Kinematic principles of primate rotational vestibulo-ocular reflex. II. Gravity-dependent modulation of primary eye position

The kinematic constraints of three-dimensional eye positions were investigated in rhesus monkeys during passive head and body rotations relative to gravity. We studied fast and slow phase components of the vestibulo-ocular reflex (VOR) elicited by constant-velocity yaw rotations and sinusoidal oscillations about an earth-horizontal axis. We found that the spatial orientation of both fast and slow phase eye positions could be described locally by a planar surface with torsional variation of <2.0 +/- 0.4 degrees (displacement planes) that systematically rotated and/or shifted relative to Listing's plane. In supine/prone positions, displacement planes pitched forward/backward; in left/right ear-down positions, displacement planes were parallel shifted along the positive/negative torsional axis. Dynamically changing primary eye positions were computed from displacement planes. Torsional and vertical components of primary eye position modulated as a sinusoidal function of head orientation in space. The torsional component was maximal in ear-down positions and approximately zero in supine/prone orientations. The opposite was observed for the vertical component. Modulation of the horizontal component of primary eye position exhibited a more complex dependence. In contrast to the torsional component, which was relatively independent of rotational speed, modulation of the vertical and horizontal components of primary position depended strongly on the speed of head rotation (i.e., on the frequency of oscillation of the gravity vector component): the faster the head rotated relative to gravity, the larger was the modulation. Corresponding results were obtained when a model based on a sinusoidal dependence of instantaneous displacement planes (and primary eye position) on head orientation relative to gravity was fitted to VOR fast phase positions. When VOR fast phase positions were expressed relative to primary eye position estimated from the model fits, they were confined approximately to a single plane with a small torsional standard deviation ( approximately 1.4-2.6 degrees). This reduced torsional variation was in contrast to the large torsional spread (well >10-15 degrees ) of fast phase positions when expressed relative to Listing's plane. We conclude that primary eye position depends dynamically on head orientation relative to space rather than being fixed to the head. It defines a gravity-dependent coordinate system relative to which the torsional variability of eye positions is minimized even when the head is moved passively and vestibulo-ocular reflexes are evoked. In this general sense, Listing's law is preserved with respect to an otolith-controlled reference system that is defined dynamically by gravity.     

Oculomotor control of primary eye position discriminates between translation and tilt

We have previously shown that fast phase axis orientation and primary eye position in rhesus monkeys are dynamically controlled by otolith signals during head rotations that involve a reorientation of the head relative to gravity. Because of the inherent ambiguity associated with primary otolith afferent coding of linear accelerations during head translation and tilts, a similar organization might also underlie the vestibulo-ocular reflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from gravity in the dynamic control of primary eye position has been investigated here by comparing the eye movements elicited by sinusoidal lateral and fore-aft oscillations (0.5 Hz +/- 40 cm, equivalent to +/- 0.4 g) with those during yaw rotations (180 degrees/s) about a vertically tilted axis (23.6 degrees). We found a significant modulation of primary eye position as a function of linear acceleration (gravity) during rotation but not during lateral and fore-aft translation. This modulation was enhanced during the initial phase of rotation when there was concomitant semicircular canal input. These findings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechanisms that discriminate between gravity and translational head acceleration.     

Optokinetic and vestibular stimulation determines the spatial orientation of negative optokinetic afternystagmus in the rabbit

Prolonged binocular optokinetic stimulation (OKS) in the rabbit induces a high-velocity negative optokinetic afternystagmus (OKAN II) that persists for several hours. We have taken advantage of this uniform nystagmus to study how changes in static head orientation in the pitch plane might influence the orientation of the nystagmus. After horizontal OKS, the rotation axis of the OKAN II remained almost constant in space as it was kept aligned with the gravity vector when the head was pitched by as much as 80 degrees up and 35 degrees down. Moreover, during reorientation, slow-phase eye velocity decreased according to the head pitch angle. Thereafter, we analyzed the space orientation of OKAN II after optokinetic stimulation during which the head and/or the OKS were pitched upward and downward. The rotation axis of OKAN II did not remain aligned with an earth vertical axis nor a head vertical axis, but it tended to be aligned with that of the OKS respace. The slow-phase eye velocity of OKAN II was also affected by the head pitch angle during OKS, because maximal OKAN II velocity occurred at the same head pitch angle as that during optokinetic stimulation. We suggest that OKAN II is coded in gravity-centered rather than in head-centered coordinates, but that this coordinate system may be influenced by optokinetic and vestibular stimulation. Moreover, the velocity attenuation of OKAN II seems to depend on the mismatch between the space-centered nystagmus rotation axis orientation and that of the "remembered" head-centered optokinetic pathway activated by OKS.     

