The neurophysiological substrate for the cervico-ocular reflex in the squirrel monkey

Passive rotation of the trunk with respect to the head evoked cervico-ocular reflex (COR) eye movements in squirrel monkeys. The amplitude of the reflex varied both within and between animals, but the eye movements were always in the same direction as trunk rotation. In the dark, the COR typically had a gain of 0.3–0.4. When animals fixated earth-stationary targets during low-frequency passive neck rotation or actively tracked moving visual targets with head movements, the COR was suppressed. The COR and vestibulo-ocular reflex (VOR) summed during passive head-on-trunk rotation producing compensatory eye movements whose gain was greater than 1.0. The firing behavior of VOR-related vestibular neurons and cerebellar flocculus Purkinje cells was studied during the COR. Passive neck rotation produced changes in firing rate related to neck position and/or neck velocity in both position-vestibular-pause neurons and eye-head-vestibular neurons, although the latter neurons were much more sensitive to the COR than the former. The neck rotation signals were reduced or reversed in direction when the COR was suppressed. Flocculus Purkinje cells were relatively insensitive to COR eye movements. However, when the COR was suppressed, their firing rate was modulated by neck rotation. These neck rotation signals summed with ocular pursuit signals when the head was used to pursue targets. We suggest that the neural substrate that produces the COR includes central VOR pathways, and that the flocculus plays an important role in suppressing the reflex when it would cause relative movement of a visual target on the retina. Electronic Publication     

Rapid adaptation of torso pointing movements to perturbations of the base of support

We investigated whether pointing movements made with the torso would adapt to movement-contingent augmentation or attenuation of their spatial amplitude. The pointing task required subjects standing on a platform in the dark to orient the mid-sagittal plane of their torso to the remembered locations of just extinguished platform-fixed visual targets without moving their feet. Subjects alternated pointing at two chest-high targets, 60° apart, (1) in a baseline period with the stance platform stationary, (2) during exposure to concomitant contra or ipsiversive platform rotations that grew incrementally to 50% of the velocity of torso rotation, and (3) after return in one step to stationary platform conditions. The velocity and amplitude of torso movements relative to space decreased 25–50% during exposure to contraversive platform rotations and increased 20–50% during ipsiversive rotations. Torso rotation kinematics relative to the platform (as well as the platform-fixed targets and feet) remained virtually constant throughout the incremental exposure period. Subjects were unaware of the altered motion of their body in space imposed by the platform and did not perceive their motor adjustments. Upon return to stationary conditions, torso rotation movements were smaller and slower following adaptation to contraversive rotations and larger and faster after ipsiversive platform rotations. These results indicate a rapid sensory-motor recalibration to the altered relationship between spatial (inertial) torso motion and intended torso motion relative to the feet, and rapid re-adaptation to normal conditions. The adaptive system producing such robust torso regulation provides a critical basis for control of arm, head, and eye movements.     

Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects

One of the signatures of balance deficits observed in vestibular loss subjects is the greater instability in the roll compared to pitch planes. Directional differences in the timing and strengths of vestibular and proprioceptive sensory signals between roll and pitch may lead to a greater miscalculation of roll than pitch motion of the body in space when vestibular input is absent. For this reason, we compared the timing and amplitude of vestibular information, (observable in stimulus-induced head accelerations when subjects are tilted in different directions), with that of proprioceptive information caused by stimulus induced rotations of ankle and hip joints [observable as short latency (SL) stretch responses in leg and trunk muscle EMG activity]. We attempted to link the possible mode of sensory interaction with the deficits in balance control. Six subjects with bilaterally absent vestibular function and 12 age-matched controls were perturbed, while standing, in 8 directions of pitch and roll support surface rotation in random order. Body segment movements were recorded with a motion analysis system, head accelerations with accelerometers, and muscle activity with surface EMG. Information on stimulus pitch motion was available sequentially. Pitch movements of the support surface were best coded in amplitude by ankle rotation velocity, and by head vertical linear acceleration, which started at 13 ms after the onset of ankle rotation. EMG SL reflex responses in soleus with onsets at 46 ms provided a distal proprioceptive correlate to the pitch motion. Roll information on the stimulus was available simultaneously. Hip adduction and lumbo-sacral angular velocity were represented neurally as directionally specific short latency stretch and unloading reflexes in the bilateral gluteus medius muscles and paraspinal muscles with onsets at 28 ms. Roll angular accelerations of the head coded roll amplitude and direction at the same time (31 ms). Significant differences in amplitude coding between vestibular loss subjects and controls were only observed as a weaker coding between stimulus motion and head roll and head lateral linear accelerations. The absence of vestibular inputs in vestibular loss subjects led to characteristic larger trunk in motion in roll in the direction of tilt compared to pitch with respect to controls. This was preceded by less uphill flexion and no downhill extension of the legs in vestibular loss subjects. Downhill arm abduction responses were also greater. These results suggest that in man vestibular inputs provide critical information necessary for the appropriate modulation of roll balance-correcting responses in the form of stabilising knee and arm movements. The simultaneous arrival of roll sensory information in controls may indicate that proprioceptive and vestibular signals can only be interpreted correctly when both are present. Thus, roll proprioceptive information may be interpreted inaccurately in vestibular loss subjects, leading to an incorrect perception of body tilt and insufficient uphill knee flexion, especially as cervico-collic signals appear less reliable in these subjects as an alternative sensory input.     

