Canal-otolith interactions in the squirrel monkey vestibulo-ocular reflex and the influence of fixation distance

Natural head movements include angular and linear components of motion. Two classes of vestibulo-ocular reflex (VOR), mediated by the semicircular canals and otoliths (the angular and linear VOR, or AVOR and LVOR, respectively), compensate for head movements and help maintain binocular fixation on targets in space. In this study, AVOR/LVOR interactions were quantified during complex head motion over a broad range of fixation distances at a fixed stimulus frequency of 4.0 Hz. Binocular eye movements were recorded (search-coil technique) in squirrel monkeys while fixation distance (assessed by vergence) was varied using brief presentations of earth-fixed targets at various distances. Stimuli consisted of rotations around an earth-vertical axis and therefore always activated the AVOR. Horizontal and vertical AVORs were assessed when the head was centered over the axis of rotation and oriented upright (UP) and right-side-down (RD), respectively. AVOR gains increased slightly with increasing vergence in darkness, as expected given the small anterior position of the eyes in the head. Combined AVOR/LVOR responses were recorded when subjects were displaced eccentrically from the rotation axis. Eccentric rotations activated the AVOR just as when the head was centered, but added a translational stimulus which generated an LVOR component in response to interaural (IA) or dorsoventral (DV) tangential accelerations, depending on whether the head was UP or RD, respectively. When the head was eccentric and facing nose-out, the AVOR and LVOR produced ocular responses in the same plane and direction (coplanar and synergistic), and response magnitudes increased with increasing vergence. With the head facing nose-in, AVOR and LVOR response components were oppositely directed (coplanar and antagonistic). The AVOR dominated the response when fixation distance was far, and phase was compensatory for head rotation. As fixation distance decreased toward the rotation axis, responses declined to near zero, and when fixation distance approached even closer, the LVOR component dominated and response phase inverted. The same pattern was observed for both horizontal (head UP) and vertical (head RD) responses. The LVOR was recorded directly by rotating subjects eccentrically but in the nose-up (NU) orientation. The AVOR then generated torsional responses to head roll, coexistent with either horizontal or vertical LVOR responses to tangential acceleration when the subject was oriented head-out or right-side-out, respectively. Only the LVOR response components were modulated by vergence. A vectorial analysis of AVOR, LVOR, and combined responses supports the conclusion that AVOR and LVOR response components combine linearly during complex head motion. Received: 27 February 1997 / Accepted: 18 June 1997     

The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey

The aim of this study was to determine if the angular vestibulo-ocular reflex (VOR) in response to pitch, roll, left anterior–right posterior (LARP), and right anterior–left posterior (RALP) head rotations exhibited the same linear and nonlinear characteristics as those found in the horizontal VOR. Three-dimensional eye movements were recorded with the scleral search coil technique. The VOR in response to rotations in five planes (horizontal, vertical, torsional, LARP, and RALP) was studied in three squirrel monkeys. The latency of the VOR evoked by steps of acceleration in darkness (3,000°/s² reaching a velocity of 150°/s) was 5.8±1.7 ms and was the same in response to head rotations in all five planes of rotation. The gain of the reflex during the acceleration was 36.7±15.4% greater than that measured at the plateau of head velocity. Polynomial fits to the trajectory of the response show that eye velocity is proportional to the cube of head velocity in all five planes of rotation. For sinusoidal rotations of 0.5–15 Hz with a peak velocity of 20°/s, the VOR gain did not change with frequency (0.74±0.06, 0.74±0.07, 0.37±0.05, 0.69±0.06, and 0.64±0.06, for yaw, pitch, roll, LARP, and RALP respectively). The VOR gain increased with head velocity for sinusoidal rotations at frequencies 4 Hz. For rotational frequencies 4 Hz, we show that the vertical, torsional, LARP, and RALP VORs have the same linear and nonlinear characteristics as the horizontal VOR. In addition, we show that the gain, phase and axis of eye rotation during LARP and RALP head rotations can be predicted once the pitch and roll responses are characterized.This work was supported by NIH grant R01 DC02390     

