The contribution of coordinated eye and head movements in hand pointing accuracy

Summary The accuracy of pointing movements of the hand, directed at visual targets 10° to 40° from the midline, was measured in normal human subjects. No visual feedback from the moving hand was available to the subjects. The head could be either maintained stationary (head-fixed condition) or free to move (head-free condition) during the pointing movements. It was found that the error in pointing was reduced for all targets in the head-free condition. This reduction was more important for the more eccentric target (40°). Improvement in accuracy was observed without any significant change in either the latency or the duration of eye, head or hand movements. In the head-free condition, it was found that the head was displaced in the direction of the target by an amount representing no more than 2/3 of the target amplitude. The improvement in accuracy was not influenced by the amplitude of the head movement. A model is proposed which shows how coordinated eye and head movements could improve the encoding of target position.Work supported by INSERM-Unité 94     

Time course of eye and head deviation in spatial neglect

Spatial neglect is characterized by a deviation of the eyes and the head during active search, as well as at rest. Here the authors investigate the hitherto unknown relationship between these striking behaviors in the course of recovery. Gaze, eye-in-head, and head-on-trunk positions were recorded separately under two experimental conditions: (i) at rest (i.e., without any specific requirements, doing nothing) and (ii) during active exploratory search in a large visual array of 240 degrees x 80 degrees over a 10-month period. The authors observed a parallel decrease of eye and head (= gaze) deviation in both conditions, accompanied by a comparable decline in neglect severity. The results strengthen the view that the marked gaze deviation toward the ipsilesional side in patients with spatial neglect is due to a very elementary disturbance of human spatial information processing.     

Contribution of tactile information to accuracy in pointing movements

Extracellular field potentials, evoked by stimulation of the cortico-NAcc border, were recorded from the nucleus accumbens (NAcc) in horizontal slices of rat ventral forebrain. The peak amplitude of the population spike/excitatory postsynaptic potential complex (PEC, N2 component) was reduced by 78±2% (n=44) by the antagonist of AMPA-type glutamate receptors, 6-cyano-7-nitroquinoxaline-2, 3-dione (CNQX, 10 μM). Dopamine (100 μM) reversibly depressed the peak amplitude of the PEC by 40±3% (n=44). The GABA_A receptor antagonists picrotoxin (10, 30 μM), or bicuculline methiodide (BMI, 20 μM), significantly reduced the PEC depression caused by dopamine (100 μM) to 9±3% (n=20), 12±7% (n=8) and 13±3% (n=4) of control respectively, which, in the case of BMI, was reversible on washout of BMI. In slices with the frontal cortex removed (decorticated), dopamine (100 μM) was without effect on the PEC (n=14). In contrast, the inhibition of the PEC by adenosine (by 40±9% in control, n=4), which was blocked by the A1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine (DPCPX, 200 nM), was unaffected by picrotoxin (50 μM, n=4), and persisted in decorticated slices, albeit increased to 88±2% (n=4) of control. These results indicate that the depression of the cortico-NAcc synaptic transmission by dopamine in this preparation is due to an action in frontal, possibly piriform, cortex, which may involve modulation of intracortical GABAergic circuitry. In contrast, depression by adenosine is consistent with a presynaptic action via A1 receptors on intra-NAcc glutamate-releasing terminals, although there may be an additional action of adenosine within the cortex that also influences the cortico-NAcc PEC. Electronic Publication     

Effect of target size on spatial and temporal characteristics of a pointing movement in man

Summary The effects of constraints related to movement accuracy on the spatial and temporal characteristics of pointing movements of the arm to a target were investigated. It was found that movement time increased, even at slow speeds, when target size decreased. Spatial variability of the trajectory of the index finger was also reduced, but only in proximity to the target, when higher accuracy was demanded while variability of motion at the wrist showed little change. The effect of varying the angular orientation of the target on the trajectories of the wrist and finger was also investigated. The data support the hypothesis that motion at the shoulder and elbow joints, which is closely linked, is determined primarily by target position while motion at the wrist joint, which is only loosely coupled to the motion at the more proximal joints, is related principally to the angular orientation of the target in space. The data also suggest that wrist motion is controlled separately from motion at the more proximal joints.     

