Eye Movements During Multi-Axis Whole-Body Rotations

2003 ◽  
Vol 89 (1) ◽  
pp. 355-366 ◽  
Author(s):  
Christopher J. Bockisch ◽  
Dominik Straumann ◽  
Thomas Haslwanter
Keyword(s):  
Eye Movements ◽  
Rotation Axis ◽  
Human Subjects ◽  
Whole Body ◽  
Velocity Storage ◽  
Head Orientation ◽  
Otolith Organs ◽  
Velocity Signal ◽  
Eye Velocity ◽  
Cue Conflict

The semi-circular canals and the otolith organs both contribute to gaze stabilization during head movement. We investigated how these sensory signals interact when they provide conflicting information about head orientation in space. Human subjects were reoriented 90° in pitch or roll during long-duration, constant-velocity rotation about the earth-vertical axis while we measured three-dimensional eye movements. After the reorientation, the otoliths correctly indicated the static orientation of the subject with respect to gravity, while the semicircular canals provided a strong signal of rotation. This rotation signal from the canals could only be consistent with a static orientation with respect to gravity if the rotation-axis indicated by the canals was exactly parallel to gravity. This was not true, so a cue-conflict existed. These conflicting stimuli elicited motion sickness and a complex tumbling sensation. Strong horizontal, vertical, and/or torsional eye movements were also induced, allowing us to study the influence of the conflict between the otoliths and the canals on all three eye-movement components. We found a shortening of the horizontal and vertical time constants of the decay of nystagmus and a trend for an increase in peak velocity following reorientation. The dumping of the velocity storage occurred regardless of whether eye velocity along that axis was compensatory to the head rotation or not. We found a trend for the axis of eye velocity to reorient to make the head-velocity signal from the canals consistent with the head-orientation signal from the otoliths, but this reorientation was small and only observed when subjects were tilted to upright. Previous models of canal-otolith interaction could not fully account for our data, particularly the decreased time constant of the decay of nystagmus. We present a model with a mechanism that reduces the velocity-storage component in the presence of a strong cue-conflict. Our study, supported by other experiments, also indicates that static otolith signals exhibit considerably smaller effects on eye movements in humans than in monkeys.

Role of the Cerebellar Flocculus Region in the Coordination of Eye and Head Movements During Gaze Pursuit

2000 ◽  
Vol 84 (3) ◽  
pp. 1614-1626 ◽  
Author(s):  
Timothy Belton ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Head Movements ◽  
Whole Body ◽  
Head Tracking ◽  
Smooth Pursuit Eye Movements ◽  
Body Rotation ◽  
Pursuit Eye Movements ◽  
Smooth Tracking ◽  
Eye Velocity

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive (≈43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.

scholarly journals Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects

2015 ◽  
Vol 113 (10) ◽  
pp. 3866-3892 ◽  
Author(s):  
James O. Phillips ◽  
Leo Ling ◽  
Kaibao Nie ◽  
Elyse Jameyson ◽  
Christopher M. Phillips ◽  
...  
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Human Subjects ◽  
Vestibular Function ◽  
Slow Phase ◽  
Vestibular Loss ◽  
Stimulation Current ◽  
Eye Velocity ◽  
Over Time ◽  
Stimulation Of

Animal experiments and limited data in humans suggest that electrical stimulation of the vestibular end organs could be used to treat loss of vestibular function. In this paper we demonstrate that canal-specific two-dimensionally (2D) measured eye velocities are elicited from intermittent brief 2 s biphasic pulse electrical stimulation in four human subjects implanted with a vestibular prosthesis. The 2D measured direction of the slow phase eye movements changed with the canal stimulated. Increasing pulse current over a 0–400 μA range typically produced a monotonic increase in slow phase eye velocity. The responses decremented or in some cases fluctuated over time in most implanted canals but could be partially restored by changing the return path of the stimulation current. Implantation of the device in Meniere's patients produced hearing and vestibular loss in the implanted ear. Electrical stimulation was well tolerated, producing no sensation of pain, nausea, or auditory percept with stimulation that elicited robust eye movements. There were changes in slow phase eye velocity with current and over time, and changes in electrically evoked compound action potentials produced by stimulation and recorded with the implanted device. Perceived rotation in subjects was consistent with the slow phase eye movements in direction and scaled with stimulation current in magnitude. These results suggest that electrical stimulation of the vestibular end organ in human subjects provided controlled vestibular inputs over time, but in Meniere's patients this apparently came at the cost of hearing and vestibular function in the implanted ear.

