Eyes on Target: What Neurons Must do for the Vestibuloocular Reflex During Linear Motion

2004 ◽  
Vol 92 (1) ◽  
pp. 20-35 ◽  
Author(s):  
Dora E. Angelaki
Keyword(s):  
Sensory Information ◽  
Semicircular Canals ◽  
Linear Acceleration ◽  
Head Rotation ◽  
Oculomotor System ◽  
Eye Position ◽  
Otolith Organs ◽  
Vestibuloocular Reflex ◽  
Linear Motion ◽  
Gaze Stabilization

A gaze-stabilization reflex that has been conserved throughout evolution is the rotational vestibuloocular reflex (RVOR), which keeps images stable on the entire retina during head rotation. An ethological newer reflex, the translational or linear VOR (TVOR), provides fast foveal image stabilization during linear motion. Whereas the sensorimotor processing has been extensively studied in the RVOR, much less is currently known about the neural organization of the TVOR. Here we summarize the computational problems faced by the system and the potential solutions that might be used by brain stem and cerebellar neurons participating in the VORs. First and foremost, recent experimental and theoretical evidence has shown that, contrary to popular beliefs, the sensory signals driving the TVOR arise from both the otolith organs and the semicircular canals. Additional unresolved issues include a scaling by both eye position and vergence angle as well as the temporal transformation of linear acceleration signals into eye-position commands. Behavioral differences between the RVOR and TVOR, as well as distinct differences in neuroanatomical and neurophysiological properties, raise multiple functional questions and computational issues, only some of which are readily understood. In this review, we provide a summary of what is known about the functional properties and neural substrates for this oculomotor system and outline some specific hypotheses about how sensory information is centrally processed to create motor commands for the VORs.

Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum

2007 ◽  
Vol 98 (1) ◽  
pp. 295-302 ◽  
Author(s):  
Mark F. Walker ◽  
Jing Tian ◽  
David S. Zee
Keyword(s):  
Tilt Angle ◽  
Three Dimensional ◽  
Head Rotation ◽  
Normal Subjects ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Gaze Stabilization ◽  
Eye Rotation ◽  
Axis Rotation ◽  
Head Impulses

We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibuloocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, three-dimensional (3-D) eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200°/s2 to 40°/s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0°, ±15°) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations, the effect was not seen at the onset of head rotation when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed.

Human Horizontal Vestibulo-Ocular Reflex Initiation: Effects of Acceleration, Target Distance, and Unilateral Deafferentation

1998 ◽  
Vol 80 (3) ◽  
pp. 1151-1166 ◽  
Author(s):  
Benjamin T. Crane ◽  
Joseph L. Demer
Keyword(s):  
Semicircular Canals ◽  
Linear Acceleration ◽  
Head Rotation ◽  
Target Distance ◽  
Whole Body ◽  
Viewing Distance ◽  
Gaze Stabilization ◽  
Ocular Reflex ◽  
Acceleration Period ◽  
Vestibulo Ocular Reflex

Crane, Benjamin T. and Joseph L. Demer. Human horizontal vestibulo-ocular reflex initiation: effects of acceleration, target distance, and unilateral deafferentation. J. Neurophysiol. 80: 1151–1166, 1998. The vestibulo-ocular reflex (VOR) generates compensatory eye movements in response to angular and linear acceleration sensed by semicircular canals and otoliths respectively. Gaze stabilization demands that responses to linear acceleration be adjusted for viewing distance. This study in humans determined the transient dynamics of VOR initiation during angular and linear acceleration, modification of the VOR by viewing distance, and the effect of unilateral deafferentation. Combinations of unpredictable transient angular and linear head rotation were created by whole body yaw rotation about eccentric axes: 10 cm anterior to eyes, centered between eyes, centered between otoliths, and 20 cm posterior to eyes. Subjects viewed a target 500, 30, or 15 cm away that was extinguished immediately before rotation. There were four stimulus intensities up to a maximum peak acceleration of 2,800°/s2. The normal initial VOR response began 7–10 ms after onset of head rotation. Response gain (eye velocity/head velocity) for near as compared with distant targets was increased as early as 1–11 ms after onset of eye movement; this initial effect was independent of linear acceleration. An otolith mediated effect modified VOR gain depending on both linear acceleration and target distance beginning 25–90 ms after onset of head rotation. For rotational axes anterior to the otoliths, VOR gain for the nearest target was initially higher but later became less than that for the far target. There was no gain correction for the physical separation between the eyes and otoliths. With lower acceleration, there was a nonlinear reduction in the early gain increase with close targets although later otolith-mediated effects were not affected. In subjects with unilateral vestibular deafferentation, the initial VOR was quantitatively normal for rotation toward the intact side. When rotating toward the deafferented side, VOR gain remained less than half of normal for at least the initial 55 ms when head acceleration was highest and was not modulated by target distance. After this initial high acceleration period, gain increased to a degree depending on target distance and axis eccentricity. This behavior suggests that the commissural VOR pathways are not modulated by target distance. These results suggest that the VOR is initially driven by short latency ipsilateral target distance dependent and bilateral target-distance independent canal pathways. After 25 ms, otolith inputs contribute to the target distance dependent pathway. The otolith input later grows to eventually dominate the target distance mediated effect. When otolith input is unavailable the target distance mediated canal component persists. Modulation of canal mediated responses by target distance is a nonlinear effect, most evident for high head accelerations.