Eccentric eye and head positions in darkness induce deviation from the intended path

Head and gaze are aligned with the actual path during locomotion. Before a turn is made, gaze changes in the direction of the planned trajectory. We investigated whether eccentric horizontal head and/or eye position without vision causes deviations from the intended straight path. Twenty blindfolded healthy volunteers were asked to walk toward a previously seen target 10 m straight ahead. Various combinations of head and eye positions were tested (eye-in-head gaze straight ahead or 35° left or right with head straight ahead or 70° left or right). Head rotation to the left caused a gait deviation to the right (3.7°) and head rotation to the right caused a deviation to the left (2.7°; F(2,40)=34.966; P<0.00001). Eye position also showed a tendency to cause gait deviations opposite in direction to gaze, which was, however, not significant. Deviations from the intended straight path were largest with head rotation and eyes straight ahead (gaze 70° off target) or eyes opposite to head rotation (gaze 35° off target). Notably, when lateral eye deviation added to head rotation (gaze 105° off target), i.e., gaze is directed backward, mean deviations decreased (2.3° to the right and 1.2° to the left). Thus, we show that (1) eccentric head positions induce direction-specific gait deviations that are independent of concurrent environmental visual information, and (2) that gait deviations are contraversive to eye-head gaze rather than ipsiversive as reported by others for visually controlled locomotion. The direction of deviation may reflect the compensation of an expected or perceived deviation in the direction of gaze.     

The coordination of eye, head, and arm movements during rapid gaze orienting and arm pointing

This study aimed to investigate the coordination of multiple control actions involved in human horizontal gaze orienting or arm pointing to a common visual target. The subjects performed a visually triggered reaction time task in three conditions: (1) gaze orienting with a combined eye saccade and head rotation (EH), (2) arm pointing with gaze orienting by an eye saccade without head rotation (EA), and (3) arm pointing with gaze orienting by a combined eye saccade and head rotation (EHA). The subjects initiated eye movement first with nearly constant latencies across all tasks, followed by head movement in the EH task, by arm movement in the EA task, and by head and then arm movements in the EHA task. The differences of onset times between eye and head movements in the EH task, and between eye and arm movements in the EA task, were both preserved in the EHA task, leading to an eye-to-head-to-arm sequence. The onset latencies of eye and head in the EH task, eye and arm in the EA task, and eye, head and arm in the EHA task, were all positively correlated on a trial-by-trial basis. In the EHA task, however, the correlation coefficients of eye–head coupling and of eye–arm coupling were reduced and increased, respectively, compared to those estimated in the two-effector conditions (EH, EA). These results suggest that motor commands for different motor effectors are linked differently to achieve coordination in a task-dependent manner.     

Vestibular and non-vestibular contributions to eye movements that compensate for head rotations during viewing of near targets

Geometry dictates that when subjects view a near target during head rotation the eyes must rotate more than the head. The relative contribution to this compensatory response by adjustment of the vestibulo-ocular reflex gain (Gvor), visual tracking mechanisms including prediction, and convergence is debated. We studied horizontal eye movements induced by sinusoidal 0.2–2.8 Hz, en-bloc yaw rotation as ten normal humans viewed a near target that was either earth-fixed (EFT) or head-fixed (HFT). For EFT, group median gain was 1.49 at 0.2 Hz declining to 1.08 at 2.8 Hz. For HFT, group median gain was 0.03 at 0.2 Hz increasing to 0.71 at 2.8 Hz. By applying transient head perturbations (peak acceleration >1,000° s^–2) during sinusoidal rotation, we determined that Gvor was similar during either EFT or HFT conditions, and contributed only ~75% to the compensatory response. We confirmed that retinal image slip contributed to the compensatory response by demonstrating reduced gain during EFT viewing under strobe illumination. Gain also declined during sum-of-sines head rotations, confirming the contribution of predictive mechanisms. The gain of compensatory eye movements was similar during monocular or binocular viewing, although vergence angle was greater during binocular viewing. Comparison with previous studies indicates that mechanisms for generation of eye rotations during near viewing depend on head stimulus type (rotation or translation), waveform (transient or sinusoidal), and the species being tested.     