Rotation Axes of the Head During Positioning, Head Shaking, and Locomotion

2007 ◽  
Vol 98 (5) ◽  
pp. 3095-3108 ◽  
Author(s):  
Mikhail Kunin ◽  
Yasuhiro Osaki ◽  
Bernard Cohen ◽  
Theodore Raphan
Keyword(s):  
Rotation Axis ◽  
Human Subjects ◽  
Head Orientation ◽  
Pivot Point ◽  
Rotation Axes ◽  
Static Head ◽  
Head Positions ◽  
Occipital Condyles ◽  
Digital Human ◽  
Incremental Rotation

Static head orientations obey Donders’ law and are postulated to be rotations constrained by a Fick gimbal. Head oscillations can be voluntary or generated during natural locomotion. Whether the rotation axes of the voluntary oscillations or during locomotion are constrained by the same gimbal is unknown and is the subject of this study. Head orientation was monitored with an Optotrak (Northern Digital). Human subjects viewed visual targets wearing pin-hole goggles to achieve static head positions with the eyes centered in the orbit. Incremental rotation axes were determined for pitch and yaw by computing the velocity vectors during head oscillation and during locomotion at 1.5 m/s on a treadmill. Static head orientation could be described by a generalization of the Fick gimbal by having the axis of the second rotation rotate by a fraction, k, of the angle of the first rotation without a third rotation. We have designated this as a k-gimbal system. Incremental rotation axes for both pitch and yaw oscillations were functions of the pitch but not the yaw head positions. The pivot point for head oscillations was close to the midpoint of the interaural line. During locomotion, however, the pivot point was considerably lower. These findings are well explained by an implementation of the k-gimbal model, which has a rotation axis superimposed on a Fick-gimbal system. This could be realized physiologically by the head interface with the dens and occipital condyles during head oscillation with a contribution of the lower spine to pitch during locomotion.

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.

Bilateral Vestibular Neurectomy for Treatment of Vertigo

1993 ◽  
Vol 109 (1) ◽  
pp. 101-107 ◽  
Author(s):  
Andreas BÖhmer ◽  
Ugo Fisch
Keyword(s):  
Eye Movements ◽  
Vestibular Function ◽  
Nerve Fibers ◽  
The Other ◽  
Whole Body ◽  
Velocity Storage ◽  
Body Rotation ◽  
Vestibular Neurectomy ◽  
Storage Mechanism ◽  
Subtotal Petrosectomy

The effects of bilateral vestibular neurectomy on equilibrium and vestibular function were clinically evaluated in two patients more than 15 years after surgery. Both patients had bilateral Ménière's disease and their vertiginous spells were permanently resolved after the second vestibular neurectomy. Symptoms of disequilibrium were absent in one patient and mild in the other. Reflexive horizontal eye movements on whole body rotation in darkness were absent on low angular accelerations (2°/s2), but could be elicited with angular accelerations of 20°/s2 or higher. Extravestlbular cues generating these eye movements seemed to be unlikely because a “control” patient with complete peripheral vestibular ablation after bilateral subtotal petrosectomy did not present reflexive eye movements under the same stimulus paradigms. An incomplete deafferentiation of the vestibular end organ (rather than regeneration of vestibular nerve fibers) and a consecutive Impairment of the central velocity storage mechanism may explain the good functional outcome in our bilateral neurectomized patients.

Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys

2002 ◽  
Vol 88 (5) ◽  
pp. 2445-2462 ◽  
Author(s):  
Keisuke Kushiro ◽  
Mingjia Dai ◽  
Mikhail Kunin ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
...  
Keyword(s):  
Eye Movements ◽  
Vertical Axis ◽  
Velocity Storage ◽  
Eye Position ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Time Constants ◽  
Head Velocity ◽  
Axis Rotation ◽  
Eye Velocity

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.

