Cerebellar nodulectomy impairs spatial memory of vestibular and optokinetic stimulation in rabbits

Natural vestibular and optokinetic stimulation were used to investigate the possible role of the cerebellar nodulus in the regulation and modification of reflexive eye movements in rabbits. The nodulus and folium 9d of the uvula were destroyed by surgical aspiration. Before and after nodulectomy the vertical and horizontal vestibuloocular reflexes (VVOR, HVOR) were measured during sinusoidal vestibular stimulation about the longitudinal (roll) and vertical (yaw) axes. Although the gain of the HVOR (G(HVOR) = peak eye movement velocity/peak head velocity) was not affected by the nodulectomy, the gain of the VVOR (G(VVOR)) was reduced. The gains of the vertical and horizontal optokinetic reflexes (G(VOKR), G(HOKR)) were measured during monocular, sinusoidal optokinetic stimulation (OKS) about the longitudinal and vertical axes. Following nodulectomy, there was no reduction in G(VOKR) or G(HOKR). Long-term binocular OKS was used to generate optokinetic afternystagmus, OKAN II, that lasts for hours. After OKAN II was induced, rabbits were subjected to static pitch and roll, to determine how the plane and velocity of OKAN II is influenced by a changing vestibular environment. During static pitch, OKAN II slow phase remained aligned with earth-horizontal. This was true for normal and nodulectomized rabbits. During static roll, OKAN II remained aligned with earth-horizontal in normal rabbits. During static roll in nodulectomized rabbits, OKAN II slow phase developed a centripetal vertical drift. We examined the suppression and recovery of G(VVOR) following exposure to conflicting vertical OKS for 10-30 min. This vestibular-optokinetic conflict reduced G(VVOR) in both normal and nodulectomized rabbits. The time course of recovery of G(VVOR) after conflicting OKS was the same before and after nodulectomy. In normal rabbits, the head pitch angle, at which peak OKAN II velocity occurred, corresponded to the head pitch angle maintained during long-term OKS. If the head was maintained in a "pitched-up" or "pitched-down" orientation during long-term OKS, the subsequently measured OKAN II peak velocity occurred at the same orientation. This was not true for nodulectomized rabbits, who had OKAN II peak velocities at head pitch angles independent of those maintained during long-term OKS. We conclude that the nodulus participates in the regulation of compensatory reflexive movements. The nodulus also influences "remembered" head position in space derived from previous optokinetic and vestibular stimulation.     

Weightlessness alters up/down asymmetries in the perception of self-motion

In the present study, we investigated the effect of weightlessness on the ability to perceive and remember self-motion when passing through virtual 3D tunnels that curve in different direction (up, down, left, right). We asked cosmonaut subjects to perform the experiment before, during and after long-duration space flight aboard the International Space Station (ISS), and we manipulated vestibular versus haptic cues by having subjects perform the task either in a rigidly fixed posture with respect to the space station or during free-floating, in weightlessness. Subjects were driven passively at constant speed through the virtual 3D tunnels containing a single turn in the middle of a linear segment, either in pitch or in yaw, in increments of 12.5°. After exiting each tunnel, subjects were asked to report their perception of the turn’s angular magnitude by adjusting, with a trackball, the angular bend in a rod symbolizing the outside view of the tunnel. We demonstrate that the strong asymmetry between downward and upward pitch turns observed on Earth showed an immediate and significant reduction when free-floating in weightlessness and a delayed reduction when the cosmonauts were firmly in contact with the floor of the station. These effects of weightlessness on the early processing stages (vestibular and optokinetics) that underlie the perception of self-motion did not stem from a change in alertness or any other uncontrolled factor in the ISS, as evidenced by the fact that weightlessness had no effect on the perception of yaw turns. That the effects on the perception of pitch may be partially overcome by haptic cues reflects the fusion of multisensory cues and top-down influences on visual perception.     

