons in the nucleus prepositus hypoglossi/medial vestibular nucleus play an important role in the generation of unequal eye movements during disjunctive saccades, and carry appropriate information to shape the saccadic discharges of the abducens nucleus neurons to which they project.


1975 ◽  
Vol 38 (5) ◽  
pp. 1140-1161 ◽  
Author(s):  
A. F. Fuchs ◽  
J. Kimm

Single units were recorded from the vestibular nuclei of unanesthetized monkeys that were rotated in the horizontal plane while simultaneously pressing individual buttons in a controlled array which turned with hem. Using this behavioral paradigm, it was possible to 1) determine the relationship of unit discharge to eye movements measured by the DC-coupled electrooculogram and calibrated by the button-press task, and 2) determine the relationship of unit discharge to horizontal acceleration, either with or without the compensatory eye movements evoked by vestibular stimulation. Based on their responses during vestibular stimulation and/or eye movements, neurons in the vestibular nuclei (77% of our sample was in the medial nucleus) could be divided into four groups...


1988 ◽  
Vol 60 (5) ◽  
pp. 1753-1764 ◽  
Author(s):  
J. Kasper ◽  
R. H. Schor ◽  
V. J. Wilson

1. We have studied, in decerebrate cats, the responses of neurons in the lateral and descending vestibular nuclei to whole-body rotations in vertical planes that activated vertical semicircular canal and utricular receptors. Some neurons were identified as vestibulospinal by antidromic stimulation with floating electrodes placed in C4. 2. The direction of tilt that caused maximal excitation (response vector orientation) of each neuron was determined. Neuron dynamics were then studied with sinusoidal stimuli closely aligned with the response vector orientation, in the range 0.02-1 Hz. A few cells, for which we could not identify a response vector, probably had spatial-temporal convergence. 3. On the basis of dynamics, neurons were classified as receiving their input primarily from vertical semicircular canals, primarily from the otolith organs, or from canal+otolith convergence. 4. Response vector orientations of canal-driven neurons were often near +45 degrees or -45 degrees with respect to the transverse (roll) plane, suggesting these neurons received excitatory input from the ipsilateral anterior or posterior canal, respectively. Some neurons had canal-related dynamics but vector orientations near roll, presumably because they received convergent input from the ipsilateral anterior and posterior canals. Few neurons had their vectors near pitch. 5. In the lateral vestibular nucleus, neurons with otolith organ input (pure otolith or otolith+canal) tended to have vector orientations closer to roll than to pitch. In the descending nucleus the responses were evenly divided between the roll and pitch quadrants. 6. We conclude that most of our neurons have dynamics and response vector orientations that make them good candidates to participate in vestibulospinal reflexes acting on the limbs, but not those acting on the neck.


2016 ◽  
Vol 116 (4) ◽  
pp. 1785-1794 ◽  
Author(s):  
Andrew A. McCall ◽  
Derek M. Miller ◽  
William M. DeMayo ◽  
George H. Bourdages ◽  
Bill J. Yates

The limbs constitute the sole interface with the ground during most waking activities in mammalian species; it is therefore expected that somatosensory inputs from the limbs provide important information to the central nervous system for balance control. In the decerebrate cat model, the activity of a subset of neurons in the vestibular nuclei (VN) has been previously shown to be modulated by hindlimb movement. However, decerebration can profoundly alter the effects of sensory inputs on the activity of brain stem neurons, resulting in epiphenomenal responses. Thus, before this study, it was unclear whether and how somatosensory inputs from the limb affected the activity of VN neurons in conscious animals. We recorded brain stem neuronal activity in the conscious cat and characterized the responses of VN neurons to flexion and extension hindlimb movements and to whole body vertical tilts (vestibular stimulation). Among 96 VN neurons whose activity was modulated by vestibular stimulation, the firing rate of 65 neurons (67.7%) was also affected by passive hindlimb movement. VN neurons in conscious cats most commonly encoded hindlimb movement irrespective of the direction of movement ( n = 33, 50.8%), in that they responded to all flexion and extension movements of the limb. Other VN neurons overtly encoded information about the direction of hindlimb movement ( n = 27, 41.5%), and the remainder had more complex responses. These data confirm that hindlimb somatosensory and vestibular inputs converge onto VN neurons of the conscious cat, suggesting that VN neurons integrate somatosensory inputs from the limbs in computations that affect motor outflow to maintain balance.