Three-dimensional orientation of the eye rotation axis during the Purkinje sensation

The otolith-semicircular canal interaction during postrotatory nystagmus was studied in six normal human subjects by applying fast, short-lasting, passive head and body tilts (90 degrees in the roll or pitch plane) 2 s after sudden stop from a constant velocity rotation (100 degrees/s) about the earth-vertical axis in yaw. Eye movements were measured with 3-D 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. Pitch (roll) tilts away from upright during postrotatory nystagmus after yaw rotation elicited a transient vertical (torsional) VOR. 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). These results suggest that postrotary nystagmus is largely organized in head-centered rather than gravity-centered coordinates in humans as suggested by the Purkinje-sensation.     

Semicircular canal contributions to the three-dimensional vestibuloocular reflex: a model-based approach

1. We studied the contribution of the individual semicircular canals to the generation of horizontal and torsional eye movements in cynomolgus monkeys. Eye movements were elicited by sinusoidal rotation about a vertical (gravitational) axis at 0.2 Hz with the animals tilted in various attitudes of static forward or backward pitch. The gains of the horizontal and torsional components of the vestibuloocular reflex (VOR) were measured for each tilt position. The gains as a function of tilt position were fit with sinusoidal functions, and spatial gains and phases were determined. After control responses were recorded, the semicircular canals were plugged, animals were allowed to adapt, and the test procedure was repeated. Animals were prepared with only the anterior and posterior canals intact [vertical canal (VC) animals], with only the lateral canals intact [lateral canal (LC) animal], and with only one anterior and the contralateral posterior canals intact [right anterior and left posterior canal (RALP) animals; left anterior and right posterior canal (LARP) animals]. 2. In normal animals, the gain of the horizontal (yaw axis) velocity of the compensatory eye movements decreased as they were pitched forward or backward, and a torsional velocity appeared, reversing phase at the peak of the horizontal gain. After the anterior and posterior canals were plugged (LC animal), the horizontal component was reduced when the animal was tilted backward; the gain was zero with about -60 degrees of backward tilt. The spatial phase of the torsional component had the same characteristics. This is consistent with the fact that both responses were produced by the lateral canals, which from our results are tilted between 28 and 39 degrees above the horizontal stereotaxic plane. 3. After both lateral canals were plugged (VC animals), horizontal velocity was reduced in the upright position but increased as the animals were pitched backward relative to the axis of rotation. Torsional velocities, which were zero in the upright position in the normal animal, were now 180 degrees out of phase with the horizontal velocity. The peak values of the horizontal and torsional components were significantly shifted from the normal data and were closely aligned with each other, reaching peak values at approximately -56 degrees pitched back (-53 degrees horizontal, -58 degrees torsional). The same was true for the LARP and RALP animals; the peak values were at -59 degrees pitched back (-55 degrees horizontal, -62 degrees torsional). Likewise, in the LC animal the peak yaw and roll gains occurred at about the same angle of forward tilt, 35 degrees (30 degrees horizontal, 39 degrees torsional). Thus, in each case, the canal plugging had transformed the VOR from a compensatory to a direction-fixed response with regard to the head. Therefore there was no adaptation of the response planes of the individual canals after plugging. 4. The data were compared with eye velocity predictions of a model based on the geometric organization of the canals and their relation to a head coordinate frame. The model used the normal to the canal planes to form a nonorthogonal coordinate basis for representing eye velocity. An analysis of variance was used to define the goodness of fit of model predictions to the data. Model predictions and experimental data agreed closely for both normal animals and for the animals with canal lesions. Moreover, if horizontal and roll components from the LC and VC animals were combined, the summation overlay the response of the normal monkeys and the predictions of the model. In addition, a combination of the RALP and LARP animals predicted the response of the lateral-canal-plugged (VC) animals. 5. When operated animals were tested in light, the gains, peak values, and spatial phases of horizontal and roll eye velocity returned to the preoperative values, regardless of the type of surgery performed. This indicates that vision compensated for the lack o     

Directional organization of eye movement and visual signals in the floccular lobe of the monkey cerebellum