Eye-position dependence of three-dimensional ocular rotation-axis orientation during head impulses in humans

 If horizontal saccades or smooth-pursuit eye movements are made with the line-of-sight at different elevations, the three-dimensional (3D) angular rotation axis of the globe tilts by half the vertical eye eccentricity. This phenomenon is named ”half-angle rule” and is a consequence of Listing’s law. It was recently found that the ocular rotation axis during the horizontal vestibulo-ocular reflex (VOR) on a turntable also tilts in the direction of the line-of-sight by about a quarter of the eye’s vertical eccentricity. This is surprising, since, in a ”perfect” VOR, the angular rotation axis of the eye should be independent from the position of the eye to fully compensate for the 3D angular head rotation. We asked whether this quarter-angle strategy is a general property of the VOR or whether the 3D kinematics of ocular movements evoked by vestibular stimulation would be less eye-position dependent at higher stimulus frequencies. Nine healthy subjects were exposed to horizontal head impulses (peak velocity ∼250°/s). The line-of-sight was systematically changed along the vertical meridian of a tangent screen. Three-dimensional eye and head movements were monitored with dual search coils. The 3D orientation of the angular eye-in-head rotation axis was determined by calculating the average angular velocity vectors of the initial 10° displacements. Then, the difference between the tilt angles of the ocular rotation axis during upward and downward viewing was determined and divided by the difference of vertical eccentricity (”tilt angle coefficient”). Control experiments included horizontal saccades, smooth-pursuit eye movements, and eye movements evoked by slow, passive head rotations at the same vertical eye eccentricities. On average, the ocular rotation axis during horizontal head-impulse testing at different elevations of the line-of-sight was closely aligned with the rotation axis of the head (tilt angle coefficient of pooled abducting and adducting eye movements: 0.11±0.17 SD). Values for slow head impulses, however, exceeded somewhat the quarter angle (0.33±0.12), while smooth-pursuit movements (0.50±0.09) and saccades (0.44±0.11) were closest to the half angle. These results demonstrate that the 3D orientation of the ocular rotation axis during rapid head thrusts is relatively independent of the direction of the line-of-sight and that ocular rotations elicited by head impulses are kinematically different from saccades, despite similar movement dynamics. Received: 17 July 1998 / Accepted: 17 May 1999     

Temporal dynamics of semicircular canal and otolith function following acute unilateral vestibular deafferentation in humans

Dynamic changes of deficits in canal and otolith vestibulo-ocular reflexes (VORs) to high acceleration, eccentric yaw rotations were investigated in five subjects aged 25–65 years before and at frequent intervals 3–451 days following unilateral vestibular deafferentation (UVD) due to labyrinthectomy or vestibular neurectomy. Eye and head movements were recorded using magnetic search coils during transients of directionally random, whole-body rotation in darkness at peak acceleration 2,800°/s². Canal VORs were characterized during rotation about a mid-otolith axis, viewing a target 500 cm distant until rotation onset in darkness. Otolith VOR responses were characterized by the increase in VOR gain during identical rotation about an axis 13 cm posterior to the otoliths, initially viewing a target 15 cm distant. Pre-UVD canal gain was directionally symmetrical, averaging 0.87 ± 0.02 (±SEM). Contralesional canal gain declined from pre-UVD by an average of 22% in the first 3–5 days post-UVD, before recovering to an asymptote of close 90% of pre-UVD level at 1–3 months. This recovery corresponded to resolution of spontaneous nystagmus. Ipsilesional gain declined to 59%, and showed no consistent recovery afterwards. Pre-UVD otolith gain was directionally symmetrical, averaging 0.56 ± 0.02. Immediately after UVD, the contralesional otolith gain declined to 0.30 ± 0.02, and did not recover. Ipsilesional otolith gain declined profoundly to 0.08 ± 0.03 (P < 0.01), and never recovered. In contrast to the modest and directionally symmetrical effect of UVD on the human otolith VOR during pure translational acceleration, otolith gain during eccentric yaw rotation exhibited a profound and lasting deficit that might be diagnostically useful in lateralizing otolith pathology. Most recovery of the human canal gain to high acceleration transients following UVD is for contralesional head rotation, occurring within 3 months as spontaneous nystagmus resolves. Grant support: United States Public Health Service grants DC-02952 and AG-09693. JLD is Leonard Apt Professor of Ophthalmology.     

Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt

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 degrees in darkness to one of eight different evenly spaced final orientations, a so-called "dumping" protocol. Three speeds (200, 100, and 50 degrees /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 degrees /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.     

Linearity of canal-otolith interaction during eccentric rotation in humans

During natural behavior, the head may simultaneously undergo rotation, transduced by the semicircular canals, and translation, transduced by the otolith organs. It has been demonstrated in monkey that the vestibulo-ocular reflexes (VORs) elicited by both endorgans (i.e., the angular and linear VORs, or AVOR and LVOR) sum linearly during combined rotation and translation, but this finding has proven more elusive in humans. To investigate the combined AVOR/LVOR response, six human subjects underwent yaw eccentric rotation at 3 Hz in darkness while displaced from the axis of rotation. Responses to on-center yaw rotation (AVOR alone) and interaural translation (LVOR alone) were also recorded. During eccentric rotation with the subject facing away from the axis of rotation (i.e., nose out), in which a yaw to the right occurs simultaneously with a translation to the right (i.e., translation in phase with rotation), the AVOR and LVOR acted synergistically. Responses were always out of phase with rotation, and became larger in magnitude as vergence increased. For nose-in eccentric rotation, during which translation is out of phase with rotation, the LVOR acted antagonistically to the AVOR. During near viewing, the LVOR often dominated the overall response when eccentricity was sufficiently large, producing eye movements that were in phase with the rotational stimuli. As vergence decreased, the LVOR influence diminished, eventually resulting in responses that were out of phase with rotation at lowest vergence. When the response to pure yaw rotation was vectorially removed from the responses to eccentric rotation, the results proved statistically indistinguishable from the LVOR recorded during interaural translation, suggesting that the ocular response to combined angular and linear motion reflects the linear combination of the AVOR and LVOR.     

Canal-otolith interactions driving vertical and horizontal eye movements in the squirrel monkey

The vestibulo-ocular reflex (VOR) was studied in three squirrel monkeys subjected to rotations with the head either centered over, or displaced eccentrically from, the axis of rotation. This was done for several different head orientations relative to gravity in order to determine how canal-mediated angular (aVOR) and otolithmediated linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by rotating the head about the axis of rotation in the upright (UP), right-side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25–4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR gains increased with increasing stimulation frequency. In the NU orientation, compensatory torsional aVOR responses were of relatively low gain (0.54) compared with horizontal and vertical responses, and gains remained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added linear stimulus components, due to the centripetal and tangential accelerations acting on the head. By manipulating the orientation of the head relative to gravity and relative to the axis of rotation, the lVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and lVOR responses which acted in the same head plane. Horizontal aVOR-lVOR interactions were recorded when the head was in the UP orientation and facing toward (nose-in) or away from (nose-out) the rotation axis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear motion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR driving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and gains declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and lVOR interactions were also assessed when the two components acted in orthogonal response planes. By rotating the monkeys into the NU orientation, the aVOR acted primarily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical ocular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible at 0.25 Hz and increased dramatically with increasing frequency. Comparison of the combined responses (UP and RD orientations) with the isolated aVOR (head-centered) and lVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.     

Torsional and horizontal vestibular ocular reflex adaptation: three-dimensional eye movement analysis

