Dynamics and viewing distance dependence of eye movements during transient lateral motion
No abstract available
NASA Discipline Neuroscience↗
Engineering topics
Angelaki, D. E.
Publications and source records attributed to Angelaki, D. E..
Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses
Spatiotemporal convergence and two-dimensional (2-D) neural tuning have been proposed as a major neural mechanism in the signal processing of linear acceleration. To examine this hypothesis, we studied the firing properties of primary otolith afferents and central otolith neurons that respond exclusively to horizontal linear accelerations of the head (0.16-10 Hz) in alert rhesus monkeys. Unlike primary afferents, the majority of central otolith neurons exhibited 2-D spatial tuning to linear acceleration. As a result, central otolith dynamics vary as a function of movement direction. During movement along the maximum sensitivity direction, the dynamics of all central otolith neurons differed significantly from those observed for the primary afferent population. Specifically at low frequencies (</=0.5 Hz), the firing rate of the majority of central otolith neurons peaked in phase with linear velocity, in contrast to primary afferents that peaked in phase with linear acceleration. At least three different groups of central response dynamics were described according to the properties observed for motion along the maximum sensitivity direction. "High-pass" neurons exhibited increasing gains and phase values as a function of frequency. "Flat" neurons were characterized by relatively flat gains and constant phase lags (approximately 20-55 degrees ). A few neurons ("low-pass") were characterized by decreasing gain and phase as a function of frequency. The response dynamics of central otolith neurons suggest that the approximately 90 degrees phase lags observed at low frequencies are not the result of a neural integration but rather the effect of nonminimum phase behavior, which could arise at least partly through spatiotemporal convergence. Neither afferent nor central otolith neurons discriminated between gravitational and inertial components of linear acceleration. Thus response sensitivity was indistinguishable during 0.5-Hz pitch oscillations and fore-aft movements. The fact that otolith-only central neurons with "high-pass" filter properties exhibit semicircular canal-like dynamics during head tilts might have important consequences for the conclusions of previous studies of sensory convergence and sensorimotor transformations in central vestibular neurons.
NASA Discipline Neuroscience↗
Low-frequency otolith and semicircular canal interactions after canal inactivation
During sustained constant velocity and low-frequency off-vertical axis rotations (OVAR), otolith signals contribute significantly to slow-phase eye velocity. The adaptive plasticity of these responses was investigated here after semicircular canal plugging. Inactivation of semicircular canals results in a highly compromised and deficient vestibulo-ocular reflex (VOR). Based on the VOR enhancement hypothesis, one could expect an adaptive increase of otolith-borne angular velocity signals due to combined otolith/canal inputs after inactivation of the semicircular canals. Contrary to expectations, however, the steady-state slow-phase velocity during constant velocity OVAR decreased in amplitude over time. A similar progressive decrease in VOR gain was also observed during low-frequency off-vertical axis oscillations. This response deterioration was present in animals with either lateral or vertical semicircular canals inactivated and was limited to the plane(s) of the plugged canals. The results are consistent with the idea that the low-frequency otolith signals do not simply enhance VOR responses. Rather, the nervous system appears to correlate vestibular sensory information from the otoliths and the semicircular canals to generate an integral response to head motion.
Non-NASA Center↗
Primate translational vestibuloocular reflexes. IV. Changes after unilateral labyrinthectomy
The effects of unilateral labyrinthectomy on the properties of the translational vestibuloocular reflexes (trVORs) were investigated in rhesus monkeys trained to fixate near targets. Translational motion stimuli consisted of either steady-state lateral and fore-aft sinusoidal oscillations or short-lasting transient displacements. During small-amplitude, steady-state sinusoidal lateral oscillations, a small decrease in the horizontal trVOR sensitivity and its dependence on viewing distance was observed during the first week after labyrinthectomy. These deficits gradually recovered over time. In addition, the vertical response component increased, causing a tilt of the eye velocity vector toward the lesioned side. During large, transient lateral displacements, the deficits were larger and longer lasting. Responses after labyrinthectomy were asymmetric, with eye velocity during movements toward the side of the lesion being more compromised. The most profound effect of the lesions was observed during fore-aft motion. Whereas responses were kinematically appropriate for fixation away from the side of the lesion (e.g., to the left after right labyrinthectomy), horizontal responses were anticompensatory during fixation at targets located ipsilateral to the side of the lesion (e.g., for targets to the right after right labyrinthectomy). This deficit showed little recovery during the 3-mo post-labyrinthectomy testing period. These results suggest that inputs from both labyrinths are important for the proper function of the trVORs, although the details of how bilateral signals are processed and integrated remain unknown.
