The induction and compensation of asymmetric eye movements following unilateral blockage of a horizontal semicircular canal in the rabbit

The influence of unilateral plugs of the left horizontal semicircular canal (LHC plugs) of rabbits on the development and compensation of asymmetric eye movements evoked by horizontal vestibular stimulation was studied. LHC plugs caused an immediate reduction of 50-65% in the gain of the horizontal vestibuloocular reflex (HVOR). This reduction in gain was achieved without altering the symmetry of the HVOR, and was accompanied by a change in the axial alignment of eye movements evoked by vestibular stimulation about the vertical (HVOR) and longitudinal (VVOR) axes. Postoperative asymmetry of eye movements developed 12-48 hr after the plugging operation. The development of asymmetry was reduced if the rabbit was restrained for 24 hr, thereby minimizing vestibular stimulation following the plugging operation. Over a 3-4 week period, the normal symmetry of eye movements was restored and the axial alignments of the HVOR and VVOR returned to the preoperative values. The gain of the HVOR did not recover. The horizontal cervicoocular reflex (HCOR) was examined before the plugging operation and after compensation of asymmetry was complete. The gain and phase of the HCOR were not altered. A relatively simple set of explanations at a cellular level is proposed to account for the induction and compensation of asymmetric eye movements following a unilateral plug of the horizontal semicircular canal.     

The influence of gravity on horizontal and vertical vestibulo-ocular and optokinetic reflexes in the rabbit

The influence of the linear acceleration of gravity on the vertical and horizontal vestibulo-ocular reflexes (VVOR, HVOR) as well as the vertical and horizontal optokinetic reflexes (VOKR, HOKR) has been examined in rabbits. Rabbits were mounted in a biaxial rate table in front of a rear projection tangent screen. Eye movements were measured with a light projection technique. The HVOR, VVOR, HOKR and VOKR were measured in rabbits which were maintained both prone and supine. The gain of the HVOR for the supine orientation was reduced at all frequencies tested (0.01-0.80 Hz). Similarly there was a reduction in the gain of the HOKR. By contrast, the gain of the VVOR in the supine orientation was enhanced over a lower range of frequencies (0.02-0.04 Hz) and reduced at higher frequencies (0.10-0.80 Hz). The gain of the VOKR was not reduced in the supine orientation. The range of eye positions over which compensatory eye movements occurred was restricted in the supine orientation. The altered orientation of the medio-laterally polarized hair cells of the utricular maculae with respect to gravity in the supine orientation may cause postural instability and facilitate 'righting reflexes'. A reduction in the gains of the HVOR, VVOR and HOKR caused by linear accelerations in the sagittal plane during locomotion may decrease automatic postural responses during certain movements in which these automatic postural adjustments would not necessarily be adaptive.     

Effect upon eye movements of rabbits induced by severance of mossy fiber visual pathway to the cerebellar flocculus

In albino rabbits the visual mossy fiber pathway to the cerebellar flocculus was interrupted by placing lesions in the nucleus reticularis tegmenti pontis (NRTP). After recovery of more than 3 days, eye movements were tested by means of a television eye tracking system. The optokinetic response (OKR) in one eye induced by sinusoidally moving a vertical slit light on the horizontal plane (2.5° peak-to-peak amplitude) at 0.17-0.033 Hz in front of that eye. In rabbits with unilateral NRTP lesions, the OKR gain was reduced significantly in the eye contralateral to lesions, whereas that in the ipsilateral eye did not differ from control rabbits. The horizontal vestibulo-ocular reflex (HVOR) exhibited no change attributable to NRTP lesions. The operated rabbits were rotated (5° peak-to-peak amplitude) at 0.1 Hz continuously for 3 h, while the slit light was presented to the eye contralateral to the NRTP lesions. During the rotation, the HVOR gain in the test eye increased adaptively as in control rabbits. It is concluded that the visual mossy fiber pathway to the flocculus contributes to the OKR, but not to visually-guided adaptive modification of the HVOR.     