This study used visual-vestibular conflict to effect short-term torsional and horizontal adaptation of the vestibulo-ocular reflex (VOR). Seven normal subjects underwent sinusoidal whole-body rotation about the earth-vertical axis for 40 min (±37°/s, 0.3 Hz) while viewing a stationary radial pattern fixed to the chair (×0 viewing). During adaptation and testing in darkness, the head was pitched either up or down 35° to excite both the horizontal and torsional VOR. The eyes were kept close to zero orbital elevation. Eye movements were recorded with a dual search coil in a three-field magnetic system. VOR gain was determined by averaging peak eye velocity from ten cycles of chair oscillation in complete darkness. The gain of the angular horizontal VOR (response to rotation about the head rostral-caudal axis) was significantly reduced after training in both head orientations. Angular torsional VOR gain (head rotation about the naso-occipital axis) was reduced in both head orientations, but this reached statistical significance only in the head down position. These results suggest that torsional and horizontal VOR gain adaptation, even when elicited together, may be subject to different influences depending upon head orientation. Differences between head up and down could be due to the relatively greater contribution of the horizontal semicircular canals with nose-down pitch. Alternatively, different VOR-adaptation processes could depend on the usual association of the head down posture to near viewing, in which case the torsional VOR is relatively suppressed.     

Eye movement responses to combined linear and angular head movement

Summary Lateral eye movements evoked by linear head motion were evaluated in human subjects by subtracting the eye movement responses to headcentred angular oscillation in the dark, about a vertical axis, from the responses evoked by similar oscillation with the head displaced 30 cm eccentrically from the axis. The centred oscillation gave a purely angular stimulus whereas the eccentric oscillation gave an additional tangential linear acceleration acting laterally to the head. The stimuli used were relatively unpredictable, enveloped sinewaves at 0.02 to 1.2 Hz, 60°/s peak angular velocity, 0.004 to 0.24 g peak tangential acceleration, and subjects were either given no instructions or were told to imagine fixating on targets at 60 cm or 5 m distance. Eye movements of significantly higher velocity were evoked in the eccentric position, particularly at the higher frequencies and when subjects imagined near targets. The increase in velocity of eye movement was attributed to the linear stimulus and probably derives from stimulation of the otolith organs. The frequency response of the gain (°/s/g) of these movements gave an approximate slope of –1, indicating that the eye velocity bears a constant proportionality to linear head velocity. The findings are in accord with the theoretical prediction that eye movements compensating for linear head motion should only be required for viewing near targets. These otolithic influences on eye movements could either the mediated by a direct otolith-ocular reflex which is subservient to viewing conditions or, alternatively, the otolith signals may modify the activity of other oculomotor mechanisms.A. M. Bronstein was supported by The Brain Research Trust     

The human vertical vestibulo-ocular reflex during combined linear and angular acceleration with near-target fixation

The purpose of this study was to examine the effect of fixation target distance on the human vestibuloocular reflex (VOR) during eccentric rotation in pitch. Such rotation induces both angular and linear acceleration. Eight normal subjects viewed earth-fixed targets that were either remote or near to the eyes during wholebody rotation about an earth-horizontal axis that was either oculocentric or 15 cm posterior (eccentric) to the eyes. Eye and head movements were recorded using magnetic search coils. Using a servomotor-driven chair, passive whole-body rotations were delivered as trains of single-frequency sinusoids at frequencies from 0.8 to 2.0 Hz and as pseudorandom impulses of acceleration. In the light, the visually enhanced VOR (VVOR) was recorded while subjects were asked to fixate targets at one of several distances. In darkness, subjects were asked to remember targets that had been viewed immediately prior to the rotation. In order to eliminate slip of the retinal image of a near target when the axis of rotation of the head is posterior to the eyes, the ideal gain (compensatory eye velocity divided by head velocity) of the VVOR and VOR must exceed 1.0. Both the VOR and VVOR were found to have significantly enhanced gains during sinusoidal and pseudorandom impulses of rotation (P<0.05). Enhancement of VVOR gain was greatest at low frequencies of head rotation and decreased with increasing frequency. However, enhanced VOR gain only slightly exceeded 1.0, and VVOR gain enhancement was significantly lower than the expected ideal values for the stimulus conditions employed (P<0.05). During oculocentric rotations with near targets, both the VOR and VVOR tended to exhibit small phase leads that increased with rotational frequency. In contrast, during eccentric rotations with near targets, there were small phase lags that increased with frequency. Visual tracking contributes during ocular compensatory responses to sustained head rotation, although the latency of visual tracking reflexes exceeds 100 ms. In order to study initial vestibular responses prior to modification by visual tracking, we presented impulses of head acceleration in pseudorandom sequence of initial positions and directions, and evaluated the ocular response in the epoch from 25 to 80 ms after movement onset. As with sinusoidal rotations, pseudorandom eccentric head rotation in the presence of a near, earth-fixed target was associated with enhancement of VVOR and VOR gains in the interval from 25 to 80 ms from movement onset. Despite the inability of visual tracking to contribute to these responses, VVOR gain significantly exceeded VOR gain for pseudorandom accelerations. This gain enhancement indicates that target distance and linear motion of the head are considered by the human ocular motor system in adjustment of performance of the early VOR, prior to a contribution by visual following reflexes. Vergence was appropriate to target distance during all VVOR rotations, but varied during VOR rotations with remembered targets. For the 3-m target distance, vergence during the VOR was stable over each entire trial but slightly exceeded the ideal value. For the 0.1-m near target, instantaneous vergence during the VOR typically declined gradually in a manner not corresponding to the time course of instantaneous VOR gain change; mean vergence over entire trials ranged from 60 to 90% of ideal, corresponding to target distances for which ideal gain would be much higher than actually observed. These findings suggest a dissociation between vergence and VOR gain during eccentric rotation with near targets in the frequency range from 0.8 to 2.0 Hz.     

Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation

To compare and contrast the neural mechanisms that contribute to vestibular perception and action, we measured vestibuloocular reflexes (VOR) and perceptions of tilt and translation. We took advantage of the well-known ambiguity that the otolith organs respond to both linear acceleration and tilt with respect to gravity and investigated the mechanisms by which this ambiguity is resolved. A new motion paradigm that combined roll tilt with inter-aural translation ("Tilt&Translation") was used; subjects were sinusoidally (0.8 Hz) roll tilted but with their ears above or below the rotation axis. This paradigm provided sinusoidal roll canal cues that were the same across trials while providing otolith cues that varied linearly with ear position relative to the earth-horizontal rotation axis. We found that perceived tilt and translation depended on canal cues, with substantial roll tilt and inter-aural translation perceptions reported even when the otolith organs measured no inter-aural force. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs that varied linearly with radius; a minimal response was measured when the otolith organs transduced little or no inter-aural force. Hence, the horizontal translational VOR was dependent on otolith cues but independent of canal cues. These findings match predictions that translational VORs are elicited by simple filtering of otolith signals. We conclude that internal models govern human perception of tilt and translation at 0.8 Hz and that high-pass filtering governs the human translational VOR at this same frequency.     

Impairments in the initial horizontal vestibulo-ocular reflex of older humans

To determine age-related changes, the initial horizontal vestibulo-ocular reflex (VOR) of 11 younger normal subjects (aged 20–32 years) was compared with that of 12 older subjects (aged 58–69 years) in response to random transients of whole-body acceleration of 1,000 and 2,800°/s² delivered around eccentric vertical axes ranging from 10 cm anterior to 20 cm posterior to the eyes. Eye and head positions were sampled at 1,200 Hz using magnetic search coils. Subjects fixed targets 500 cm or 15 cm distant immediately before the unpredictable onset of rotation in darkness. For all testing conditions, younger subjects exhibited compensatory VOR slow phases with early gain (eye velocity/head velocity, interval 35–45 ms from onset of rotation) of 0.90±0.02 (mean ± SEM) for the higher head acceleration, and 0.79±0.02 for the lower acceleration. Older subjects had significantly (P<0.0001) lower early gain of 0.77±0.04 for the higher head acceleration and 0.70±0.02 for the lower acceleration. Late gain (125–135 ms from onset of rotation) was similar for the higher and lower head accelerations in younger subjects. Older subjects had significantly lower late gain at the higher head acceleration, but gain similar to the younger subjects at the lower acceleration. All younger subjects maintained slow-phase VOR eye velocity to values ≥200°/s throughout the 250-ms rotation, but, after an average of 120 ms rotation (mean eccentricity 13°), 8 older subjects consistently had abrupt declines (ADs) in slow-phase VOR velocity to 0°/s or even the anticompensatory direction. These ADs were failures of the VOR slow phase rather than saccades and were more frequent with the near target at the higher acceleration. Slow-phase latencies were 14.4±0.4 ms and 16.8±0.4 ms for older subjects at the higher and lower accelerations, significantly longer than comparable latencies of 10.0±0.5 ms and 12.0±0.6 ms for younger subjects. Late VOR gain modulation with target distance was significantly attenuated in older subjects only for the higher head acceleration. Electronic Publication     