NASA Discipline Neuroscience↗
Primate translational vestibuloocular reflexes. III. Effects of bilateral labyrinthine electrical stimulation
The effects of functional, reversible ablation and potential recruitment of the most irregular otolith afferents on the dynamics and sensitivity of the translational vestibuloocular reflexes (trVORs) were investigated in rhesus monkeys trained to fixate near and far targets. Translational motion stimuli consisted of either steady-state lateral and fore-aft sinusoidal oscillations or short-lasting transient lateral head displacements. Short-duration (usually <2 s) anodal (inhibitory) and cathodal (excitatory) currents (50-100 microA) were delivered bilaterally during motion. In the presence of anodal labyrinthine stimulation, trVOR sensitivity and its dependence on viewing distance were significantly decreased. In addition, anodal currents significantly increased phase lags. During transient motion, anodal stimulation resulted in significantly lower initial eye acceleration and more sluggish responses. Cathodal currents tended to have opposite effects. The main characteristics of these results were simulated by a simple model where both regularly and irregularly discharging afferents contribute to the trVORs. Anodal labyrinthine currents also were found to decrease eye velocity during long-duration, constant velocity rotations, although results were generally more variable compared with those during translational motion.
NASA Program Biomedical Research and Countermeasur↗
Primate translational vestibuloocular reflexes. II. Version and vergence responses to fore-aft motion
To maintain binocular fixation on near targets during fore-aft translational disturbances, largely disjunctive eye movements are elicited the amplitude and direction of which should be tuned to the horizontal and vertical eccentricities of the target. The eye movements generated during this task have been investigated here as trained rhesus monkeys fixated isovergence targets at different horizontal and vertical eccentricities during 10 Hz fore-aft oscillations. The elicited eye movements complied with the geometric requirements for binocular fixation, although not ideally. First, the corresponding vergence angle for which the movement of each eye would be compensatory was consistently less than that dictated by the actual fixation parameters. Second, the eye position with zero sensitivity to translation was not straight ahead, as geometrically required, but rather exhibited a systematic dependence on viewing distance and vergence angle. Third, responses were asymmetric, with gains being larger for abducting and downward compared with adducting and upward gaze directions, respectively. As frequency was varied between 4 and 12 Hz, responses exhibited high-pass filter properties with significant differences between abduction and adduction responses. As a result of these differences, vergence sensitivity increased as a function of frequency with a steeper slope than that of version. Despite largely undercompensatory version responses, vergence sensitivity was closer to ideal. Moreover, the observed dependence of vergence sensitivity on vergence angle, which was varied between 2.5 and 10 MA, was largely linear rather than quadratic (as geometrically predicted). We conclude that the spatial tuning of eye velocity sensitivity as a function of gaze and viewing distance follows the general geometric dependencies required for the maintenance of foveal visual acuity. However, systematic deviations from ideal behavior exist that might reflect asymmetric processing of abduction/adduction responses perhaps because of different functional dependencies of version and vergence eye movement components during translation.