Velocity storage in the human vertical rotational vestibulo-ocular reflex

Human horizontal rotational vestibulo-ocular reflex (rVOR) has been extensively investigated: the horizontal semicircular canals sense yaw rotations with high-pass filter dynamics and a time constant (TC) around 5 s, yet the rVOR response shows a longer TC due to a central processing stage, known as velocity storage mechanism (VSM). It is generally assumed that the vertical rVOR behaves similarly to the horizontal one; however, VSM processing of the human vertical rVOR is still to be proven. We investigated the vertical rVOR in eight healthy human subjects using three experimental paradigms: (1) per- and post-rotatory around an earth-vertical axis (ear down rotations, EDR), (2) post-rotatory around an earth-horizontal axis with different stopping positions (static otolith stimulation), (3) per-rotatory around an earth-horizontal axis (dynamic otolith stimulation). We found that the TC of vertical rVOR responses ranged 3–10 s, depending both on gravity and on the direction of rotation. The shortest TC were found in response to post-rotatory earth-horizontal stimulation averaging 3.6 s, while they were prolonged in EDR stimulation, i.e. when the head angular velocity vector is aligned with gravity, with a mean value of about 6.0 s. Overall, the longest TC were observed in per-rotatory earth-horizontal stimulation, averaging 7.8 s. The finding of longer TC in EDR than in post-rotatory earth-horizontal stimulation indicates a role for the VSM in the vertical rVOR, although its contribution appears to be weaker than on the horizontal rVOR and may be directionally asymmetric. The results from per-rotatory earth-horizontal stimulation, instead, imply a role for the otoliths in controlling the duration of the vertical rVOR response. We found no reorientation of the response toward earth horizontal, indicating a difference between human and monkey rVOR.     

Vestibular perception of passive whole-body rotation about horizontal and vertical axes in humans: goal-directed vestibulo-ocular reflex and vestibular memory-contingent saccades

This study was aimed at complementing the existing knowledge about vestibular perception of self-motion in humans. Both goal-directed vestibulo-ocular reflex and vestibular memory-contingent saccade (VM-CS) tasks were used, respectively as concurrent and retrospective magnitude estimators for passive whole-body rotation. Rotations were applied about the earth-vertical and earth-horizontal axes to study the effect of the otolith signal in self-rotation evaluation, and both in yaw and pitch to examine the horizontal and vertical semi-circular canals. Two different magnitudes of constant angular acceleration (50°/s² and 100°/s²) were used. The main findings were (1) strong correlation between both oculomotor responses of both tasks, (2) greater accuracy with rotations about the earth-vertical than the earth: -horizontal axis, (3) greater accuracy for yaw than for pitch rotations, (4) greater accuracy for high acceleration than for low, and (5) no effect of the delay (2s or 12s) in the VMCS task. Adequacy of both tasks as subjective magnitude estimators of vestibular perception of self-motion is discussed.On leave from the Laboratoíre de Physiologie Neurosensorielle, CNRS, Paris, FrancePresent address: Laboratoire de Physiologie de la Perception et de l'Action, CNRS, Collége de France, 15, rue de l'Ecole de Médecine, F-75270 Paris Cedex 06, France     

Visual and vestibular signals in the lateral mesencephalic tegmental region of the cat

Summary Single unit recordings from two alert cats were used in an attempt to further elucidate the function of the lateral mesencephalic tegmental region (LTR), a part of the mesencephalon forming a link between the superior colliculus and the lower brain stem. A total of 155 units recorded from the LTR were tested with visual, vestibular and acoustic stimuli. Of these, 54 cells (36%) were characterized as either visually (n=33) or vestibularly (n=21) responsive and an additional 13 cells were driven by complex acoustic stimuli. Visually responsive cells typically were directionally selective with large, mainly contralateral receptive fields. Vestibularly responsive cells were modulated by stimulation of either the horizontal canals (yaw stimulation; n = 16) or of both pairs of vertical canals (pitch stimulation; n=5). About half of the cells with activity modulated by rotation about the yaw axis increased discharge during ipsiversive (Type I), the other half during contraversive rotation (Type II). Of the 5 cells with activity modulated by pitch stimulation, 4 preferred the nose-down and only 1 the nose-up direction. Although the discharge of units responsive to yaw stimulation was roughly in phase with head velocity (mean phase lag with respect to head velocity: 10.6 deg), none of the vestibular cells had activity correlated with eye position, eye velocity or movement of visual stimuli. Our observations suggest that the LTR might introduce visual and vestibular signals into the tecto-facial pathway which may be used to adjust the size of pinna movements with respect to the size of ongoing head- or body movements.     

