Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range

Gaze, the direction of the visual axis in space, is the sum of the eye position relative to the head (E) plus head position relative to space (H). In the old explanation, which we call the oculocentric motor strategy, of how a rapid orienting gaze shift is controlled, it is assumed that 1) a saccadic eye movement is programmed with an amplitude equal to the target's offset angle, 2) this eye movement is programmed without reference to whether a head movement is planned, 3) if the head turns simultaneously the saccade is reduced in size by an amount equal to the head's contribution, and 4) the saccade is attenuated by the vestibuloocular reflex (VOR) slow phase. Humans have an oculomotor range (OMR) of about +/- 55 degrees. The use of the oculocentric motor strategy to acquire targets lying beyond the OMR requires programming saccades that cannot be made physically. We have studied in normal human subjects rapid horizontal gaze shifts to visible and remembered targets situated within and beyond the OMR at offsets ranging from 30 to 160 degrees. Heads were attached to an apparatus that permitted short unexpected perturbations of the head trajectory. The acceleration and deceleration phases of the head perturbation could be timed to occur at different points in the eye movement. 4. Single-step rapid gaze shifts of all sizes up to at least 160 degrees (the limit studied) could be accomplished with the classic single-eye saccade and an accompanying saccadelike head movement. In gaze shifts less than approximately 45 degrees, when head motion was prevented totally by the brake, the eye attained the target. For larger target eccentricities the gaze shift was interrupted by the brake and the average eye saccade amplitude was approximately 45 degrees, well short of the OMR. Thus saccadic eye movement amplitude was neurally, not mechanically, limited. When the head's motion was not perturbed by the brake, the eye saccade amplitude was a function of head velocity: for a given target offset, the faster the head the smaller the saccade. For gaze shifts to targets beyond the OMR and when head velocity was low, the eye frequently attained the 45 degrees position limit and remained there, immobile, until gaze attained the target.(ABSTRACT TRUNCATED AT 400 WORDS)     

Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades

1. The behavior of the combined eye-head gaze saccade mechanism was investigated in the rhesus monkey under both normal circumstances and in the presence of perturbations delivered to the head by a torque motor. Animals were trained to follow a target light that stepped at regular intervals through an angle of 68 degrees (+/- 34 degrees with respect to the midsagittal plane). Thus all primary saccades were center crossing. On randomly occurring trials the torque motor was pulsed so as to perturb the trajectory of the head, thus allowing us to assess both the functional state of the vestibuloocular reflex (VOR) and the effects of such perturbations on gaze saccade accuracy (gaze is defined as the sum of eye-in-head plus head-in-space, and a gaze saccade as a combined eye-head saccadic gaze shift). 2. Gaze shifts can be divided into two discrete sections: the portion during which the gaze angle is changing (the saccadic portion), and the portion during which the gaze is stationary but the head continues to move (the terminal head-movement portion). For the system to accurately acquire eccentric targets, at least two criteria must be met: 1) the saccadic portion must be accurate, and 2) the compensatory eye movement that occurs during the terminal head-movement portion must be equal and opposite to the head movement, thereby maintaining gaze stability. Perturbations delivered during the terminal head-movement portion of the gaze shift indicated that VOR was functioning normally, and thus we concluded that the compensatory eye movements that accompany head movements were vestibular in origin. 3. As reported previously, during the saccadic portion of large-amplitude gaze saccades, the VOR ceases to function. In spite of this observation, the accuracy of the gaze saccade is not affected by perturbations delivered to the head. Gaze accuracy is maintained both by changing the duration of the saccadic portion and by altering the head trajectory. 4. Because rhesus monkeys often make very rapid head movements (1,200 degrees/s), we wished to discover the velocity range over which the monkey VOR might be expected to operate. Accordingly, in a second series of experiments, VOR function was assessed during passive whole-body rotations with the head fixed. By the use of spring-assisted manual rotations, peak velocities up to 850 degrees/s were achieved. When VOR gain was measured during such rotations, it was found to be equal to 0.9 up to the maximum velocities used.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans

1. In natural conditions, gaze (i.e., eye + head) orientation is a complex behavior involving simultaneously the eye and head motor systems. Thus one of the key problems of gaze control is whether or not the vestibuloocular reflex (VOR) elicited by head rotation and saccadic eye movement linearly add. 2. Kinematics of human gaze saccades within the oculomotor range (OMR) were quantified under different conditions of head motion. Saccades were visually triggered while the head was fixed or passively moving at a constant velocity (200 deg/s) either in the same direction as, or opposite to, the saccade. Active eye-head coordination was also studied in a session in which subjects were trained to actively rotate their head at a nearly constant velocity during the saccade and, in another session, during natural gaze responses. 3. When the head was passively rotated toward the visual target, both maximum and mean gaze velocities increased with respect to control responses with the head fixed; these effects increased with gaze saccade amplitude. In addition, saccade duration was reduced so that corresponding gaze accuracy, although poorer than for control responses, was not dramatically affected by head motion. 4. The same effects on gaze velocity were present during active head motion when a constant head velocity was maintained throughout saccade duration, and gaze saccades were as accurate as with the head fixed. 5. During natural gaze responses, an increased gaze velocity and a decreased saccade duration with respect to control responses became significant only for gaze displacement larger than 30 degrees, due to the negligible contribution of head motion for smaller responses. 6. When the head was passively rotated in the opposite direction to target step, gaze saccades were slower than those obtained with the head fixed; but their average accuracy was still maintained. 7. These results confirm a VOR inhibition during saccadic eye movements within the OMR. This inhibition, present in all 16 subjects studied, ranged from 40 to 96% (for a 40 degree target step) between subjects and increased almost linearly with target step amplitude. Furthermore, the systematic difference between instantaneous VOR gain estimated at the time of maximum gaze velocity and mean VOR gain estimated over the whole saccadic duration indicates a decay of VOR inhibition during the ongoing saccade. 8. A simplified model is proposed with a varying VOR inhibition during the saccade. It suggests that VOR inhibition is not directly controlled by the saccadic pulse generator.(ABSTRACT TRUNCATED AT 400 WORDS)     

Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex

The mechanisms of eye-head coordination were studied in two alert juvenile rhesus monkeys. Animals were trained to follow a target light to obtain a water reward and the combined eye-head gaze shifts in response to target steps with a variably sized horizontal components were studied. During a certain random portion of the gaze shifts, a torque motor was used to perturb the head to investigate the operational state of the vestibuloocular reflex (VOR) during the saccadic gaze shift. The effects of perturbing the head were assessed during five different conditions: horizontal target steps ranging from 10 to 80 degrees in amplitude; oblique target steps where the vertical component was larger than the horizontal component; purely vertical target steps 10-40 degrees in amplitude; both horizontal and oblique target steps delivered while the animals' saccades had been slowed by the use of diazepam; and large spontaneous gaze shifts in response to both sounds and visual stimuli. Comparison of perturbed and unperturbed large-amplitude (greater than 40 degrees) gaze shifts indicate that the VOR is turned off for most of the duration of the movement. Nonetheless, there is an apparent interaction between the saccadic eye movement and the head movement, thus, as the head velocity increases, the eye velocity decreases so that gaze velocity remains nearly constant throughout the gaze shift. Since the VOR is turned off when this interaction occurs, it must represent an interaction between the actual eye and head movement motor programs themselves. Although the results were not quite as clear for small saccades (less than 20 degrees), experiments on animals whose saccades had been slowed either by the use of diazepam or by combining a small horizontal component with a large vertical component indicate that the VOR is left on during these smaller gaze shifts. During quite small gaze shifts (less than 10 degrees), the VOR is clearly functioning; however, as the size of the gaze shift is increased, this becomes less clear, and there appears to be a region where the VOR operates with a gain substantially less than normal before it enters the large gaze shift region where the VOR is turned off entirely.(ABSTRACT TRUNCATED AT 400 WORDS)     

Head-unrestrained gaze shifts after muscimol injection in the caudal fastigial nucleus of the monkey