NASA Program Biomedical Research and Countermeasur↗
Primate translational vestibuloocular reflexes. I. High-frequency dynamics and three-dimensional properties during lateral motion
The dynamics and three-dimensional (3-D) properties of the primate translational vestibuloocular reflex (trVOR) for high-frequency (4-12 Hz, +/-0.3-0.4 g) lateral motion were investigated during near-target viewing at center and eccentric targets. Horizontal response gains increased with frequency and depended on target eccentricity. The larger the horizontal and vertical target eccentricity, the steeper the dependence of horizontal response gain on frequency. In addition to horizontal eye movements, robust torsional response components also were present at all frequencies. During center-target fixation, torsional response phase was opposite (anticompensatory) to that expected for an "apparent" tilt response. Instead torsional response components depended systematically on vertical-target eccentricity, increasing in amplitude when looking down and reversing phase when looking up. As a result the trVOR eye velocity vector systematically tilted away from a purely horizontal direction, through an angle that increased with vertical eccentricity with a slope of approximately 0.7. This systematic dependence of torsional eye velocity tilt on vertical eye position suggests that the trVOR might follow the 3-D kinematic requirements that have been shown to govern visually guided eye movements and near-target fixation.
NASA Discipline Neuroscience↗
Three-dimensional organization of vestibular-related eye movements to off-vertical axis rotation and linear translation in pigeons
During linear accelerations, compensatory reflexes should continually occur in order to maintain objects of visual interest as stable images on the retina. In the present study, the three-dimensional organization of the vestibulo-ocular reflex in pigeons was quantitatively examined during linear accelerations produced by constant velocity off-vertical axis yaw rotations and translational motion in darkness. With off-vertical axis rotations, sinusoidally modulated eye-position and velocity responses were observed in all three components, with the vertical and torsional eye movements predominating the response. Peak torsional and vertical eye positions occurred when the head was oriented with the lateral visual axis of the right eye directed orthogonal to or aligned with the gravity vector, respectively. No steady-state horizontal nystagmus was obtained with any of the rotational velocities (8-58 degrees /s) tested. During translational motion, delivered along or perpendicular to the lateral visual axis, vertical and torsional eye movements were elicited. No significant horizontal eye movements were observed during lateral translation at frequencies up to 3 Hz. These responses suggest that, in pigeons, all linear accelerations generate eye movements that are compensatory to the direction of actual or perceived tilt of the head relative to gravity. In contrast, no translational horizontal eye movements, which are known to be compensatory to lateral translational motion in primates, were observed under the present experimental conditions.
NASA Discipline Neuroscience↗
Short-latency primate vestibuloocular responses during translation
Short-lasting, transient head displacements and near target fixation were used to measure the latency and early response gain of vestibularly evoked eye movements during lateral and fore-aft translations in rhesus monkeys. The latency of the horizontal eye movements elicited during lateral motion was 11.9 +/- 5.4 ms. Viewing distance-dependent behavior was seen as early as the beginning of the response profile. For fore-aft motion, latencies were different for forward and backward displacements. Latency averaged 7.1 +/- 9.3 ms during forward motion (same for both eyes) and 12.5 +/- 6.3 ms for the adducting eye (e.g., left eye during right fixation) during backward motion. Latencies during backward motion were significantly longer for the abducting eye (18.9 +/- 9.8 ms). Initial acceleration gains of the two eyes were generally larger than unity but asymmetric. Specifically, gains were consistently larger for abducting than adducting eye movements. The large initial acceleration gains tended to compensate for the response latencies such that the early eye movement response approached, albeit consistently incompletely, that required for maintaining visual acuity during the movement. These short-latency vestibuloocular responses could complement the visually generated optic flow responses that have been shown to exhibit much longer latencies.
Non-NASA Center↗
Inertial processing of vestibulo-ocular signals
New evidence for a central resolution of gravito-inertial signals has been recently obtained by analyzing the properties of the vestibulo-ocular reflex (VOR) in response to combined lateral translations and roll tilts of the head. It is found that the VOR generates robust compensatory horizontal eye movements independent of whether or not the interaural translatory acceleration component is canceled out by a gravitational acceleration component due to simultaneous roll-tilt. This response property of the VOR depends on functional semicircular canals, suggesting that the brain uses both otolith and semicircular canal signals to estimate head motion relative to inertial space. Vestibular information about dynamic head attitude relative to gravity is the basis for computing head (and body) angular velocity relative to inertial space. Available evidence suggests that the inertial vestibular system controls both head attitude and velocity with respect to a gravity-centered reference frame. The basic computational principles underlying the inertial processing of otolith and semicircular canal afferent signals are outlined.