Interaction between cervico-ocular and vestibulo-ocular reflexes in normal adults

Summary The interaction of the cervico-ocular reflex (COR) and the vestibulo-ocular reflex (VOR) was studied in 20 human Subjects (Ss) during application of synergistic and antagonistic combinations of neck and vestibular stimuli, and during two different psychophysical tasks related to the Ss' self-motion sensation. Slow and quick eye movement responses were analyzed separately. Neck stimulation produced by horizontal rotation of the trunk about the stationary head elicited slow COR eye movements of very low gain; COR direction was anticompensatory, unlike the compensatory one of the VOR. During either a synergistic combination of neck and labyrinthine stimuli (head rotation on stationary trunk) or an antagonistic combination (head-to-trunk rotation counter to head-in-space rotation), the resulting slow eye movements were slightly larger than those during labyrinthine stimulation alone (whole body rotation). This weak neck contribution could be described by a directionally non-specific enhancement of VOR gain and a linear summation of VOR and COR slow phases. These effects were essentially independent of whether the Ss estimated the magnitude of their head turning or trunk turning in space. If Ss were estimating their trunk turning, neck stimulation also evoked quick eye movements, but these were small and hardly affected the VOR quick phases during the combined stimulations. In contrast, if Ss estimated their head turning, neck stimulation evoked large quick phases, which interfered with the quick phases of the VOR; during the synergistic combination of head and neck stimuli. COR quick phases added to those of the VOR, thereby shifting the gaze in the direction of head rotation (reorientation of gaze). With the antagonistic combination they subtracted, so that the VOR slow phase could compensate the head rotation in space (stabilization of gaze). These findings suggest that (1) the slow phase of the COR has no functional significance in intact humans and (2) the quick phase of the COR plays a role for both stabilization and reorientation of gaze depending on the behavioural context.Supported by DFG grants Ju 163/1-1 and Me 715/1-2     

