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.     

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)     

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 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.     

Expansion of visual space during optokinetic afternystagmus (OKAN)

The mechanisms underlying visual perceptual stability are usually investigated using voluntary eye movements. In such studies, errors in perceptual stability during saccades and pursuit are commonly interpreted as mismatches between actual eye position and eye-position signals in the brain. The generality of this interpretation could in principle be tested by investigating spatial localization during reflexive eye movements whose kinematics are very similar to those of voluntary eye movements. Accordingly, in this study, we determined mislocalization of flashed visual targets during optokinetic afternystagmus (OKAN). These eye movements are quite unique in that they occur in complete darkness and are generated by subcortical control mechanisms. We found that during horizontal OKAN slow phases, subjects mislocalize targets away from the fovea in the horizontal direction. This corresponds to a perceived expansion of visual space and is unlike mislocalization found for any other voluntary or reflexive eye movement. Around the OKAN fast phases, we found a bias in the direction of the fast phase prior to its onset and opposite to the fast-phase direction thereafter. Such a biphasic modulation has also been reported in the temporal vicinity of saccades and during optokinetic nystagmus (OKN). A direct comparison, however, showed that the modulation during OKAN was much larger and occurred earlier relative to fast-phase onset than during OKN. A simple mismatch between the current eye position and the eye-position signal in the brain is unlikely to explain such disparate results across similar eye movements. Instead, these data support the view that mislocalization arises from errors in eye-centered position information.     

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)     

Role of irregular otolith afferents in the steady-state nystagmus during off-vertical axis rotation.

1. During constant velocity off-vertical axis rotations (OVAR) in the dark a compensatory ocular nystagmus is present throughout rotation despite the lack of a maintained signal from the semicircular canals. Lesion experiments and canal plugging have attributed the steady-state ocular nystagmus during OVAR to inputs from the otolith organs and have demonstrated that it depends on an intact velocity storage mechanism. 2. To test whether irregularly discharging otolith afferents play a crucial role in the generation of the steady-state eye nystagmus during OVAR, we have used anodal (inhibitory) currents bilaterally to selectively and reversibly block irregular vestibular afferent discharge. During delivery of DC anodal currents (100 microA) bilaterally to both ears, the slow phase eye velocity of the steady-state nystagmus during OVAR was reduced or completely abolished. The disruption of the steady-state nystagmus was transient and lasted only during the period of galvanic stimulation. 3. To distinguish a possible effect of ablation of the background discharge rates of irregular vestibular afferents on the velocity storage mechanism from specific contributions of the dynamic responses from irregular otolith afferents to the circuit responsible for the generation of the steady-state nystagmus, bilateral DC anodal galvanic stimulation was applied during optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN). No change in OKN and OKAN was observed.(ABSTRACT TRUNCATED AT 250 WORDS)     

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)     

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     

Slow eye movements induced by apparent target motion in monkey

Summary Slow eye movements were observed while the monkey fixated on a subject-stationary, small target light in front of a moving optokinetic drum in an attempt to suppress optokinetic nystagmus (OKN). These slow eye movements of low amplitude were directed opposite to the moving optokinetic stimulus and, hence, were not identical to slow phases of incompletely suppressed OKN. It is assumed, based on comparable findings in humans, that these slow eye movements are induced by a perceived target motion, i.e. by the perception of an apparent motion of the subject-stationary fixation light opposite to the actual motion of the optokinetic drum.Supported by a grant from the Swiss National Foundation (3.510-0.86)     

Effects of static tilt about the roll axis on horizontal and vertical optokinetic nystagmus and optokinetic after-nystagmus in humans

Summary Horizontal and vertical OKN and OKAN were recorded in four conditions using the EOG technique. Instructions to subjects were aimed at obtaining a look type OKN. Two optokinetic stimulators, a stationary sphere and a binocular portable model, were compared with the subject in the upright condition. Three posture orientations, upright, 90° roll (horizontal), and upside-down, were then compared using the portable stimulator to determine the effect of roll-axis tilt on OKN at three velocities and on OKAN. Vertical OKN asymmetry was found to increase in the 90° roll position and to tend toward a reversal in the upside-down position. The time constant of vertical OKAN with slow phase up increased in both the 90° roll and upside-down positions. And finally, cross-coupled vertical eye movements during and after horizontal OKN were clearly observed. These results confirm the data obtained in monkeys, and are in accordance with the hypothesis of a three-dimensional organization of the velocity storage mechanism.     