NASA Discipline Neuroscience↗
Functional organization of primate translational vestibulo-ocular reflexes and effects of unilateral labyrinthectomy
Translational vestibulo-ocular reflexes (trVORs) are characterized by distinct spatio-temporal properties and sensitivities that are proportional to the inverse of viewing distance. Anodal (inhibitory) labyrinthine stimulation (100 microA, < 2 s) during motion decreased the high-pass filtered dynamics, as well as horizontal trVOR sensitivity and its dependence on viewing distance. Cathodal (excitatory) currents had opposite effects. Translational VORs were also affected after unilateral labyrinthectomy. Animals lost their ability to modulate trVOR sensitivity as a function of viewing distance acutely after the lesion. These deficits partially recovered over time, albeit a significant reduction in trVOR sensitivity as a function of viewing distance remained in compensated animals. During fore-aft motion, the effects of unilateral labyrinthectomy were more dramatic. Both acute and compensated animals permanently lost their ability to modulate fore-aft trVOR responses as a function of target eccentricity. These results suggest that (1) the dynamics and viewing distance-dependent properties of the trVORs are very sensitive to changes in the resting firing rate of vestibular afferents and, consequently, vestibular nuclei neurons; (2) the most irregularly firing primary otolith afferents that are most sensitive to labyrinthine electrical stimulation might contribute to reflex dynamics and sensitivity; (3) inputs from both labyrinths are necessary for the generation of the translational VORs.
Non-NASA Center↗
Oculomotor control of primary eye position discriminates between translation and tilt
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 degrees/s) about a vertically tilted axis (23.6 degrees). 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.
NASA Discipline Neuroscience↗
Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation
The three-dimensional (3-D) properties of the translational vestibulo-ocular reflexes (translational VORs) during lateral and fore-aft oscillations in complete darkness were studied in rhesus monkeys at frequencies between 0.16 and 25 Hz. In addition, constant velocity off-vertical axis rotations extended the frequency range to 0.02 Hz. During lateral motion, horizontal responses were in phase with linear velocity in the frequency range of 2-10 Hz. At both lower and higher frequencies, phase lags were introduced. Torsional response phase changed more than 180 degrees in the tested frequency range such that torsional eye movements, which could be regarded as compensatory to "an apparent roll tilt" at the lowest frequencies, became anticompensatory at all frequencies above approximately 1 Hz. These results suggest two functionally different frequency bandwidths for the translational VORs. In the low-frequency spectrum (<<0.5 Hz), horizontal responses compensatory to translation are small and high-pass-filtered whereas torsional response sensitivity is relatively frequency independent. At higher frequencies however, both horizontal and torsional response sensitivity and phase exhibit a similar frequency dependence, suggesting a common role during head translation. During up-down motion, vertical responses were in phase with translational velocity at 3-5 Hz but phase leads progressively increased for lower frequencies (>90 degrees at frequencies <0.2 Hz). No consistent dependence on static head orientation was observed for the vertical response components during up-down motion and the horizontal and torsional response components during lateral translation. The frequency response characteristics of the translational VORs were fitted by "periphery/brain stem" functions that related the linear acceleration input, transduced by primary otolith afferents, to the velocity signals providing the input to the velocity-to-position neural integrator and the oculomotor plant. The lowest-order, best-fit periphery/brain stem model that approximated the frequency dependence of the data consisted of a second order transfer function with two alternating poles (at 0.4 and 7.2 Hz) and zeros (at 0.035 and 3.4 Hz). In addition to clearly differentiator dynamics at low frequencies (less than approximately 0.5 Hz), there was no frequency bandwidth where the periphery/brain stem function could be approximated by an integrator, as previously suggested. In this scheme, the oculomotor plant dynamics are assumed to perform the necessary high-frequency integration as required by the reflex. The detailed frequency dependence of the data could only be precisely described by higher order functions with nonminimum phase characteristics that preclude simple filtering of afferent inputs and might be suggestive of distributed spatiotemporal processing of otolith signals in the translational VORs.