The floccular lobe of the monkey is critical for the generation of visually-guided smooth eye movements. The present experiments reveal physiological correlates of the directional organization in the primate floccular lobe by examining the selectivity for direction of eye motion and visual stimulation in the firing of individual Purkinje cells (PCs) and mossy fibers. During tracking of sinusoidal target motion along different axes in the frontoparallel plane, PCs fell into two classes based on the axis that caused the largest modulation of simple-spike firing rate. For "horizontal" PCs, the response was maximal during horizontal eye movements, with increases in firing rate during pursuit toward the side of recording (ipsiversive). For "vertical" PCs, the response was maximal during eye movement along an axis just off pure vertical, with increases in firing rate during pursuit directed downward and slightly contraversive. During pursuit of target motion at constant velocity, PCs again fell into horizontal and vertical classes that matched the results from sinusoidal tracking. In addition, the directional tuning of the sustained "eye velocity" and transient "visual" components of the neural responses obtained during constant velocity tracking were very similar. PCs displayed very broad tuning approximating a cosine tuning curve; the mean half-maximum bandwidth of their tuning curves was 170-180 degrees. Other cerebellar elements, related purely to eye movement and presumed to be mossy fibers, exhibited tuning approximately 40 degrees narrower than PCs and had best directions that clustered around the four cardinal directions. Our data indicate that the motion signals encoded by PCs in the monkey floccular lobe are segregated into channels that are consistent with a coordinate system defined by the vestibular apparatus and eye muscles. The differences between the tuning properties exhibited by PCs compared with mossy fibers indicate that a spatial transformation occurs within the floccular lobe.     

Spatial coordination by descending vestibular signals. 2. Response properties of medial and lateral vestibulospinal tract neurons in alert and decerebrate cats

Spatial response properties of medial (MVST) and lateral (LVST) vestibulospinal tract neurons were studied in alert and decerebrate cats during sinusoidal angular rotations of the whole body in the horizontal and many vertical planes. Of 220 vestibulospinal neurons with activity modulated during 0.5-Hz sinusoidal rotations, 200 neurons exhibited response gains that varied as a cosine function of stimulus orientation and phases that were near head velocity for rotation planes far from the minimum response plane. A maximum activation direction vector (MAD), which represents the axis and direction of rotation that maximally excites the neuron, was calculated for these neurons. Spatial properties of secondary MVST neurons in alert and decerebrate animals were similar. The responses of 88 of 134 neurons (66%) could be accounted for by input from one semicircular canal pair. Of these, 84 had responses consistent with excitation from the ipsilateral canal of the pair (13 horizontal, 27 anterior, 44 posterior) and 4 with excitation from the contralateral horizontal canal. The responses of the remaining 46 (34%) neurons suggested convergent inputs. The activity of 38 of these was significantly modulated by both horizontal and vertical rotations. Twelve neurons (9%) had responses that were consistent with input from both vertical canal pairs, including 9 cells with MADs near the roll axis. Thirty-two secondary MVST neurons (24%) had type II yaw and/or roll responses. The spatial response properties of 18 secondary LVST neurons, all studied in decerebrate animals, were different from those of secondary MVST neurons. Sixteen neurons (89%) had type II yaw and/or roll responses, and 12 (67%) appeared to receive convergent canal pair input. Convergent input was more common on higher-order vestibulospinal neurons than on secondary neurons. These results suggest that MVST and LVST neurons and previously reported vestibulo-ocular neurons transmit functionally different signals. LVST neurons, particularly those with MADs close to the roll axis, may be involved in the vestibular-limb reflex. The combination of vertical and ipsilateral horizontal canal input on many secondary MVST neurons suggests a contribution to the vestibulocollic reflex. However, in contrast to most neck muscles, very few neurons had maximum vertical responses near pitch.     

Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation

The three-dimensional (3-D) properties of the translational vestibulo-ocular reflexes (translational VORs) during lateral and fore-aft oscillations in complete darkness were studied in rhesus monkeys at frequencies between 0.16 and 25 Hz. In addition, constant velocity off-vertical axis rotations extended the frequency range to 0.02 Hz. During lateral motion, horizontal responses were in phase with linear velocity in the frequency range of 2-10 Hz. At both lower and higher frequencies, phase lags were introduced. Torsional response phase changed more than 180 degrees in the tested frequency range such that torsional eye movements, which could be regarded as compensatory to "an apparent roll tilt" at the lowest frequencies, became anticompensatory at all frequencies above approximately 1 Hz. These results suggest two functionally different frequency bandwidths for the translational VORs. In the low-frequency spectrum (<0.5 Hz), horizontal responses compensatory to translation are small and high-pass-filtered whereas torsional response sensitivity is relatively frequency independent. At higher frequencies however, both horizontal and torsional response sensitivity and phase exhibit a similar frequency dependence, suggesting a common role during head translation. During up-down motion, vertical responses were in phase with translational velocity at 3-5 Hz but phase leads progressively increased for lower frequencies (>90 degrees at frequencies <0.2 Hz). No consistent dependence on static head orientation was observed for the vertical response components during up-down motion and the horizontal and torsional response components during lateral translation. The frequency response characteristics of the translational VORs were fitted by "periphery/brain stem" functions that related the linear acceleration input, transduced by primary otolith afferents, to the velocity signals providing the input to the velocity-to-position neural integrator and the oculomotor plant. The lowest-order, best-fit periphery/brain stem model that approximated the frequency dependence of the data consisted of a second order transfer function with two alternating poles (at 0.4 and 7.2 Hz) and zeros (at 0.035 and 3.4 Hz). In addition to clearly differentiator dynamics at low frequencies (less than approximately 0.5 Hz), there was no frequency bandwidth where the periphery/brain stem function could be approximated by an integrator, as previously suggested. In this scheme, the oculomotor plant dynamics are assumed to perform the necessary high-frequency integration as required by the reflex. The detailed frequency dependence of the data could only be precisely described by higher order functions with nonminimum phase characteristics that preclude simple filtering of afferent inputs and might be suggestive of distributed spatiotemporal processing of otolith signals in the translational VORs.     

Convergence of ampullar and macular inputs on vestibular nuclei unit of the rat

181 vestibular nucleus neurons were examined for their responsiveness to rotation about the vertical axis and static tilts in roll and pitch planes in the rat. 68 of these units were sensitive to rotation and tilts (canal-otolith cells). In other words, 41.0% of the neurons responded to rotation (68/166). There was no significant difference in percentage of canal-otolith cells in type I and II neurons, which were 48.6% and 37.0% respectively. Vertical axis rotation when the head was tilted produced a simultaneous stimulation of the canal and otoliths. Using this stimulus method, the bias effect was observed in 72.5% of the canal-otolith cells (29/40). Furthermore, since vertical axis rotation with the head tilted elicited vertical canal responses, the rate of ampullary convergence was estimated by analysing response profiles obtained such rotations. The results obtained in the rat were compared with those in other species.     

Three-dimensional modeling of static vestibulo-ocular brain stem syndromes

Static vestibulo-ocular brain stem syndromes characterized by skew deviation, a vertical disconjugacy of the eyes, and ocular torsion are the result of a vestibular tone imbalance in the frontal (roll) plane. Similar physiological changes in static eye position, ocular counter-roll and conjugated deviations of vertical eye position, are caused by the influence of gravity mediated by the utricles. These observations prompted our approach with the model described here: based on the known deviations of static eye position, we devised a three-dimensional mathematical model of otolith-ocular function including detailed brain stem anatomy. This model is able to explain and predict the differential effects of unilateral and bilateral peripheral or central vestibular lesions on static eye position in roll, pitch, and yaw planes.     

Deficits in vertical and torsional eye movements after uni- and bilateral muscimol inactivation of the interstitial nucleus of Cajal of the alert monkey