Visual object localisation in space

Perceptual updating of the location of visual targets in space after intervening eye, head or trunk movements requires an interaction between several afferent signals (visual, oculomotor efference copy, vestibular, proprioceptive). The nature of the interaction is still a matter of debate. To address this problem, we presented subjects (n=6) in the dark with a target (light spot) at various horizontal eccentricities (up to +/-20 degrees ) relative to the initially determined subjective straight-ahead direction (SSA). After a memory period of 12 s in complete darkness, the target reappeared at a random position and subjects were to reproduce its previous location in space using a remote control. For both the presentation and the reproduction of the target's location, subjects either kept their gaze in the SSA (retinal viewing condition) or fixated the eccentric target (visuo-oculomotor). Three experimental series were performed: A, "visual-only series": reproduction of the target's location in space was found to be close to ideal, independently of viewing condition; estimation curves (reproduced vs presented positions) showed intercepts approximately 0 degrees and slopes approximately 1; B, "visual-vestibular series": during the memory period, subjects were horizontally rotated to the right or left by 10 degrees or 18 degrees at 0.8-Hz or 0.1-Hz dominant frequency. Following the 0.8-Hz body rotation, reproduction was close to ideal, while at 0.1 Hz it was partially shifted along with the body, in line with the known vestibular high-pass characteristics. Additionally, eccentricity of target presentation reduced the slopes of the estimation curves (less than 1); C, "visual-vestibular-neck series": a shift toward the trunk also occurred after low-frequency neck stimulation (trunk rotated about stationary head). When vestibular and neck stimuli were combined (independent head and trunk rotations), their effects summed linearly, such that the errors cancelled each other during head rotation on the stationary trunk. Variability of responses was always lowest for targets presented at SSA, irrespective of intervening eye, head or trunk rotations. We conclude that: (1) subjects referenced "space" to pre-rotatory SSA and that the memory trace of the target's location in space was not altered during the memory period; and that (2) they used internal estimates of eye, head and trunk displacements with respect to space to match current target position with the memory trace during reproduction; these estimates would be obtained by inverting the physical coordinate transformations produced by these displacements. We present a model which is able to describe these operations and whose predictions closely parallel the experimental results. In this model the estimate of head rotation in space is not obtained directly from the vestibular head-in-space signal, but from a vestibular estimate of the kinematic state of the body support.     

The effects of head and trunk position on torsional vestibular and optokinetic eye movements in humans

We measured torsional vestibular and optokinetic eye movements in human subjects with the head and trunk erect, with the head supine and the trunk erect, and with the head and trunk supine, in order to quantify the effects of otolithic and proprioceptive modulation. During active head movements, the torsional vestibulo-ocular reflex (VOR) had significantly higher gain with the head upright than with the head supine, indicating that dynamic otolithic inputs can supplement the semicircular canal-ocular reflex. During passive earth-vertical axis rotation, torsional VOR gain was similar with the head and trunk supine and with the head supine and the trunk erect. This finding implies that static proprioceptive information from the neck and trunk has little effect upon the torsional VOR. VOR gain with the head supine was not increased by active, self-generated head movement compared with passive, whole body rotation, indicating that the torsional VOR is not augmented by dynamic proprioceptive inputs or by an efference copy of a command for head movement. Viewing earth-fixed surroundings enhanced the torsional VOR, while fixating a chair-fixed target suppressed the VOR, especially at low frequencies. Torsional optokinetic nystagmus (OKN) evoked by a full-field stimulus had a mean slow-phase gain of 0.22 for 10°/s drum rotation, but gain fell to 0.06 for 80°/s stimuli. Despite this fall in gain, mean OKN slow-phase velocities increased with drum speed, reaching maxima of 2.5°/s–8.0°/s in our subjects. Optokinetic afternystagmus (OKAN) was typically absent. Torsional OKN and OKAN were not modified by otolithic or proprioceptive changes caused by altering head and trunk position with respect to gravity. Torsional velocity storage is negligible in humans, regardless of head orientation.Presented in part at the Society for Neuroscience Annual Meeting, October 31, 1989, Phoenix, AZ     

Neck proprioception compensates for age-related deterioration of vestibular self-motion perception