Non-NASA Center↗
Visually induced adaptation in three-dimensional organization of primate vestibuloocular reflex
The adaptive plasticity of the spatial organization of the vestibuloocular reflex (VOR) has been investigated in intact and canal-plugged primates using 2-h exposure to conflicting visual (optokinetic, OKN) and vestibular rotational stimuli about mutually orthogonal axes (generating torsional VOR + vertical OKN, torsional VOR + horizontal OKN, vertical VOR + horizontal OKN, and horizontal VOR + vertical OKN). Adaptation protocols with 0.5-Hz (+/-18 degrees ) head movements about either an earth-vertical or an earth-horizontal axis induced orthogonal response components as high as 40-70% of those required for ideal adaptation. Orthogonal response gains were highest at the adapting frequency with phase leads present at lower and phase lags present at higher frequencies. Furthermore, the time course of adaptation, as well as orthogonal response dynamics were similar and relatively independent of the particular visual/vestibular stimulus combination. Low-frequency (0. 05 Hz, vestibular stimulus: +/-60 degrees ; optokinetic stimulus: +/-180 degrees ) adaptation protocols with head movements about an earth-vertical axis induced smaller orthogonal response components that did not exceed 20-40% of the head velocity stimulus (i.e., approximately 10% of that required for ideal adaptation). At the same frequency, adaptation with head movements about an earth-horizontal axis generated large orthogonal responses that reached values as high as 100-120% of head velocity after 2 h of adaptation (i.e., approximately 40% of ideal adaptation gains). The particular spatial and temporal response characteristics after low-frequency, earth-horizontal axis adaptation in both intact and canal-plugged animals strongly suggests that the orienting (and perhaps translational) but not inertial (velocity storage) components of the primate otolith-ocular system exhibit spatial adaptability. Due to the particular nested arrangement of the visual and vestibular stimuli, the optic flow pattern exhibited a significant component about the third spatial axis (i.e., orthogonal to the axes of rotation of the head and visual surround) at twice the oscillation frequency. Accordingly, the adapted VOR was characterized consistently by a third response component (orthogonal to both the axes of head and optokinetic drum rotation) at twice the oscillation frequency after earth-horizontal but not after earth-vertical axis 0.05-Hz adaptation. This suggests that the otolith-ocular (but not the semicircular canal-ocular) system can adaptively change its spatial organization at frequencies different from those of the head movement.
Non-NASA Center↗
Inertial vestibular coding of motion: concepts and evidence
Central processing of inertial sensory information about head attitude and motion in space is crucial for motor control. Vestibular signals are coded relative to a non-inertial system, the head, that is virtually continuously in motion. Evidence for transformation of vestibular signals from head-fixed sensory coordinates to gravity-centered coordinates have been provided by studies of the vestibulo-ocular reflex. The underlying central processing depends on otolith afferent information that needs to be resolved in terms of head translation related inertial forces and head attitude dependent pull of gravity. Theoretical solutions have been suggested, but experimental evidence is still scarce. It appears, along these lines, that gaze control systems are intimately linked to motor control of head attitude and posture.
Review↗
Response properties of pigeon otolith afferents to linear acceleration
In the present study, the sensitivity to sinusoidal linear accelerations in the plane of the utricular macula was tested in afferents. The head orientation relative to the translation axis was varied in order to determine the head position that elicited the maximal and minimal responses for each afferent. The response gain and phase values obtained to 0.5-Hz and 2-Hz linear acceleration stimuli were then plotted as a function of head orientation and a modified cosine function was fit to the data. From the best-fit cosine function, the predicted head orientations that would produce the maximal and minimal response gains were estimated. The estimated maximum response gains to linear acceleration in the utricular plane for the afferents varied between 75 and 1420 spikes s-1 g-1. The mean maximal gains for all afferents to 0.5-Hz and 2-Hz sinusoidal linear acceleration stimuli were 282 and 367 spikes s-1 g-1, respectively. The minimal response gains were essentially zero for most units. The response phases always led linear acceleration and remained constant for each afferent, regardless of head orientation. These response characteristics indicate that otolith afferents are cosine tuned and behave as one-dimensional linear accelerometers. The directions of maximal sensitivity to linear acceleration for the afferents varied throughout the plane of the utricle; however, most vectors were directed out of the opposite ear near the interaural axis. The response dynamics of the afferents were tested using stimulus frequencies ranging between 0.25 Hz and 10 Hz (0.1 g peak acceleration). Across stimulus frequencies, most afferents had increasing gains and constant phase values. These dynamic properties for individual afferents were fit with a simple transfer function that included three parameters: a mechanical time constant, a gain constant, and a fractional order distributed adaptation operator.