A non-visual mechanism for voluntary cancellation of the vestibulo-ocular reflex

Summary Squirrel monkeys were trained to cancel their vestibulo-ocular reflex (VOR) by fixating a visual target that was head stationary during passive vestibular stimulation. The monkeys were seated on a vestibular turntable, and their heads were restrained. A small visual target (0.2°) was projected from the vestibular turntable onto a tangent screen. The monkeys' ability to suppress their VOR by fixating a head stationary target while the turntable was moving was compared to their ability to pursue the target when it was moved in the same manner.Squirrel monkeys were better able to suppress their VOR when the turntable was moved at high velocities than they were able to pursue targets that were moving at high velocities. The gaze velocity gain during VOR cancellation began to decrease when the head velocity was above 80°/s, and was greater than 0.6 when the head velocity was above 150°/s. However, gaze velocity gain during smooth pursuit decreased significantly when the target velocity was greater than 60°/s, and was less than 0.4 when the target velocity was 150°/s or more.The latency of VOR suppression was significantly shorter than the latency of smooth pursuit while the monkey was cancelling its VOR. When an unpredictable step change in head acceleration was generated while the monkey was cancelling its VOR, the VOR evoked by the head acceleration step began to be suppressed shortly after the initiation of the step ( 30 ms). On the other hand, the latency of the smooth pursuit eye movement elicited when the visual target was accelerated in the same manner during VOR cancellation was 100 ms. The comparison between these two results suggests that the monkeys did not use visual information related to target motion to suppress their VOR at an early latency.The monkeys' ability to suppress the VOR evoked by an unexpected change in head acceleration depended on the size of the head acceleration step. The VOR evoked by unexpected step changes in head acceleration was progressively less suppressed at an early latency as the size of the acceleration step increased, and was not suppressed at an early latency when the step change in head acceleration was greater than 500°/s².During smooth pursuit eye movements, unexpected step changes in head acceleration evoked a VOR that was suppressed at an early latency ( 50 ms) if the head movement was in the same direction as the ongoing smooth pursuit eye movement. The amount of early VOR suppression increased as the pursuit eye velocity increased.We conclude that squirrel monkeys utilize a fast, non-visual mechanism for cancelling their VOR while they are fixating a visual target and their head is moving. This non-visual mechanism appears to be turned on when the head is moving and the monkey is fixating a head stationary target. The mechanism probably utilizes a voluntarily gated vestibular signal to cancel the signals in VOR pathways at the level of the extraocular motorneurons. Although the VOR cancellation mechanism is not capable of completely suppressing the VOR evoked by large unexpected changes in head acceleration, we suggest that it is capable of suppressing the VOR generated by most voluntary head movements during combined eye and head gaze pursuit and that the function of this gated VOR cancellation system is to extend the range and accuracy of eye-head tracking movements.     

Effect of adaptation to telescopic spectacles on the initial human horizontal vestibuloocular reflex