Spatial Organization of the Maculo-Ocular Reflex of the Rat: Responses During Off-Vertical Axis Rotation

Pigmented, head restrained rats were rotated on a turntable about a tilted axis (off-vertical axis rotation; OVAR) in darkness. Evoked eye movements in the horizontal, vertical and torsional planes were recorded simultaneously with a dual search coil in a magnetic field, horizontal response components of both eyes were recorded with a coil on either eye. OVAR resulted in a persisting horizontal, unidirectional ocular nystagmus, compensatory in direction for the rotation of head in space. Superimposed upon this nystagmus were slower cyclic responses of the eye in the vertical and torsional movement planes, that were tightly phase locked with changing head positions in space: ocular depression/elevation with right ear up/down and ocular intorsion/extorsion with nose up/down. Simultaneous recordings of horizontal response components from both eyes revealed phase and gain differences between the horizontal movement components of both eyes, that resulted in a cyclic modulation of the vergence angle. Convergence of the lines of sight during nose up and divergence during nose down, adequate compensatory responses in light for changes in the viewing distance, were actually observed in darkness. Thus the utricular maculo-ocular reflex takes part of the visual consequences of a translational gaze shift into account. It reduces expected retinal disparities by appropriate and rapid vertical, torsional and vergence response components in the same way as canal-ocular reflexes 'compensate' for direction and velocity of expected retinal image slip during head rotation.     

Influence of long-term optokinetic stimulation on eye movements of the rabbit

Two kinds of optokinetic afternystagmus (OKAN) have been studied in rabbits; positive and negative OKAN. Positive OKAN is the persistence of eye movements evoked by optokinetic stimulation following the termination of the stimulus, with the slow phase of the eye movements in the same direction as the inducing stimulus. Negative OKAN is evoked by long duration optokinetic stimulation, and has a slow phase of opposite direction to the inducing stimulus. The stimulus conditions which are optimal for inducing and maintaining negative OKAN were characterized. Rabbits were placed in an optokinetic drum for periods of 12-96 h (with appropriate intervening periods for food and water). Eye movements were recorded during and after the termination of optokinetic stimulation. The optimum optokinetic stimulus velocity for the induction of negative OKAN was 5 degrees/s. The minimum duration of stimulation for the induction of negative OKAN of maximum velocity was 48 h. Once induced, the slow phase of negative OKAN attained velocities of 50-100 degrees/s. Three conditions of restraint of the rabbits were studied after negative OKAN was induced during the intervening periods when eye movements were not being recorded. These conditions were: (1) unrestrained (full freedom of movement) without visual stimulation (in a dark enclosure); (2) restrained (horizontal head and body movement prevented) without visual stimulation; and (3) restrained with visual stimulation (in the stationary optokinetic drum). Conditions 1 and 2 caused negative OKAN to dissipate within 24 h. Condition 3 caused negative OKAN to be maintained for more than 70 h. The velocity imbalance of the horizontal vestibuloocular reflex (HVOR) was measured at different times following the induction of negative OKAN. It provided a more sensitive index of the central imbalance which caused negative OKAN, than did spontaneous nystagmus. One of the consequences of optokinetic stimulation measured over a 16 h period was a decrease in the gain of the optokinetic reflex. This reduction in gain could represent a central adaptation to maintained stimulation which in the absence of continued optokinetic stimulation is expressed as a nystagmus.     

Characteristics of saccades induced by neck torsions: a re-examination in the normal guinea pig.

Torsion of the neck relative to the fixed head results in several reflexes involving the eyes, the neck and the body. One of these reflexes, the cervico-ocular reflex, has been described as having a small gain in the normal animal. However, when the body of a guinea pig is moved relative to the fixed head with a ramp-like velocity profile, saccades are systematically elicited in the direction of body movement. We re-examined the characteristics of this reflex in the normal guinea pig and demonstrated that: (1) it occurs mainly in the range of high velocity body movements; (2) the latency of the saccades is shorter than previously suspected; (3) the saccades are triggered at specific positions relative to the starting and ending positions of rotation, revealing some degree of flexibility in the reflex. We hypothesize that these saccades of nuchal origin are under the control of the same neuronal circuit as visually triggered saccades and quick phases of vestibular nystagmus. Thus, this nuchal reflex may fundamentally subserve orienting behaviour in normal animal.     

