Velocity storage in the vestibulo-ocular reflex arc (VOR)

Summary Vestibular and optokinetic nystagmus (OKN) of monkeys were induced by platform and visual surround rotation. Vision prolonged per-rotatory nystagmus and cancelled or reduced post-rotatory nystagmus recorded in darkness. Presumably, activity stored during OKN summed with activity arising in the semicircular canals. The limit of summation was about 120 °/s, the level of saturation of optokinetic after-nystagmus (OKAN). OKN and vestibular nystagmus, induced in the same or in opposite directions diminished or enhanced post-rotatory nystagmus up to 120 °/s. We postulate that a common storage mechanism is used for producing vestibular nystagmus, OKN, and OKAN. Evidence for this is the similar time course of vestibular nystagmus and OKAN and their summation. In addition, stored activity is lost in a similar way by viewing a stationary surround during either OKAN or vestibular nystagmus (fixation suppression).These responses were modelled using direct pathways and a non-ideal integrator coupled to the visual and peripheral vestibular systems. The direct pathways are responsible for rapid changes in eye velocity while the integrator stores activity and mediates slower changes. The integrator stabilizes eye velocity during whole field rotation and extends the time over which the vestibulo-ocular reflex can compensate for head movement.     

Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus

1. Velocity characteristics of optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) induced by constant velocity full field rotation were studied in rhesus monkeys. A technique is described for estimating the dominant time constant of slow phase velocity curves and of monotonically changing data. Time constants obtained by this technique were used in formulating a model of the mechanism responsible for producing OKN and OKAN.2. Slow phase velocity of optokinetic nystagmus in response to steps in stimulus velocity was shown to be composed of two components, a rapid rise, followed by a slower rise to a steady-state value. Peak values of OKN slow phase velocity increased linearly with increases in stimulus velocity to 180 degrees /sec. Maximum slow phase eye velocities in the monkey are 2-3 times as great as in humans.3. At the onset of OKAN, slow phase velocity falls by about 10-20%, followed by a slower decline to zero. Peak OKAN slow phase velocities were linearly related to optokinetic stimulus velocities up to 90-120 degrees /sec. Above 120 degrees /sec OKAN slow phase velocity saturated although OKN slow phase velocity continued to increase.4. The charge and discharge characteristics of OKAN were studied. The OKAN mechanism charged in 5-10 sec and discharged over 20-60 sec in darkness. The time constants of decay in OKAN slow phase velocity decreased as stimulus velocities increased. They also decreased on repeated testing. In several monkeys there was a consistent difference in the rate of decay of OKAN slow phase velocity to the right and left.5. Extended visual fixation discharged the activity responsible for producing OKAN. Short fixation times caused only a partial discharge of the OKAN mechanism. Following brief periods of fixation, OKAN resumed but with depressed slow phase velocities.6. A model based on a state realisation of a peak detector was formulated which approximately reproduces the salient characteristics of OKN and OKAN. This model predicts the three dominant characteristics of OKAN: (1) charge over 5-7 sec, (2) slow discharge in darkness, and (3) rapid discharge with visual fixation. With the addition of direct fast forward pathways, it also correctly predicts the rapid and slow rise in OKN. We postulate that OKAN is produced by a central integrator which is also active during OKN. Presumably this integrator acts to maximize velocities during OKN and to smooth and stabilize ocular following during movement of the visual surround.     

Optokinetic nystagmus in the rabbit and its modulation by bilateral microinjection of carbachol in the cerebellar flocculus

Summary 1. In the alert, pigmented rabbit, eye movements were recorded during optokinetic nystagmus (OKN) and during optokinetic afternystagmus (OKAN). These responses were elicited by steps in surround-velocity ranging from 5–110°/s during binocular as well as monocular viewing. 2. In the baseline condition, OKN showed an approximately linear build-up of eye velocity to a steady-state, followed by a linear decay of eye velocity during OKAN after the lights were turned off. Build-up during binocular viewing was characterized by a constant, maximum eye-acceleration (about 1°/s²) for stimulus velocities up to 60°/s. OKAN, instead, was characterized by a fixed duration (about 10 s) for stimulus velocities up to 20°/s. Steady-state eye velocity saturated at about 50°/s. 3. Monocular stimulation in the preferred (nasal) direction elicited a build-up that was on average twice as slow as during binocular stimulation. Steady-state velocity during monocular stimulation saturated at about 20°/s. OKAN was of equal duration as during binocular stimulation. In the non-preferred direction, a very irregular nystagmus was elicited without velocity build-up. The stronger response to binocular stimulation, compared to the responses under monocular viewing condition in either nasal and temporal direction suggests potentiation of the signals of either eye during binocular viewing. 4. OKN and OKAN were re-assessed after intra-floccular microinjection of the nonselective cholinergic agonist carbachol. In the binocular viewing condition, eye-acceleration during build-up was strongly enhanced from 1°/s² before to 2.5°/s² after injection. The saturation level of steady-state eye velocity was also increased, from 50°/s before to more than 60°/s after carbachol. The duration of OKAN, however, was shortened from 10 s before to 6 s after injection. The response to monocular stimulation in the preferred direction revealed similar changes. 5. The flocculus appears to be involved in the control of the dynamics of OKN in the rabbit. Cholinergic mechanisms affect the floccular control of the rate at which slow-phase velocity can be built up and the rate of decay of eye velocity during OKAN. Cholinergic stimulation of the flocculus enhances the dynamics of OKN, while velocity storage is shortened.     

Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey

Summary 1. The nucleus of the optic tract (NOT) was electrically stimulated in alert rhesus monkeys. In darkness stimulation evoked horizontal nystagmus with ipsilateral slow phases, followed by after-nystagmus in the same direction. The rising time course of the slow phase velocity was similar to the slow rise in optokinetic nystagmus (OKN) and to the charge time of optokinetic after-nystagmus (OKAN). The maximum velocity of the steady state nystagmus was approximately the same as that of OKAN, and the falling time course of the after-nystagmus paralled OKAN. 2. Increases in frequency and duration of stimulation caused the rising and falling time constants of the nystagmus and after-nystagmus to become shorter. Changes in the falling time constant of the after-nystagmus were similar to changes in the time constant of OKAN produced by increases in the velocity or duration of optokinetic stimulation. 3. Stimulus-induced nystagmus was combined with OKN, OKAN and per- and post-rotatory nystagmus. The slow component of OKN as well as OKAN could be prolonged or blocked by stimulation, leaving the rapid component of OKN unaffected. Activity induced by electrical stimulation could also sum with activity arising in the semicircular canals to reduce or abolish post-rotatory nystagmus. 4. Positive stimulus sites for inducing nystagmus were located in the posterolateral pretectum. This included portions of NOT that lie in and around the brachium of the superior colliculus and adjacent regions of the dorsal terminal nucleus (DTN). 5. The data indicate that NOT stimulation had elicited the component of OKN which is responsible for the slow rise in slow phase velocity and for OKAN. The functional implication is that NOT, and possibly DTN, are major sources of visual information related to retinal slip in the animal's yaw plane for semicircular canal-related neurons in the vestibular nuclei. Analyzed in terms of a model of OKN and OKAN (Cohen et al. 1977; Waespe et al. 1983), the indirect pathway, which excites the velocity storage mechanism in the vestibular system to produce the slow component of OKN and OKAN, lies in NOT in the monkey, as it probably also does in cat, rat and rabbit. Pathways carrying activity for the rapid rise in slow phase velocity during OKN or for ocular pursuit appear to lie outside NOT.Supported by NIH grants EY02296, EY04148, EY01867 and PSC-CUNY FRAP award 6-63231     

Characteristics of eye velocity storage during periods of suppression and reversal of eye velocity in monkeys

Summary An eye velocity storage mechanism has been postulated in the vestibulo-optokinetic system to account for the prolongation of vestibular nystagmus (VN) and the occurrence of optokinetic afternystagmus (OKAN). Presentation of a subject-stationary full-field surround during VN and OKAN (= full-field fixation) rapidly reduces activity related to eye velocity of the storage mechanism. If the subject-stationary full-field surround is presented for short periods during VN or OKAN, nystagmus resumes when the animal is again in darkness, but at a lesser velocity than would be predicted from a control response. This reduction in peak eye velocity after fixation reflects a decrease in activity of the storage mechanism due to full-field fixation. This decrease in activity occurs with a shorter time constant compared to that in control trials, it has been called dumping. We demonstrate that a subject-stationary small target light presented during VN or OKAN (= target fixation) also reduces activity of the storage mechanism with a time constant slightly greater than that for full-field fixation, but still considerably smaller than that in control trials. In 3 monkeys the time constant of discharge was reduced during the post-rotatory period from 20 s in control trials to 4.6 s by fixation of a single target light and to 2.9 s by fixation of a full-field. The time constant of discharge was reduced during OKAN from 13.2 s in control trials to 3.8 s by target fixation and to 2.6 s by full-field fixation. We report a second experimental paradigm with which the dynamics of visual-vestibular interaction involving the eye velocity storage mechanism is analysed by means of transient step responses. In this paradigm eye velocity due to activation of the storage mechanism (OKAN) is forced to reverse by a short exposure to a full-field moving in the opposite direction of the slow phases of nystagmus. Short periods of eye velocity reversal did not reduce activity of the storage mechanism more rapidly than fixation, i.e. suppression of eye velocity alone. Fixation of a full-field or of a single target light during vestibular or optokinetic stimulation reduces peak nystagmus velocity after stimulation when monkeys are in darkness. Suppression of OKN by target fixation during full-field stimulation reduces the initial eye velocity of OKAN to 15–20% compared to the OKAN velocity when OKN is allowed to occur. Fixation during vestibular or optokinetic stimulation obviously inhibits full activation of the eye velocity storage mechanism. The results are discussed in relation to current models of visual-vestibular interaction.Supported by Swiss National Foundation for Scientific Research (no. 3.593-0.84)     

Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: Effects of lesions

Optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN), vestibular nystagmus and visual-vestibular interactions were studied in monkeys after surgical ablation of the flocculus and paraflocculus. After bilateral flocculectomy the initial rapid rise in slow phase eye velocity of horizontal and vertical OKN was severely attenuated, and maximum velocities fell to the preoperative saturation level of OKAN. There is generally little or no upward OKAN in the normal monkey, and upward OKN was lost after bilateral lesions. Unilateral flocculectomy affected the rapid rise in horizontal velocity to both sides. Consistent with the absence of a rapid response to steps of surround velocity, animals were unable to follow acceleration of the visual field with eye accelerations faster than about 3-5 degrees/s2. The slow rise in OKN slow phase velocity to a steady state level was prolonged after operation. However, rates of rise were approximately equal for the same initial retinal slips before and after operation. The similarity in the time course of OKN when adjusted for initial retinal slip, and in the gain, saturation level and time course of OKAN before and after flocculectomy indicates that the lesions had not significantly altered the coupling of the visual system to the velocity storage integrator or its associated time constant. When animals were rotated in a subject-stationary visual surround after flocculectomy, they could not suppress the initial jump in eye velocity at the onset of the step. Despite this, they could readily suppress the subsequent nystagmus. The time constant of decline in the conflict situations was almost as short as in the normal monkey and was in the range of the peripheral vestibular time constant. This suggests that although the animals were unable to suppress rapid changes in eye velocity due to activation of direct vestibulo-oculomotor pathways, they had retained their ability to discharge activity from the velocity storage mechanism. Consistent with this, animals had no difficulty in suppressing OKAN after flocculectomy. Visual-vestibular interactions utilizing the velocity storage mechanism were normal after flocculectomy, as was nystagmus induced by rotation about a vertical axis or about axes tilted from the vertical. Also unaffected were the discharge of nystagmus caused by tilting the head out of the plane of the response and visual suppression of nystagmus induced by off-vertical axis rotation. The flocculus does not appear to play an important role in mediating these responses. The data before and after flocculectomy were simulated by a model which is homeomorphic to that presented previously.(ABSTRACT TRUNCATED AT 400 WORDS)     

Shortening of vestibular nystagmus in response to velocity steps by microinjection of carbachol in the rabbit's cerebellar flocculus

Summary It has been proposed that a common velocity-storage mechanism is responsible for the prolongation of vestibular nystagmus beyond the duration of the change in firing frequency of primary vestibular fibers in response to a step in velocity, and for the production of optokinetic afternystagmus (OKAN). In a previous study, bilateral injection of the aselective cholinergic agonist carbachol in the flocculus shortened the duration of buildup of optokinetic nystagmus (OKN) and the duration of OKAN, suggesting floccular involvement in velocity storage (Tan et al. 1992). In extension to that study of OKN, the present study assesses the effects of floccular carbachol on vestibular nystagmus in response to velocity steps. Our results show that injection of carbachol shortens the duration of vestibular nystagmus from about 13 to about 8 s; a finding which supports a common velocity-storage mechanism for optokinetic and vestibular signals. We propose that the indistinguishable effects of carbachol on OKAN and vestibular nystagmus are due to modification of the transmission of an oculomotor corollary signal, which has been identified electrophysiologically in the flocculus.     

Eye movements induced by off-vertical axis rotation (OVAR) at small angles of tilt

Summary Off-vertical rotation (OVAR) in darkness induced continuous horizontal nystagmus in humans at small tilts of the rotation axis (5 to 30 degrees). The horizontal slow eye velocity had two components: a mean velocity in the direction opposite to head rotation and a sinusoidal modulation around the mean. Mean velocity generally did not exceed 10 deg/s, and was less than or equal to the maximum velocity of optokinetic after-nystagmus (OKAN). Both the mean and modulation components of horizontal nystagmus increased with tilt angle and rotational velocity. Vertical slow eye velocity was also modulated sinusoidally, generally around zero. The amplitude of the vertical modulation increased with tilt angle, but not with rotational velocity. In addition to modulations in eye velocity, there were also modulations in horizontal and vertical eye positions. These would partially compensate for head position changes in the yaw and pitch planes during each cycle of OVAR. Modulations in vertical eye position were regular, increased with increases in tilt angle and were separated from eye velocity by 90 deg. These results are compatible with the interpretation that, during OVAR, mean slow velocity of horizontal nystagmus is produced by the velocity storage mechanism in the vestibular system. In addition, they indicate that the otolith organs induce compensatory eye position changes with regard to gravity for tilts in the pitch, yaw and probably also the roll planes. Such compensatory changes could be utilized to study the function of the otolith organs. A functional interpretation of these results is that nystagmus attempts to stabilize the image on the retina of one point of the surrounding world. Mean horizontal velocity would then be opposite to the estimate of head rotational velocity provided by the output of the velocity storage mechanism, as charged by an otolithic input during OVAR. In spite of the lack of actual translation, an estimate of head translational velocity could, in this condition, be constructed from the otolithic signal. The modulation in horizontal eye position would then be compensatory for the perceived head translation. Modulation of vertical eye velocity would compensate for actual changes in head orientation with respect to gravity.     

Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex

Summary 1. Crossing fibers were sectioned at the midline of the medulla caudal to the abducens nucleus in four cynomolgus monkeys. In two animals the lesions caused the time constant of horizontal and vertical per- and post-rotatory nystagmus to fall to 5–8 s. The slow rise in optokinetic nystagmus (OKN), as well as optokinetic after-nystagmus (OKAN) and cross-coupling of horizontal to vertical OKN and OKAN were abolished. Steady state velocities could not be maintained during off-vertical axis rotation (OVAR). Pitch and yaw nystagmus were affected similarly. We conclude that the ability to store activity related to slow phase eye velocity, i.e., velocity storage, was lost in these monkeys for nystagmus about any axis. Velocity storage was partially affected by a small midline lesion in the same region in a third animal. There was no effect of a more superficial midline section in a fourth monkey, and it served as a control. 2. The gain (eye velocity/head velocity) of the vestibuloocular reflex (VOR) was unaffected by the midline lesions. Saccades were normal, as was the ability to hold the eyes in eccentric gaze positions. The gain of the fast component of OKN increased in one monkey to compensate for the loss of the slow component. 3. One animal was tested for its ability to adapt the gain of the VOR due to visual-vestibular mismatch after lesion. Average changes in gain in response to wearing magnifying (2.2 x) and reducing (0.5 x) lenses, were + 35% and — 30%, respectively. This is within the range of normal monkeys. Thus, a midline lesion that abolished velocity storage did not alter that animal's ability to adapt the gain of the VOR. 4. Lesions that reduced or abolished velocity storage interrupted crossing fibers in the rostral medulla, caudal to the abducens nuclei. Cells that contributed axons to this portion of the crossing fibers are most likely located in central portions of the medial vestibular nucleus (MVN) and/or in rostral portion of the descending vestibular nucleus (DVN). The implication is that velocity storage arises from neurons in MVN and DVN whose axons cross the midline.Supported by NS-00294, SFB 220-D8 and Core Center Grant EY-01867     

Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis

Summary Horizontal and vertical eye movements were recorded from cats in response to either a) off-vertical axis rotation (OVAR) at a range of velocities (5–72 deg/s) and a range of tilts (0–60 deg) or b) horizontal (with respect to the cat) optokinetic stimulation (10–80 deg/s), also around a range of tilted axes (0–60 deg). The responses to stopping either of these stimuli were also measured: post-rotatory nystagmus (PRN) following actual rotation, and optokinetic after nystagmus (OKAN) following optokinetic stimulation. The response found during OVAR was a nystagmus with a bias slow-phase velocity that was sinusoidally modulated. The bias was dependent on the tilt and reached 50% of its maximum velocity (maximum was 73±23% of the table velocity) at a tilt of 16 deg. The phase of modulation in horizontal eye velocity bore no consistent relation to the angular rotation. The amplitude of this modulation was roughly correlated with the bias with a slope of 0.13 (deg/s) modulation/(deg/s) bias velocity. There was also a low-velocity vertical bias with the slow-phases upwardly directed. The vertical bias was also modulated and the amplitude depended on the bias velocity (0.27 (deg/s) modulation/ (deg/s) bias velocity). When separated from the canal dependent response, the build up of the OVAR response had a time constant of 5.0±0.8 s. Following OVAR there was no decline in the time constant of PRN which remained at the value measured during earth-vertical axis rotation (EVAR) (6.3±2 s). The peak amplitude of PRN was reduced, dependent on the tilt, reaching only 20% of its EVAR value for a tilt of 20 deg. When a measurable PRN was found, it was accompanied by a slowly-emerging vertical component (time constant 5.4±2s) the effect of which was to vector the PRN accurately onto the earth horizontal. OKN measured about a tilted axis showed no differences in magnitude or direction from EVAR OKN even for tilts as large as 60 deg. OKAN following optokinetic stimulation around a tilted axis appeared normal in the horizontal plane (with respect to the animal) but was accompanied by a slowly emerging (time constant 4.1±2 s) vertical component, the effect of which was to vector the overall OKAN response onto the earth horizontal for tilts less than 20 deg. These results are compared with data from monkey and man and discussed in terms of the involvement of the velocity storage mechanism.     

Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic,vestibular and visuo-vestibular stimulations in the alert pigeon (Columbia livia)

Summary Extracellular recordings were performed in the nucleus of the basal optic root (nBOR) of alert pigeons during optokinetic nystagmus (OKN), vestibulo-ocular reflex (VOR) and combined visuo-vestibular stimulation. Cell identification was assessed either by histological control or by electrophysiological testing (antidromic response to vestibulo-cerebellar or oculomotor complex stimulation). 1) OKN was induced in 8 directions by a binocular stimulation. During the fast phase of OKN, optokinetic after nystagmus (OKAN) or reversed OKAN, most cells showed an inhibition which varied in magnitude independent of the direction of stimulation. A few cells however showed a phasic discharge for some OKN directions. 2) During the slow phase of OKN induced by a binocular stimulation, cells displayed either a tonic activation or a more or less strong inhibition according to the direction of the OKN. Cells were classified in 4 groups, according to their degree of directional specificity. The best OKN direction (slow phase) for maximal cell activation was upwards and naso-upwards, and next to best, nasotemporal and downwards. Maximal cell inhibition occurred during downward, and for some cells during upward, directions. 3) During OKN induced by stimulating the eye contralateral to the recorded nBOR, cell responses resembled those obtained during binocular stimulation, but, during ipsilaterally induced OKN, the cells lost their directional specificity. As a result of binocular integration, neuronal activation seems to originate from contralateral input whereas cell inhibition would mainly come from ipsilateral input. 4) During sinusoidal optokinetic stimulation induced in the temporo downward-naso upward axis, cells showed a more or less marked modulation (according to their directional selectivity) that was closely in phase with the stimulation velocity, and therefore probably with retinal slip. 5) nBOR cells appeared generally unaffected during both the slow phase and the fast phase of the VOR. However, some cells showed a slight but irregular modulation which might imply a weak vestibular input. During visuo-vestibular stimulation, the response resembled that obtained with sinusoidal optokinetic stimulation but the fast phase inhibition was often strengthened in the downwards direction (fast phase).     

Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation

Summary Activity of vestibular only (VO) and vestibular plus saccade (VPS) units was recorded in the rostral part of the medial vestibular nucleus and caudal part of the superior vestibular nucleus of alert rhesus monkeys. By estimating the null axes of recorded units (n = 79), the optimal plane of activation was approximately the mean plane of reciprocal semicircular canals, i.e., lateral canals, left anterior-right posterior (LARP) canals or right anterior-left posterior (RALP) canals. All units were excited by rotation in a direction that excited a corresponding ipsilateral semicircular canal. Thus, they all displayed a type I response. With the animal upright, there were rapid changes in firing rates of both VO and VPS units in response to steps of angular velocity about a vertical axis. The units were bidirectionally activated during vestibular nystagmus (VN), horizontal optokinetic nystagmus (OKN), optokinetic afternystagmus (OKAN) and off-vertical axis rotation (OVAR). The rising and falling time constants of the responses to rotation indicated that they were closely linked to velocity storage. There were differences between VPS and VO neurons in that activity of VO units followed the expected time course in response to a stimulus even during periods of drowsiness, when eye volocity was reduced. Firing rates of VPS units, on the other hand, were significantly reduced in the drowsy state. Lateral canal-related units had average firing rates that were linearly related to the bias or steady state level of horizontal eye velocity during OVAR over a range of ±60 deg/s. These units could be further divided into two classes according to whether they were modulated during OVAR. Non-modulated units (n = 5) were VO types and all modulated units (n = 5) were VPS types. There was no significant difference between the bias level sensitivities relative to eye velocity of the units with and without modulation (P>0.05). The modulated units had no sustained change in firing rate in response to static head tilts and their phases relative to head position varied from unit to unit. The phase did not appear to be linked to the modulation of horizontal eye velocity during OVAR. The sensitivities of unit activity to eye velocity were similar during all stimulus modalities despite the different gains of eye velocity vs stimulus velocity during VN, OKN and OVAR. Therefore, VO and VPS units are likely to carry an eye velocity signal related to velocity storage. For example, when unit sensitivities were related to head or surround velocity, sensitivity relative to OVAR was less than for VN or OKN. Firing rates of both vertical canal-related VO and VPS units (n= 19) were strongly modulated during OVAR, although they did not show changes in discharge rate during static head tilts relative to the spatial vertical up to a maximal 25 deg. In some cases the amplitude of the modulation increased with increases in head velocity and eye velocity. Average activity of vertical canal-related units was linearly related to steady state horizontal eye velocity in the ipsilateral direction during OVAR. The mean sensitivities of RALP units were not significantly different from those of LARP neurons (P>0.05). Together, their mean sensitivity during OVAR about a subject yaw axis was 0.34 (imp/s)/(deg/s) relative to horizontal eye velocity. This could be explained as a contribution of the vertical canals to horizontal eye velocity due to their orientation in the head. During OVAR to the ipsilateral side, the bias level of neuronal activity decreased and saturated. For steps of rotation about a vertical axis with the animal upright, the firing rates of RALP and LARP units were linearly related to stimulus velocity and eye velocity. Contralateral rotation excited the units reflecting the orientation of the semicircular canals relative to the yaw axis of rotation. RALP and LARP units also responded during horizontal optokinetic stimulation producing both OKN and OKAN. All the vertical canal units had dynamic characteristics closely related to velocity storage. Their response characteristics were consistent with the model that they contribute to horizontal slow phase velocity as part of a three-dimensional system based on a semicircular canal frame of reference. Otolith-related units (n= 5) in the vestibular nuclei showed no evidence of velocity storage and were modulated in accordance with head position during OVAR. Mean amplitude of the modulation of activity during OVAR at a 20 deg tilt and 60 deg/s rotational velocity was 24 imp/s. The data indicate that the vestibular nuclei contain the requisite signals to generate horizontal eye velocity during OVAR. VO and VPS units probably contribute to the bias or velocity storage component while otolith units mainly contribute to the oscillations in eye velocity by generating gravity dependent eye position changes during OVAR. In addition to the velocity storage component of horizontal eye velocity, the vertical VO neurons also have oscillations in their discharge patterns probably related to the vertical component of eye movements generated by the velocity storage integrator.     