1984 ◽  
Vol 51 (6) ◽  
pp. 1121-1136 ◽  
Author(s):  
R. D. Tomlinson ◽  
D. A. Robinson

The action potentials of single neurons were recorded extracellularly throughout the rostral vestibular nuclei and subadjacent reticular formation in three alert, juvenile, rhesus monkeys. Neuronal responses were tested during a) sinusoidal pitch oscillations in darkness, b) cancellation of the vestibuloocular reflex (VOR) during similar oscillations by fixation of a target moving with the head, c) sinusoidal vertical smooth pursuit, d) vertical saccades, and e) fixation with the head stationary. Eye movements were measured using the magnetic field-search coil technique. Of the 527 neurons isolated, 318 responded to pitch oscillation and/or vertical eye movements. The latter cells could be classified into six categories. Of this group, 273 cells were recorded from for sufficient time to allow them to be fully tested and form the basis of this report. Cells were classified as follows: pure-vestibular cells with firing rates modulated only by head velocity (15%), vestibular-pause cells that were similar to the pure-vestibular cells but paused for saccades in all directions (10%), gaze-velocity cells that modulated their rates in proportion to vertical eye velocity in space (7%), position cells with rates modulated by changes in eye position in the head but that did not burst or pause during saccades (33%), position-burst cells that also carried an eye-position signal but did burst during saccades in one direction and paused in the opposite direction (15%), and position-vestibular-pause cells that carried signals proportional to eye position in the head and head velocity and paused during all saccades (20%). Most cells that carried an eye-position signal also carried an eye-velocity signal during pursuit. Position and position-burst cells could be divided into two subcategories. Position cells that also reported head velocity represented 20% of the total sample, while those without head-velocity signals made up the remaining 13%. Position-burst cells were divided into two subcategories based on their behavior during pitch oscillation in darkness. Both carried eye-velocity signals during pursuit, but only one type (8% of the total sample) also carried an eye-velocity signal during vestibular eye movements in the dark, while the other (7%) did not. Some cells in all six categories except the pure-vestibular cells responded antidromically to stimulation of the medial longitudinal fasciculus (MLF). Only the position-vestibular-pause, position-burst, and gaze-velocity cells, however, were judged to be commonly antidromically activated, suggesting that these three cell types are the major contributors to the MLF from the rostral vestibular nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
pp. 1-16
Author(s):  
Alexander Yang Hui Xiang ◽  
Prashanna Khwaounjoo ◽  
Yusuf Ozgur Cakmak

BACKGROUND: Neural circuits allow whole-body yaw rotation to modulate vagal parasympathetic activity, which alters beat-to-beat variation in heart rate. The overall output of spinning direction, as well as vestibular-visual interactions on vagal activity still needs to be investigated. OBJECTIVE: This study investigated direction-dependent effects of visual and natural vestibular stimulation on two autonomic responses: heart rate variability (HRV) and pupil diameter. METHODS: Healthy human male subjects (n = 27) underwent constant whole-body yaw rotation with eyes open and closed in the clockwise (CW) and anticlockwise (ACW) directions, at 90°/s for two minutes. Subjects also viewed the same spinning environments on video in a VR headset. RESULTS: CW spinning significantly decreased parasympathetic vagal activity in all conditions (CW open p = 0.0048, CW closed p = 0.0151, CW VR p = 0.0019,), but not ACW spinning (ACW open p = 0.2068, ACW closed p = 0.7755, ACW VR p = 0.1775,) as indicated by an HRV metric, the root mean square of successive RR interval differences (RMSSD). There were no direction-dependent effects of constant spinning on sympathetic activity inferred through the HRV metrics, stress index (SI), sympathetic nervous system index (SNS index) and pupil diameter. Neuroplasticity in the CW eyes closed and CW VR conditions post stimulation was observed. CONCLUSIONS: Only one direction of yaw spinning, and visual flow caused vagal nerve neuromodulation and neuroplasticity, resulting in an inhibition of parasympathetic activity on the heart, to the same extent in either vestibular or visual stimulation. These results indicate that visual flow in VR can be used as a non-electrical method for vagus nerve inhibition without the need for body motion in the treatment of disorders with vagal overactivity. The findings are also important for VR and spinning chair based autonomic nervous system modulation protocols, and the effects of motion integrated VR.


