Interaction of the body, head, and eyes during walking and turning

Body, head, and eye movements were measured in five subjects during straight walking and while turning corners. The purpose was to determine how well the head and eyes followed the linear trajectory of the body in space and whether head orientation followed changes in the gravito-inertial acceleration vector (GIA). Head and body movements were measured with a video-based motion analysis system and horizontal, vertical, and torsional eye movements with video-oculography. During straight walking, there was lateral body motion at the stride frequency, which was at half the frequency of stepping. The GIA oscillated about the direction of heading, according to the acceleration and deceleration associated with heel strike and toe flexion, and the body yawed in concert with stepping. Despite the linear and rotatory motions of the head and body, the head pointed along the forward motion of the body during straight walking. The head pitch/roll component appeared to compensate for vertical and horizontal acceleration of the head rather than orienting to the tilt of the GIA or anticipating it. When turning corners, subjects walked on a 50-cm radius over two steps or on a 200-cm radius in five to seven steps. Maximum centripetal accelerations in sharp turns were ca.0.4 g, which tilted the GIA ca.21 degrees with regard to the heading. This was anticipated by a roll tilt of the head of up to 8 degrees. The eyes rolled 1-1.5 degrees and moved down into the direction of linear acceleration during the tilts of the GIA. Yaw head deviations moved smoothly through the turn, anticipating the shift in lateral body trajectory by as much as 25 degrees. The trunk did not anticipate the change in trajectory. Thus, in contrast to straight walking, the tilt axes of the head and the GIA tended to align during turns. Gaze was stable in space during the slow phases and jumped forward in saccades along the trajectory, leading it by larger angles when the angular velocity of turning was greater. The anticipatory roll head movements during turning are likely to be utilized to overcome inertial forces that would destabilize balance during turning. The data show that compensatory eye, head, and body movements stabilize gaze during straight walking, while orienting mechanisms direct the eyes, head, and body to tilts of the GIA in space during turning.     

Human updating of visual motion direction during head rotations

Previous studies have demonstrated that human subjects update the location of visual targets for saccades after head and body movements and in the absence of visual feedback. This phenomenon is known as spatial updating. Here we investigated whether a similar mechanism exists for the perception of motion direction. We recorded eye positions in three dimensions and behavioral responses in seven subjects during a motion task in two different conditions: when the subject's head remained stationary and when subjects rotated their heads around an anteroposterior axis (head tilt). We demonstrated that after head-tilt subjects updated the direction of saccades made in the perceived stimulus direction (direction of motion updating), the amount of updating varied across subjects and stimulus directions, the amount of motion direction updating was highly correlated with the amount of spatial updating during a memory-guided saccade task, subjects updated the stimulus direction during a two-alternative forced-choice direction discrimination task in the absence of saccadic eye movements (perceptual updating), perceptual updating was more accurate than motion direction updating involving saccades, and subjects updated motion direction similarly during active and passive head rotation. These results demonstrate the existence of an updating mechanism for the perception of motion direction in the human brain that operates during active and passive head rotations and that resembles the one of spatial updating. Such a mechanism operates during different tasks involving different motor and perceptual skills (saccade and motion direction discrimination) with different degrees of accuracy.     

Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region

Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.     

Spatial orientation and balance control changes induced by altered gravitoinertial force vectors