Primate translational vestibuloocular reflexes. III. Effects of bilateral labyrinthine electrical stimulation

The effects of functional, reversible ablation and potential recruitment of the most irregular otolith afferents on the dynamics and sensitivity of the translational vestibuloocular reflexes (trVORs) were investigated in rhesus monkeys trained to fixate near and far targets. Translational motion stimuli consisted of either steady-state lateral and fore-aft sinusoidal oscillations or short-lasting transient lateral head displacements. Short-duration (usually <2 s) anodal (inhibitory) and cathodal (excitatory) currents (50-100 microA) were delivered bilaterally during motion. In the presence of anodal labyrinthine stimulation, trVOR sensitivity and its dependence on viewing distance were significantly decreased. In addition, anodal currents significantly increased phase lags. During transient motion, anodal stimulation resulted in significantly lower initial eye acceleration and more sluggish responses. Cathodal currents tended to have opposite effects. The main characteristics of these results were simulated by a simple model where both regularly and irregularly discharging afferents contribute to the trVORs. Anodal labyrinthine currents also were found to decrease eye velocity during long-duration, constant velocity rotations, although results were generally more variable compared with those during translational motion.     

Optokinetic nystagmus and afternystagmus in human beings: relationship to nonlinear processing of information about retinal slip

Summary In four normal human subjects we measured eye movements during full-field optokinetic stimulation (10–220 deg/s) and determined the relationship among retinal-slip velocity (drum velocity minus slow-phase eye velocity), the slow-phase velocity of optokinetic nystagmus (OKN) and the initial value of the slow-phase velocity of optokinetic afternystagmus (OKAN) measured in darkness. OKN and OKAN were maximum (63–84 and 11–19 deg/s, respectively) when retinal slip ranged from 30–100 deg/s. For higher values of retinal slip, OKN and OKAN fell (in 3 subjects) or reached a plateau (in the fourth). The amplitude of OKAN in human beings was much less than that reported in monkeys. The shape, however, of the curve relating retinal slip to the amplitude of OKAN was similar to that of monkeys. Furthermore, in both cases the curve resembles that obtained by plotting the results of experimental recordings of neural discharge in the nucleus of the optic tract as a function of retinal slip. These results imply that the processing of visual information for generation of OKAN is similar in monkeys and human beings but that the gain of the system is much less in human beings. We also found that fixation of a small target during optokinetic stimulation nearly completely prevented the development of OKAN while fixation of a small target for short periods after optokinetic stimulation did not alter the pattern of decay of OKAN. Thus, fixation may actively prevent the coupling of visual information into the velocity-storage mechanism.     

Optokinetic-vestibular interaction in patients with increased gain of the vestibulo-ocular reflex

We studied optokinetic nystagmus (OKN), optokinetic afternystagmus (OKAN) and visual-vestibular interaction in five patients with markedly elevated vestibulo-ocular reflex (VOR) gain due to cerebellar atrophy. All had impaired smooth pursuit, decreased initial slow phase velocity of OKN, and impaired ability to suppress the VOR with real or imagined targets. OKN slow phase velocity gradually built up over 25–45 s, reaching normal values for low stimulus velocities (30 deg/s). Initial velocity of OKAN was increased, but the rate of decay of OKAN was normal. These findings can be explained by models that include separate velocity storage and variable gain elements shared by the vestibular and optokinetic systems.     

Difference between horizontal and vertical optokinetic nystagmus in cats at upright position