Adaptation of the angular vestibulo-ocular reflex to head movements in rotating frames of reference

Head movements in a rotating frame of reference are commonly encountered, but their long term effects on the angular vestibulo-ocular reflex (aVOR) are not well understood. To study this, monkeys were oscillated about a naso-occipital (roll) axis for several hours while rotating about a spatial vertical axis (roll-while-rotating, RWR). This induced oscillations in roll and pitch eye velocity and continuous horizontal (yaw) nystagmus. For several hours thereafter, simple roll in darkness induced horizontal nystagmus and pitch and roll oscillations. The rising and falling time constants of the horizontal velocity indicated that the nystagmus arose in velocity storage. The continuous nystagmus was correlated with a phase shift of vertical eye velocity from 90° to 0° re head position. As the phases reverted toward pre-adaptive values, the horizontal velocity declined. Similar yaw nystagmus and pitch and roll velocities were produced by oscillation in roll after adaptation with roll and horizontal optokinetic nystagmus (OKN), but not after adaptation with pitch-while-rotating (PWR). Findings were explained by a model that shifted the roll orientation vector of velocity storage toward the pitch axis during adaptation with RWR and Roll & OKN. This shift produced modulation in vertical eye velocity in the post adaptive state, which was approximately in phase with roll head position, generating horizontal nystagmus. Similar orientation changes to prolonged exposure to complex motion environments may be responsible for producing post-stimulus motion sickness and/or mal de debarquement. Supported by DC007847, EY04148, DC05204, EY01867, DC05222.     

Direction detection thresholds of passive self-motion in artistic gymnasts

In this study, we compared direction detection thresholds of passive self-motion in the dark between artistic gymnasts and controls. Twenty-four professional female artistic gymnasts (ranging from 7 to 20 years) and age-matched controls were seated on a motion platform and asked to discriminate the direction of angular (yaw, pitch, roll) and linear (leftward–rightward) motion. Gymnasts showed lower thresholds for the linear leftward–rightward motion. Interestingly, there was no difference for the angular motions. These results show that the outstanding self-motion abilities in artistic gymnasts are not related to an overall higher sensitivity in self-motion perception. With respect to vestibular processing, our results suggest that gymnastic expertise is exclusively linked to superior interpretation of otolith signals when no change in canal signals is present. In addition, thresholds were overall lower for the older (14–20 years) than for the younger (7–13 years) participants, indicating the maturation of vestibular sensitivity from childhood to adolescence.     

Latency of adaptive vergence eye movements induced by vergence-vestibular interaction training in monkeys

Clear vision of objects that move in depth toward or away from an observer requires vergence eye movements. The vergence system must interact with the vestibular system to maintain the object images on the foveae of both eyes during head movement. Previous studies have shown that training with sinusoidal vergence-vestibular interaction improves the frequency response of vergence eye movements during pitch rotation: vergence eye velocity gains increase and phase-lags decrease. To further understand the changes in eye movement responses in this adaptation, we examined latencies of vergence eye movements before and after vergence-vestibular training. Two head-stabilized Japanese monkeys were rewarded for tracking a target spot moving in depth that required vergence eye movements of 10°/s. This target motion was synchronized with pitch rotation at 20°/s. Both target and chair moved in a trapezoidal waveform interspersed with random inter-trial intervals. Before training, pitch rotation in complete darkness without a target did not induce vergence eye movements. Mean latencies of convergence and divergence eye movements induced by vergence target motion alone were 182 and 169 ms, respectively. After training, mean latencies of convergence and divergence eye movements to a target synchronized with pitch rotation shortened to 65 and 53 ms, and vergence eye velocity gains (relative to vergence target velocity) at the normal latencies were 0.68 and 1.53, respectively. Pitch rotation alone without a target induced vergence eye movements with similar latencies after training. These results indicate that vestibular information can be used effectively to initiate vergence eye movements following vergence-vestibular training.     

Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys

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

Cerebellar disease alters the axis of the high-acceleration vestibuloocular reflex

L. W. Schultheis and D. A. Robinson showed that the axis of the rotational vestibuloocular reflex (RVOR) cannot be altered by visual-vestibular mismatch ("cross-axis adaptation") when the vestibulocerebellum is lesioned. This suggests that the cerebellum may calibrate the axis of eye velocity of the RVOR under natural conditions. Thus we asked whether patients with cerebellar disease have alterations in the RVOR axis and, if so, what might be the mechanism. We used three-axis scleral coils to record head and eye movements during yaw, pitch, and roll head impulses in 18 patients with cerebellar disease and in a comparison group of eight subjects without neurologic disease. We found distinct shifts of the eye-velocity axis in patients. The characteristic finding was a disconjugate upward eye velocity during yaw. Measured at 70 ms after the onset of head rotation, the median upward gaze velocity was 15% of yaw head velocity for patients and <1% for normal subjects (P < 0.001). Upward eye velocity was greater in the contralateral (abducting) eye during yaw and in the ipsilateral eye during roll. Patients had a higher gain (eye speed/head speed) for downward than for upward pitch (median ratio of downward to upward gain: 1.3). In patients, upward gaze velocities during both yaw and roll correlated with the difference in anterior (AC) and posterior canal excitations, scaled by the respective pitch gains. Our findings support the hypothesis that upward eye velocity during yaw results from AC excitation, which must normally be suppressed by the intact cerebellum.     

An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans

Both optokinetic nystagmus (OKN) and smooth-pursuit eye movements (SPEM) are subclasses of so-called slow eye movements. However, optokinetic responses are reflexive whereas smooth pursuit requires the voluntary tracking of a moving target. We used functional magnetic resonance imaging (fMRI) to determine the neural basis of OKN and SPEM, and to uncover whether the two underlying neural systems overlap or are independent at the cortical level. The results showed a largely overlapping neural circuitry. A direct comparison between activity during the execution of OKN and SPEM yielded no oculomotor-related area exclusively dedicated to one or the other eye movement type. Furthermore, the performance of SPEM evoked a bilateral deactivation of the human equivalent of the parietoinsular vestibular cortex. This finding might indicate that the reciprocally inhibitory visual–vestibular interaction involves not only OKN but also SPEM, which are both linked with the encoding of object-motion and self-motion. Moreover, we could show differential activation patterns elicited by look-nystagmus and stare-nystagmus. Look-nystagmus is characterized by large amplitudes and low-frequency resetting eye movements rather resembling SPEM. Look-nystagmus evoked activity in cortical oculomotor centers. By contrast, stare-nystagmus is usually characterized as being more reflexive in nature and as showing smaller amplitudes and higher frequency resetting eye movements. Stare-nystagmus failed to elicit significant signal changes in the same regions as look-nystagmus/SPEM. Thus, less reflexive eye movements correlated with more pronounced signal intensity. Finally, on the basis of a general investigation of slow eye movements, we were interested in a cortical differentiation between subtypes of SPEM. We compared activity associated with predictable and unpredictable SPEM as indicated by appropriate visual cues. In general, predictable and unpredictable SPEM share the same neural network, yet information about the direction of an upcoming target movement reduced the cerebral activity level.     