The effects of unilateral cFN inactivation on horizontal and vertical gaze shifts generated from a central target toward peripheral ones were tested in two head unrestrained monkeys. After muscimol injection, the eye component was hypermetric during ipsilesional gaze shifts, hypometric during contralesional ones and deviated toward the injected side during vertical gaze shifts. The ipsilesional gaze hypermetria increased with target eccentricity until approximately 24 degrees after which it diminished and became smaller than the hypermetria of the eye component. Contrary to eye saccades, the amplitude and peak velocity of which were enhanced, the amplitude and peak velocity of head movements were reduced during ipsilesional gaze shifts. These changes in head movement were not correlated with those affecting the eye saccades. Head movements were also delayed relative to the onset of eye saccades. The alterations in head movement and the faster eye saccades likely explained the reduced head contribution to the amplitude of ipsilesional gaze shifts. The contralesional gaze hypometria increased with target eccentricity and was associated with uncorrelated reductions in eye and head peak velocities. When compared with control movements of similar amplitude, contralesional eye saccades had lower peak velocity and longer duration. This slowing likely accounted for the increase in head contribution to the amplitude of contralesional gaze shifts. These data suggest different pathways for the fastigial control of eye and head components during gaze shifts. Saccade dysmetria was not compensated by appropriate changes in head contribution, raising the issue of the feedback control of movement accuracy during combined eye-head gaze shifts.     

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization.

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. To study the contribution of the vestibular system to the coordinated eye and head movements of a gaze shift, we plugged the lumens of just the horizontal (n = 2) or all six semicircular canals (n = 1) in monkeys trained to make horizontal head-unrestrained gaze shifts to visual targets. After the initial eye saccade of a gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) near one has been attributed to the vestibuloocular reflex (VOR). One day after horizontal canal plugging, the gain of the passive horizontal VOR at frequencies between 0.1 and 1.0 Hz was <0.10 in the horizontal-canal-plugged animals and zero in the all-canal-plugged animal. One day after surgery, counterrotation gain was approximately 0.3 in the animals with horizontal canals plugged and absent in the animal with all canals plugged. As the time after plugging increased, so too did counterrotation gain. In all three animals, counterrotation gain recovered to between 0.56 and 0.75 within 80-100 days. The initial loss of compensatory counterrotation after plugging resulted in a gaze shift that ended long after the eye saccade and just before the end of the head movement. With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of the duration of reduced gain counterrotation occurred both because head movements ended sooner and counterrotation gain returned to 1.0 more rapidly relative to the end of the eye saccade. Eye counterrotation was not due to activation of pursuit eye movements as it persisted when gaze shifts were executed to extinguished targets. Also counterrotation was not due simply to activation of neck receptors because counterrotation persisted after head movements were arrested in midflight. We suggest that the neural signal that is used to cause counterrotation in the absence of vestibular input is an internal copy of the intended head movement.     

Combined eye-head gaze shifts in the primate. I. Metrics

Gaze (eye-in-space) velocity-duration and velocity-amplitude curves were prepared for head-fixed and head-free gaze shifts in the rhesus monkey with an emphasis on large amplitudes. These plots revealed the presence of two distinct gaze reorientation mechanisms, one used when the gaze shift was small (less than 20 degrees) and the other utilized for large coordinated gaze shifts when the head was free. When head-free and head-fixed saccadic gaze shifts were compared in the same animal, no differences in the metrics were found for amplitudes less than 20 degrees. However, for large gaze shifts where contribution of the head to the change in gaze angle was considerable, head-free saccades were found to exhibit lower peak gaze velocities and greater durations than those recorded with the head-fixed paradigm. In order to differentiate between the eye saccades and combined saccadic eye-head gaze shifts, the latter have been termed gaze saccades. Change in head position and change in eye position were both measured during the actual gaze shift and were plotted against the gaze-shift amplitude to determine whether the head movement contributed significantly to the change in gaze angle. The results indicate that below 20 degrees the gaze shift is accomplished almost exclusively with the eyes and the head moves very little; however, for larger saccades, the head contributes approximately 80% of the total change in gaze angle with the eyes contributing only approximately 20%. Large saccadic eye-head gaze shifts do not exhibit 'bell-shaped' velocity profiles as do smaller head-fixed saccades; instead, gaze accelerates to reach a peak velocity after approximately 30-40 ms. This velocity is then maintained for the duration of the gaze shift. Close scrutiny of the fine structure of the velocity profiles of the eye, head, and gaze channels indicates that during gaze saccades, the eye and head movement motor programs interact to maintain gaze velocity nearly constant, unaffected by changes in head velocity. Previous authors had stated that when velocity-duration plots are obtained for oblique saccades of constant amplitude, the resulting points could be fitted with a hyperbolic function. These results were confirmed for head-free gaze saccades and extended to larger amplitudes. When an oblique saccade is made, the smaller component is stretched in duration to match the duration of the larger component. However, as the gaze shift becomes large (greater than 40 degrees), the relationship becomes more complex.(ABSTRACT TRUNCATED AT 400 WORDS)     