Eye and head movements during vestibular stimulation in the alert rabbit

Rabbits passively oscillated in the horizontal plane with a free head tended to stabilize their head in space (re: earth-fixed surroundings) by moving the head on the trunk (neck angular deviation, NAD) opposite the passively imposed body rotation. The gain (NAD/body rotation) of head stabilization varied from 0.0 to 0.95 (nearly perfect stability) and was most commonly above 0.5. Horizontal eye movement (HEM) was inversely proportional to head-in-space stability, i.e. the gaze (sum of HEM, NAD, and body rotation) was stable in space (regardless of the gain of head stabilization). When the head was fixed to the rotating platform, attempted head movements (head torque) mimicked eye movements in both the slow and fast phases of vestibular nystagmus; tonic eye position was also accompanied by conjugate shifts in tonic head torque. Thus, while eye and head movements may at times be linked, that the slow eye and head movements vary inversely during vestibular stimulation with a free head indicates that the linkage is not rigid.Absence of a textured stationary visual field consistently produced a response termed ‘visual inattentiveness,’ which was characterized by, among other things, a reduction of head and gaze stability in space. This behavioral response could also be reproduced in a subject allowed vision during prolonged vestibular stimulation in the absence of other environmental stimuli. It is suggested that rabbits optimize gaze stability (re: stationary surroundings), with the head contributing variably, as long as the animal is attending to its surroundings.     

The vestibulo-ocular reflex in the cat during linear acceleration in the sagittal plane

The horizontal and vertical components of the vestibulo-ocular reflex (VOR) were recorded in alert cats that were rotated with their head placed on or 45 cm eccentric from the axis of rotation. During off-axis rotation there was a centripetal acceleration along the animal's naso-occipital axis that changed the direction and the magnitude of the resultant otolith force in the animal's sagittal plane. When the animal was upright and eccentric from the axis of rotation, the horizontal VOR (HVOR) had a shorter time constant and smaller amplitude compared to the on-axis HVOR. The effect was symmetrical for both directions of the naso-occipital linear acceleration. When the animal was on its side and faced away from the axis of rotation, there was a decrease in the time constant of the down VOR. When the animal faced the opposite direction, the down VOR time constant was increased. No statistically significant effect was found on the amplitude of the VVOR and the time constant of the up VOR.     

Prediction of the body rotation-induced torques on the arm during reaching movements: evidence from a proprioceptively deafferented subject

Reaching for a target while rotating the trunk generates substantial Coriolis and centrifugal torques that push the arm in the opposite direction of the rotations. These torques rarely perturb movement accuracy, suggesting that they are compensated for during the movement. Here we tested whether signals generated during body motion (e.g., vestibular) can be used to predict the torques induced by the body rotation and to modify the motor commands accordingly. We asked a deafferented subject to reach for a memorized visual target in darkness. At the onset of the reaching, the patient was rotated 25° or 40° in the clockwise or the counterclockwise directions. During the rotation, the patient's head remained either fixed in space (Head-Fixed condition) or fixed on the trunk (Head Rotation condition). At the rotation onset, the deafferented patient's hand largely deviated from the mid-sagittal plane in both conditions. The hand deviations were compensated for in the Head Rotation condition only. These results highlight the computational faculty of the brain and show that body rotation-related information can be processed for predicting the consequence of the rotation dynamics on the reaching arm movements.     