Neural Processing of Gravito-Inertial Cues in Humans. IV. Influence of Visual Rotational Cues During Roll Optokinetic Stimuli

2003 ◽  
Vol 89 (1) ◽  
pp. 390-400 ◽  
Author(s):  
L. H. Zupan ◽  
D. M. Merfeld
Keyword(s):  
Visual Cues ◽  
Gravitational Force ◽  
Sensory Information ◽  
Inertial Force ◽  
Linear Acceleration ◽  
Otolith Organs ◽  
Optokinetic Stimulation ◽  
The Difference ◽  
The Right ◽  
Roll Tilt

Sensory systems often provide ambiguous information. For example, otolith organs measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. However, according to Einstein's equivalence principle, a change in gravitational force due to tilt is indistinguishable from a change in inertial force due to translation. Therefore the central nervous system (CNS) must use other sensory cues to distinguish tilt from translation. For example, the CNS might use dynamic visual cues indicating rotation to help determine the orientation of gravity (tilt). This, in turn, might influence the neural processes that estimate linear acceleration, since the CNS might estimate gravity and linear acceleration such that the difference between these estimates matches the measured GIF. Depending on specific sensory information inflow, inaccurate estimates of gravity and linear acceleration can occur. Specifically, we predict that illusory tilt caused by roll optokinetic cues should lead to a horizontal vestibuloocular reflex compensatory for an interaural estimate of linear acceleration, even in the absence of actual linear acceleration. To investigate these predictions, we measured eye movements binocularly using infrared video methods in 17 subjects during and after optokinetic stimulation about the subject's nasooccipital (roll) axis (60°/s, clockwise or counterclockwise). The optokinetic stimulation was applied for 60 s followed by 30 s in darkness. We simultaneously measured subjective roll tilt using a somatosensory bar. Each subject was tested in three different orientations: upright, pitched forward 10°, and pitched backward 10°. Five subjects reported significant subjective roll tilt (>10°) in directions consistent with the direction of the optokinetic stimulation. In addition to torsional optokinetic nystagmus and afternystagmus, we measured a horizontal nystagmus to the right during and following clockwise (CW) stimulation and to the left during and following counterclockwise (CCW) stimulation. These measurements match predictions that subjective tilt in the absence of real tilt should induce a nonzero estimate of interaural linear acceleration and, therefore, a horizontal eye response. Furthermore, as predicted, the horizontal response in the dark was larger for Tilters ( n = 5) than for Non-Tilters ( n= 12).

scholarly journals Contribution of intravestibular sensory conflict to motion sickness and dizziness in migraine disorders

2016 ◽  
Vol 116 (4) ◽  
pp. 1586-1591 ◽  
Author(s):  
Joanne Wang ◽  
Richard F. Lewis
Keyword(s):  
Motion Sickness ◽  
Semicircular Canals ◽  
Inverse Correlation ◽  
Normal Subjects ◽  
Otolith Organs ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Sensory Conflict ◽  
Velocity Signal ◽  
Episodic Vertigo

Migraine is associated with enhanced motion sickness susceptibility and can cause episodic vertigo [vestibular migraine (VM)], but the mechanisms relating migraine to these vestibular symptoms remain uncertain. We tested the hypothesis that the central integration of rotational cues (from the semicircular canals) and gravitational cues (from the otolith organs) is abnormal in migraine patients. A postrotational tilt paradigm generated a conflict between canal cues (which indicate the head is rotating) and otolith cues (which indicate the head is tilted and stationary), and eye movements were measured to quantify two behaviors that are thought to minimize this conflict: suppression and reorientation of the central angular velocity signal, evidenced by attenuation (“dumping”) of the vestibuloocular reflex and shifting of the rotational axis of the vestibuloocular reflex toward the earth vertical. We found that normal and migraine subjects, but not VM patients, displayed an inverse correlation between the extent of dumping and the size of the axis shift such that the net “conflict resolution” mediated through these two mechanisms approached an optimal value and that the residual sensory conflict in VM patients (but not migraine or normal subjects) correlated with motion sickness susceptibility. Our findings suggest that the brain normally controls the dynamic and spatial characteristics of central vestibular signals to minimize intravestibular sensory conflict and that this process is disrupted in VM, which may be responsible for the enhance motion intolerance and episodic vertigo that characterize this disorder.