Vestibular functions are known to show some deterioration with age. Vestibular deterioration is often thought to be compensated for by an increase in neck proprioceptive gain. We studied this presumed compensatory mechanism by measuring psychophysical responses to vestibular (horizontal canal), neck and combined stimuli in 50 healthy human subjects as a function of age (range 15–76 years). After passive horizontal rotations of head and/or trunk (torso) in complete darkness (dominant frequencies 0.05, 0.1, and 0.4 Hz), subjects readjusted a visual target to its remembered prerotational location in space. (1) Vestibular-only stimulus (whole-body rotation); subjects' responses were shifted towards postrotatory body position, this only slightly at 0.4 Hz and pronounced at 0.1 and 0.05 Hz. These errors reflect the known physiological drop of vestibular gain at low rotational frequency. They exhibited a slight but significant increase with age. (2) Neck-only stimulus (trunk rotated, head stationary); the responses showed errors similar to those upon vestibular stimulation (with offset towards postrotatory trunk position) and this again slightly more with increasing age. (3) Vestibular-neck stimulus combination during head rotation on stationary trunk; the errors were close to zero, independent of stimulus frequency and the subjects' age. (4) Opposite stimulus combination (trunk rotated in the same direction as the head, but with double amplitude); the errors were clearly enhanced, essentially reflecting the sum of those with vestibular-only and neck-only stimulation. Taken together, we find a parallel increase in neck- and vestibular-related errors with age, in seeming contrast to previous studies. We explain our and the previous findings by a vestibular-neck interaction model in which two different neck signals are involved. One neck signal is used, in combination with the vestibular signal, for estimating trunk-in-space rotation. It is internally shaped to always match the vestibular signal, so that these two signals cancel each other out when summed during head rotation on stationary trunk. Because of this matching, perceived trunk stationariness during head rotation on the stationary trunk is independent of vestibular deterioration (related to stimulus frequency, age, ototoxic medication, etc.). The other neck proprioceptive signal, coding head-on-trunk rotation, is superimposed on the estimate of trunk-in-space rotation, thereby yielding a notion of head-in-space. This neck signal remains essentially unchanged with vestibular deterioration. Generally, we hold that the transformation of the vestibular signal from the head down to the trunk proceeds further to include the hip and the legs as well as the haptically perceived body support surface; by this, subjects yield a notion of support kinematics in space. As a consequence, spatial orientation is impaired by chronic vestibular deterioration only to the extent that the body support is moving in space, while it is unimpaired (determined by proprioception alone) during body motion with respect to a stationary support. Electronic Publication     

Eye movements during multi-axis whole-body rotations

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

Interaction of the body, head, and eyes during walking and turning

Body, head, and eye movements were measured in five subjects during straight walking and while turning corners. The purpose was to determine how well the head and eyes followed the linear trajectory of the body in space and whether head orientation followed changes in the gravito-inertial acceleration vector (GIA). Head and body movements were measured with a video-based motion analysis system and horizontal, vertical, and torsional eye movements with video-oculography. During straight walking, there was lateral body motion at the stride frequency, which was at half the frequency of stepping. The GIA oscillated about the direction of heading, according to the acceleration and deceleration associated with heel strike and toe flexion, and the body yawed in concert with stepping. Despite the linear and rotatory motions of the head and body, the head pointed along the forward motion of the body during straight walking. The head pitch/roll component appeared to compensate for vertical and horizontal acceleration of the head rather than orienting to the tilt of the GIA or anticipating it. When turning corners, subjects walked on a 50-cm radius over two steps or on a 200-cm radius in five to seven steps. Maximum centripetal accelerations in sharp turns were ca.0.4 g, which tilted the GIA ca.21 degrees with regard to the heading. This was anticipated by a roll tilt of the head of up to 8 degrees. The eyes rolled 1-1.5 degrees and moved down into the direction of linear acceleration during the tilts of the GIA. Yaw head deviations moved smoothly through the turn, anticipating the shift in lateral body trajectory by as much as 25 degrees. The trunk did not anticipate the change in trajectory. Thus, in contrast to straight walking, the tilt axes of the head and the GIA tended to align during turns. Gaze was stable in space during the slow phases and jumped forward in saccades along the trajectory, leading it by larger angles when the angular velocity of turning was greater. The anticipatory roll head movements during turning are likely to be utilized to overcome inertial forces that would destabilize balance during turning. The data show that compensatory eye, head, and body movements stabilize gaze during straight walking, while orienting mechanisms direct the eyes, head, and body to tilts of the GIA in space during turning.     

Optically induced plasticity of the cervico-ocular reflex in patients with bilateral absence of vestibular function