Horizontal and vertical vestibulo-ocular and cervico-ocular reflexes in the monkey during high frequency rotation

In the alert monkey the horizontal vestibulo-ocular reflex (VOR) is basically compensatory over the range of 0.5 to 6 Hz with a gain near unity, and with the phase of the compensatory eye position having a minimal lag with respect to head position. Typical frequency-dependent eye movement patterns were observed. Vertical VOR is also compensatory having the same phase relations but with a reduced gain (-2.5 to -3.7 dB). In this range, vestibular input appears to be the predominant sensory influence on reflex eye movements. Additional optokinetic reflexes do not improve the VOR above 0.5 Hz. The horizontal cervico-ocular reflex (COR) is minimal or absent in normal monkeys.     

The ocular following reflex in cats deprived of pattern vision from birth

An investigation of vertical ocular following reflexes evoked from retinal sites of different horizontal eccentricity was carried out on visually deprived cats. The recording was performed in pretrigeminal preparations where horizontal eye movements are absent. A light slit or a black stick (1° × 4°) were moved with 10°/sec speed for 2 sec along the vertical meridian or parallelly up to 40° in the nasal or temporal hemified. As in previously described normally reared cats, the following reflexes were evoked from the whole area, but the pursuit movements had longer latency and lower velocity at the periphery than in the center of the retina. However, irrespectively of the place of stimulation, the latency of the pursuit movements was longer, their velocity lower and the course less regular than in normally reared cats. It therefore follows that in visually deprived cats the ocular following reflex is impaired.     

Effects of Sustained Otolith-Only Stimulation on Post-Rotational Nystagmus

Constant velocity rotations in darkness evoke vestibulo-ocular reflex in form of pre- and post-rotational nystagmus under cerebellar supervision. Reorientation of the head with respect to gravity, stimulating otolith and semicircular canal, during post-rotational phase rapidly suppresses the post-rotational nystagmus. We asked if pure otolith stimulation without semicircular canal signal is sufficient for the suppression of post-rotational nystagmus. The experimental paradigm comprised of on-axis rotations in the horizontal plane when the subject was sitting upright, followed by a novel stimulus that combined off-axis centrifugation in the horizontal plane with amplitude matched, yet out-of-phase, on-axis horizontal rotation—double centrifugation. The resultant effect of double centrifugation was pure otolith stimulation that constantly changed direction, yet completely canceled out angular velocity (no horizontal semicircular canal stimulation). Double centrifugation without pre-existing on-axis rotations evoked mixture of horizontal and vertical eye movements, latter reflected the known uncertainty of the vestibular system to differentiate whether the sensory signal is related to low-frequency translations in horizontal plane or head tilts relative to the gravity. Double centrifugation during post-rotational phase suppressed the peak slow phase eye velocity of the post-rotational nystagmus, hence affecting the vestibular ocular reflex gain (eye velocity/head velocity) matrix. The decay time constant, however, was unchanged. Amount of suppression of the peak slow phase eye velocity of the post-rotational nystagmus during double centrifugation correlated with the peak vertical eye velocity evoked by the pure otolith stimuli in the absence of pre-existing on axis rotations. In post-rotational phase, the pure otolith signal affects vestibular ocular reflex gain matrix but does not affect the time constant.     

Video-oculography in the gerbil

Normative vestibulo-ocular and optokinetic reflexes (VOR and OKR) and pupil diameter were measured in young adult gerbils using infrared video-oculography with 60 Hz sampling during head-fixed binocular recordings. The pupillary light-sink technique was preferred over a single-beam retinal reflection method because its measurements were less affected by pupil size. Eye movements were generally conjugate with occasional independent saccadic movements, and independent drifting movements in the dark. The horizontal optokinetic response to sinusoidal motion of a randomly spaced white dot pattern was maximal at low velocities (5 degrees/s), stronger temporonasally, and dropped off quickly at approximately 20 degrees/s. Constant velocity gain was near unity through 60-80 degrees/s with a sharp drop-off. Monocular viewing revealed almost no nasotemporal optokinetic response. Pupil diameter was found to vary as a saddle function with optokinetic gain from cycle to cycle, but also have a circadian rhythm (smaller at dusk) that related inversely to mean horizontal VOR gain. Gerbils with eyes open sometimes had no optokinetic response during long stimulus periods, which then resumed after a brief vestibular stimulus. The horizontal angular VOR gain was relatively flat across 0.1-1.0 Hz and 30-120 d/s sines (phase near zero), with a mean gain of approximately 0.78 in the dark, and 1.0 with the fixed pattern surround (n=15, for both raw calibrated and normalized data). Most animals also revealed a strong slow phase eye velocity asymmetry (dominant during ipsilateral rotation) in the half-cycle gain of their horizontal angular VOR response in the dark. A constant velocity horizontal optokinetic bias velocity did not change the gain or symmetry of the sinusoidal VOR response, but shifted the VOR response velocity in an additive (linear) fashion. Both cross-coupling (pitch or roll while rotating) and pseudo-OVAR (off-axis counter-rotation) stimuli generated horizontal nystagmus. The findings suggest that the gerbil, like other lateral-eyed rodents, relies on otolith cues to interpret angular motion.     