Gain of the vestibuloocular reflex (VOR) not only varies with target distance and rotational axis, but can be chronically modified in response to prolonged wearing of head-mounted magnifiers. This study examined the effect of adaptation to telescopic spectacles on the variation of the VOR with changes in target distance and yaw rotational axis for head velocity transients having peak accelerations of 2,800 and 1,000 degrees /s(2). Eye and head movements were recorded with search coils in 10 subjects who underwent whole body rotations around vertical axes that were 10 cm anterior to the eyes, centered between the eyes, between the otoliths, or 20 cm posterior to the eyes. Immediately before each rotation, subjects viewed a target 15 or 500 cm distant. Lighting was extinguished immediately before and was restored after completion of each rotation. After initial rotations, subjects wore 1.9x magnification binocular telescopic spectacles during their daily activities for at least 6 h. Test spectacles were removed and measurement rotations were repeated. Of the eight subjects tolerant of adaptation to the telescopes, six demonstrated VOR gain enhancement after adaptation, while gain in two subjects was not increased. For all subjects, the earliest VOR began 7-10 ms after onset of head rotation regardless of axis eccentricity or target distance. Regardless of adaptation, VOR gain for the proximate target exceeded that for the distant target beginning at 20 ms after onset of head rotation. Adaptation increased VOR gain as measured 90-100 ms after head rotation onset by an average of 0.12 +/- 0.02 (SE) for the higher head acceleration and 0.19 +/- 0.02 for the lower head acceleration. After adaptation, four subjects exhibited significant increases in the canal VOR gain only, whereas two subjects exhibited significant increases in both angular and linear VOR gains. The latencies of linear and early angular target distance effects on VOR gain were unaffected by adaptation. The earliest significant change in angular VOR gain in response to adaptation occurred 50 and 68 ms after onset of the 2,800 and 1,000 degrees /s(2) peak head accelerations, respectively. The latency of the adaptive increase in linear VOR gain was approximately 50 ms for the peak head acceleration of 2,800 degrees /s(2), and 100 ms for the peak head acceleration of 1,000 degrees /s(2). Thus VOR gain changes and latency were consistent with modification in the angular VOR in most subjects, and additionally in the linear VOR in a minority of subjects.     

Interaural self-motion linear velocity thresholds are shifted by roll vection

The otolith organs respond equivalently to changes in gravitational force due to head tilt and to changes in inertial force due to linear acceleration. It has been shown that the central nervous system (CNS) uses internal models of the laws of physics to distinguish tilt from translation. Models with these internal models predict that illusory tilt, if large enough, will be accompanied by an illusion of linear motion. To investigate this prediction, we measured interaural, self-motion, direction-detection thresholds in darkness and with roll optokinetic stimulation. Each lateral translation consisted of a single cycle of sinusoidal acceleration, after which subjects indicated whether they translated to the left or right. We found that the interaural direction-detection threshold measured during clockwise and counterclockwise optokinetic stimulation shifted in opposite directions relative to thresholds in darkness. Using a generalized linear model, we determined that this finding was statistically significant (P < 0.005) and is consistent with the prediction that illusory tilt should be accompanied by a non-zero neural estimate of linear velocity that, if large enough (supra-threshold), contributes to translation perception.

Noncommutative control in the rotational vestibuloocular reflex

To investigate the role of noncommutative computations in the oculomotor system, three-dimensional (3D) eye movements were measured in seven healthy subjects using a memory-contingent vestibulooculomotor paradigm. Subjects had to fixate a luminous point target that appeared briefly at an eccentricity of 20 degrees in one of four diagonal directions in otherwise complete darkness. After a fixation period of approximately 1 s, the subject was moved through a sequence of two rotations about mutually orthogonal axes in one of two orders (30 degrees yaw followed by 30 degrees pitch and vice versa in upright and 30 degrees yaw followed by 20 degrees roll and vice versa in both upright and supine orientations). We found that the change in ocular torsion induced by consecutive rotations about the yaw and the pitch axis depended on the order of rotations as predicted by 3D rotation kinematics. Similarly, after rotations about the yaw and roll axis, torsion depended on the order of rotations but now due to the change in final head orientation relative to gravity. Quantitative analyses of these ocular responses revealed that the rotational vestibuloocular reflexes (VORs) in far vision closely matched the predictions of 3D rotation kinematics. We conclude that the brain uses an optimal VOR strategy with the restriction of a reduced torsional position gain. This restriction implies a limited oculomotor range in torsion and systematic tilts of the angular eye velocity as a function of gaze direction.     