The horizontal cervico-ocular reflex (COR) was examined in five labyrinthine-defictive subjects (LDS), during both passive oscillations of the head on the trunk (HTexam) and of the trunk under the earthfixed head (THexam) at 0.1–0.5 Hz, peak angular displacement ±30°. Subjects were tested in the dark, before and immediately after adaptation to binocular magnifying (x1.9) and reducing (x0.6) lenses. During long-term adaptation, the LDS were exposed to the normal environment for 5 h while wearing lenses. Short-term adaptation experiments (15–20 min) consisted of sustained ocular following of a small LED in an otherwise dark room and in full-room illumination. This LED was either stationary in space whilst the subjects moved their head actively, or fixed on the chair and rotating with the trunk during head-fixed stimulation. In all five patients, magnifying lenses increased COR gain (peak slow-phase eye velocity/peak stimulus velocity), whereas reducing lenses reduced the gain. Under HTexam the gain changes were greater, more consistent and the phases approximately compensatory to head displacement, whereas during THexam the gain decreased and phase increased at higher frequencies. COR adaptation was observed during foveal stimulation alone, but the effects were stronger with added background illumination. Results during an imaginary target task showed that the gain can be influenced strongly by mental set. Our findings indicate a highly modifiable COR in subjects with loss of vestibular function. Both peripheral and foveal retinal information contribute to the plastic changes in COR gain. Somatosensory cues from the trunk as well as cognitive/perceptual factors may be involved in the modification of the COR, by providing information about the relevance of eye movements, and contribute to the stabilisation of gaze in space.     

Perception of horizontal head and trunk rotation: modification of neck input following loss of vestibular function

Chronic loss of vestibular function modifies the role of neck afferents in human perception of self-motion. We characterized this change by comparing the self-motion perception of patients with chronic vestibular loss (Ps) to that of normal subjects (Ns). Stimuli consisted of sinusoidal horizontal rotations (0.025–0.4 Hz) of the trunk relative to the head (neck stimulation) and/or of the head in space (vestibular stimulation). Perception of head rotation relative to the trunk, of trunk rotation in space, or of head rotation in space was assessed in terms of gain and phase (veridical perception, G=1 and =0°) as well as detection threshold using a pointing procedure. (1) Perception of head rotation relative to the trunk (neck proprioception). Ps' detection threshold of head-to-trunk rotation was normal (i.e. similar to that of Ns) across all frequencies tested. Also, with peak angular velocities above 5°/s, the gain of their perception was approximately normal. When peak velocity was decreased below this value, however, either by lowering stimulus frequency with peak displacement kept constant (±8°) or by decreasing peak displacement at constant frequency (0.05 Hz), the gain increased above unity, unlike in Ns. In contrast, the phase remained normal (approximately 0°). (2) Perception of trunk rotation in space. Ps perceived their trunks as stationary during neck stimulation and all vestibular-neck combinations at medium to low frequencies. At 0.4 Hz, however, Ps consistently perceived the trunk rotation, conceivably due to somatosensory selfmotion cues arising from high body acceleration. In contrast, Ns perceive a trunk-in-space rotation with the neck stimulation and most of the stimulus combinations across the whole frequency range tested. Ns perceived their trunks as stationary only during head rotation on the stationary trunk (presumed to reflect a mutual cancellation of neck and vestibular signals). (3) Perception of head rotation in space. In Ps, unlike Ns, this perception always resembled that of head rotation relative to the trunk. (4) When Ps were presented with a visual or somatosensory space reference (not motion cues), their perception of trunk and head rotation in space became approximately normal. (5) We suggest that there are basically two changes in the neck induced self motion perception associated with chronic vestibular loss. First, neck proprioception shows a non linear gain that overemphasizes low stimulus velocities, for unknown reasons. Second, the neck signal which normally is used for the perception of trunk rotation in space is suppressed (Ps in the dark, deprived of any space reference, resort to the notion that their trunks are stationary). The change in Ps' perception of head rotation in space is attributed to the former two changes (assuming that they superimposed their notion of head on trunk rotation on that of a stationary trunk).     

Galvanic stimulation of the vestibular periphery in guinea pigs during passive whole body rotation and self-generated head movement

Irregular vestibular afferents exhibit significant phase leads with respect to angular velocity of the head in space. This characteristic and their connectivity with vestibulospinal neurons suggest a functionally important role for these afferents in producing the vestibulo-collic reflex (VCR). A goal of these experiments was to test this hypothesis with the use of weak galvanic stimulation of the vestibular periphery (GVS) to selectively activate or suppress irregular afferents during passive whole body rotation of guinea pigs that could freely move their heads. Both inhibitory and excitatory GVS had significant effects on compensatory head movements during sinusoidal and transient whole body rotations. Unexpectedly, GVS also strongly affected the vestibulo-ocular reflex (VOR) during passive whole body rotation. The effect of GVS on the VOR was comparable in light and darkness and whether the head was restrained or unrestrained. Significantly, there was no effect of GVS on compensatory eye and head movements during volitional head motion, a confirmation of our previous study that demonstrated the extravestibular nature of anticipatory eye movements that compensate for voluntary head movements.     

