scholarly journals Tests of linearity in the responses of eye-movement-sensitive vestibular neurons to sinusoidal yaw rotation

2013 ◽  
Vol 109 (10) ◽  
pp. 2571-2584 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei

The rotational vestibulo-ocular reflex in primates is linear and stabilizes gaze in space over a large range of head movements. Best evidence suggests that position-vestibular-pause (PVP) and eye-head velocity (EHV) neurons in the vestibular nuclei are the primary mediators of vestibulo-ocular reflexes for rotational head movements, yet the linearity of these neurons has not been extensively tested. The current study was undertaken to understand how varying magnitudes of yaw rotation are coded in these neurons. Sixty-six PVP and 41 EHV neurons in the rostral vestibular nuclei of 7 awake rhesus macaques were recorded over a range of frequencies (0.1 to 2 Hz) and peak velocities (7.5 to 210°/s at 0.5 Hz). The sensitivity (gain) of the neurons decreased with increasing peak velocity of rotation for all PVP neurons and EHV neurons sensitive to ipsilateral rotation (type I). The sensitivity of contralateral rotation-sensitive (type II) EHV neurons did not significantly decrease with increasing peak velocity. These data show that, like non-eye-movement-related vestibular nuclear neurons that are believed to mediate nonlinear vestibular functions, PVP neurons involved in the linear vestibulo-ocular reflex also behave in a nonlinear fashion. Similar to other sensory nuclei, the magnitude of the vestibular stimulus is not linearly coded by the responses of vestibular neurons; rather, amplitude compression extends the dynamic range of PVP and type I EHV vestibular neurons.

1992 ◽  
Vol 2 (3) ◽  
pp. 193-212 ◽  
Author(s):  
G.R. Barnes ◽  
M.A. Grealy

Head and eye movements of human subjects have been recorded during head-free pursuit in the horizontal plane of a target executing sinusoidal motion at a frequency of 0.26 to 0.78 Hz and a peak velocity of ±96∘/s. The target was not presented continuously but was exposed for brief durations of 120 to 320 ms as it passed through the centre of the visual field at peak velocity. This technique allowed the timing of each response to be assessed in relation to the onset of target appearance. During the first 3 to 4 target presentations, there was a progressive buildup of both head velocity and the smooth component of gaze velocity, while, simultaneously, the responses became more phase-advanced with respect to target onset. In the steady state, similar temporal response trajectories were observed for head and gaze velocity, which were initiated approximately 500 ms prior to target on-set, rose to a peak that increased with the duration of target exposure, and then decayed with a time constant of 0.5 to 1 s. Whenever the target failed to appear as expected, the gaze and head velocity trajectories continued to be made, indicating that predictive suppression of the vestibulo-ocular reflex (VOR) was taking place in darkness. In a further experiment, subjects attempted to suppress the VOR during whole body oscillation at 0.2 or 0.4 Hz on a turntable by fixating, a head-fixed target that appeared for 10 to 160 ms at the time of peak head velocity. Again, VOR suppression was initiated prior to target appearance in the same manner as for natural head movements, and when the target suddenly disappeared but rotation continued, predictive VOR suppression was observed in darkness. The similarity of these predictive effects to those obtained previously for head-fixed pursuit provides further support for the hypothesis that both pursuit and visual suppression of the VOR are controlled primarily by identical visual feedback mechanisms.


1999 ◽  
Vol 82 (1) ◽  
pp. 436-449 ◽  
Author(s):  
Greg T. Gdowski ◽  
Robert A. McCrea

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20°/s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non–eye-movement ( n = 52) and eye-movement–related ( n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 ± 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement–related units tended to have rotational responses that were correlated with head velocity. On the other hand, non–eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.


2009 ◽  
Vol 102 (3) ◽  
pp. 1388-1397 ◽  
Author(s):  
Shawn D. Newlands ◽  
Nan Lin ◽  
Min Wei

Vestibular afferents display linear responses over a range of amplitudes and frequencies, but comparable data for central vestibular neurons are lacking. To examine the effect of stimulus frequency and magnitude on the response sensitivity and linearity of non-eye movement central vestibular neurons, we recorded from the vestibular nuclei in awake rhesus macaques during sinusoidal yaw rotation at frequencies between 0.1 and 2 Hz and between 7.5 and 210°/s peak velocity. The dynamics of the neurons' responses across frequencies, while holding peak velocity constant, was consistent with previous studies. However, as the peak velocity was varied, while holding the frequency constant, neurons demonstrated lower sensitivities with increasing peak velocity, even at the lowest peak velocities tested. With increasing peak velocity, the proportion of neurons that silenced during a portion of the response increased. However, the decrease in sensitivity of these neurons with higher peak velocities of rotation was not due to increased silencing during the inhibitory portion of the cycle. Rather the neurons displayed peak firing rates that did not increase in proportion to head velocity as the peak velocity of rotation increased. These data suggest that, unlike vestibular afferents, the central vestibular neurons without eye movement sensitivity examined in this study do not follow linear systems principles even at low velocities.