Three dimensional kinematics of rapid compensatory eye movements in humans with unilateral vestibular deafferentation

Saccades executed with the head stationary have kinematics conforming to Listing’s law (LL), confining the ocular rotational axis to Listing’s plane (LP). In unilateral vestibular deafferentation (UVD), the vestibulo-ocular reflex (VOR), which does not obey LL, has at high head acceleration a slow phase that has severely reduced velocity during ipsilesional rotation, and mildly reduced velocity during contralesional rotation. Studying four subjects with chronic UVD using 3D magnetic search coils, we investigated kinematics of stereotypic rapid eye movements that supplement the impaired VOR. We defined LP with the head immobile, and expressed eye and head movements as quaternions in LP coordinates. Subjects underwent transient whole body yaw at peak acceleration 2,800°/s² while fixating targets centered, or 20° up or down prior to rotation. The VOR shifted ocular torsion out of LP. Vestibular catch-up saccades (VCUS) occurred with mean latency 90 ± 44 ms (SD) from ipsilesional rotation onset, maintained initial non-LL torsion so that their quaternion trajectories paralleled LP, and had velocity axes changing by half of eye position. During contralesional rotation, rapid eye movements occurred at mean latency 135 ± 36 ms that were associated with abrupt decelerations (ADs) of the horizontal slow phase correcting 3D deviations in its velocity axis, with quaternion trajectories not paralleling LP. Rapid eye movements compensating for UVD have two distinct kinematics. VCUS have velocity axis dependence on eye position consistent with LL, so are probably programmed in 2D by neural circuits subserving visual saccades. ADs have kinematics that neither conform to LL nor match the VOR axis, but appear instead programmed in 3D to correct VOR axis errors. United States Public Health Service grants DC-005224. Joseph L. Demer is Leonard Apt Professor of Ophthalmology. Benjamin T. Crane was supported by a grant from the Giannini Family Foundation.     

Tilt and translation motion perception during off-vertical axis rotation

The effect of stimulus frequency on tilt and translation motion perception was studied during constant velocity off-vertical axis rotation (OVAR), and compared to the effect of stimulus frequency on eye movements. Fourteen healthy subjects were rotated in darkness about their longitudinal axis 10° and 20° off-vertical at 45°/s (0.125 Hz) and 20° off-vertical at 180°/s (0.5 Hz). Perceived motion was evaluated using verbal reports and a joystick capable of recording tilt and translation in both sagittal and lateral planes. Eye movements were also recorded using videography. At the lower frequency, subjects reported the perception of progressing along the edge of a cone, whereas at the higher frequency they had the sensation of progressing along the edge of an upright cylinder. Tilt perception and ocular torsion significantly increased as the tilt angle increased from 10° to 20° at the lower frequency, and then decreased at the higher frequency. The phase lag of ocular torsion increased as a function of frequency, while the phase lag of tilt perception did not change. Horizontal eye movements were small at the lower frequency and showed a phase lead relative to the linear acceleration stimulus. While the phase lead of horizontal eye movements decreased at 0.5 Hz, the phase of translation perception did not vary with stimulus frequency and was similar to the phase of tilt perception during all conditions. A second data set was obtained in 12 subjects to compare motion perception phase when using a simple push-button to indicate nose-up orientation, continuous setting of pitch tilt alone, or continuous setting of tilt and translation in both pitch and roll planes as in the first data set. This set of measurements indicated that in the frequency range studied subjects tend to lead the stimulus when using a push-button task while lagging the stimulus when using a continuous setting of tilt with a joystick. Both amplitude and phase of tilt perception using the joystick were not different whether concentrating on pitch tilt alone or attempting a more complex reporting of tilt and translation in both sagittal and lateral planes. During dynamic linear stimuli in the absence of canal and visual input, a change in stimulus frequency alone elicits similar changes in the amplitude of both self-motion perception and eye movements. However, in contrast to the eye movements, the phase of both perceived tilt and translation motion is not altered by stimulus frequency over this limited range. These results are consistent with the hypothesis that neural processing to distinguish tilt and translation stimuli differs between eye movements and motion perception.     