To better understand the mechanisms of human adaptation to rotating environments, we exposed 19 healthy subjects and 8 vestibular-deficient subjects ("abnormal"; four bilateral and four unilateral lesions) to an interaural centripetal acceleration of 1g (resultant 45° roll-tilt of 1.4g) on a 0.8-m-radius centrifuge for periods of 90 min. The subjects sat upright (body z-axis parallel to centrifuge rotation axis) in the dark with head stationary, except during 4 min of every 10 min, when they performed head saccades toward visual targets switched on at 3- to 5-s intervals at random locations (within ±30°) in the earth-horizontal plane. Eight of the normal subjects also performed the head saccade protocol in a stationary chair adjusted to a static roll-tilt angle of 45° for 90 min (reproducing the change in orientation but not the magnitude of the gravitoinertial force on the centrifuge). Eye movements, including voluntary saccades directed along perceived earth- and head-referenced planes, were recorded before, during, and immediately after centrifugation. Postural center of pressure (COP) and multisegment body kinematics were also gathered before and within 10 min after centrifugation. Normal subjects overestimated roll-tilt during centrifugation and revealed errors in perception of head-vertical provided by directed saccades. Errors in this perceptual response tended to increase with time and became significant after approximately 30 min. Motion-sickness symptoms caused approximately 25% of normal subjects to limit their head movements during centrifugation and led three normal subjects to stop the test early. Immediately after centrifugation, subjects reported feeling tilted 10° in the opposite direction, which was in agreement with the direction of their earth-referenced directed saccades. Postural COP, segmental body motion amplitude, and hip-sway frequency increased significantly after centrifugation. These postural effects were short-lived, however, with a recovery time of several postural test trials (minutes). There were also asymmetries in the direction of postcentrifugation COP and head tilt which depended on the subject's orientation during the centrifugation adaptation period (left ear or right ear out). The amount of total head movements during centrifugation correlated poorly or inversely with postcentrifugation postural stability, and the most unstable subject made no head movements. There was no decrease in postural stability after static tilt, although these subjects also reported a perceived tilt briefly after return to upright, and they also had COP asymmetries. Abnormal subjects underestimated roll-tilt during centrifugation, and their directed saccades revealed permanent spatial distortions. Bilateral abnormal subjects started out with poor postural control, but showed no postural decrements after centrifugation, while unilateral abnormal subjects had varying degrees of postural decrement, both in their everyday function and as a result of experiencing the centrifugation. In addition, three unilateral, abnormal subjects, who rode twice in opposite orientations, revealed a consistent orthogonal pattern of COP offsets after centrifugation. These results suggest that both orientation and magnitude of the gravitoinertial vector are used by the central nervous system for calibration of multiple orientation systems. A change in the background gravitoinertial force (otolith input) can rapidly initiate postural and perceptual adaptation in several sensorimotor systems, independent of a structured visual surround. Electronic Publication     

Gaze anticipation during human locomotion

During locomotion, a top-down organization has been previously demonstrated with the head as a stabilized platform and gaze anticipating the horizontal direction of the trajectory. However, the quantitative assessment of the anticipatory sequence from gaze to trajectory and body segments has not been documented. The present paper provides a detailed investigation into the spatial and temporal anticipatory relationships among the direction of gaze and body segments during locomotion. Participants had to walk along several mentally simulated complex trajectories, without any visual cues indicating the trajectory to follow. The trajectory shapes were presented to the participants on a sheet of paper. Our study includes an analysis of the relationships between horizontal gaze anticipatory behavior direction and the upcoming changes in the trajectory. Our findings confirm the following: 1) The hierarchical ordered organization of gaze and body segment orientations during complex trajectories and free locomotion. Gaze direction anticipates the head orientation, and head orientation anticipates reorientation of the other body segments. 2) The influence of the curvature of the trajectory and constraints of the tasks on the temporal and spatial relationships between gaze and the body segments: Increased curvature resulted in increased time and spatial anticipation. 3) A different sequence of gaze movements at inflection points where gaze plans a much later segment of the trajectory.     

Eye-position dependence of three-dimensional ocular rotation-axis orientation during head impulses in humans

 If horizontal saccades or smooth-pursuit eye movements are made with the line-of-sight at different elevations, the three-dimensional (3D) angular rotation axis of the globe tilts by half the vertical eye eccentricity. This phenomenon is named ”half-angle rule” and is a consequence of Listing’s law. It was recently found that the ocular rotation axis during the horizontal vestibulo-ocular reflex (VOR) on a turntable also tilts in the direction of the line-of-sight by about a quarter of the eye’s vertical eccentricity. This is surprising, since, in a ”perfect” VOR, the angular rotation axis of the eye should be independent from the position of the eye to fully compensate for the 3D angular head rotation. We asked whether this quarter-angle strategy is a general property of the VOR or whether the 3D kinematics of ocular movements evoked by vestibular stimulation would be less eye-position dependent at higher stimulus frequencies. Nine healthy subjects were exposed to horizontal head impulses (peak velocity ∼250°/s). The line-of-sight was systematically changed along the vertical meridian of a tangent screen. Three-dimensional eye and head movements were monitored with dual search coils. The 3D orientation of the angular eye-in-head rotation axis was determined by calculating the average angular velocity vectors of the initial 10° displacements. Then, the difference between the tilt angles of the ocular rotation axis during upward and downward viewing was determined and divided by the difference of vertical eccentricity (”tilt angle coefficient”). Control experiments included horizontal saccades, smooth-pursuit eye movements, and eye movements evoked by slow, passive head rotations at the same vertical eye eccentricities. On average, the ocular rotation axis during horizontal head-impulse testing at different elevations of the line-of-sight was closely aligned with the rotation axis of the head (tilt angle coefficient of pooled abducting and adducting eye movements: 0.11±0.17 SD). Values for slow head impulses, however, exceeded somewhat the quarter angle (0.33±0.12), while smooth-pursuit movements (0.50±0.09) and saccades (0.44±0.11) were closest to the half angle. These results demonstrate that the 3D orientation of the ocular rotation axis during rapid head thrusts is relatively independent of the direction of the line-of-sight and that ocular rotations elicited by head impulses are kinematically different from saccades, despite similar movement dynamics. Received: 17 July 1998 / Accepted: 17 May 1999     

Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15 degrees, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15-90 degrees, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7-0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABA(B) agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by approximately 90 degrees, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3 degrees /g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0 degrees /g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ~180 degrees relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.     

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.     

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.     

Stimulation of the caudate nucleus induces contraversive saccadic eye movements as well as head turning in the cat.

The effects of stimulation of the caudate nucleus were investigated in alert cats, with special reference to the induction of eye and head movements. Stimulation of caudal portions of the caudate nucleus on one side with trains of current pulses induced gaze shifts towards the contralateral side. When the head of the animal was restrained, the majority of evoked eye movements were single conjugate saccades. The amplitude and direction of the evoked saccade varied depending on the initial eye position. The amplitude of the horizontal component tended to be larger for saccades initiated from more ipsilateral positions, and became gradually smaller as the initial eye position shifted to the contralateral side. If the eye was far into the contralateral positions, no saccades were induced. Furthermore, the saccades tended to have a downward component when the eye was initially focused upward, and an upward component when the eye was focused downward. When the head was made free to move, the same stimulation induced a sequence of contraversive staircase gaze shifts composed of coordinated eye and head movements. The eye movements in the orbit resembled nystagmus, consisting of contraversive saccades followed by reverse compensatory movements. The head turning, though smooth and continuous, was also suggested to consist of a series of movements coupled with saccadic eye movements. This study indicates a potential role of the caudate nucleus in the control of orienting reflexes.     

Coupling between horizontal and vertical components of saccadic eye movements during constant amplitude and direction gaze shifts in the rhesus monkey

When the head is free to move, changes in the direction of the line of sight (gaze shifts) can be accomplished using coordinated movements of the eyes and head. During repeated gaze shifts between the same two targets, the amplitudes of the saccadic eye movements and movements of the head vary inversely as a function of the starting positions of the eyes in the orbits. In addition, as head-movement amplitudes and velocities increase, saccade velocities decline. Taken together these observations lead to a reversal in the expected correlation between saccade duration and amplitude: small-amplitude saccades associated with large head movements can have longer durations than larger-amplitude saccades associated with small head movements. The data in this report indicate that this reversal occurs during gaze shifts along the horizontal meridian and also when considering the horizontal component of oblique saccades made when the eyes begin deviated only along the horizontal meridian. Under these conditions, it is possible to determine whether the variability in the duration of the constant amplitude vertical component of oblique saccades is accounted for better by increases in horizontal saccade amplitude or increases in horizontal saccade duration. Results show that vertical saccade duration can be inversely related to horizontal saccade amplitude (or unrelated to it) but that horizontal saccade duration is an excellent predictor of vertical saccade duration. Modifications to existing hypotheses of gaze control are assessed based on these new observations and a mechanism is proposed that can account for these data.     

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.     

Gravity modulates Listing's plane orientation during both pursuit and saccades

Previous studies have shown that the spatial organization of all eye orientations during visually guided saccadic eye movements (Listing's plane) varies systematically as a function of static and dynamic head orientation in space. Here we tested if a similar organization also applies to the spatial orientation of eye positions during smooth pursuit eye movements. Specifically, we characterized the three-dimensional distribution of eye positions during horizontal and vertical pursuit (0.1 Hz, +/-15 degrees and 0.5 Hz, +/-8 degrees) at different eccentricities and elevations while rhesus monkeys were sitting upright or being statically tilted in different roll and pitch positions. We found that the spatial organization of eye positions during smooth pursuit depends on static orientation in space, similarly as during visually guided saccades and fixations. In support of recent modeling studies, these results are consistent with a role of gravity on defining the parameters of Listing's law.     