Discharge properties of morphologically identified vestibular neurons recorded during horizontal eye movements in the goldfish

2019 ◽  
Vol 121 (5) ◽  
pp. 1865-1878 ◽  
Author(s):  
A. M. Pastor ◽  
P. M. Calvo ◽  
R. R. de la Cruz ◽  
R. Baker ◽  
H. Straka
Keyword(s):  
Eye Movements ◽  
Velocity Storage ◽  
Slow Phase ◽  
Eye Position ◽  
Type I ◽  
Abducens Nucleus ◽  
Ancestral Condition ◽  
Vestibular Neurons ◽  
Prepositus Hypoglossi ◽  
Eye Velocity

Computational capability and connectivity are key elements for understanding how central vestibular neurons contribute to gaze-stabilizing eye movements during self-motion. In the well-characterized and segmentally distributed hindbrain oculomotor network of goldfish, we determined afferent and efferent connections along with discharge patterns of descending octaval nucleus (DO) neurons during different eye motions. Based on activity correlated with horizontal eye and head movements, DO neurons were categorized into two complementary groups that either increased discharge during both contraversive (type II) eye (e) and ipsiversive (type I) head (h) movements (eIIhI) or vice versa (eIhII). Matching time courses of slow-phase eye velocity and corresponding firing rates during prolonged visual and head rotation suggested direct causality in generating extraocular motor commands. The axons of the dominant eIIhI subgroup projected either ipsi- or contralaterally and terminated in the abducens nucleus, Area II, and Area I with additional recurrent collaterals of ipsilaterally projecting neurons within the parent nucleus. Distinct feedforward commissural pathways between bilateral DO neurons likely contribute to the generation of eye velocity signals in eIhII cells. The shared contribution of DO and Area II neurons to eye velocity storage likely represents an ancestral condition in goldfish that is clearly at variance with the task separation between mammalian medial vestibular and prepositus hypoglossi neurons. This difference in signal processing between fish and mammals might correlate with a larger repertoire of visuo-vestibular-driven eye movements in the latter species that potentially required a shift in sensitivity and connectivity within the hindbrain-cerebello-oculomotor network. NEW & NOTEWORTHY We describe the structure and function of neurons within the goldfish descending octaval nucleus. Our findings indicate that eye and head velocity signals are processed by vestibular and Area II velocity storage integrator circuitries whereas the velocity-to-position Area I neural integrator generates eye position solely. This ancestral condition differs from that of mammals, in which vestibular neurons generally lack eye position signals that are processed and stored within the nucleus prepositus hypoglossi.

Dynamic properties of medial rectus motoneurons during vergence eye movements

1992 ◽  
Vol 67 (1) ◽  
pp. 64-74 ◽  
Author(s):  
P. D. Gamlin ◽  
L. E. Mays
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Smooth Pursuit ◽  
Dynamic Properties ◽  
Medial Rectus ◽  
Velocity Signal ◽  
Velocity Sensitivity ◽  
The Difference ◽  
Eye Velocity ◽  
The Relationship

1. An early study by Keller reported that medial rectus motoneurons display a step change in firing rate during accommodative vergence movements. However, a later study by Mays and Porter reported gradual changes in firing rate during symmetrical vergence movements. Furthermore, subsequent inspection of the activity of individual medial rectus motoneurons during vergence movements indicated transient changes in their firing rate that had not been noted by Mays and Porter. For conjugate eye movements, in addition to a position signal, motoneurons display an eye velocity signal that compensates for the characteristics of the oculomotor plant. This suggested that the transient change in firing rate seen during vergence movements represented a velocity signal. Therefore the present study used single-unit recording techniques in alert rhesus monkeys to examine the dynamic behavior of medial rectus motoneurons during vergence eye movements. 2. The relationship between firing rate and eye velocity was first studied for vergence responses to step changes in binocular disparity and accommodative demand. Inspection of single trials showed that medial rectus motoneurons display transient changes in firing rate during vergence eye movements. To better visualize the dynamic signal during vergence movements, an expected firing rate (eye position multiplied by position sensitivity of the cell plus its baseline firing rate) was subtracted from the actual firing rate to yield a difference firing rate, which was displayed along with the eye velocity trace for individual trials. During all smooth symmetrical vergence movements, the profile of the difference firing rate very closely resembled the velocity profile. 3. To quantify the relationship between eye velocity and firing rate, two approaches were taken. In one, peak eye velocity was plotted against the difference firing rate. This plot yielded a measure of the velocity sensitivity of the cell (prv). In the other, a scatter plot was produced in which horizontal eye velocity throughout the vergence eye movement was plotted against the difference firing rate. This plot yielded a second measure of the velocity sensitivity of the cell (rv). 4. The behavior of 10 cells was studied during both sinusoidal vergence tracking and conjugate smooth pursuit over a range of frequencies from 0.125 to 1.0 Hz. This enabled the frequency sensitivity of the medial rectus motoneurons to be assessed for both types of movements. Both vergence velocity sensitivity and smooth pursuit velocity sensitivity decreased with increasing frequency. This is similar to a finding by Fuchs and co-workers for lateral rectus motoneurons during smooth pursuit eye movements.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals A displacement and velocity based dual model of saccadic eye movements best explains kinematic variability

