Dynamics and viewing distance dependence of eye movements during transient lateral motion.
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Acceleration↗
Biomedical subjects
D E Angelaki
Publications and source records attributed to D E Angelaki.
Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation.
Rotational and translational vestibulo-ocular reflexes (RVOR and TrVOR) function to maintain stable binocular fixation during head movements. Despite similar functional roles, differences in behavioral, neuroanatomical, and sensory afferent properties suggest that the sensorimotor processing may be partially distinct for the RVOR and TrVOR. To investigate the currently poorly understood neural correlates for the TrVOR, the activities of eye movement-sensitive neurons in the rostral vestibular nuclei were examined during pure translation and rotation under both stable gaze and suppression conditions. Two main conclusions were made. First, the 0.5 Hz firing rates of cells that carry both sensory head movement and motor-like signals during rotation were more strongly related to the oculomotor output than to the vestibular sensory signal during translation. Second, neurons the firing rates of which increased for ipsilaterally versus contralaterally directed eye movements (eye-ipsi and eye-contra cells, respectively) exhibited distinct dynamic properties during TrVOR suppression. Eye-ipsi neurons demonstrated relatively flat dynamics that was similar to that of the majority of vestibular-only neurons. In contrast, eye-contra cells were characterized by low-pass filter dynamics relative to linear acceleration and lower sensitivities than eye-ipsi cells. In fact, the main secondary eye-contra neuron in the disynaptic RVOR pathways (position-vestibular-pause cell) that exhibits a robust modulation during RVOR suppression did not modulate during TrVOR suppression. To explain these results, a simple model is proposed that is consistent with the known neuroanatomy and postulates differential projections of sensory canal and otolith signals onto eye-contra and eye-ipsi cells, respectively, within a shared premotor circuitry that generates the VORs.
Action Potentials↗
Cross-axis adaptation of the translational vestibulo-ocular reflex.
The adaptive plasticity of the translational vestibulo-ocular reflex (VOR) was investigated in rhesus monkeys after 2-h exposure to either vertical or torsional optic flow stimulation accompanied by lateral translation stimuli (0.5 Hz). Because of the inherent ambiguity in the otolith system for the detection of gravitoinertial accelerations, we hypothesized that cross-axis adaptation of the translational VOR during lateral motion would be preferentially selective for a torsional optic flow stimulus that would mimic a roll tilt movement. However, we found that both vertical and torsional adaptation was possible. Furthermore, there was no significant preference for whether the torsional adaptation was in phase or out of phase with the apparent tilt induced by the motion stimulus. These results suggest that, at least at 0.5 Hz, there seems to be no preferential, visually induced adaptive capacity of the otolith system for tilt/translation reinterpretation during motion. Like the rotational VOR, translational VOR appears to exhibit a general form of cross-axis adaptation that operates for different directions of optic flow stimulation.
Adaptation, Physiological↗
Head unrestrained horizontal gaze shifts after unilateral labyrinthectomy in the rhesus monkey.
Following the orienting saccade of a combined eye-head gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) of near unity, is a manifestation of the vestibulo-ocular reflex (VOR). Acute unilateral labyrinthectomy (UL) causes severe asymmetry in the VOR during passive head rotations that recovers incompletely over time. The purpose of this investigation was to compare the recovery of the counterrotation gain during horizontal gaze shifts with that of the passive VOR after UL. During the 1st week after UL, counterrotation gains were asymmetric, being lower for head movements towards the lesion but nearly normal for head movements towards the intact side. Whereas this asymmetry in the counterrotation gain resolved within a week after UL, asymmetries in the passive VOR persisted. During the 1st week after UL, behavioral performance was generally poor, with a high incidence of inaccurate gaze shifts and larger latencies. In addition, animals used slower head movements such that peak head amplitude during the eye saccade was significantly lower during the 1st week after UL as compared to control values. Bilateral labyrinthectomy (BL) resulted in larger but symmetric deficits in counterrotation, which, contrary to the passive VOR, exhibited significant recovery over time. It is hypothesized that recovery of counterrotation gain after UL has contributions from multiple sources, including the contralateral intact labyrinth and an efference copy of the head movement.
Adaptation, Physiological↗
Direction of heading and vestibular control of binocular eye movements.