The slow-phase velocity (SPV) of optokinetic nystagmus (OKN) and optokinetic after nystagmus (OKAN) in response to a velocity step of surround rotation in the horizontal direction is composed of the rapid and slow components in the cat: a rapid rise, a slow rise to a steady state, a rapid fall, and a slow decline to 0 deg/s. The rapid and slow components are attributed to the direct pathway and velocity storage neuronal mechanisms, respectively. The difference between horizontal and vertical OKN has been reported in the monkey at the upright position, but the slow and rapid components have not been distinguished. The present study compared horizontal OKN-OKAN with vertical OKN-OKAN in the cat at the upright position, distinguishing the rapid and slow components. Constant velocity rotation of a random dot pattern at a velocity of 5 to 160 deg/s was used for optokinetic stimulation. The results: First, the amplitude of the rapid rise was relatively small in all SPV directions and all stimulus velocities investigated, with a slight upward-SPV preference to the downward-SPV (maximum 6.4, 6.0, and 3.4 deg/s in horizontal, upward, and downward SPV directions, respectively). Second, the steady state velocity was large during horizontal OKN (maximum 69.0 deg/s), small during upward-SPV OKN (12.9 deg/s), and missing (SPV is negligibly small and irregular) during downward-SPV OKN, indicating a large directional difference of OKN. Third, the acceleration of the slow rise decreased with the stimulus velocity at higher stimulus velocities >20 deg/s during both horizontal and upward-SPV OKN, suggesting strong nonlinearity in the velocity charge system. Fourth, the decay time course of the OKAN was described by the time constant of the exponential function, and the time constant was longer during horizontal (mean, 8.3 s at a stimulus velocity of 20 deg/s) than during upward-SPV (5.4 s) OKAN, suggesting that the velocity discharge system is relatively linear compared with the velocity charge system. It is concluded that horizontal OKN-OKAN is much larger than vertical OKN-OKAN in the cat at the upright position, and this directional difference is caused mainly by the directional difference in the velocity storage mechanism, but not in the direct pathway mechanism.     

Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey

1. The nucleus of the optic tract (NOT) and the dorsal terminal nucleus (DTN) of the accessory optic system were lesioned electrolytically or with kainic acid in rhesus monkeys. When lesions involved NOT and DTN, peak velocities of optokinetic nystagmus (OKN) with slow phases toward the side of the lesion were reduced, and optokinetic after-nystagmus (OKAN) was reduced or abolished. The jump in slow phase eye velocity at the onset of OKN was smaller in most animals, but was not lost. Initially, there was spontaneous nystagmus with contralateral slow phases. OKN and OKAN with contralateral slow phases were unaffected. 2. Damage to adjacent regions had no effect on OKN or OKAN with two exceptions: 1. A vascular lesion in the MRF, medial to NOT and adjacent to the central gray matter, caused a transient loss of the initial jump in OKN. The slow rise in slow phase velocity was prolonged, but the gain of OKAN was unaffected. There was no effect after a kainic acid lesion in this region in another animal. 2. Lesions of the fiber tract in the pulvinar that inputs to the brachium of the superior colliculus caused a transient reduction in the buildup and peak velocity of OKN and OKAN. 3. In terms of a previous model (Cohen et al. 1977; Waespe et al. 1983), the findings suggest that the indirect pathway that activates the velocity storage integrator in the vestibular system to produce the slow rise in ipsilateral OKN and OKAN, lies in NOT and DTN. Activity for the rapid rise in OKN, carried in the direct pathway, is probably transmitted to the pontine nuclei and flocculus via an anatomically separate fiber pathway that lies in the MRF. A fiber tract in the pulvinar that inputs to the brachium of the superior colliculus appears to carry activity related to retinal slip from the visual cortex to NOT and DTN.     

Purkinje cell activity in the flocculus of vestibular neurectomized and normal monkeys during optokinetic nystagmus (OKN) and smooth pursuit eye movements

Summary 1. Single unit activity was recorded in the primate flocculus after the vestibular nerves were cut (bilateral vestibular neurectomy) during optokinetic nystagmus (OKN), smooth pursuit eye movements (SP) and whole field visual stimulation with gaze fixed on a stationary target light (OKN-suppression). Following vestibular neurectomy monkeys had no vestibular responses and no optokinetic after-nystagmus (OKAN) in the horizontal plane. However, OKN slow phases still reached steady state velocities of up to 100 deg/s. 2. After neurectomy, simple spike (SS) activity of Purkinje cells (P-cells) was modulated in relation to eye velocity, regardless of whether eye velocity was induced by a small target light moving in darkness (SP) or by a moving visual surround (OKN). In over 90% of the P-cells firing rate increased with eye velocity to the ipsilateral side and decreased with velocities to the contralateral side. Modulation in firing rate increased monotonically with increasing eye velocity. The strength of modulation was similar during SP and OKN for the same eye velocity. 3. The change in firing rate of P-cells in response to a sudden change in optokinetic stimulus velocity contained a component related to eye velocity and a component related to eye acceleration. Only a few P-cells were also modulated with image slip velocity during OKN-suppression. 4. The modulation of P-cells during SP and OKN was compared in normal and vestibular neurectomized monkeys. The sensitivity of floccular P-cells to eye velocity during SP was 1.14 imp·s^–1/deg·s^–1 in normal monkey and 1.28 imp·s^–1/deg·s^–1 after neurectomy. The similarity of eye velocity sensitivities demonstrates that neurectomy does not change the characteristics of floccular P-cell modulation during SP. In contrast, during OKN modulation of P-cells is quite different in normal and neurectomized monkey. In normal monkey, P-cells are modulated during steady state OKN for eye velocities above 40–60 deg/s only. This threshold velocity corresponds approximately to the maximal initial OKAN velocity (i.e. OKAN saturation velocity). After neurectomy, the threshold velocity is 0 deg/s and P-cells are modulated during steady state OKN also over ranges of eye velocities that do not cause a response in normal monkey. Sensitivities of P-cells to eye velocity during OKN for eye velocities above the threshold velocity are 1.0 imp·s^–1/deg·s^–1 in neurectomized monkey and 1.43 imp·s^–1/deg·s^–1 in normal monkey. 5. The hypothesis has been put forward that OKN slow phase velocity in normal monkey has two dynamically different components, a fast and a slow component. The results strongly suggest that the two components depend on different neuronal populations. Firing rate of floccular P-cells is modulated in relation to the fast component only. The results furthermore support the idea that it is the smooth pursuit system which may generate the fast component in the OKN slow phase velocity response.Supported by Swiss National Foundation for Scientific Research (Nr. 3.718-0.80 and 3.593-0.84)     

Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity.

1. Monkeys received optokinetic stimulation at 60 degrees/s about their yaw (animal vertical) and pitch (animal horizontal) axes, as well as about other head-centered axes in the coronal plane. The animals were upright or tilted in right-side-down positions with regard to gravity. The stimuli induced horizontal, vertical, and oblique optokinetic nystagmus (OKN). OKN was followed by optokinetic after-nystagmus (OKAN), which was recorded in darkness. 2. When monkeys were tilted, stimulation that generated horizontal or yaw axis eye velocity during OKN induced a vertical or pitch component of slow phase velocity during OKAN. This has been designated as "cross-coupling" of OKAN. Eigenvalues and eigenvectors associated with the system generating OKAN were found as a function of tilt. They were determined by use of the Levenberg-Marquardt algorithm to minimize the mean square error between the output of a model of OKAN and the data. 3. The eigenvector associated with yaw OKAN (yaw axis eigenvector) was maintained close to the spatial vertical regardless of the angle of tilt. The eigenvector associated with pitch OKAN (pitch axis eigenvector) was always aligned with the body axis. The data indicate that velocity storage can be modeled by a piecewise linear system, the structure of which is dependent on gravity and the yaw axis eigenvector, which tends to align with gravity. 4. Yaw axis eigenvectors were also determined by giving optokinetic stimulation about head-centered axes in the coronal plane with the animal in various angles of tilt. A technique using a spectral analysis of residuals was developed to estimate whether yaw and pitch OKAN slow phase velocities decayed concurrently at the same relative rate and over the same time course. The eigenvectors determined by this method were in agreement with those obtained by analyzing OKAN elicited by yaw OKN. 5. During yaw OKN with the animal in tilted positions, the mean vector of the ensuing nystagmus was closer to the body axis than to the spatial vertical. This suggests that there is suppression of the cross-coupled pitch component during OKN. The direction of the stimulus may be utilized to suppress components of velocity storage not coincident with the direction of stimulus motion. 6. There were similarities between the monkey eigenvectors and human perception of the spatial vertical, and the mean of eigenvectors for upward and downward eye velocities overlay human 1-g perceptual data.(ABSTRACT TRUNCATED AT 400 WORDS)     

Asymmetry of visuo-vestibular mechanisms contributes to reversal of optokinetic after-nystagmus

When the visual background is moving while subject fixate a visual target, optokinetic eye movements (OKN) are suppressed and the after response, called optokinetic after nystagmus (OKAN), occurring at the stimuli offset is often inverted as compared to the situation when the OKN movements are allowed. In this study, we investigated whether this reversal of OKAN results from a perceptual or extra-retinal feedback in relation with the pursuit system and/or the vestibular indirect system. Optokinesis performance was studied in normal subjects in four experiments always using the same background motion (1) to characterize the OKN and OKAN performance elicited by the whole visual field motion while fixating or not a central visual target, (2) to investigate the 3D characteristics of the OKAN reversal by using different orientations of the visual stimulation, (3) to correlate the occurrence of an inverted OKAN with functional asymmetry of the visuo-vestibular system, by studying the effects of ocular fixation deviations and finally (4) to examine the effects of the depth plane of gaze fixation on the OKAN characteristics. In Experiments 1 and 2, we observed that the visual fixation during full-field motion induced either a dumping effect or an inversion of the OKAN response that could occur in the different planes of eye movements. The time constant was significantly increased in the inverted after-responses as compared to the not inverted ones. In Experiment 3, we found that the occurrence of an OKAN reversal after eye movement inhibition was significantly related to the presence of right/left asymmetrical OKAN responses. Moreover, the OKAN time constant was strikingly dependent on the eye fixation position during the visual stimulation and this time constant/eye position relation diverged between OKAN responses with and without inversion. Finally, Experiment 4 showed that the OKAN inversion tended to disappear when the visual target to fixate was in the near space as compared to the far space included in the background. These results argue in favor of an extraretinal influence in relation to the dynamics of the vestibulo-motor system, rather than for a perceptual influence on the inverted OKAN mechanisms. More precisely, we postulate that the reversal of OKAN could be linked to an inhibition issued from pursuit signals combined with an asymmetrical activity in the VSM vestibular complex. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.