2006 ◽  
Vol 95 (4) ◽  
pp. 2530-2540 ◽  
Author(s):  
Hui Meng ◽  
Dora E. Angelaki

To stabilize objects of interest on the fovea during translation, vestibular-driven compensatory eye movements [translational vestibulo-ocular reflex (TVOR)] must scale with both target distance and eccentricity. To identify the neural correlates of these properties, we recorded from different groups of eye movement–sensitive neurons in the prepositus hypoglossi and vestibular nuclei of macaque monkeys during lateral and fore-aft displacements. All neuron types exhibited some increase in modulation amplitude as a function of target distance during high-frequency (4 Hz) lateral motion in darkness, with slopes that were correlated with the cell's pursuit gain, but not eye position sensitivity. Vergence angle dependence was largest for burst-tonic (BT) and contralateral eye-head (EH) neurons and smallest for ipsilateral EH and position-vestibular-pause (PVP) cells. On the other hand, the EH and PVP neurons with ipsilateral eye movement preferences exhibited the largest vergence-independent responses, which would be inappropriate to drive the TVOR. In addition to target distance, the TVOR also scales with target eccentricity, as evidenced during fore-aft motion, where eye velocity amplitude exhibits a “V-shaped ” dependence and phase shifts 180° for right versus left eye positions. Both the modulation amplitude and phase of BT and contralateral EH cells scaled with eye position, similar to the evoked eye movements during fore-aft motion. In contrast, the response modulation of ipsilateral EH and PVP cells during fore-aft motion was characterized by neither the V-shaped scaling nor the phase reversal. These results show that distinct premotor cell types carry neural signals that are appropriately scaled by vergence angle and eye position to generate the geometrically appropriate compensatory eye movements in the translational vestibulo-ocular reflex.


2017 ◽  
Vol 372 (1718) ◽  
pp. 20160199 ◽  
Author(s):  
D. S. Zee ◽  
P. Jareonsettasin ◽  
R. J. Leigh

A fundamental challenge to the brain is how to prevent intrusive movements when quiet is needed. Unwanted limb movements such as tremor impair fine motor control and unwanted eye drifts such as nystagmus impair vision. A stable platform is also necessary to launch accurate movements. Accordingly, nature has designed control systems with agonist (excitation) and antagonist (inhibition) muscle pairs functioning in push–pull, around a steady level of balanced tonic activity, the set-point . Sensory information can be organized similarly, as in the vestibulo-ocular reflex, which generates eye movements that compensate for head movements. The semicircular canals, working in coplanar pairs, one in each labyrinth, are reciprocally excited and inhibited as they transduce head rotations. The relative change in activity is relayed to the vestibular nuclei, which operate around a set-point of stable balanced activity. When a pathological imbalance occurs, producing unwanted nystagmus without head movement, an adaptive mechanism restores the proper set-point and eliminates the nystagmus. Here we used 90 min of continuous 7 T magnetic field labyrinthine stimulation (MVS) in normal humans to produce sustained nystagmus simulating vestibular imbalance. We identified multiple time-scale processes towards a new zero set-point showing that MVS is an excellent paradigm to investigate the neurobiology of set-point adaptation. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.


2021 ◽  
Vol 15 ◽  
Author(s):  
Tianwen Chen ◽  
Jun Huang ◽  
Yue Yu ◽  
Xuehui Tang ◽  
Chunming Zhang ◽  
...  

Vestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contributions to the VEMPs. To better understand the neural mechanisms underlying the VEMPs and develop discriminative VEMP protocols, we further examined sound-evoked responses of the vestibular nucleus neurons and the abducens neurons, which have the interneurons and motoneurons of the vestibulo-ocular reflex (VOR) pathways. Air-conducted clicks (50–80 dB SL re ABR threshold, 0.1 ms duration) or tone bursts (60–80 dB SL, 125–4,000 Hz, 8 ms plateau, 1 ms rise/fall) were delivered to the ears of Sprague-Dawley or Long-Evans rats. Among 425 vestibular nucleus neurons recorded in anesthetized rats and 18 abducens neurons recorded in awake rats, sound activated 35.9% of the vestibular neurons that increased discharge rates for ipsilateral head rotation (Type I neuron), 15.7% of the vestibular neurons that increased discharge rates for contralateral head rotation (Type II neuron), 57.2% of the vestibular neurons that did not change discharge rates during head rotation (non-canal neuron), and 38.9% of the abducens neurons. Sound sensitive vestibular nucleus neurons and abducens neurons exhibited characteristic tuning curves that reflected convergence of canal and otolith inputs in the VOR pathways. Tone bursts also evoked well-defined eye movements that increased with tone intensity and duration and exhibited peak frequency of ∼1,500 Hz. For the left eye, tone bursts evoked upward/rightward eye movements for ipsilateral stimulation, and downward/leftward eye movements for contralateral stimulation. These results demonstrate that sound stimulation results in activation of the canal and otolith VOR pathways that can be measured by eye tracking devices to develop discriminative tests of vestibular function in animal models and in humans.