Three-dimensional eye-head coordination during gaze saccades in the primate

The purpose of this investigation was to describe the neural constraints on three-dimensional (3-D) orientations of the eye in space (Es), head in space (Hs), and eye in head (Eh) during visual fixations in the monkey and the control strategies used to implement these constraints during head-free gaze saccades. Dual scleral search coil signals were used to compute 3-D orientation quaternions, two-dimensional (2-D) direction vectors, and 3-D angular velocity vectors for both the eye and head in three monkeys during the following visual tasks: radial to/from center, repetitive horizontal, nonrepetitive oblique, random (wide 2-D range), and random with pin-hole goggles. Although 2-D gaze direction (of Es) was controlled more tightly than the contributing 2-D Hs and Eh components, the torsional standard deviation of Es was greater (mean 3.55 degrees ) than Hs (3.10 degrees ), which in turn was greater than Eh (1.87 degrees ) during random fixations. Thus the 3-D Es range appeared to be the byproduct of Hs and Eh constraints, resulting in a pseudoplanar Es range that was twisted (in orthogonal coordinates) like the zero torsion range of Fick coordinates. The Hs fixation range was similarly Fick-like, whereas the Eh fixation range was quasiplanar. The latter Eh range was maintained through exquisite saccade/slow phase coordination, i.e., during each head movement, multiple anticipatory saccades drove the eye torsionally out of the planar range such that subsequent slow phases drove the eye back toward the fixation range. The Fick-like Hs constraint was maintained by the following strategies: first, during purely vertical/horizontal movements, the head rotated about constantly oriented axes that closely resembled physical Fick gimbals, i.e., about head-fixed horizontal axes and space-fixed vertical axes, respectively (although in 1 animal, the latter constraint was relaxed during repetitive horizontal movements, allowing for trajectory optimization). However, during large oblique movements, head orientation made transient but dramatic departures from the zero-torsion Fick surface, taking the shortest path between two torsionally eccentric fixation points on the surface. Moreover, in the pin-hole goggle task, the head-orientation range flattened significantly, suggesting a task-dependent default strategy similar to Listing's law. These and previous observations suggest two quasi-independent brain stem circuits: an oculomotor 2-D to 3-D transformation that coordinates anticipatory saccades with slow phases to uphold Listing's law, and a flexible "Fick operator" that selects head motor error; both nested within a dynamic gaze feedback loop.     

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)     

Role of eye, head, and shoulder geometry in the planning of accurate arm movements

Eye-hand coordination requires the brain to integrate visual information with the continuous changes in eye, head, and arm positions. This is a geometrically complex process because the eyes, head, and shoulder have different centers of rotation. As a result, head rotation causes the eye to translate with respect to the shoulder. The present study examines the consequences of this geometry for planning accurate arm movements in a pointing task with the head at different orientations. When asked to point at an object, subjects oriented their arm to position the fingertip on the line running from the target to the viewing eye. But this eye-target line shifts when the eyes translate with each new head orientation, thereby requiring a new arm pointing direction. We confirmed that subjects do realign their fingertip with the eye-target line during closed-loop pointing across various horizontal head orientations when gaze is on target. More importantly, subjects also showed this head-position-dependent pattern of pointing responses for the same paradigm performed in complete darkness. However, when gaze was not on target, compensation for these translations in the rotational centers partially broke down. As a result, subjects tended to overshoot the target direction relative to current gaze; perhaps explaining previously reported errors in aiming the arm to retinally peripheral targets. These results suggest that knowledge of head position signals and the resulting relative displacements in the centers of rotation of the eye and shoulder are incorporated using open-loop mechanisms for eye-hand coordination, but these translations are best calibrated for foveated, gaze-on-target movements.     

Spatial organization of linear vestibuloocular reflexes of the rat: responses during horizontal and vertical linear acceleration.