Oculomotor Control of Primary Eye Position Discriminates Between Translation and Tilt

1999 ◽  
Vol 81 (1) ◽  
pp. 394-398 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki
Keyword(s):  
Dynamic Control ◽  
Linear Acceleration ◽  
Oculomotor System ◽  
Oculomotor Control ◽  
Eye Position ◽  
Axis Orientation ◽  
Fast Phase ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

Hess, Bernhard J. M. and Dora E. Angelaki. Oculomotor control of primary eye position discriminates between translation and tilt. J. Neurophysiol. 81: 394–398, 1999. We have previously shown that fast phase axis orientation and primary eye position in rhesus monkeys are dynamically controlled by otolith signals during head rotations that involve a reorientation of the head relative to gravity. Because of the inherent ambiguity associated with primary otolith afferent coding of linear accelerations during head translation and tilts, a similar organization might also underlie the vestibulo-ocular reflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from gravity in the dynamic control of primary eye position has been investigated here by comparing the eye movements elicited by sinusoidal lateral and fore-aft oscillations (0.5 Hz ± 40 cm, equivalent to ± 0.4 g) with those during yaw rotations (180°/s) about a vertically tilted axis (23.6°). We found a significant modulation of primary eye position as a function of linear acceleration (gravity) during rotation but not during lateral and fore-aft translation. This modulation was enhanced during the initial phase of rotation when there was concomitant semicircular canal input. These findings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechanisms that discriminate between gravity and translational head acceleration.

scholarly journals Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques

2018 ◽  
Vol 119 (1) ◽  
pp. 73-83 ◽  
Author(s):  
Shawn D. Newlands ◽  
Ben Abbatematteo ◽  
Min Wei ◽  
Laurel H. Carney ◽  
Hongge Luan
Keyword(s):  
Eye Movement ◽  
Multisensory Integration ◽  
Vestibular Nucleus ◽  
Semicircular Canals ◽  
Linear Acceleration ◽  
Vestibular Nuclei ◽  
Otolith Organs ◽  
Angular Rotation ◽  
Sensory Signals ◽  
Nonlinear Integration

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.

Role of Muscle Pulleys in Producing Eye Position-Dependence in the Angular Vestibuloocular Reflex: A Model-Based Study

2000 ◽  
Vol 84 (2) ◽  
pp. 639-650 ◽  
Author(s):  
Matthew J. Thurtell ◽  
Mikhail Kunin ◽  
Theodore Raphan
Keyword(s):  
Initial Period ◽  
Semicircular Canals ◽  
Pulse Signal ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Primary Position ◽  
Head Velocity ◽  
Model Based ◽  
Head Impulses ◽  
Eye Velocity

It is well established that the head and eye velocity axes do not always align during compensatory vestibular slow phases. It has been shown that the eye velocity axis systematically tilts away from the head velocity axis in a manner that is dependent on eye-in-head position. The mechanisms responsible for producing these axis tilts are unclear. In this model-based study, we aimed to determine whether muscle pulleys could be involved in bringing about these phenomena. The model presented incorporates semicircular canals, central vestibular pathways, and an ocular motor plant with pulleys. The pulleys were modeled so that they brought about a rotation of the torque axes of the extraocular muscles that was a fraction of the angle of eye deviation from primary position. The degree to which the pulleys rotated the torque axes was altered by means of a pulley coefficient. Model input was head velocity and initial eye position data from passive and active yaw head impulses with fixation at 0°, 20° up and 20° down, obtained from a previous experiment. The optimal pulley coefficient required to fit the data was determined by calculating the mean square error between data and model predictions of torsional eye velocity. For active head impulses, the optimal pulley coefficient varied considerably between subjects. The median optimal pulley coefficient was found to be 0.5, the pulley coefficient required for producing saccades that perfectly obey Listing's law when using a two-dimensional saccadic pulse signal. The model predicted the direction of the axis tilts observed in response to passive head impulses from 50 ms after onset. During passive head impulses, the median optimal pulley coefficient was found to be 0.21, when roll gain was fixed at 0.7. The model did not accurately predict the alignment of the eye and head velocity axes that was observed early in the response to passive head impulses. We found that this alignment could be well predicted if the roll gain of the angular vestibuloocular reflex was modified during the initial period of the response, while pulley coefficient was maintained at 0.5. Hence a roll gain modification allows stabilization of the retinal image without requiring a change in the pulley effect. Our results therefore indicate that the eye position–dependent velocity axis tilts could arise due to the effects of the pulleys and that a roll gain modification in the central vestibular structures may be responsible for countering the pulley effect.