Reorientation of visually evoked postural responses by different eye-in-orbit and head-on-trunk angular positions

We examined the question of whether the position of the eyes in the head and of the head on the trunk influence the direction of visually elicited postural reactions. Normal subjects stood on a force platform viewing a large disc, rotating in the roll plane, always maintained orthogonal to the line of sight. The disc was presented at 0°, 30° and 90° to the right or left with respect to the mid-frontal plane of the subject's body and was viewed with various combinations of horizontal eye-in-orbit and head-on-trunk deviations. It was found that the main direction of body sway was always reoriented to be parallel to the disc (e.g. viewing the disc at 30° oriented sway responses at a mean angle of 33°). The largest sway responses were obtained when the disc was parallel to the sagittal plane of the body and was viewed with an ipsilateral eye-neck deviation totalling 90° (head-on-trunk 60°+eye-in-orbit 30°). When eye and head deviations cancelled each other (i.e. eye-in-orbit +30° combined with head-on-trunk -30°), directional effects on sway also cancelled each other out. This result demonstrates that signals of eye-in-orbit and head-on-trunk position have the capability to redirect visuo-motor commands to the appropriate postural muscles. This allows vision to regulate postural balance whatever the position of the eyes in space. We speculate that this function is mediated by eye and neck proprioceptive signals (or alternatively by efference copy) with access to gain control mechanisms in the visuo-postural system.     

Differential contributions of vision and proprioception to movement accuracy

We examined the relative roles of visual and proprioceptive information about initial hand position on movement accuracy. A virtual reality environment was employed to dissociate visual information about hand position from the actual hand position. Previous studies examining the effects of such dissociations on perception of hand location have indicated a bias toward the visually displayed position. However, an earlier study, which employed optical prisms to dissociate visual and proprioceptive information prior to targeted movements, suggested a bias in movement direction toward that defined by the actual hand position. This implies that visual and proprioceptive information about hand position may be differentially employed for perceptual judgments and movement planning, respectively. We now employ a virtual reality environment to systematically manipulate the visual display of the hand start position from the actual hand position during movements made to a variety of directions. We asked whether subjects would adjust their movements in accord with the virtual or the actual hand location. Subjects performed a series of baseline movements toward one of three targets in each of three blocks of trials. Interspersed among these trials were "probe" trials in which the cursor location, but not the hand location, was displaced relative to the baseline start position. In all cases, cursor feedback was blanked at movement onset. Our findings indicated that subjects systematically adjusted the direction of movement in accord with the virtual, not the actual, start location of the hand. These findings support the hypothesis that visual information about hand position predominates in specifying movement direction.     