To optimize visual fixation on near targets against translational disturbances, the eyes must move in compliance with geometrical constraints that are related to the distance as well as the speed and direction relative to the target. It is often assumed that the oculomotor system uses the vestibular signals during such movements mainly to stabilize the foveal image irrespective of the peripheral vision. To test this hypothesis, trained rhesus monkeys were asked to maintain fixation on isovergence targets at different horizontal eccentricities during 10 Hz oscillations along different horizontal directions. We found that the two eyes moved in compliance with the geometrical constraints of the gaze-stabilization hypothesis, although response gains were generally small ( approximately 0.5). The best agreement with the gaze stabilization hypothesis occurred for heading directions within +/-30 degrees from straight-ahead, whereas lateral movements exhibited greater variability and larger directional errors that reflected the statistical response variability inherent in the non-linear dependence on heading direction. In contrast to undercompensatory version (conjugate) components, the disjunctive part of the response (vergence) exhibited unity or higher than unity gains. The high vergence gains might reflect a strategy that aims at maintaining the binocular coordination of the gaze lines despite the low gain of the version movements.
Analysis of Variance↗
Vestibular discrimination of gravity and translational acceleration.
According to Einstein's equivalence principle, linear accelerations experienced during translational motion are physically indistinguishable from changes in orientation relative to gravity experienced during tilting movements. Nevertheless, despite these ambiguous sensory cues provided by the primary otolith afferents, perceptual and motor responses discriminate between gravity and translational acceleration. There is growing evidence to suggest that the brain resolves this ambiguity primarily by combining signals from multiple sensors, the semicircular canals being a main extra otolith contributor. Here, we summarize the experimental evidence in support of the canal influences on the neural processing of otolith cues, provide specific experimental results in rhesus monkeys, and discuss and compare previously proposed models that combine otolith and semicircular-canal signals in order to provide neural estimates of gravity and linear acceleration.
Animals↗
Differential coding of sensorimotor signals on eye-movement-sensitive neurons during rotation and translation.
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Eye Movements↗
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.
Animals↗
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.
Algorithms↗
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.
Acceleration↗
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.
Algorithms↗
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.
Animals↗
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.
Acceleration↗
Central versus peripheral origin of vestibuloocular reflex recovery following semicircular canal plugging in rhesus monkeys.
We have previously shown that there is a slowly progressing, frequency-specific recovery of the gain and phase of the horizontal vestibuloocular reflex (VOR) in rhesus monkeys following plugging of the lateral semicircular canals. The adapted VOR response exhibited both dynamic and spatial characteristics that were distinctly different from responses in intact animals. To discriminate between adaptation or recovery of central versus peripheral origin, we have tested the recovered vestibuloocular responses in three rhesus monkeys in which either one or both coplanar pairs of vertical semicircular canals had been plugged previously by occluding the remaining semicircular canals in a second plugging operation. We measured the spatial tuning of the VOR in two or three different mutually orthogonal planes in response to sinusoidal oscillations (1.1 Hz, +/-5 degrees, +/-35 degrees /s) over a period of 2-3 and 12-14 mo after each operation. Apart from a significant recovery of the torsional/vertical VOR following the first operation we found that these recovered responses were preserved following the second operation, whereas the responses from the newly operated semicircular canals disappeared acutely as expected. In the follow-up period of up to 3 mo after the second operation, responses from the last operated canals showed recovery in two of three animals, whereas the previously recovered responses persisted. The results suggest that VOR recovery following plugging may depend on a regained residual sensitivity of the plugged semicircular canals to angular head acceleration.
Analysis of Variance↗
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.
Adaptation, Physiological↗
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.
Animals↗
Computation of inertial motion: neural strategies to resolve ambiguous otolith information.
According to Einstein's equivalence principle, inertial accelerations during translational motion are physically indistinguishable from gravitational accelerations experienced during tilting movements. Nevertheless, despite ambiguous sensory representation of motion in primary otolith afferents, primate oculomotor responses are appropriately compensatory for the correct translational component of the head movement. The neural computational strategies used by the brain to discriminate the two and to reliably detect translational motion were investigated in the primate vestibulo-ocular system. The experimental protocols consisted of either lateral translations, roll tilts, or combined translation-tilt paradigms. Results using both steady-state sinusoidal and transient motion profiles in darkness or near target viewing demonstrated that semicircular canal signals are necessary sensory cues for the discrimination between different sources of linear acceleration. When the semicircular canals were inactivated, horizontal eye movements (appropriate for translational motion) could no longer be correlated with head translation. Instead, translational eye movements totally reflected the erroneous primary otolith afferent signals and were correlated with the resultant acceleration, regardless of whether it resulted from translation or tilt. Therefore, at least for frequencies in which the vestibulo-ocular reflex is important for gaze stabilization (>0.1 Hz), the oculomotor system discriminates between head translation and tilt primarily by sensory integration mechanisms rather than frequency segregation of otolith afferent information. Nonlinear neural computational schemes are proposed in which not only linear acceleration information from the otolith receptors but also angular velocity signals from the semicircular canals are simultaneously used by the brain to correctly estimate the source of linear acceleration and to elicit appropriate oculomotor responses.
Animals↗
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.
Animals↗