Sympathetic nerve activity during natural stimulation of horizontal semicircular canals in humans

1998 ◽  
Vol 275 (4) ◽  
pp. R1274-R1278 ◽  
Author(s):  
Chester A. Ray ◽  
Keith M. Hume ◽  
Samuel L. Steele
Keyword(s):  
Sympathetic Nerve ◽  
Sympathetic Nerve Activity ◽  
Semicircular Canals ◽  
Head Rotation ◽  
Otolith Organs ◽  
Nerve Activity ◽  
Natural Stimulation ◽  
Vascular Beds ◽  
Static Head ◽  
Stimulation Of

We have shown that static head-down neck flexion elicits increases in muscle (MSNA) but not skin sympathetic nerve activity (SSNA) in humans. These findings suggest that stimulation of the otolith organs causes differential sympathetic outflow to vascular beds. The purpose of the present study was to determine whether yaw head rotation (YHR), which stimulates the horizontal semicircular canals, elicits sympathetic nerve responses. To test this question, we recorded MSNA ( n = 33) and SSNA ( n = 25) before and during 3 min of sinusoidal YHR performed at 0.1, 0.6, and 1.0 Hz. At all frequencies, YHR elicited no significant changes in heart rate and mean arterial pressure. Likewise, YHR did not significantly change either MSNA or SSNA at all frequencies. Our results indicate that stimulation of the horizontal semicircular canals by YHR does not alter SNA to either muscle or skin. Moreover, these results provide evidence to support the concept that the otolith organs but not the horizontal semicircular canals participate in the regulation of SNA in humans.

scholarly journals The effect of binocular eye position and head rotation plane on the human torsional vestibuloocular reflex

2006 ◽  
Vol 46 (16) ◽  
pp. 2475-2486 ◽  
Author(s):  
Americo A. Migliaccio ◽  
Charles C. Della Santina ◽  
John P. Carey ◽  
Lloyd B. Minor ◽  
David S. Zee
Keyword(s):  
Head Rotation ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Rotation Plane

Neural Processing of Gravito-Inertial Cues in Humans. I. Influence of the Semicircular Canals Following Post-Rotatory Tilt

2000 ◽  
Vol 84 (4) ◽  
pp. 2001-2015 ◽  
Author(s):  
L. H. Zupan ◽  
R. J. Peterka ◽  
D. M. Merfeld
Keyword(s):  
Eye Movements ◽  
Information Integration ◽  
Constant Velocity ◽  
Gravitational Force ◽  
Inertial Force ◽  
Semicircular Canals ◽  
Linear Acceleration ◽  
Head Orientation ◽  
Otolith Organs ◽  
Sensory Cues

Sensory systems often provide ambiguous information. Integration of various sensory cues is required for the CNS to resolve sensory ambiguity and elicit appropriate responses. The vestibular system includes two types of sensors: the semicircular canals, which measure head rotation, and the otolith organs, which measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. According to Einstein's equivalence principle, gravitational force is indistinguishable from inertial force due to linear acceleration. As a consequence, otolith measurements must be supplemented with other sensory information for the CNS to distinguish tilt from translation. The GIF resolution hypothesis states that the CNS estimates gravity and linear acceleration, so that the difference between estimates of gravity and linear acceleration matches the measured GIF. Both otolith and semicircular canal cues influence this estimation of gravity and linear acceleration. The GIF resolution hypothesis predicts that inaccurate estimates of both gravity and linear acceleration can occur due to central interactions of sensory cues. The existence of specific patterns of vestibuloocular reflexes (VOR) related to these inaccurate estimates can be used to test the GIF resolution hypothesis. To investigate this hypothesis, we measured eye movements during two different protocols. In one experiment, eight subjects were rotated at a constant velocity about an earth-vertical axis and then tilted 90° in darkness to one of eight different evenly spaced final orientations, a so-called “dumping” protocol. Three speeds (200, 100, and 50°/s) and two directions, clockwise (CW) and counterclockwise (CCW), of rotation were tested. In another experiment, four subjects were rotated at a constant velocity (200°/s, CW and CCW) about an earth-horizontal axis and stopped in two different final orientations (nose-up and nose-down), a so-called “barbecue” protocol. The GIF resolution hypothesis predicts that post-rotatory horizontal VOR eye movements for both protocols should include an “induced” VOR component, compensatory to an interaural estimate of linear acceleration, even though no true interaural linear acceleration is present. The GIF resolution hypothesis accurately predicted VOR and induced VOR dependence on rotation direction, rotation speed, and head orientation. Alternative hypotheses stating that frequency segregation may discriminate tilt from translation or that the post-rotatory VOR time constant is dependent on head orientation with respect to the GIF direction did not predict the observed VOR for either experimental protocol.

Sign in / Sign up

Export Citation Format

Share Document