The mesencephalic interstitial nucleus of Cajal (iC) is considered the neural integrator for vertical and torsional eye movements and has also been proposed to be involved in saccade generation. The aim of this study was to elucidate the function of iC in neural integration of different types of eye movements and to distinguish eye movement deficits due to iC impairment from that of the immediately adjacent rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). We addressed the following questions: (1) According to the neural integrator hypothesis, all eye movements including the saccadic system and the vestibulo-ocular reflex (VOR) share a common neural integrator. Do iC lesions impair gaze-holding function for vertical and torsional eye positions and the torsional and vertical VOR gain to a similar degree? (2) What are the dynamic properties of vertical and torsional eye movements deficits after iC lesions, e.g., the specificity of torsional and vertical nystagmus? (3) Is iC involved in saccade generation? We performed 13 uni- and three bilateral iC inactivations by muscimol microinjections in four alert monkeys. Three-dimensional eye movements were studied under head-stationary conditions during vertical and torsional VOR. Under static conditions, unilateral iC injections evoked a shift of Listing's plane to the contralesional side (up to 20 degrees), which increased (ipsilesional ear down) or decreased (ipsilesional ear up) by additional static vestibular stimulation in the roll plane, i.e., ocular counterroll was preserved. The monkeys showed a spontaneous torsional nystagmus with a profound downbeat component. The fast phases of torsional nystagmus always beat toward the lesion side (ipsilesional). Pronounced gaze-holding deficit for torsional and vertical eye positions (neural integrator failure) was reflected by the reduction of time constants of the exponential decay of the slow phase to 330-370 ms. Whereas the vertical oculomotor range was profoundly decreased (up to 50%) and vertical saccades were reduced in amplitude, saccade velocity remained normal and horizontal eye movements were not affected. Bilateral iC injections reduced the shift of Listing's plane caused by unilateral injections, i.e., back toward the plane of zero torsion. Torsional nystagmus reversed its direction and ceased, whereas vertical nystagmus persisted. In contrast to unilateral injection, there was additional upbeating nystagmus. Time constants of the position integrator of the gaze-holding system did not differ between unilateral and bilateral injections. The range of stable vertical eye positions and saccade amplitude was smaller when compared with unilateral injections, but the main sequence remained normal. Dynamic vestibular stimulation after unilateral iC injections had virtually no effect on torsional and vertical VOR gain and phase at the same time when time constants already indicated severe integrator failure. Torsional VOR elicited a constant slow-phase velocity offset up to 30 degrees toward the contralesional side, i.e., in the opposite direction to spontaneous torsional nystagmus. Likewise, vertical VOR showed a velocity offset in an upward direction, i.e., opposite to the spontaneous downbeat nystagmus. Contralesional torsional and upward vertical quick phases were missing or severely reduced in amplitude but showed normal velocity. In contrast, bilateral iC injections reduced the gain of the torsional and vertical VOR by 50% and caused a phase lead of 10-20 degrees (eye compared with head velocity). We propose that the slow-phase velocity offset during torsional and vertical VOR reflects a vestibular imbalance. It therefore appears likely that the vertical and torsional nystagmus after iC lesions is not only caused by a neural integrator failure but also by a vestibular imbalance. Unilateral iC injections have clearly differential effects on the VOR and the gaze-holding function. (ABSTRACT TRUNCATED)     

Responses of Purkinje cells of cerebellar vermis to sinusoidal rotation of neck

1. The response of Purkinje (P) cells located in the vermal cortex of the cerebellar anterior lobe to sinusoidal rotation of the neck was investigated in precollicular decerebrate cats. The head of the animal was fixed in a sterotaxic frame while the spinous process of the second cervical vertebra was held by a clamp rigidly fixed to the tilting table. It was then possible to elicit a selective neck input by rotating the neck and the body simultaneously along the longitudinal axis of the animal while maintaining the head in horizontal position. 2. Among the 95 P-cells tested for neck stimulation, 35 units showed a mossy fiber (MF) or a climbing fiber (CF) response to sinusoidal rotation of the axis vertebra at the frequency of 0.026 Hz and at the peak amplitude of displacement of 5--10 degrees. The response consisted in a periodic modulation of the discharge frequency during sinusoidal rotation of the neck. Most of these units were excited during side-down rotation of the neck, but were inhibited during side-up rotation. 3. The threshold amplitude of neck rotation responsible for the MF-induced responses varied in different units from 1 to 3 degrees at the frequency of 0.026 Hz. The sensitivity of the units, expressed in percentage change of the average firing rate per degree of displacement, either did not change or very slightly decreased as a result of increasing amplitude of stimulation from 1--3 degrees to 10--15 degrees at the frequency of 0.026 Hz or by increasing frequency of neck rotation from 0.015 to 0.15 Hz at the amplitude of neck displacement of 5--10 degrees. 4. Changes in amplitude or frequency of stimulation at the parameters reported above did not greatly modify the phase of the unit responses relative to the side-down position of the neck. These findings indicate that the MF and CF responses of P-cells to sinusoidal rotation of the neck depended on changes in neck position and not on changes in velocity of neck rotation. 5. The observation that the majority of responding P-cells located in the vermal cortex of the cerebellar anterior lobe increased their firing rate during side-down rotation of the neck is discussed in relation to the results of stimulation and lesion experiments, indicating that postural changes can be elicited either during asymmetric stimulation of neck receptors or by unilateral interruption of the neck afferents.     

Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements

The fastigial nucleus (FN) receives vestibular information predominantly from Purkinje cells of the vermis. FN in the monkey can be divided in a rostral part, related to spinal mechanisms, and a caudal part with oculomotor functions. To understand the role of FN during movements in space, single-unit activity in alert monkeys was recorded during passive three-dimensional head movements from rostral FN. Seated monkeys were rotated sinusoidally around a horizontal earth-fixed axis (vertical stimulation) at different orientations 15 degrees apart (including roll, pitch, vertical canal plane and intermediate planes). In addition, sinusoidal rotations around an earth-vertical axis (yaw stimulus) included different roll and pitch positions (+/-10 degrees, +/-20 degrees). The latter positions were also used for static stimulation. One hundred fifty-eight neurons in two monkeys were modulated during the sinusoidal vertical search stimulation. The vast majority showed a uniform response pattern: a maximum at a specific head orientation (response vector orientation) and a null response 90 degrees apart. Detailed analysis was obtained from 111 neurons. On the basis of their phase relation during dynamic stimulation and their response to static tilt, these neurons were classified as vertical semicircular canal related (n = 79, 71.2%) or otolith related (n = 25; 22.5%). Only seven neurons did not follow the usual response pattern and were classified as complex neurons. For the vertical canal-related neurons (n = 79) all eight major response vector orientations (ipsilateral or contralateral anterior canal, posterior canal, roll, and nose-down and nose-up pitch) were found in Fn on one side. Neurons with ipsilateral orientations were more numerous and on average more sensitive than those with contralateral orientations. Twenty-eight percent of the vertical canal-related neurons also responded to horizontal canal stimulation. None of the vertical canal-related neurons responded to static tilt. Otolith-related neurons (n = 25) had a phase relation close to head position and were considerably less numerous than canal-related neurons. Except for pitch, all other response vector orientations were found. Seventy percent of these neurons responding during dynamic stimulation also responded during static tilt. The sensitivity during dynamic stimulation was always higher than during static stimulation. Sixty-one percent of the otolith-related neurons responded also to horizontal canal stimulation. These results show that in FN, robust vestibular signals are abundant. Canal-related responses are much more common than otolith-related responses. Although for many canal neurons the responses can be related to single canal planes, convergence between vertical canals but also with horizontal canals is common.     

Eye movements evoked by proprioceptive stimulation along the body axis in humans

Proprioceptive input arising from torsional body movements elicits small reflexive eye movements. The functional relevance of these eye movements is still unknown so far. We evaluated their slow components as a function of stimulus frequency and velocity. The horizontal eye movements of seven adult subjects were recorded using an infrared device, while horizontal rotations were applied at three segmental levels of the body [i.e., between head and shoulders (neck stimulus), shoulders and pelvis (trunk stimulus), and pelvis and feet (leg stimulus)]. The following results were obtained: (1) Sinusoidal leg stimulation evoked an eye response with the slow component in the direction of the movement of the feet, while the response to trunk and neck stimulation was oriented in the opposite direction (i.e., in that of the head). (2) In contrast, the gain behavior of all three responses was similar, with very low gain at mid- to high frequencies (tested up to 0.4 Hz) but increasing gain at low frequencies (down to 0.0125 Hz). We show that this gain behavior is mainly due to a gain nonlinearity for low angular velocities. (3) The responses were compatible with linear summation when an interaction series was tested in which the leg stimulus was combined with a vestibular stimulus. (4) There was good correspondence of the median gain curves when eye responses were compared with psychophysical responses (perceived body rotation in space; additionally recorded in the interaction series). However, correlation of gain values on a single-trial basis was poor. (5) During transient neck stimulation (smoothed position ramp), the neck response noticeably consisted of two components -- an initial head-directed eye shift (phasic component) followed by a shift in the opposite direction (compensatory tonic component). Both leg and neck responses can be described by one simple, dynamic model. In the model the proprioceptive input is fed into the gaze network via two pathways which differ in their dynamics and directional sign. The model simulates either leg or neck responses by selecting an appropriate weight for the gain of one of the pathways (phasic component). The interaction results can also be simulated when a vestibular path is added. This model has similarities to one we recently proposed for human self-motion perception and postural control. A major difference, though, is that the proprioceptive input to the gaze-stabilizing network is weak (restricted to low velocities), unlike that used for perception and postural control. We hold that the former undergoes involution during ontogenesis, as subjects depend on the functionally more appropriate vestibulo-ocular reflex. Yet, the weak proprioceptive eye responses that remain may have some functional relevance. Their tonic component tends to stabilize the eyes by slowly shifting them toward the primary head position relative to the body support. This applies solely to the earth-horizontal plane in which the vestibular signal has no static sensitivity.     