Head unrestrained horizontal gaze shifts after unilateral labyrinthectomy in the rhesus monkey

Following the orienting saccade of a combined eye-head gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) of near unity, is a manifestation of the vestibulo-ocular reflex (VOR). Acute unilateral labyrinthectomy (UL) causes severe asymmetry in the VOR during passive head rotations that recovers incompletely over time. The purpose of this investigation was to compare the recovery of the counterrotation gain during horizontal gaze shifts with that of the passive VOR after UL. During the 1st week after UL, counterrotation gains were asymmetric, being lower for head movements towards the lesion but nearly normal for head movements towards the intact side. Whereas this asymmetry in the counterrotation gain resolved within a week after UL, asymmetries in the passive VOR persisted. During the 1st week after UL, behavioral performance was generally poor, with a high incidence of inaccurate gaze shifts and larger latencies. In addition, animals used slower head movements such that peak head amplitude during the eye saccade was significantly lower during the 1st week after UL as compared to control values. Bilateral labyrinthectomy (BL) resulted in larger but symmetric deficits in counterrotation, which, contrary to the passive VOR, exhibited significant recovery over time. It is hypothesized that recovery of counterrotation gain after UL has contributions from multiple sources, including the contralateral intact labyrinth and an efference copy of the head movement. Electronic Publication     

Coordination of the eyes and head: movement kinematics

When the head is restrained, saccades are characterized by lawful relationships between movement amplitude, peak velocity, and duration. In addition, the spatiotemporal progression of saccades (i.e., movement kinematics) is predictable if saccade amplitude and direction are known. However, when the head is free to move, changes in the direction of the line of sight (gaze shifts) often involve saccades associated with simultaneous head movements. The metrics (duration, amplitude, peak velocity) and kinematics of saccades occurring in conjunction with head movements cannot be predicted on the basis of saccade amplitude and direction alone. For example, when the head is unrestrained, velocity profiles of 35 degree eye movements can be symmetrical and might have peaks approximately 600 degrees/s. But, 35 degrees eye movements can also have peak velocities of approximately 300 degrees/s and have velocity profiles with two pronounced peaks: an initial peak followed by a reduction and subsequent increase in velocity. Saccade amplitude and direction are insufficient to predict the shape of the velocity profile. However, as illustrated in this report, if the amplitude of the concurrent head movement is taken into account, saccade kinematics are predictable even during gaze shifts with large head components. The data presented here are indicative of an interaction between eye and head motor systems in which head movement commands alter the execution of concurrent saccades.     

Action of the brain stem saccade generator during horizontal gaze shifts. I. Discharge patterns of omnidirectional pause neurons

Omnidirectional pause neurons (OPNs) pause for the duration of a saccade in all directions because they are part of the neural mechanism that controls saccade duration. In the natural situation, however, large saccades are accompanied by head movements to produce rapid gaze shifts. To determine whether OPNs are part of the mechanism that controls the whole gaze shift rather than the eye saccade alone, we monitored the activity of 44 OPNs that paused for rightward and leftward gaze shifts but otherwise discharged at relatively constant average rates. Pause duration was well correlated with the duration of either eye or gaze movement but poorly correlated with the duration of head movement. The time of pause onset was aligned tightly with the onset of either eye or gaze movement but only loosely aligned with the onset of head movement. These data suggest that the OPN pause does not encode the duration of head movement. Further, the end of the OPN pause was often better aligned with the end of the eye movement than with the end of the gaze movement for individual gaze shifts. For most gaze shifts, the eye component ended with an immediate counterrotation owing to the vestibuloocular reflex (VOR), and gaze ended at variable times thereafter. In those gaze shifts where eye counterrotation was delayed, the end of the pause also was delayed. Taken together, these data suggest that the end of the pause influences the onset of eye counterrotation, not the end of the gaze shift. We suggest that OPN neurons act to control only that portion of the gaze movement that is commanded by the eye burst generator. This command is expressed by driving the saccadic eye movement directly and also by suppressing VOR eye counterrotation. Because gaze end is less well correlated with pause end and often occurs well after counterrotation onset, we conclude that elements of the burst generator typically are not active till gaze end, and that gaze end is determined by another mechanism independent of the OPNs.     