Effects of walking velocity on vertical head and body movements during locomotion

 Trunk and head movements were characterized over a wide range of walking speeds to determine the relationship between stride length, stepping frequency, vertical head translation, pitch rotation of the head, and pitch trunk rotation as a function of gait velocity. Subjects (26–44 years old) walked on a linear treadmill at velocities of 0.6–2.2 m/s. The head and trunk were modeled as rigid bodies, and rotation and translation were determined using a video-based motion analysis system. At walking speeds up to 1.2 m/s there was little head pitch movement in space, and the head pitch relative to the trunk was compensatory for trunk pitch. As walking velocity increased, trunk pitch remained approximately invariant, but a significant head translation developed. This head translation induced compensatory head pitch in space, which tended to point the head at a fixed point in front of the subject that remained approximately invariant with regard to walking speed. The predominant frequency of head translation and rotation was restricted to a narrow range from 1.4 Hz at 0.6 m/s to 2.5 Hz at 2.2 m/s. Within the range of 0.8–1.8 m/s, subjects tended to increase their stride length rather than step frequency to walk faster, maintaining the predominant frequency of head movement at close to 2.0 Hz. At walking speeds above 1.2 m/s, head pitch in space was highly coherent with, and compensatory for, vertical head translation. In the range 1.2–1.8 m/s, the power spectrum of vertical head translation was the most highly tuned, and the relationship between walking speed and head and trunk movements was the most linear. We define this as an optimal range of walking velocity with regard to head-trunk coordination. The coordination of head and trunk movement was less coherent at walking velocities below 1.2 m/s and above 1.8 m/s. These results suggest that two mechanisms are utilized to maintain a stable head fixation distance over the optimal range of walking velocities. The relative contribution of each mechanism to head orientation depends on the frequency of head movement and consequently on walking velocity. From consideration of the frequency characteristics of the compensatory head pitch, we infer that compensatory head pitch movements may be produced predominantly by the angular vestibulocollic reflex (aVCR) at low walking speeds and by the linear vestibulocollic reflex (lVCR) at the higher speeds. Received: 23 October 1998 / Accepted: 27 January 1999     

Guidance of visual direction by topographical vibrotactile cues on the torso

Vibration on localised areas of skin can be used to signal spatial orientation, multi-directional motion and also to guide arm and hand movements. This study investigated the possibility that vibration at loci on the skin might also be used to cue gaze direction. Eight subjects made eye or (head + eye) gaze saccades in the dark cued by vibration stimulation at discrete loci spaced on a horizontal contour across the chest. Saccade and gaze amplitudes, latencies, and directions were analysed. In the first experiment, performed without training, subjects could only use vibration cues to direct their gaze in cardinal directions and gross quadrature. There was a high variability in the relationship between locus on the trunk and gaze direction in space, both within and between subjects. Saccade latencies ranged from 377 to 433 ms and were related to the loci of vibration; the further from the body midline the quicker the response. Since the association of skin loci with gaze direction did not appear intuitive a sub-group of four subjects were retested after intensive training with feedback until they attained criterion on midline ≡ 0° and 15 cm (to right/left of midline) ≡ 45° gaze shifts right and left. Training gave a moderate improvement in directional specificity of gaze to a particular locus on the skin. Gaze direction was linearly rescaled with respect to skin loci but variability and saccade latencies remained high. The uncertainty in the relationship between vibration locus and gaze direction and the prolonged latencies of responses indicate circuitous neuronal processing. There appears to be no pre-existing stimulus-response compatibility mapping between loci on the skin and gaze direction. Vibrotactile cues on the skin of the trunk only serve a gross indication of visual direction in space.     