Reflex and mechanical contributions to head stabilization in alert cats

Five alert cats were tested for their responses to rotation in a device that allowed rotation of the head on the trunk about a vertical axis passing through the C1-C2 vertebral joint. Electrodes were implanted to record the horizontal and vertical electrooculogram and electromyographic (EMG) activity of the dorsal neck muscles splenius, biventer cervicus, and complexus. Head rotation and torque acting on the head were recorded in the horizontal plane during rotations in the 0.05-5.0 Hz frequency range. Responses were interpreted with reference to a closed-loop dynamic model of the head-neck system. Whole-body rotation (WBR) with no neck movement elicited a vestibulocollic reflex (VCR). Neck muscle EMG lagged the sinusoidal platform rotation by approximately 120 degrees at low frequencies, which represents a 60 degrees lead relative to a perfectly compensatory 180 degrees lag. This phase lead was related to the cumulative eye position of the accompanying horizontal vestibular nystagmus as reported by Vidal et al. Horizontal head torque exhibited a similar low-frequency behavior. At high frequencies, EMG exhibited a progressively increasing phase lead and gain increase typical of a second-order lead system as described in decerebrate cats. Torque, however, showed much less lead and gain increase, presumably because of the low-pass filter properties of the process coupling muscle excitation to torque. Head torque did exhibit a steep increase in gain with frequency and a phase approaching that of platform acceleration at high frequencies when weights were attached to the head to increase its moment of inertia. The same +40 dB/decade gain slope and phase approaching 0 degree was observed during WBR rotation of the anesthetized cat in which head inertia is the only factor contributing to the torque. This dynamic behavior was predicted by the inertial component of the model. In the alert unweighted cat, the inertial torque was smaller than VCR-generated torque at frequencies below 4 Hz. Rotation of the neck with the head held fixed in space (HFS rotation) elicited a cervicocollic reflex (CCR). Neck EMG response was very similar to that observed during WBR, both in dynamic behavior and overall gain. Torque, however, was consistently greater than that generated by WBR and showed a steady increase of 8 dB/decade as frequency rose. The added torque can be attributed to the viscoelastic properties of neck muscles. Driven rotation of the head on the fixed body elicited torques that could be closely approximated by a vector sum of torques observed during WBR and HFS rotations.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vestibular and somatosensory contributions to responses to head and body displacements in stance

The relative contribution of vestibular and somatosensory information to triggering postural responses to external body displacements may depend on the task and on the availability of sensory information in each system. To separate the contribution of vestibular and neck mechanisms to the stabilization of upright stance from that of lower body somatosensory mechanisms, responses to displacements of the head alone were compared with responses to displacements of the head and body, in both healthy subjects and in patients with profound bilateral vestibular loss. Head displacements were induced by translating two 1-kg weights suspended on either side of the head at the level of the mastoid bone, and body displacements were induced translating the support surface. Head displacements resulted in maximum forward and backward head accelerations similar to those resulting from body displacements, but were not accompanied by significant center of body mass, ankle, knee, or hip motions. We tested the effect of disrupting somatosensory information from the legs on postural responses to head or body displacements by sway-referencing the support surface. The subjects' eyes were closed during all testing to eliminate the effects of vision. Results showed that head displacements alone can trigger medium latency (48–84 ms) responses in the same leg and trunk muscles as body displacements. Nevertheless, it is unlikely that vestibular signals alone normally trigger directionally specific postural responses to support surface translations in standing humans because: (1) initial head accelerations resulting from body and head displacements were in opposite directions, but were associated with activation of the same leg and trunk postural muscles; (2) muscle responses to displacements of the head alone were only one third of the amplitude of responses to body displacements with equivalent maximum head accelerations; and (3) patients with profound bilateral vestibular loss showed patterns and latencies of leg and trunk muscle responses to body displacements similar to those of healthy subjects. Altering somatosensory information, by sway-referencing the support surface, increased the amplitude of ankle muscle activation to head displacements and reduced the amplitude of ankle muscle activation to body displacements, suggesting context-specific reweighting of vestibular and somatosensory inputs for posture. In contrast to responses to body displacements, responses to direct head displacements appear to depend upon a vestibulospinal trigger, since trunk and leg muscle responses to head displacements were absent in patients who had lost vestibular function as adults. Patients who lost vestibular function as infants, however, had near normal trunk and leg response to head displacements, suggesting a substitution of upper trunk and neck somatosensory inputs for missing vestibular inputs during development.     

Safety aspects of transcranial brain stimulation in man tested by single photon emission-computed tomography

Single photon emission-computed tomography (SPECT) using 99mTc-labelled hexamethylpropyleneamine oxime (99mTc-HMPAO), a new method to visualize regional cerebral blood flow (rCBF) and epileptogenic foci, was used to study acute and long-term effects of transcranial brain stimulation. Magnetic and electric brain stimulation increase rCBF not more than voluntary muscle activation mimicking the motor effects of transcranial brain stimulation. Focal rCBF increase, typical for epileptogenic foci, or other pathological findings could not be detected even when the subject had received several thousand stimulations in the past. Transcranial brain stimulation does not produce rCBF patterns indicating acute or chronic adverse effects.     