Firing behaviour of squirrel monkey eye movement-related vestibular nucleus neurons during gaze saccades

The firing behaviour of vestibular nucleus neurons putatively involved in producing the vestibulo-ocular reflex (VOR) was studied during active and passive head movements in squirrel monkeys. Single unit recordings were obtained from 14 position-vestibular (PV) neurons, 30 position-vestibular-pause (PVP) neurons and 9 eye-head-vestibular (EHV) neurons. Neurons were sub-classified as type I or II based on whether they were excited or inhibited during ipsilateral head rotation. Different classes of cell exhibited distinctive responses during active head movements produced during and after gaze saccades. Type I PV cells were nearly as sensitive to active head movements as they were to passive head movements during saccades. Type II PV neurons were insensitive to active head movements both during and after gaze saccades. PVP and EHV neurons were insensitive to active head movements during saccadic gaze shifts, and exhibited asymmetric sensitivity to active head movements following the gaze shift. PVP neurons were less sensitive to ondirection head movements during the VOR after gaze saccades, while EHV neurons exhibited an enhanced sensitivity to head movements in their on direction. Vestibular signals related to the passive head movement were faithfully encoded by vestibular nucleus neurons. We conclude that central VOR pathway neurons are differentially sensitive to active and passive head movements both during and after gaze saccades due primarily to an input related to head movement motor commands. The convergence of motor and sensory reafferent inputs on VOR pathways provides a mechanism for separate control of eye and head movements during and after saccadic gaze shifts.     

3-Dimensional eye-head coordination in gaze shifts evoked during stimulation of the lateral intraparietal cortex

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 μA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46° for M1 and 8.25° for M2, with average head components of only 0.36 and 0.62° respectively. The head's amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders' law and Listing's law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listing's plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listing's plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listing's plane, but in the absence of subsequent head movement the stimulation-induced torsion was “left hanging”. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.     

Saccade dysmetria in head-unrestrained gaze shifts after muscimol inactivation of the caudal fastigial nucleus in the monkey

Lesions in the caudal fastigial nucleus (cFN) severely impair the accuracy of visually guided saccades in the head-restrained monkey. Is the saccade dysmetria a central perturbation in issuing commands for orienting gaze (eye in space) or is it a more peripheral impairment in generating oculomotor commands? This question was investigated in two head-unrestrained monkeys by analyzing the effect of inactivating one cFN on horizontal gaze shifts generated from a straight ahead fixation light-emitting diode (LED) toward a 40 degrees eccentric target LED. After muscimol injections, when viewing the fixation LED, the starting position of the head was changed (ipsilesional and upward deviations). Ipsilesional gaze shifts were associated with a 24% increase in the eye saccade amplitude and a 58% reduction in the amplitude of the head contribution. Contralesional gaze shifts were associated with a decrease in the amplitude of both eye and head components (40 and 37% reduction, respectively). No correlation between the changes in the eye amplitude and in head contribution was observed. The amplitude of the complete head movement was decreased for ipsilesional movements (57% reduction) and unaffected for contralesional movements. For both ipsilesional and contralesional gaze shifts, the changes in eye saccade amplitude were strongly correlated with the changes in gaze amplitude and largely accounted for the gaze dysmetria. These results indicate a major role of cFN in the generation of appropriate saccadic oculomotor commands during head-unrestrained gaze shifts.     

Enhancement of the vestibulo-ocular reflex by prior eye movements.

We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by approximately 20% of head velocity; gaze velocity subsequently declined to zero within approximately 300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0. 8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects (P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this "priming" effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.     

Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture

Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eye-head gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were > or =40 degrees in amplitude. Furthermore, as gaze shift amplitude increased (40-120 degrees ), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of approximately 250-300 degrees /s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at approximately 35 and 60 degrees , respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.     