2020 ◽  
Author(s):  
V Varsha ◽  
Radhakant Padhi ◽  
Aditya Murthy
Keyword(s):  
Eye Movements ◽  
Human Subjects ◽  
Saccadic Eye Movements ◽  
Behavioral Variability ◽  
Dual Model ◽  
Dual Control ◽  
Deterministic Models ◽  
Velocity Signal ◽  
Neural Recordings ◽  
Velocity Information

Noise is a ubiquitous component of motor systems which leads to behavioral variability of all types of movements, including saccadic eye movements. Nonetheless, systems-based models of saccadic eye movements are deterministic and do not explain the observed saccade variability, only their central tendencies. Using stochastic models, we studied the variability in saccade behavior to test and distinguish between previously proposed deterministic saccade models. For this, the inter-trial variability in saccade displacement trajectories of human subjects was quantified while they performed repeated saccadic eye movements to a peripheral target. Based on fits to the data, we showed that existing models based on either displacement or velocity failed to capture the observed patterns in the variability of saccade trajectories. However, the observed behavior was captured by a dual control system, using a combination of displacement and velocity signal. The proposed model fits the mean displacement trajectory as well as the existing deterministic models. Taken together, our results suggest that the saccade system uses both desired displacement and velocity information.New and NoteworthyWe studied saccade behavior with a focus on the variability of the saccade trajectory. A stochastic model of the saccade system suggests that a dual control involving the control of displacement and velocity explains saccade behavior better than previously proposed models that utilize only displacement or velocity information. Our study resolves previous ambiguity regarding the use of displacement or velocity signals to guide saccades and provides a natural explanation for neural recordings that indicate multiplexing of displacement and velocity related information in the firing activity of neurons in the superior colliculus, a critical node in the oculomotor network that codes for saccadic eye movements.

Model-based study of the human cupular time constant

1999 ◽  
Vol 9 (4) ◽  
pp. 293-301 ◽  
Author(s):  
Mingjia Dai ◽  
Avniel Klein ◽  
Bernard Cohen ◽  
Theodore Raphan
Keyword(s):  
Time Constant ◽  
Human Subjects ◽  
Vestibular Nerve ◽  
Velocity Storage ◽  
Slow Phase ◽  
Initial Portion ◽  
Time Constants ◽  
Model Based ◽  
Double Exponential ◽  
Eye Velocity

The time constant of the angular vestibulo-ocular reflex (aVOR), measured from the response to steps of rotation about a yaw axis, has frequently been estimated as a single exponential. However, the slow phase velocity envelope during per- or post-rotatory nystagmus is more accurately represented by two exponential modes. One represents activity in the vestibular nerve induced by deflection of the cupula, the other by activation that the input from the canals produces in the central velocity storage integrator. The sum of the cupula and the integrator responses describes the overall response of slow phase eye velocity and can be approximated by a double exponential. Frequently, there is a plateau in the initial portion of eye velocity response, but this may be masked by habituation, making the cupula contribution unobservable and impossible to estimate. Using a model-based technique to analyze responses with a clear plateau, we estimated peripheral and central vestibular time constants by double exponential fits to slow phase eye velocity. Cupular time constants were varied from 1 to 10 s to identify values that gave optimal fits of the data according to a Chi-square criterion. The mean cupular time constant for 10 human subjects was 4.2 ± 0.6 s. Fits of the data were also good for time constants between 3.5 to 7 s, but not for 1 to 3 or 7.5 to 10 s. The estimated cupular time constants also fit responses where there was no plateau. In 8 monkeys, cupular time constants were estimated as 3.9 ± 0.5 s, which agreed with those derived from activity in the vestibular nerve. There was no difference between monkey and human cupular time constants from these estimates. It is likely that the human cupular time constant is similar to that of the monkey and shorter than previously thought.

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