Optokinetic nystagmus in the ferret: including selected comparisons with the cat

Summary The aim of this study was to evaluate the functional significance of similarities observed in the anatomy and the physiology of cat and ferret visual systems. Optokinetic nystagmus (OKN) in response to movement of the entire visual field, and optokinetic after nystagmus (OKAN) were measured in 8 ferrets with binocular stimulation. A shift of the beating field in the same direction as the fast phase of eye movements was observed both in ferret and cat. The absence of a fast rise in slow phase velocity (SPV) and similarities in the time constant to reach the steady state OKN gain, using step velocity stimuli are noted. As in the cat, primary OKAN was observed with a gradual decrease in its SPV. Following termination of stimulation, no sudden fall in SPV was noted for either species. However, for the ferret, the decrease was more rapid. With monocular stimulation, small differences were observed in OKN gain when responses to temporonasal and nasotemporal directions of the stimulus were compared in the two species. In contrast, the ferret displays a OKN gain which is approximatively twice that of the cat at stimulus velocities of 100°/sec. Even at 200°/sec., visual movement still induces a discernable OKN response (gain.0.07). Secondary OKAN, always present in the cat, was observed in only 43% of ferret records. Taken together with other considerations, these findings recommend the ferret as an alternative to the cat for the study of OKN and of other visuo-motor capacities in carnivores.     

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 primate flocculus during optokinetic stimulation,smooth pursuit eye movements and VOR-suppression

Summary Purkinje cell (PC), activity in the flocculus of trained monkeys was recorded during: 1) Vestibular stimulation in darkness. 2) Suppression of the vestibulo-ocular reflex (VOR-supp) by fixation of a small light spot stationary with respect to the monkey. 3) Visual-vestibular conflict (i.e. the visual surround moves together with the monkey during vestibular stimulation), which leads to attenuation or suppression of vestibular nystagmus. 4) Smooth pursuit eye movements. 5) Optokinetic nystagmus (OKN). 6) Suppression of nystagmus during optokinetic stimulation (OKN-supp) by fixation of a small light spot; whereby stimulus velocity corresponds then to image slip velocity.Results were obtained from PCs, which were activated with VOR-supp during rotation to the ipsilateral side. The same PCs were also modulated during smooth pursuit and visual-vestibular conflict. No tonic modulation during constant velocity OKN occurred with slow-phase nystagmus velocities below 40–60 deg/s. Tonic responses were only seen at higher nystagmus velocities. Transient activity changes appeared at the beginning and end of optokinetic stimulation. PCs were not modulated by image slip velocity during OKN-supp.The results show that in primates the same population of floccular PCs is involved in different mechanisms of visual-vestibular interaction and that smooth pursuit and certain components of OKN slow-phase velocity share the same neural pathway. It is argued that the activity of these neurons can neither be related strictly to gaze, eye or image slip velocity; instead, their activity pattern can be best interpreted by assuming a modulation, which is complementary to that of central vestibular neurons of the vestibular nuclei, in the control of slow eye movements.Supported by Swiss National Foundation for Scientific Research 3.343-2.78, and Deutsche Forschungsgemeinschaft, SFB 200, A2     

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.     

fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation

Small-field optokinetic nystagmus (OKN) was performed in seven healthy volunteers in order to analyze the activation and deactivation patterns of visual motion, ocular motor, and multisensory vestibular cortex areas by means of fMRI during coherent visual motion stimulation. BOLD signal decreases (deactivations) were found in the first and second long insular gyri and retroinsular areas (the human homologue of the parietoinsular vestibular cortex and the visual posterior sylvian area in the monkey) of both hemispheres, extending into the transverse temporal gyrus and inferior-anterior parts of the superior temporal gyrus (BA 22), and the precentral gyri at two separate sites (BA 4 and 6). Further deactivations were found in cranioposterior parts of the superior temporal gyrus (BA 22) and the adjacent inferior parietal lobule (BA 40), anterior cingulate gyrus, hippocampus, and corpus callosum. Most of these BOLD signal decreases involved parts of the "multisensory vestibular cortical circuit". These findings support the concept of a reciprocally inhibitory visual–vestibular interaction that has now been demonstrated not only for large-field visual motion stimulation that induces vection (without eye movements) but also for optokinetically induced eye movements (without vection). The functional significance of this concept may be related to the perception of self-motion, since both large-field visual motion stimulation and optokinetic nystagmus are linked to the visual control of self-motion. With respect to activation of the cortical ocular motor system two separate and distinct areas of activations were delineated in the precentral sulcus of both hemispheres, one ventrolaterally (in BA 9) and the other dorsomedially at the junction of the superior frontal sulcus with the precentral sulcus (in BA 6). Both probably correspond to different subregions of the frontal eye field and the premotor cortex for the ocular motor performance of OKN. Electronic Publication     

Neuronal substrates of motor learning in the velocity storage generated during optokinetic stimulation in the squirrel monkey

Chronic motor learning in the vestibuloocular reflex (VOR) results in changes in the gain of this reflex and in other eye movements intimately associated with VOR behavior, e.g., the velocity storage generated by optokinetic stimulation (OKN velocity storage). The aim of the present study was to identify the plastic sites responsible for the change in OKN velocity storage after chronic VOR motor learning. We studied the neuronal responses of vertical eye movement flocculus target neurons (FTNs) during the optokinetic after-nystagmus (OKAN) phase of the optokinetic response (OKR) before and after VOR motor learning. Our findings can be summarized as follows. 1) Chronic VOR motor learning changes the horizontal OKN velocity storage in parallel with changes in VOR gain, whereas the vertical OKN velocity storage is more complex, increasing with VOR gain increases, but not changing following VOR gain decreases. 2) FTNs contain an OKAN signal having opposite directional preferences after chronic high versus low gain learning, suggesting a change in the OKN velocity storage representation of FTNs. 3) Changes in the eye-velocity sensitivity of FTNs during OKAN are correlated with changes in the brain stem head-velocity sensitivity of the same neurons. And 4) these changes in eye-velocity sensitivity of FTNs during OKAN support the new behavior after high gain but not low gain learning. Thus we hypothesize that the changes observed in the OKN velocity storage behavior after chronic learning result from changes in brain stem pathways carrying head velocity and OKN velocity storage information, and that a parallel pathway to vertical FTNs changes its OKN velocity storage representation following low, but not high, gain VOR motor learning.     

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.     

The eye movements of the dark-reared cat

Summary Cats reared in total darkness to adulthood have abnormal eye movements. A spontaneous nystagmus is found in the dark before any visual experience. The eye movements evoked by vestibular or optokinetic stimulation are less effective at compensation than for a normal cat. The vestibuloocular reflex (VOR) has a low gain (around 0.3) and a frequency dependent phase relation. The efficiency of optokinetic nystagmus (OKN) is poorer than for a normal cat, except for downwards stimulus movement which is followed better than normal. OKN is poorest in response to a stimulus viewed monocularly moving in the nasal to temporal direction. Neither VOR nor OKN of a dark-reared cat recover in efficiency within 5 months of the animal being brought into the light. A normal cat put into the dark for 135 days shows none of these abnormalities except an occasional spontaneous nystagmus.This research was supported by USPHS grant EY02248 and by grants from the M.R.C. (MT5201) and NSERC (A9939) of CanadaL. R. Harris was in receipt of a Wellcome travel grant     

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.