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

Constant frequency microstimulation of the paramedian pontine reticular formation (PPRF) in head-restrained monkeys evokes a constant velocity eye movement. Since the PPRF receives significant projections from structures that control coordinated eye-head movements, we asked whether stimulation of the pontine reticular formation in the head-unrestrained animal generates a combined eye-head movement or only an eye movement. Microstimulation of most sites yielded a constant-velocity gaze shift executed as a coordinated eye-head movement, although eye-only movements were evoked from some sites. The eye and head contributions to the stimulation-evoked movements varied across stimulation sites and were drastically different from the lawful relationship observed for visually-guided gaze shifts. These results indicate that the microstimulation activated elements that issued movement commands to the extraocular and, for most sites, neck motoneurons. In addition, the stimulation-evoked changes in gaze were similar in the head-restrained and head-unrestrained conditions despite the assortment of eye and head contributions, suggesting that the vestibulo-ocular reflex (VOR) gain must be near unity during the coordinated eye-head movements evoked by stimulation of the PPRF. These findings contrast the attenuation of VOR gain associated with visually-guided gaze shifts and suggest that the vestibulo-ocular pathway processes volitional and PPRF stimulation-evoked gaze shifts differently.     

Head–eye interactions during vertical gaze shifts made by rhesus monkeys

Changing the direction of the line of sight (gaze) can involve coordinated movements of the eyes and head. During gaze shifts directed along the horizontal meridian, the contribution of the eyes and head depends upon the position of the eyes in the orbits; the contribution of the head to accomplishing the overall shift in gaze declines as the eyes increasingly are deviated away from the direction of the ensuing gaze shift. Also during horizontal gaze shifts, changes in the metrics and kinematics of the saccadic (eye movement) portion of coordinated movements, are correlated with the amplitude and velocity of the concurrent head movement. With increasing head contributions, saccade peak velocities decline, durations increase and velocity profiles develop two peaks. It remains unknown whether the interaction between head and eyes observed during horizontal gaze shifts also occurs during vertical gaze shifts. Yet, a full understanding of the neural control of eye–head coordination will depend upon the correlation of neural activity and features of vertical as well as horizontal movements. This report describes the metrics and kinematics of vertical gaze shifts made by head-unrestrained rhesus monkeys. Key observations include: (1) during vertical gaze shifts of a particular amplitude, relative eye and head contributions depend upon the initial vertical positions of the eyes in the orbits; (2) as head contribution increases, peak eye velocities decline, durations increase and vertical velocity profiles develop two peaks; (3) head movement metrics and kinematics are accurately predictable given knowledge only of head movement amplitude. In these ways, vertical gaze shifts were found to be qualitatively similar to horizontal gaze shifts. It seems probable that similar mechanisms mediate head–eye interactions during both horizontal and vertical movements. These observations are consistent with the hypothesis that a signal proportional to vertical head velocity reduces the gain of the vertical saccade burst generator.     

Eye position and target amplitude effects on human visual saccadic latencies

Gaze shifts vary in the extent of eye and head contribution; a large amplitude and/or an eccentric ocular orbital starting position alter the participation of head movement in the shift. The interval between eye onset and head onset determines compensatory counterrolling before and after the shift and the extent of vestibular ocular reflex reduction during the shift. The latency of eye saccades in the head-fixed condition was measured with respect to target amplitude and orbital position in order to establish base-line operations of these two variables as they apply to the headfree condition. Eye movements were measured during single-step saccades in nine young adult humans. The target step, hereafter called a jump, started from three possible fixation lights; e.g., rightward saccades started from the midline (0°) or from -20 or -40° left of the midline, with a maximum amplitude of 80°. The latency of saccades starting from the primary position increased with jump amplitude (amplitude-latency relation). When the eye started eccentrically, the latency was decreased (orbital position-latency relation), with the largest jump amplitudes most affected. These changes can be related to active eye-head coordination. Thus, with a leftward maximal orbital eccentricity, compensatory eye rotation would be impossible with a rightward head movement; however, incorporating the orbital position-latency relation, the forward ocular saccade is expedited by 90 ms. Conversely, with a primary starting position, the ocular component of an 80° gaze saccade could be slowed 125 ms by incorporating the amplitude-latency relation, thus facilitating a head contribution to the gaze shift. The orbital position and amplitude-latency relations were prominent in those subjects with habitually large head contributions to the gaze shift and minimal in individuals with typically small head contributions.     