Localization of proprioceptive reflexes in the splenius muscle of the cat

Activity of the cat splenius muscle was modulated by sinusoidal rotation of the head around the C₁-C₂ joint in decerebrate cats with labyrinth intact or with all semicircular canals plugged, or, in on intact and alert cat, by rotation of the body with the head fixed in space. EMG modulation, recorded from the areas of splenius innervated by the C₁-C₄ nerves, was due to the cervicocollic reflex. Modulation was not uniform, but decreased with progressively more caudal recording locations; with stimuli of small amplitude it was often possible to obtain modulation of the rostral part of the muscle only. The results demonstrate localization of proprioceptive reflexes, including the stretch reflex, within the splenius muscle.     

Eye movements evoked by electrical stimualtion of the brain in anesthetized fishes.

Several eye movements were evoked by electrical stimulation of the brain in anesthetized sunfish and goldfish. Conjugate lateral rolling movements, similar to eye movements observed when an unoperated fish is rotated about its long axis, were evoked from the acoustico-lateral area of the medulla and the eminentia granularis and an adjacent medial portion of the cerebellum. Bilateral and unilateral backward rotations, similar to the eye movements observed when unoperated fish are rotated forward about the interpupillary axis, were evoked from the medial longitudinal fasciculus and areas related to the oculomotor nerve. Bilateral forward rotations, comparable to the eye movements resulting when unoperated fish are rotated backward about the interpupillary axis, were elicited by stimulation near the trochlear nerve roots in the valvula of the cerebellum; unilateral responses resulted from stimulation near the exiting trochlear nerves. Convergence was elicited by stimulation in the midline near the oculomotor complex and the medial longitudinal fasciculus while unilateral vergence responses were triggered by stimulation in the medial longitudinal fasciculus and areas lateral to the oculomotor nucleus. Conjugate eye movements in the horizontal plane were frequently evoked but were not studied in detail.     

Frames of reference for eye–head gaze shifts evoked during frontal eye field stimulation

The frontal eye field (FEF), in the prefrontal cortex, participates in the transformation of visual signals into saccade motor commands and in eye–head gaze control. The FEF is thought to show eye‐fixed visual codes in head‐restrained monkeys, but it is not known how it transforms these inputs into spatial codes for head‐unrestrained gaze commands. Here, we tested if the FEF influences desired gaze commands within a simple eye‐fixed frame, like the superior colliculus (SC), or in more complex egocentric frames like the supplementary eye fields (SEFs). We electrically stimulated 95 FEF sites in two head‐unrestrained monkeys to evoke 3D eye–head gaze shifts and then mathematically rotated these trajectories into various reference frames. In theory, each stimulation site should specify a specific spatial goal when the evoked gaze shifts are plotted in the appropriate frame. We found that these motor output frames varied site by site, mainly within the eye‐to‐head frame continuum. Thus, consistent with the intermediate placement of the FEF within the high‐level circuits for gaze control, its stimulation‐evoked output showed an intermediate trend between the multiple reference frame codes observed in SEF‐evoked gaze shifts and the simpler eye‐fixed reference frame observed in SC‐evoked movements. These results suggest that, although the SC, FEF and SEF carry eye‐fixed information at the level of their unit response fields, this information is transformed differently in their output projections to the eye and head controllers.     