1. The spatial properties of linear vestibuloocular reflexes (LVOR) were studied in pigmented rats in response to sinusoidal linear acceleration on a sled. The orientation of the animal on the sled was altered in 15 degrees steps over the range of 360 degrees. Horizontal, vertical, and torsional components of eye movements were recorded with the magnetic field search coil technique in complete darkness. Conjugacy of the two eyes was studied in the horizontal movement plane. 2. Acceleration along the optic axis of one eye (approximately 50 degrees lateral) induced maximal vertical responses in the ipsilateral eye and, at the same time, maximal torsional responses in the contralateral eye. These vertical and torsional responses of the LVOR coincide with those obtained when the respective coplanar vertical semicircular canals are stimulated. Such a congruence suggests a common reference frame for LVOR and angular vestibuloocular reflexes (AVOR), with the result that direct combination of signals indicating apparent and real head tilt is facilitated. 3. Transformations of vertical and torsional responses into head coordinates (pitch and roll) show that these movements are compensatory in direction for any combination of apparent head tilt in pitch and roll planes. 4. Gain (rotation of the eye/apparent rotation of the gravity direction) was approximately 0.3 at 0.1 Hz and decreased to approximately 0.1 at 1.0 Hz. Vertical responses tended to have a larger gain than torsional responses. Phase lag relative to peak acceleration increased from about -9 degrees to about -47 degrees over the same frequency range. 5. Vertical linear acceleration evoked only vertical eye movements at a frequency of 1.0 Hz. 6. Horizontal responses of both eyes were symmetric or asymmetric in amplitude and in-phase (conjugate) or out-of-phase (disconjugate) with respect to each other, depending on the direction of linear acceleration. Translation in the transverse direction evoked conjugate compensatory horizontal responses. Forward-backward translation evoked movements of both eyes that were symmetric in amplitude, but 180 degrees out-of-phase. Translation along diagonal axes evoked almost no horizontal responses in the eye facing in the direction of linear motion but maximal horizontal responses in the eye facing away from the direction of linear motion. These disconjugate movements resulted in a modulation of the vergence angle of the eyes. 7. Disconjugate horizontal responses in darkness are best explained by the assumption that part of the visual consequences of a translational head displacement (i.e., change of viewing distance in light) is taken into account centrally.(ABSTRACT TRUNCATED AT 400 WORDS)     

Coordination of the eyes and head during visual orienting

Changing the direction of the line of sight is essential for the visual exploration of our environment. When the head does not move, re-orientation of the visual axis is accomplished with high velocity, conjugate movements of the eyes known as saccades. Our understanding of the neural mechanisms that control saccadic eye movements has advanced rapidly as specific hypotheses have been developed, evaluated and sometimes rejected on the basis of new observations. Constraints on new hypotheses and new tests of existing models have often arisen from the careful assessment of behavioral observations. The definition of the set of features (or rules) of saccadic eye movements was critical in the development of hypotheses of their neural control. When the head is free to move, changes in the direction of the line of sight can involve simultaneous saccadic eye movements and movements of the head. When the head moves in conjunction with the eyes to accomplish these shifts in gaze direction, the rules that helped define head-restrained saccadic eye movements are altered. For example, the slope relationship between duration and amplitude for saccadic eye movements is reversed (the slope is negative) during gaze shifts of similar amplitude initiated with the eyes in different orbital positions. Modifications to the hypotheses developed in head-restrained subjects may be needed to account for these new observations. This review briefly recounts features of head-restrained saccadic eye movements, and then describes some of the characteristics of coordinated eye–head movements that have led to development of new hypotheses describing the mechanisms of gaze shift control.     

Neural processing of gravito-inertial cues in humans. II. Influence of the semicircular canals during eccentric rotation

All linear accelerometers, including the otolith organs, respond equivalently to gravity and linear acceleration. To investigate how the nervous system resolves this ambiguity, we measured perceived roll tilt and reflexive eye movements in humans in the dark using two different centrifugation motion paradigms (fixed radius and variable radius) combined with two different subject orientations (facing-motion and back-to-motion). In the fixed radius trials, the radius at which the subject was seated was held constant while the rotation speed was changed to yield changes in the centrifugal force. In variable radius trials, the rotation speed was held constant while the radius was varied to yield a centrifugal force that nearly duplicated that measured during the fixed radius condition. The total gravito-inertial force (GIF) measured by the otolith organs was nearly identical in the two paradigms; the primary difference was the presence (fixed radius) or absence (variable radius) of yaw rotational cues. We found that the yaw rotational cues had a large statistically significant effect on the time course of perceived tilt, demonstrating that yaw rotational cues contribute substantially to the neural processing of roll tilt. We also found that the orientation of the subject relative to the centripetal acceleration had a dramatic influence on the eye movements measured during fixed radius centrifugation. Specifically, the horizontal vestibuloocular reflex (VOR) measured in our human subjects was always greater when the subject faced the direction of motion than when the subjects had their backs toward the motion during fixed radius rotation. This difference was consistent with the presence of a horizontal translational VOR response induced by the centripetal acceleration. Most importantly, by comparing the perceptual tilt responses to the eye movement responses, we found that the translational VOR component decayed as the subjective tilt indication aligned with the tilt of the GIF. This was true for both the fixed radius and variable radius conditions even though the time course of the responses was significantly different for these two conditions. These findings are consistent with the hypothesis that the nervous system resolves the ambiguous measurements of GIF into neural estimates of gravity and linear acceleration. More generally, these findings are consistent with the hypothesis that the nervous system uses internal models to process and interpret sensory motor cues.     

Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts

The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 microA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60 degrees. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.