Eye-head coordination and the variation of eye-movement accuracy with orbital eccentricity

Different humans vary widely in the tendency to move the head during saccadic shifts in gaze. The reasons for this variation are unknown. Because combined eye-head movements are associated with a recentering of the eyes in the orbits, humans who are "head movers" tend to maintain the eyes within a narrower range than do non-head movers. We explored the possibility that variations in the ability to control eye movements at eccentric positions lead to variations in customary ocular motor range and, by extension, explain the variations in head-movement tendencies. We studied ten normal adults. In each, we measured the full-scale ocular motor range and customary ocular motor range (the eccentricity range within which the eye was found at the conclusion of eye- or eye-head saccades). We also determined the eye-only range, the orbital range within which the probability of a head movement accompanying a gaze shift was low. Customary, eye-only, and full-scale ranges spanned (mean +/-SD) 41.1+/-16.9 degrees, 30.2+/-18.8 degrees, and 92.8+/- 9.1 degrees, respectively. We then assessed variations in kinematics of several ocular motor behaviors as functions of eye eccentricity. The stable fixation range, defined by the range over which drift velocities were below 1 degree/s, spanned 81.1+/-11.2 degrees in the light and 69.5+/-21.5 degrees in the dark. The range over which the gains of the vestibulo-ocular reflex in the light and smooth pursuit approached their values at zero eccentricity spanned 66.3+/-7.1 degrees and 69.0+/-10.0 degrees, respectively. Small centrifugal saccades (5-10 degrees) tended to become either slowed or hypometric with increasing eccentricity. Sensitive to both slowing and hypometria, the ratio of peak gaze velocity to target shift amplitude was flat over a range spanning 65.7+/-14.9 degrees. Finally, the ranges over which the initial saccade placed the fovea upon the target averaged 35.5+/-10.7 degrees for eye-only saccades and 36.6+/-15.0 degrees for eye-head saccades. With the exception of the range of stable fixation in the light, the kinematic ranges were either unrelated or inconsistently related to full-scale range, indicating that the deterioration of eye movements with increasing ocular eccentricity is not a simple consequence of the eyes encountering the limits of their excursion. None of the kinematic ranges correlated positively with customary or eye-only range. Thus, while head movements may be orchestrated so as to maintain the eyes within a desired range, that range (and thus head movement tendencies) is not predicated upon the range of ocular eccentricity over which eye movements are accurately controlled.     

Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation

A series of studies were carried out to investigate the role of the cerebellar flocculus and ventral paraflocculus in the ability to voluntarily cancel the vestibuloocular reflex (VOR). Squirrel monkeys were trained to pursue moving visual targets and to fixate a head stationary or earth stationary target during passive whole body rotation (WBR). The firing behavior of 187 horizontal eye movement-related Purkinje (Pk) cells in the flocculus region was recorded during smooth pursuit eye movements and during WBR. Half of the Pk cells encountered were eye velocity Pk cells whose firing rates were related to eye movements during smooth pursuit and WBR. Their sensitivity to eye velocity during WBR was reduced when a visual target was not present, and their response to unpredictable steps in WBR was delayed by 80-100 ms, which suggests that eye movement sensitivity depended on visual feedback. They were insensitive to WBR when the VOR was canceled. The other half of the Purkinje cells encountered were sensitive to eye velocity during pursuit and to head velocity during VOR cancellation. They resembled the gaze velocity Pk cells previously described in rhesus monkeys. The head velocity signal tended to be less than half as large as the eye velocity-related signal and was observable at a short ( approximately 40 ms) latency when the head was unpredictably accelerated during ongoing VOR cancellation. Gaze and eye velocity type Pk cells were found to be intermixed throughout the ventral paraflocculus and flocculus. Most gaze velocity Pk cells (76%) were sensitive to ipsilateral eye and head velocity, but nearly half (48%) of the eye velocity Pk cells were sensitive to contralateral eye velocity. Thus the output of flocculus region is modified in two ways during cancellation of the VOR. Signals related to both ipsilateral and contralateral eye velocity are removed, and in approximately half of the cells a relatively weak head velocity signal is added. Unilateral injections of muscimol into the flocculus region had little effect on the gain of the VOR evoked either in the presence or absence of visual targets. However, ocular pursuit velocity and the ability to suppress the VOR by fixating a head stationary target were reduced by approximately 50%. These observations suggest that the flocculus region is an essential part of the neural substrate for both visual feedback-dependent and nonvisual mechanisms for canceling the VOR during passive head movements.