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° in the roll of pitch plane) 2 s after sudden stop from a constant velocity rotation (100°/s) about the earth-vertical axis in yaw. Eye movements were measured with 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.     

Tonic cervical influences on eye nystagmus following hemilabyrinthectomy: immediate and plastic effects

In intact guinea pigs a passive horizontal rotation of the body about the fixed head induces compensatory ocular movements (cervico-ocular reflex). When the static neck deviation is maintained, a significant ocular displacement is observed. In acutely hemilabyrinthectomized animals, static body deviation towards the lesion side tonically alters eyenystagmus. It affects slow phase eye velocity and quick phase amplitude and frequency causing the eye to reach a less eccentric orbital position. Apart from such immediate influences, a plastic effect on eye nystagmus abatement is induced. In the animals restrained with no body-on-head deviation, abatement of nystagmus is delayed with respect to the animals restrained with 35° body deviation towards the lesion side. Thus the head position signal is not only a contributing factor for the correction of postural deficits but also influences the time course of the ocular balancing process following unilateral vestibular damage.     

Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey

The activity of single cells in the vestibular nuclei in alert, behaving monkey was studied by extracellular recording. A majority of the neurons found in the superior and the rostral medial vestibular nuclei can be divided into two classes on the basis of their discharge relationship to eye movements evoked during head rotation, visual target pursuit, or visual suppression of the vestibulo-ocular reflex. The firing rate of the first unit type is proportional to head rotational velocity (and the resulting compensatory eye velocity) but is not modulated during slow eye movements of pure visual origin. During visual suppression of the vestibulo-ocular reflex, the relationship of this type of unit discharge to head velocity remains unchanged, although the eye velocity is now zero. The second type of unit more closely resembles oculomotor neurons in that its discharge pattern is proportional to eye position and velocity during eye movements of both visual and vestibular origin. However during suppression of the vestibuloocular reflex this type of unit continues to show a greatly reduced but consistent modulation of discharge rate proportional to head velocity. Thus the direct projection of vestibular neurons to oculomotor neurons cannot by itself account for the ability of the monkey to completely suppress its vestibulo-ocular reflex.     

Vestibular function in severe bilateral vestibulopathy

OBJECTIVES: To assess residual vestibular function in patients with severe bilateral vestibulopathy comparing low frequency sinusoidal rotation with the novel technique of random, high acceleration rotation of the whole body. METHODS: Eye movements were recorded by electro-oculography in darkness during passive, whole body sinusoidal yaw rotations at frequencies between 0.05 and 1.6 Hz in four patients who had absent caloric vestibular responses. These were compared with recordings using magnetic search coils during the first 100 ms after onset of whole body yaw rotation at peak accelerations of 2800 degrees /s(2). Off centre rotations added novel information about otolithic function. RESULTS: Sinusoidal yaw rotations at 0.05 Hz, peak velocity 240 degrees/s yielded minimal responses, with gain (eye velocity/head velocity)<0.02, but gain increased and phase decreased at frequencies between 0.2 and 1.6 Hz in a manner resembling the vestibulo-ocular reflex. By contrast, the patients had profoundly attenuated responses to both centred and eccentric high acceleration transients, representing virtually absent responses to this powerful vestibular stimulus. CONCLUSION: The analysis of the early ocular response to random, high acceleration rotation of the whole body disclosed a profound deficit of semicircular canal and otolith function in patients for whom higher frequency sinusoidal testing was only modestly abnormal. This suggests that the high frequency responses during sinusoidal rotation were of extravestibular origin. Contributions from the somatosensory or central predictor mechanisms, might account for the generation of these responses. Random, transient rotation is better suited than steady state rotation for quantifying vestibular function in vestibulopathic patients.