Non-NASA Center↗
Kinematic principles of primate rotational vestibulo-ocular reflex. II. Gravity-dependent modulation of primary eye position
The kinematic constraints of three-dimensional eye positions were investigated in rhesus monkeys during passive head and body rotations relative to gravity. We studied fast and slow phase components of the vestibulo-ocular reflex (VOR) elicited by constant-velocity yaw rotations and sinusoidal oscillations about an earth-horizontal axis. We found that the spatial orientation of both fast and slow phase eye positions could be described locally by a planar surface with torsional variation of <2.0 +/- 0.4 degrees (displacement planes) that systematically rotated and/or shifted relative to Listing's plane. In supine/prone positions, displacement planes pitched forward/backward; in left/right ear-down positions, displacement planes were parallel shifted along the positive/negative torsional axis. Dynamically changing primary eye positions were computed from displacement planes. Torsional and vertical components of primary eye position modulated as a sinusoidal function of head orientation in space. The torsional component was maximal in ear-down positions and approximately zero in supine/prone orientations. The opposite was observed for the vertical component. Modulation of the horizontal component of primary eye position exhibited a more complex dependence. In contrast to the torsional component, which was relatively independent of rotational speed, modulation of the vertical and horizontal components of primary position depended strongly on the speed of head rotation (i.e., on the frequency of oscillation of the gravity vector component): the faster the head rotated relative to gravity, the larger was the modulation. Corresponding results were obtained when a model based on a sinusoidal dependence of instantaneous displacement planes (and primary eye position) on head orientation relative to gravity was fitted to VOR fast phase positions. When VOR fast phase positions were expressed relative to primary eye position estimated from the model fits, they were confined approximately to a single plane with a small torsional standard deviation ( approximately 1.4-2.6 degrees). This reduced torsional variation was in contrast to the large torsional spread (well >10-15 degrees ) of fast phase positions when expressed relative to Listing's plane. We conclude that primary eye position depends dynamically on head orientation relative to space rather than being fixed to the head. It defines a gravity-dependent coordinate system relative to which the torsional variability of eye positions is minimized even when the head is moved passively and vestibulo-ocular reflexes are evoked. In this general sense, Listing's law is preserved with respect to an otolith-controlled reference system that is defined dynamically by gravity.
NASA Discipline Neuroscience↗
Kinematic principles of primate rotational vestibulo-ocular reflex. I. Spatial organization of fast phase velocity axes
The spatial organization of fast phase velocity vectors of the vestibulo-ocular reflex (VOR) was studied in rhesus monkeys during yaw rotations about an earth-horizontal axis that changed continuously the orientation of the head relative to gravity ("barbecue spit" rotation). In addition to a velocity component parallel to the rotation axis, fast phases also exhibited a velocity component that invariably was oriented along the momentary direction of gravity. As the head rotated through supine and prone positions, torsional components of fast phase velocity axes became prominent. Similarly, as the head rotated through left and right ear-down positions, fast phase velocity axes exhibited prominent vertical components. The larger the speed of head rotation the greater the magnitude of this fast phase component, which was collinear with gravity. The main sequence properties of VOR fast phases were independent of head position. However, peak amplitude as well as peak velocity of fast phases were both modulated as a function of head orientation, exhibiting a minimum in prone position. The results suggest that the fast phases of vestibulo-ocular reflexes not only redirect gaze and reposition the eye in the direction of head motion but also reorient the eye with respect to earth-vertical when the head moves relative to gravity. As further elaborated in the companion paper, the underlying mechanism could be described as a dynamic, gravity-dependent modulation of the coordinates of ocular rotations relative to the head.
Non-NASA Center↗