Functional characterization of primary vestibular afferents in the frog

1. In order to more accurately identify the nature of the vestibular input to central neurons, the response properties of single semicircular canal and otolith units in the frog VIIth nerve were studied in curarized preparations. 2. An equation describing the response plane was calculated for each canal on the basis of null point measurements. These results show that the ipsilateral canal planes are orthogonal within 2-5 degrees, and the pairs of right-left synergists are essentially coplanar. A head position of 10-20 degrees maxilla nose up produces optimal horizontal canal and minimal vertical canal activation with horizontal rotation. 3. The frequency response of the horizontal canal was examined in the range 0.025-0.5 Hz. Comparatively shorter phase-lags and a 10 fold greater acceleration gain in this frequency range distinguish the frog from the mammalian species studied. 4. Otolithic responses were tonic, phasic-tonic, and phasic in nature. The preponderance of the latter two groups is stressed (94%). Tonic responses were proportional to the gravitational vector change. Phasic responses were proportional to velocity during transitions in head position and phase-led displacement (30-80%) with sinusoidal acceleration in roll and pitch. 5. Efferent vestibular neurons respond to rotation in the horizontal (usually Type III) as well as vertical planes. Responses in the vertical planes result from canal and/or otolithic input to these neurons indicating that the vestibular efferent system receives extensive multi-labyrinthine convergence.     

Torticollis due to disinhibition of the vestibulo-collic reflex in a patient with Steele-Richardson-Olszewski syndrome

A patient with the clinical picture of Steele-Richardson-Olszewski syndrome and an unusual intermittent neck twisting is reported. He had virtually no voluntary ocular movements and only very slow, low-amplitude voluntary head movements. However, in response to optokinetic or vestibular stimulation, he developed full eye deviations in the direction of the slow phase of the expected nystagmus. No quick phases were observed, and the deviation outlasted the duration of the vestibular stimuli because of defective saccades. The head also turned fully during these stimuli, quicker than on attempted voluntary movements, and remained deviated similarly to the eyes. This suggests that the neck deviations in this patient were due to a disinhibited vestibulo-collic reflex and a disturbed head position resetting mechanism. Neck electromyographic responses in response to whole-body rotation indicated that the vestibulocollic reflex responsible for the torticollis in this patient had a short latency of approximately 30 ms.     

Spatial transformation of semicircular canal signals into abducens motor signals. A comparison between grass frogs and water frogs

The spatial transformation of semicircular canal signals to extraocular motor signals was studied by recording abducens nerve responses in grass and water frogs. Both species have similar vestibular canal coordinates but dissimilar orientations of their optic axes. Before sinusoidal oscillation in darkness the static head position was systematically altered to determine the planes of head oscillation in pitch and roll associated with minimal abducens nerve responses. Measured data and known canal plane vectors were used to calculate the abducens response vector in canal coordinates. The abducens vector deviated from the horizontal canal plane vector in grass frogs by 15 degrees and in water frogs by 34 degrees but was aligned with the pulling direction of the lateral rectus muscle in each of the two species. Lesion experiments demonstrated the importance of convergent inputs from the contralateral horizontal and anterior semicircular canals for the orientation of the abducens response vector. Thus, the orientation of the optic axis and the pulling directions of extraocular muscles are taken into account by the central organization of vestibulo-ocular reflexes. Horizontal and vertical canal signals are combined species-specifically to transform the spatial coordinates of sensory signals into appropriate extraocular motor signals.     

A Rotation Invariant in 3-D Reaching.

In 3 experiments, the authors investigated changes in hand orientation during a 3-D reaching task that imposed specific position and orientation requirements on the hand's initial and final postures. Instantaneous hand orientation was described using 3-element rotation vectors representing current orientation as a rotation from a fixed reference orientation. The direction of these 3-vectors gives the rotation axis, and the length of the axis gives the rotation magnitude. Hand translation parameters (relative timing of velocity components, trajectory linearity) varied systematically with position and orientation of the target, arm load, and movement velocity. Hand orientation, however, remained constrained to 2-D planar motions in the 3-D space of all possible rotation vectors. Implications of this functional constraint for theories of trajectory formation are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effect of subacute administration of a neem pesticide on rat metabolic enzymes