GABAB receptors contribute to vestibular compensation after unilateral labyrinthectomy in pigmented rats

The horizontal vestibulo-ocular reflex was studied in pigmented rats, which had been unilaterally, chemically labyrinthectomised 6-144 days previously. During this partially compensated stage after unilateral labyrinthectomy (UL), both static and dynamic deficits remain. The former was evaluated by recording of spontaneous eye movements in darkness, and the latter by estimating the slow-phase velocity (SPV) gain of compensatory eye movements during horizontal vestibular stimulation. The GABA(B) agonist baclofen caused a reversal of the remaining ipsilesional drift of the eyes in darkness into a nystagmus with a contralesional slow phase. The GABA(B) antagonist CGP 36742 caused a decompensation by exaggerating the remaining ipsilesional eye drift. Further, baclofen equilibrated or reversed the asymmetry between ipsi- and contralesional SPV gains during horizontal sinusoidal rotations at 0.2 Hz and 0.8 Hz. This was achieved by an increase in the ipsilesional gain and a decrease in the contralesional gain. The phase lead during sinusoidal rotation (0.2 Hz) was larger following rotation to the lesioned side than to the intact side in UL rats. This asymmetry was reversed by baclofen. CGP 36742 inhibited the effects of baclofen, while the antagonist per se aggravated SPV gain and phase lead asymmetries in UL rats during vestibular stimulation. Per- and post-rotatory nystagmus induced by velocity step stimulation revealed an imperfect velocity-storage function in UL animals, which was modulated by baclofen. An investigation of the baclofen effect on SPV gain asymmetry during different time intervals after chemical UL showed a completely developed effect on the 6th day. Bilateral flocculectomy did not alter the effects of baclofen on UL animals. It is concluded that physiological stimulation of GABA(B) receptors contributes to minimise the vestibulo-oculomotor asymmetry during the partially compensated period after UL. Administration of an agonist or an antagonist changes the asymmetry towards the ipsi- or contralesional side, possibly by altering the spontaneous neuronal activity in the bilateral medial vestibular nuclei. The results are compatible with a hypothesis, supported by in vitro slice experiments, that the efficacy of GABA(B) receptors is up-regulated on the ipsilesional side and down-regulated on the contralesional side.     

Adaptive changes in smooth pursuit eye movements induced by cross-axis pursuit-vestibular interaction training in monkeys

The smooth pursuit system interacts with the vestibular system to maintain the accuracy of eye movements in space. To understand neural mechanisms of short-term modifications of the vestibulo-ocular reflex (VOR) induced by pursuit-vestibular interactions, we used a cross-axis procedure in trained monkeys. We showed earlier that pursuit training in the plane orthogonal to the rotation plane induces adaptive cross-axis VOR in complete darkness. To further study the properties of adaptive responses, we examined here the initial eye movements during tracking of a target while being rotated with a trapezoidal waveform (peak velocity 30 or 40°/s). Subjects were head-stabilized Japanese monkeys that were rewarded for accurate pursuit. Whole body rotation was applied either in the yaw or pitch plane while presenting a target moving in-phase with the chair with the same trajectory but in the orthogonal plane. Eye movements induced by equivalent chair rotation with or without the target were examined before and after training. Before training, chair rotation alone resulted only in the collinear VOR, and smooth eye movement-tracking of orthogonal target motion during rotation had a normal smooth pursuit latency (ca 100 ms). With training, the latency of orthogonal smooth tracking eye movements shortened, and the mean latency after 1 h of training was 42 ms with a mean gain, at 100 ms after stimulus onset, of 0.4. The cross-axis VOR induced by chair rotation in complete darkness had identical latencies with the orthogonal smooth tracking eye movements, but its gains were <0.2. After cross-axis pursuit training, target movement alone without chair rotation induced smooth pursuit eye movements with latencies ca 100 ms. Pursuit training alone for 1 h using the same trajectory but without chair rotation did not result in any clear change in pursuit latency (ca 100 ms) or initial eye velocity. When a new target velocity was presented during identical chair rotation after training, eye velocity was correspondingly modulated by just 80 ms after rotation onset, which was shorter than the expected latency of pursuit (ca 100 ms). These results indicate that adaptive changes were induced in the smooth pursuit system by pursuit-vestibular interaction training. We suggest that this training facilitates the response of pursuit-related neurons in the cortical smooth pursuit pathways to vestibular inputs in the orthogonal plane, thus enabling smooth eye movements to be executed with shorter latencies and larger eye velocities than in normal smooth pursuit driven only by visual feedback. Electronic Publication     