Modification of per- and postrotational responses by voluntary motor activity of the limbs

In order to explore interactive effects of voluntarily generated rotational stimuli on evoked vestibular responses, experiments were performed using a rotation chair in which the subject either controlled the angular motion by voluntary movement of his upper and lower limbs, or was passive-rotation being controlled by a servomotor and electromagnetic brake. In two experiments, carried out on 8 and 9 subjects respectively, it was found that cessation of sustained passive rotation by voluntary limb actions strongly suppressed the postrotational turning sensation but did not alter the evoked nystagmus. Limb movements that were directionally concordant with muscle torque in generating body rotation yielded arthrokinetic effects which augmented perrotational nystagmus and sustained the sensation of turning. The postrotational sensation of turning and postrotational nystagmus produced by voluntary cessation of active rotation were reduced relative to responses produced by passive turning and stopping. The Purkinje effect induced by postrotational head movements was similarly reduced following voluntary cessation of active rotation.     

The influence of head position and head reorientation on the axis of eye rotation and the vestibular time constant during postrotatory nystagmus

Summary Reorienting the head with respect to gravity during the postrotatory period alters the time course of postrotatory nystagmus (PRN), hastening its decline and thereby reducing the calculated vestibular time constant. One explanation for this phenomenon is that the head reorientation results in a corresponding reorientation of the axis of eye rotation with respect to head coordinates. This possibility was investigated in 10 human subjects whose eye movements were monitored with a three-dimensional magnetic field — search — coil technique using a variety of head reorientation paradigms in a randomized order during PRN following the termination of a 90°/s rotation about earth vertical. Average eye velocities were calculated over two time intervals: from 1 s to 2 s and from 7 s to 8 s after cessation of head rotation. The time constant was estimated as one third of the duration of PRN. For most conditions, a reorientation of the head with respect to gravity 2 s after the rotation had stopped did not significantly alter the direction of the eye velocity vector of PRN with respect to head coordinates. This strongly indicates that, in humans, PRN is mainly stabilized in head coordinates and not in space coordinates, even if the otolith input changes. This finding invalidates the notion that the shortening of PRN due to reorientation of the head could be due to a change of the eye velocity vector towards a direction (torsion), which is not detectable with the eye recording methods (electrooculography) used in earlier studies. The results regarding the vestibular time constant basically confirm earlier findings, showing a strong dependence on static head position, with the time constant being lowest if mainly the vertical canals are stimulated (60° nose up and 90° left ear down). In addition, the time constant was drastically shortened for tilts away from upright. The reduction in vestibular time constant with head reorientation cannot be explained solely on the basis of the dependence of the time constant on static head position. A clear example is provided by head reorientations back towards the upright position, which results in a decrease in the time constant, rather than an increase that would be expected on the basis of static head position.     

A new paradigm to investigate the roles of head and eye movements in the coordination of whole-body movements

Although previous studies have demonstrated the existence of coordinated eye and head movements during gaze shifts, none has studied the temporal and spatial characteristics of the various body segments during gaze transfers that require whole body movements. Without this information it is not possible to determine the extent of the interaction between the oculomotor control system and the motor control systems responsible for moving other body parts. Presented here is a detailed analysis of the timing and kinematic characteristics of participants (N=5) eye, head, upper body and feet during rotation of their body to align with light cues positioned at eccentric locations (45, 90, and 135°, left and right of centre). For all rotation amplitudes there was a clear sequence of body segment orientation (eye, head, upper body and feet) consistent with previous studies of locomotor steering and significant correlations between the onset latency times of the eyes and all body segments. There were also significant correlations between temporally aligned kinematic profiles of the feet and the eye in space for all movement amplitudes. The extent of correlation was significantly lower for displacement profiles of the feet versus head and of the feet versus upper body. These findings demonstrate substantial eye-foot coordination during a novel whole-body rotation paradigm and provide evidence that the output of the motor systems responsible for moving the feet is heavily influenced by the motor systems responsible for generating and coordinating eye and head movements to peripheral targets.     