1992 ◽  
Vol 68 (2) ◽  
pp. 471-484 ◽  
Author(s):  
R. Boyle ◽  
J. M. Goldberg ◽  
S. M. Highstein

1. A previous study measured the relative contributions made by regularly and irregularly discharging afferents to the monosynaptic vestibular nerve (Vi) input of individual secondary neurons located in and around the superior vestibular nucleus of barbiturate-anesthetized squirrel monkeys. Here, the analysis is extended to more caudal regions of the vestibular nuclei, which are a major source of both vestibuloocular and vestibulospinal pathways. As in the previous study, antidromic stimulation techniques are used to classify secondary neurons as oculomotor or spinal projecting. In addition, spinal-projecting neurons are distinguished by their descending pathways, their termination levels in the spinal cord, and their collateral projections to the IIIrd nucleus. 2. Monosynaptic excitatory postsynaptic potentials (EPSPs) were recorded intracellularly from secondary neurons as shocks of increasing strength were applied to Vi. Shocks were normalized in terms of the threshold (T) required to evoke field potentials in the vestibular nuclei. As shown previously, the relative contribution of irregular afferents to the total monosynaptic Vi input of each secondary neuron can be expressed as a %I index, the ratio (x100) of the relative sizes of the EPSPs evoked by shocks of 4 x T and 16 x T. 3. Antidromic stimulation was used to type secondary neurons as 1) medial vestibulospinal tract (MVST) cells projecting to spinal segments C1 or C6; 2) lateral vestibulospinal tract (LVST) cells projecting to C1, C6; or L1; 3) vestibulooculo-collic (VOC) cells projecting both to the IIIrd nucleus and by way of the MVST to C1 or C6; and 4) vestibuloocular (VOR) neurons projecting to the IIIrd nucleus but not to the spinal cord. Most of the neurons were located in the lateral vestibular nucleus (LV), including its dorsal (dLV) and ventral (vLV) divisions, and adjacent parts of the medial (MV) and descending nuclei (DV). Cells receiving quite different proportions of their direct inputs from regular and irregular afferents were intermingled in all regions explored. 4. LVST neurons are restricted to LV and DV and show a somatotopic organization. Those destined for the cervical and thoracic cord come from vLV, from a transition zone between vLV and DV, and to a lesser extent from dLV. Lumbar-projecting neurons are located more dorsally in dLV and more caudally in DV. MVST neurons reside in MV and in the vLV-DV transition zone.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (4) ◽  
pp. 1147-1156 ◽  
Author(s):  
R. H. Schor ◽  
I. Suzuki ◽  
S. J. Timerick ◽  
V. J. Wilson

The responses of interneurons in the cervical spinal cord of the decerebrate cat to whole-body tilt were studied with a goal of identifying spinal elements in the production of forelimb vestibular postural reflexes. Interneurons both in the cervical enlargement and at higher levels, from which propriospinal neurons have been identified, were examined, both in animals with intact labyrinths and in animals with nonfunctional semicircular canals (canal plugged). Most cervical interneurons responding to tilt respond best to rotations in vertical planes aligned within 30 degrees of the roll plane. Two to three times as many neurons are excited by side-up roll tilt as are excited by side-down roll. In cats with intact labyrinths, most responses have dynamics proportional either to (and in phase with) the position of the animal or to a sum of position and tilt velocity. This is consistent with input from both otolith organs and semicircular canals. In animals without functioning canals, the "velocity" response is absent. In a few cells (8 out of 76), a more complex response, characterized by an increasing gain and progressive phase lag, was observed. These response dynamics characterize the forelimb reflex in canal-plugged cats and have been previously observed in vestibular neurons in such preparations.


1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

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)


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