Non-linear interaction of angular and translational vestibulo-ocular reflex during eccentric rotation in the monkey

Eccentric sinusoidal rotation with the nose facing out or in leads to gain modulation of the vestibulo-ocular reflex (VOR), which is a result of an interaction between angular and translational VOR. There are conflicting reports with regard to the type of interaction. Combined angular and translational VOR during eccentric sinusoidal rotations over a wide range of target distances (12-180 cm), eccentricities (centric, 30 and 50 cm nose-out and nose-in eccentric) and frequencies (0.1-4 Hz) were studied in macaque monkeys trained to fixate earth-stationary light-emitting diode (LED) targets while binocular eye positions were measured using magnetic search coils. The monkeys were also exposed to sudden unpredictable position steps with peak accelerations of 500 degrees/s(2) using similar eccentricities and target distances. VOR gain enhancement during nose-out eccentric sinusoidal rotation was almost compensatory when the target was visible and was independent of stimulus frequency. Mean responses were still close to ideal when the target was extinguished; however, individual data showed increased variability. Sensitivities of the translational portion of the combined VOR were compensatory. These sensitivities were clearly reduced during nose-in eccentric sinusoidal rotation. Thus, especially for close targets at 4 Hz combined VOR was not compensatory, independent of target visibility. VOR elicited by sudden position steps showed a sequential response: (1) purely angular VOR (up to 40-45 ms); (2) additional translational VOR that was not modulated by target distance (45-65 ms); and (3) translational VOR weighted for target location (>65 ms). We conclude that angular and translational VOR have different latencies during transient accelerations and interact differently during agonistic (nose-out) and antagonistic stimulation (nose-in).     

Dynamics model for analyzing reaching movements during active and passive torso rotation

We have developed an inverse dynamics model of unrestrained natural reaching movements. Such movements are usually not planar and often involve complex deformation of the shoulder girdle as well as rotary and linear torso motion. Our model takes as its input kinematic data about the positions of the finger, wrist, elbow, left and right acromion processes, and the sternum and produces the torques and forces developed at the shoulder, elbow, and wrist joints. The model can also be used to simulate the consequences of introducing passive torso rotation or linear acceleration on arm movements and to simulate the consequences of applying mechanical perturbations to the reaching limb. It separately quantifies the contributions of inertial forces resulting from torso rotation and translation. In experimental paradigms involving arm movements, different dynamic components can be present such as active or passive torso rotation and translation, external forces and Coriolis forces. Our model provides a means of evaluating the different sources of force and the total muscle force needed to control the trajectory of the arm in their presence.

Enhancement of the vestibulo-ocular reflex by prior eye movements.

We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by approximately 20% of head velocity; gaze velocity subsequently declined to zero within approximately 300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0. 8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects (P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this "priming" effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.     

Vertical (Z-axis) acceleration alters the ocular response to linear acceleration in the rabbit

Whether ocular orientation to gravity is produced solely by linear acceleration in the horizontal plane of the head or depends on both horizontal and vertical components of the acceleration of gravity is controversial. Here, we compared orienting eye movements of rabbits during head tilt to those produced by centrifugation that generated centripetal acceleration along the naso-occipital (X-), bitemporal (Y-) and vertical (Z-) axes in a constant gravitational field. Sensitivities of ocular counter-pitch and vergence during pitch tilts were ≈25°/g and ≈26°/g, respectively, and of ocular counter-roll during roll tilts was ≈20°/g. During X-axis centripetal acceleration with 1 g of gravity along the Z-axis, pitch and vergence sensitivities were reduced to ≈13°/g and ≈16°/g. Similarly, Y-axis acceleration with 1g along the Z-axis reduced the roll sensitivity to ≈16°/g. Modulation of Z-axis centripetal acceleration caused sensitivities to drop by ≈6°/g in pitch, ≈2°/g in vergence, and ≈5°/g in roll. Thus, the constant 1g acceleration along the Z-axis reduced the sensitivity of ocular orientation to linear accelerations in the horizontal plane. Orienting responses were also modulated by varying the head Z-axis acceleration; the sensitivity of response to Z-axis acceleration was linearly related to the response to static tilt. Although the sign of the Z-axis modulation is opposite in the lateral-eyed rabbit from that in frontal-eyed species, these data provide evidence that the brain uses both the horizontal and the vertical components of acceleration from the otolith organs to determine the magnitude of ocular orientation in response to linear acceleration.