The relation of motion sickness to the spatial–temporal properties of velocity storage

Tilting the head in roll to or from the upright while rotating at a constant velocity (roll while rotating, RWR) alters the position of the semicircular canals relative to the axis of rotation. This produces vertical and horizontal nystagmus, disorientation, vertigo, and nausea. With recurrent exposure, subjects habituate and can make more head movements before experiencing overpowering motion sickness. We questioned whether promethazine lessened the vertigo or delayed the habituation, whether habituation of the vertigo was related to the central vestibular time constant, i.e., to the time constant of velocity storage, and whether the severity of the motion sickness was related to deviation of the axis of eye velocity from gravity. Sixteen subjects received promethazine and placebo in a double-blind, crossover study in two consecutive 4-day test series 1 month apart, termed series I and II. Horizontal and vertical eye movements were recorded with video-oculography while subjects performed roll head movements of approx. 45° over 2 s to and from the upright position while being rotated at 138°/s around a vertical axis. Motion sickness was scaled from 1 (no sickness) to an endpoint of 20, at which time the subject was too sick to continue or was about to vomit. Habituation was determined by the number of head movements that subjects made before reaching the maximum motion sickness score of 20. Head movements increased steadily in each session with repeated testing, and there was no difference between the number of head movements made by the promethazine and placebo groups. Horizontal and vertical angular vestibulo-ocular reflex (aVOR) time constants declined in each test, with the declines being closely correlated to the increase in the number of head movements. The strength of vertiginous sensation was associated with the amount of deviation of the axis of eye velocity from gravity; the larger the deviation of the eye velocity axis from gravity, the more severe the motion sickness. Thus, promethazine neither reduced the nausea associated with RWR, nor retarded or hastened habituation. The inverse relationship between the aVOR time constants and number of head movements to motion sickness, and the association of the severity of motion sickness with the extent, strength, and time of deviation of eye velocity from gravity supports the postulate that the spatiotemporal properties of velocity storage, which are processed between the nodulus and uvula of the vestibulocerebellum and the vestibular nuclei, are likely to represent the source of the conflict responsible for producing motion sickness.     

Unilateral vestibular deafferentation produces no long-term effects

 We tested the hypothesis that the reason some patients compensate well after unilateral vestibular deafferentation (uVD) and others do not could be due to differences in eye-head coordination or in blink characteristics during natural, active head movements. Patients with well-compensated uVDs do not report distressing postural unsteadiness or an aversive sensation of apparent motion of a visual scene (oscillopsia) or ”visual confusion” upon rapid head rotation as do those patients with poorly compensated uVDs. It has been suggested that well-compensated subjects eliminate the subjective sensations associated with retinal slip, which must occur as a result of an inadequate vestibuloocular reflex (VOR), either by restricting head movement to the lesioned side or by blinking during head turns. To test this, subjects stood at the curbside of a busy road with a 180^o view of regular, fast-moving traffic, which they scanned in preparation of crossing the road, and their eye and head movements and blinks were measured in this natural situation. Both normals and uVDs generated similar ranges of head position, head velocity and gaze magnitude, and all subjects performed a blink during the gaze saccade. Contrary to the hypothesis, no systematic differences were found between normals and either group of uVDs. Received: 8 May 1998 / Accepted: 19 June 1998     

Active linear head motion improves dynamic visual acuity in pursuing a high-speed moving object

We usually move both our eyes and our head when pursuing a high-speed moving object. However, the vestibulo-ocular reflex (VOR), evoked by head motion, seems to disturb smooth pursuit eye movement because the VOR stabilizes the gaze against head motion. To determine whether head motion is advantageous for pursuing a high-speed moving object, we examined dynamic visual acuity (DVA) for a high-speed (80°/s) rightward moving object with and without active linear rightward head motion (HM) at a maximum of 50 cm/s in nine healthy subjects. Furthermore, we analyzed eye and head movements to investigate the contribution of linear VOR (LVOR) and smooth eye movement under these conditions. In most subjects, active linear head motion improved DVA for a high-speed moving object. Subjects with higher DVA scores under HM had robust rightward gaze (eye + head) velocities (>60 cm/s), i.e., rightward smooth eye movements (>10°/s). With the head stationary (HS), faster smooth eye movements (>40°/s) were generated when the subjects pursued a high-speed moving object. They also showed anticipatory smooth eye movements under conditions HM and HS. However, the level of suppression of their LVOR abilities was equal to that of the others. These results suggest that the ability to generate anticipatory smooth pursuit eye movements for following a high-speed moving object against the LVOR is a determining factor for improvement of DVA under HM.