2016 ◽  
Vol 116 (4) ◽  
pp. 1871-1884 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei ◽  
David Morgan ◽  
Hongge Luan

After vestibular labyrinth injury, behavioral measures of vestibular performance recover to variable degrees (vestibular compensation). Central neuronal responses after unilateral labyrinthectomy (UL), which eliminates both afferent resting activity and sensitivity to movement, have been well-studied. However, unilateral semicircular canal plugging (UCP), which attenuates angular-velocity detection while leaving afferent resting activity intact, has not been extensively studied. The current study reports response properties of yaw-sensitive non-eye-movement rhesus macaque vestibular neurons after compensation from UCP. The responses at a series of frequencies (0.1–2 Hz) and peak velocities (15–210°/s) were compared between neurons recorded before and at least 6 wk after UCP. The gain (sp/s/°/s) of central type I neurons (responding to ipsilateral yaw rotation) on the side of UCP was reduced relative to normal controls at 0.5 Hz, ±60°/s [0.48 ± 0.30 (SD) normal, 0.32 ± 0.15 ipsilesion; 0.44 ± 0.2 contralesion]. Type II neurons (responding to contralateral yaw rotation) after UCP have reduced gain (0.40 ± 0.27 normal, 0.35 ± 0.25 ipsilesion; 0.25 ± 0.18 contralesion). The difference between responses after UCP and after UL is primarily the distribution of type I and type II neurons in the vestibular nuclei (type I neurons comprise 66% in vestibular nuclei normally; 51% ipsilesion UCP; 59% contralesion UCP; 38% ipsilesion UL; 65% contralesion UL) and the magnitude of the responses of type II neurons ipsilateral to the lesion. These differences suggest that the need to compensate for unilateral loss of resting vestibular nerve activity after UL necessitates a different strategy for recovery of dynamic vestibular responses compared to after UCP.


1999 ◽  
Vol 9 (3) ◽  
pp. 163-172
Author(s):  
Bernard Cohen ◽  
Susan Wearne ◽  
Mingjia Dai ◽  
Theodore Raphan

During vestibular nystagmus, optokinetic nystagmus (OKN), and optokinetic afternystagmus (OKAN), the axis of eye rotation tends to align with the vector sum of linear accelerations acting on the head. This includes gravitational acceleration and the linear accelerations generated by translation and centrifugation. We define the summed vector of gravitational and linear accelerations as gravito-inertial acceleration (GIA) and designate the phenomenon of alignment as spatial orientation of the angular vestibuloocular reflex (aVOR). On the basis of studies in the monkey, we postulated that the spatial orientation of the aVOR is dependent on the slow (velocity storage) component of the aVOR, not on the short latency, compensatory aVOR component, which is in head-fixed coordinates. Experiments in which velocity storage was abolished by midline medullary section support this postulate. The velocity storage component of the aVOR is likely to be generated in the vestibular nuclei, and its spatial orientation was shown to be controlled through the nodulus and uvula of the vestibulo-cerebellum. Separate regions of the nodulus/uvula appear to affect the horizontal and vertical/torsional components of the response differently. Velocity storage is weaker in humans than in monkeys, but responds in a similar fashion in both species. We postulate that spatial orientation of the aVOR plays an important role in aligning gaze with the GIA and in maintaining balance during angular locomotion.


2018 ◽  
Vol 23 (5) ◽  
pp. 285-289 ◽  
Author(s):  
Patricia Castro ◽  
Sara Sena Esteves ◽  
Florencia Lerchundi ◽  
David Buckwell ◽  
Michael A. Gresty ◽  
...  

Gaze stabilization during head movements is provided by the vestibulo-ocular reflex (VOR). Clinical assessment of this reflex is performed using the video Head Impulse Test (vHIT). To date, the influence of different fixation distances on VOR gain using the vHIT has not been explored. We assessed the effect of target proximity on the horizontal VOR using the vHIT. Firstly, we assessed the VOR gain in 18 healthy subjects with 5 viewing target distances (150, 40, 30, 20, and 10 cm). The gain increased significantly as the viewing target distance decreased. A second experiment on 10 subjects was performed in darkness whilst the subjects were imagining targets at different distances. There were significant inverse relationships between gain and distance for both the real and the imaginary targets. There was a statistically significant difference between light and dark gains for the 20- and 40-cm distances, but not for the 150-cm distance. Theoretical VOR gains for different target distances were calculated and compared with those found in light and darkness. The increase in gain observed for near targets was lower than predicted by geometrical calculations, implying a physiological ceiling effect on the VOR. The VOR gain in the dark, as assessed with the vHIT, demonstrates an enhancement associated with a reduced target distance.


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