Continuous theta-burst stimulation of the right superior temporal gyrus impairs self-motion perception

Sensory input from the semicircular canals (SCC) and otolith organs is centrally combined with signals from other sensory modalities to continuously update the internal estimate of self-motion. Constant velocity vertical on-axis rotation leads to decay of the nystagmus response from the horizontal SCC and of perceived angular velocity (PAV), and when the rotation stops, a similar oppositely directed post-rotatory response occurs. Case reports and electrical stimulation studies suggest an involvement of the temporo-peri-Sylvian vestibular cortex in generating the PAV. Here, we transiently inhibited the right superior temporal gyrus (STG) by use of continuous theta-burst stimulation (cTBS) and predicted an accelerated decay of PAV compared to controls (n = 5 control session first, n = 1 cTBS session first). Constant velocity (100°/s) vertical on-axis rotations were applied over 75 s before (1 block) and after (3 blocks) cTBS over the right STG in six subjects. Breaks between the rotations (75 s) were initiated by abrupt stops. By use of a rotating potentiometer, subjects indicated the PAV during and after the chair rotations. Simultaneously eye positions were recorded using a scleral search coil. One subject was excluded for per-rotary analysis. Early after cTBS, the post-rotary PAV decay time constant (DTC) was significantly (9.4 ± 5.7 vs. 13.6 ± 5.9 s; p = 0.049) reduced (no directionality to this effect observed). Overall, post-rotary PAV showed a trend toward shortened DTC compared to the control trials (p = 0.086) in the first 25 min after cTBS, while per-rotary PAV was not significantly changed. Per-rotary and post-rotary aVOR DTC were not significantly changed after cTBS (p > 0.05). These findings support the hypothesis that the right STG is involved in mediating self-motion perception and can be modulated by cTBS.     

Multifactorial interactions involved in linear self-transport distance estimate: a place for time.

As the vestibular system is the only sensory organ whose primary function is self-motion detection, we examined the conditions under which the otoliths, which detect the linear acceleration of the head, could be used to estimate traveled distance. In order to isolate the contribution of the otoliths (with the somatosensory system) from contributions of the visual and motor systems subjects were transported in darkness. We initially hypothesized that self-transport with continuously varying linear velocity should facilitate distance computation by continuously stimulating the otoliths, and that active control of self-motion should also help subjects estimate the distance traveled. However, it was found that the distance covered during self-motion is actually better estimated when transport velocity is quasi-constant. Nevertheless, such estimates strongly depend upon velocity magnitude; subjects show an idiosyncratic preferred self-motion velocity for which distance measurements are most accurate. Furthermore, the active control of self-transport improves estimates of self-motion mainly because the subjects can then adopt a constant velocity, and more precisely their preferred one. It was finally found that subjects mentally count in order to assess their displacement length, and that time perception is indeed disturbed by varying self-motion velocity.     