Dual search coils were used to record horizontal, vertical and torsional eye movement components of one eye during nystagmus caused by off-center yaw rotation (yaw centrifugation). Both normal healthy human subjects (n=7) and patients with only one functioning labyrinth (n=12) were studied in order to clarify how the concomitant linear acceleration affected the nystagmus response. Each subject was seated with head erect on the arm of a fixed-chair human centrifuge, 1 m away from the center of the rotation, and positioned to be facing along a radius; either towards (facing-in) or away from (facing-out) the center of rotation. Both yaw right and yaw left angular accelerations of 10 degrees s(-2) from 0 to 200 degrees/s were studied. During rotation a centripetal linear acceleration (increasing from 0 to 1.24xg units) was directed along the subject's naso-occipital axis resulting in a shift of the resultant angle of the gravitoinertial acceleration (GIA) of 51 degrees in the subject's pitch plane and an increase in the total GIA magnitude from 1.0 to 1.59xg. In normal subjects during the angular acceleration off-center there were, in addition to the horizontal eye velocity components, torsional and vertical eye velocities present. The magnitude of these additional components, although small, was larger than observed during similar experiments with on-center angular acceleration (Haslwanter et al. 1996), and the change in these components is attributed to the additional effect of the linear acceleration stimulation. In the pitch plane the average size of the shift of the axis of eye velocity (AEV) during the acceleration was about 8 degrees for a 51 degrees shift of the GIA (around 16% of the GIA shift) so that the AEV-GIA alignment was inadequate. There was a very marked difference in the size of the AEV shift depending on whether the person was facing-in [AEV shift forward (i.e. non-compensatory) of about 4 degrees] or facing-out [AEV shift forward (i.e. compensatory) of around 12 degrees]. The linear acceleration decreased the time constant of decay of the horizontal component of the post-rotatory nystagmus: from an average of 24.8 degrees/s facing-in to an average of 11.3 degrees/s facing-out. The linear acceleration dumps torsional eye velocity in an manner analogous to, but independent of, the dumping of horizontal eye velocity. Patients with UVD had dramatically reduced torsional eye velocities for both facing-in and facing-out headings, and there was little if any shift of the AEV in UVD patients. The relatively small effects of linear acceleration on human canal-induced nystagmus found here confirms other recent studies in humans (Fetter et al. 1996) in contrast to evidence from monkeys and emphasizes the large and important differences between humans and monkeys in otolith-canal interaction. Our results confirm the vestibular control of the axis of eye velocity of humans is essentially head-referenced whereas in monkeys that control is essentially space-referenced.     

Human horizontal vestibulo-ocular reflex initiation: effects of acceleration, target distance, and unilateral deafferentation

The vestibulo-ocular reflex (VOR) generates compensatory eye movements in response to angular and linear acceleration sensed by semicircular canals and otoliths respectively. Gaze stabilization demands that responses to linear acceleration be adjusted for viewing distance. This study in humans determined the transient dynamics of VOR initiation during angular and linear acceleration, modification of the VOR by viewing distance, and the effect of unilateral deafferentation. Combinations of unpredictable transient angular and linear head rotation were created by whole body yaw rotation about eccentric axes: 10 cm anterior to eyes, centered between eyes, centered between otoliths, and 20 cm posterior to eyes. Subjects viewed a target 500, 30, or 15 cm away that was extinguished immediately before rotation. There were four stimulus intensities up to a maximum peak acceleration of 2,800 degrees/s2. The normal initial VOR response began 7-10 ms after onset of head rotation. Response gain (eye velocity/head velocity) for near as compared with distant targets was increased as early as 1-11 ms after onset of eye movement; this initial effect was independent of linear acceleration. An otolith mediated effect modified VOR gain depending on both linear acceleration and target distance beginning 25-90 ms after onset of head rotation. For rotational axes anterior to the otoliths, VOR gain for the nearest target was initially higher but later became less than that for the far target. There was no gain correction for the physical separation between the eyes and otoliths. With lower acceleration, there was a nonlinear reduction in the early gain increase with close targets although later otolith-mediated effects were not affected. In subjects with unilateral vestibular deafferentation, the initial VOR was quantitatively normal for rotation toward the intact side. When rotating toward the deafferented side, VOR gain remained less than half of normal for at least the initial 55 ms when head acceleration was highest and was not modulated by target distance. After this initial high acceleration period, gain increased to a degree depending on target distance and axis eccentricity. This behavior suggests that the commissural VOR pathways are not modulated by target distance. These results suggest that the VOR is initially driven by short latency ipsilateral target distance dependent and bilateral target-distance independent canal pathways. After 25 ms, otolith inputs contribute to the target distance dependent pathway. The otolith input later grows to eventually dominate the target distance mediated effect. When otolith input is unavailable the target distance mediated canal component persists. Modulation of canal mediated responses by target distance is a nonlinear effect, most evident for high head accelerations.