Otolith-semicircular canal interaction during postrotatory nystagmus in humans

The otolith-semicircular canal interaction during postrotatory nystagmus was studied in ten normal human subjects by applying fast, short-lasting, passive head and body tilts (15, 30, 45, or 90° in the roll or pitch plane) 2 s after sudden stop from a constant-velocity rotation (100°/s) about the earth-vertical axis in yaw. Eye movements were measured with three-dimensional magnetic search coils. Following the head tilt, activity in the semicircular canal primary afferents continues to reflect the postrotatory angular velocity vector in head-centered coordinates, whereas otolith primary afferents signal a different orientation of the head relative to gravity. Despite the change in head orientation relative to gravity, postrotatory eye velocity decayed closely along the axis of semicircular canal stimulation (horizontal in head coordinates) for large head tilts (90°) and also for small head tilts (15–45°) for reorientations in the pitch plane. Only for small head tilts (15–45°) in the roll plane was there a reorientation of the eye rotation axis toward the gravitational vector. This reorientation was approximately compensatory for 15° head tilts. For 30° and 45° head tilts the eye rotation axis tilted toward the gravitational vector by about the same amount as for 15° head tilts. These results suggest that, with the exception of small head tilts in the roll plane, there was no compelling data showing a relationship between the eye rotation axis and head tilt and that postrotatory nystagmus is largely organized in head-centered rather than gravity-centered coordinates in humans. This indicates a rudimentary, nonlinear, and direction-specific interaction of semicircular canal and otolith signals in the central vestibular system in humans.     

Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements

To elucidate how information is processed in the vestibuloocular reflex (VOR) pathways subserving vertical eye movements, extracellular single-unit recordings were obtained from the vestibular nuclei of alert monkeys trained to track a visual target with their eyes while undergoing sinusoidal pitch oscillations (0.2-1.0 Hz). Units with activity related to vertical vestibular stimulation and/or eye movements were classified as either vestibular units (n = 53), vestibular plus eye-position units (n = 30), pursuit units (n = 10), or miscellaneous units (n = 5), which had various combinations of head- and eye-movement sensitivities. Vestibular units discharged in relation to head rotation, but not to smooth eye movements. On average, these units fired approximately in phase with head velocity; however, a broad range of phase shifts was observed. The activities of 8% of the vestibular units were related to saccades. Vestibular plus eye-position units fired in relation to head velocity and eye position and, in addition, usually to eye velocity. Their discharge rates increased for eye and head movements in opposite directions. During combined head and eye movements, the modulation in unit activity was not significantly different from the sum of the modulations during each alone. For saccades, the unit firing rate either decreased to zero or was unaffected. Pursuit units discharged in relation to eye position, eye velocity, or both, but not to head movements alone. For saccades, unit activity usually either paused or was unaffected. The eye-movement-related activities of the vestibular plus eye-position and pursuit units were not significantly different. A quantitative comparison of their firing patterns suggests that vestibular, vestibular plus eye-position, and pursuit neurons in the vestibular nucleus could provide mossy fiber inputs to the flocculus. In addition, the vertical vestibular plus eye-position neurons have discharge patterns similar to those of fibers recorded rostrally in the medial longitudinal fasciculus. Therefore, our data support the view that vertical vestibular plus eye-position neurons are interneurons of the VOR.     

Reproduction of self-rotation duration

The vestibular system detects the velocity of the head even in complete darkness, and thus contributes to spatial orientation. However, during vestibular estimation of linear passive self-motion distance in darkness, healthy human subjects mainly rely on time, and they replicate also stimulus duration when required to reproduce previous self-rotation. We then made the hypothesis that the perception of vestibular-sensed motion duration is embedded within encoding of motion kinetics. The ability to estimate time during passive self-motion in darkness was examined with a self-rotation reproduction paradigm. Subjects were required to replicate through self-driven transport the plateau velocity (30, 60 and 90 °/s) and duration (2, 3 and 4 s) of the previously imposed whole-body rotation (trapezoid velocity profile) in complete darkness; the rotating chair position was recorded (500 Hz) during the whole trials. The results showed that the peak velocity, but not duration, of the plateau phase of the imposed rotation was accurately reproduced. Suspecting that the velocity instruction had impaired the duration reproduction, we added a control experiment requiring subjects to reproduce two successive identical rotations separated by a momentary motion interruption (MMI). The MMI was of identical duration to the previous plateau phase. MMI duration was fidelitously reproduced whereas that of the plateau phase was hypometric (i.e. lesser reproduced duration than plateau) suggesting that subjective time is shorter during vestibular stimulation. Furthermore, the accurate reproduction of the whole motion duration, that was not required, indicates an automatic process and confirms that vestibular duration perception is embedded within motion kinetics.