The pattern of changes produced in the saccadic system and vestibuloocular reflex by visually patching one eye

The purpose of the present study was to determine whether, in the absence of visual input to one eye, saccades remained equal in the two eyes. The same question was addressed for the VOR gain of the two eyes. After 1 wk during which one eye was continuously patched, the saccadic properties of only the unseeing eye showed changes consisting of a change, usually a decrease, in saccadic step magnitude, postsaccadic drift with an exponentially decaying component in the temporal direction, and the appearance of a vertical component as well as vertical postsaccadic drift during horizontally directed saccades. Effects were also observed in the VOR consisting of a change in gain and a vertical component during horizontal head rotation. As with saccades, the vertical component in the patched eye was upward when the eye was deviated nasally. When the patch was removed, normal function was restored within 1 day to the previously patched eye without impairing the function of the unpatched eye. These results suggest that the conjugate nature of saccades and the VOR is in part the consequence of a selective, visually driven, calibration mechanism, which can alter commands to motoneurons of one muscle of a conjugate muscle pair without affecting commands to the other. The similarity of changes observed in the VOR and saccades after patching suggests that elements common to both are altered in the absence of vision.     

Frames of reference for saccadic command tested by saccade collision in the supplementary eye field

In what frame of reference does the supplementary eye field (SEF) encode saccadic eye movements? In this study, the "saccade collision" test was used to determine whether a saccade electrically evoked in the monkey's SEF is programmed to reach an oculocentric goal or a nonoculocentric (e.g., head or body-centered) goal. If the eyes start moving just before or when an oculocentric goal is imposed by electrical stimulation, the trajectory of the saccade to that goal should compensate for the ongoing movement. Conversely, if the goal imposed by electrical stimulation is nonoculocentric, the trajectory of the evoked saccade should not be altered. In head-fixed experiments, we mapped the trajectories of evoked saccades while the monkey fixated at each of 25 positions 10 degrees apart in a 40 x 40 degrees grid. For each studied SEF site, we calculated convergences indices and found that "convergent" and "nonconvergent" sites were separately clustered: nonconvergent rostral to convergent. Then, the "saccade collision" test was systematically applied. We found compensation at sites where saccades were of the nonconvergent type and practically no compensation at sites where saccades were of the convergent type. The results indicate that the SEF can encode saccade goals in at least two frames of reference and suggest a rostrocaudal segregation in the representation of these two modes.     

Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields.

1. The purpose of this study was to analyze the response properties of neurons in the frontal eye fields (FEF) of rhesus monkeys (Macaca mulatta) and to compare and contrast the various functional classes with those recorded in the supplementary eye fields (SEF) of the same animals performing the same go/no-go visual tracking task. Three hundred ten cells recorded in FEF provided the data for this investigation. 2. Visual cells in FEF responded to the stimuli that guided the eye movements. The visual cells in FEF responded with a slightly shorter latency and were more consistent and phasic in their activation than their counterparts in SEF. The receptive fields tended to emphasize the contralateral hemifield to the same extent as those observed in SEF visual cells. 3. Preparatory set cells began to discharge after the presentation of the target and ceased firing before the saccade, after the go/no-go cue was given. These neurons comprised a smaller proportion in FEF than in SEF. In contrast to their counterparts in SEF, the preparatory set cells in FEF did not respond preferentially in relation to contralateral movements, even though most responded preferentially for movements in one particular direction. The time course of the discharge of the FEF set cells was similar to that of their SEF counterparts, except that they reached their peak level of activation sooner. The few preparatory set cells in FEF tested with both auditory and visual stimuli tended to respond preferentially to the visual targets, whereas, in contrast, most set cells in SEF were bimodal. 4. Sensory-movement cells represented the largest population of cells recorded in FEF, responding in relation to both the presentation of the targets and the execution of the saccade. Although some of these sensory-movement cells resembled their counterparts in SEF by exhibiting a sustained elevation of activity, most of the FEF sensory-movement cells gave two discrete bursts, one after the presentation of the target and another before and during the saccade. Like their counterparts in SEF, the sensory-movement cells tended to be tuned for saccades into the contralateral hemifield, but this tendency was more pronounced in FEF than in SEF. The FEF sensory-movement cells discharged more briskly, with a shorter latency relative to the presentation of the target, than their counterparts in SEF. In addition, the FEF sensory-movement neurons reached their peak activation sooner than SEF sensory-movement neurons. Most FEF sensory-movement cells exhibited different patterns of activation in response to visual and auditory targets.(ABSTRACT TRUNCATED AT 400 WORDS)     

Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities

Summary The egocentric localization of objects in extrapersonal space requires that the retinal and extraretinal signals specifying the gaze direction be simultaneously processed. The question as to whether the extraretinal signal is of central or peripheral origin is still a matter of controversy, however. Three experiments were carried out to investigate the following hypotheses: 1) that the proprioceptive feedback originating in eye and neck muscles might provide the CNS with some indication about the gaze direction; and 2) that the retinal and proprioceptive extraretinal inputs might be jointly processed depending on whether they are of monocular or binocular origin. Application of low amplitude mechanical vibrations to either the extraocular or neck muscles (or both) of a subject looking monocularly at a small luminous target in darkness resulted in an illusory movement of the target, the direction of which depended on which muscle was stimulated. A slow upward target displacement occurred on vibrating the eye inferior rectus or the neck sterno-cleido-mastoidus muscles, whereas a downward shift was induced when the dorsal neck muscles (trapezius and splenius) were vibrated. The extent of the perceptual effects reported by subjects was measured in an open-loop pointing task in which they were asked to point at the perceived position of the target. These results extend to visually-oriented behavior the role of extraocular and neck proprioceptive inputs previously described in the case of postural regulation, since they clearly show that these messages contribute to specifying the gaze direction. This suggests that the extraretinal signal might include a proprioceptive component. The proposition that a directional body reference frame may be based on the common processing of various proprioceptive feedbacks is discussed.     

Difference between visually and electrically evoked gaze saccades disclosed by altering the head moment of inertia

Differences between gaze shifts evoked by collicular electrical stimulation and those triggered by the presentation of a visual stimulus were studied in head-free cats by increasing the head moment of inertia. This maneuver modified the dynamics of these two types of gaze shifts by slowing down head movements. Such an increase in the head moment of inertia did not affect the metrics of visually evoked gaze saccades because their duration was precisely adjusted to compensate for these changes in movement dynamics. In contrast, the duration of electrically evoked gaze shifts remained constant irrespective of the head moment of inertia, and therefore their amplitude was significantly reduced. These results suggest that visually and electrically evoked gaze saccades are controlled by different mechanisms. Whereas the accuracy of visually evoked saccades is likely to be assured by on-line feedback information, the absence of duration adjustment in electrically evoked gaze shifts suggests that feedback information necessary to maintain their metrics is not accessible or is corrupted during collicular stimulation. This is of great importance when these two types of movements are compared to infer the role of the superior colliculus in the control of orienting gaze shifts.     

Effects of body and head positions on bilateral difference in tympanic temperatures

Summary We have examined the nonparallel changes in tampanic membrane temperatures (T _ty) from the two ears in response to various changes in body and head positions. Upon assuming a lateral recumbent position, the T _ty on the lower side increased while that on the upper side decreased. Pressure application over a wide area of the lateral chest only caused inconsistent and obscure asymmetric changes in T _ty. A lateral flexion of the head with the subject sitting upright and a rotation of the head to the side in a supine position induced an increase in the T _ty on the lower side compared to that on the upper side. The temperature and blood flow of the forehead often decreased on the lower side and increased on the upper side, although such responses were not always concomitant with the asymmetric changes in T _ty. A dorsal flexion of the head with the subject in a reclining position caused a slight increase in the T _ty, whereas raising the head upright induced a slight decrease in them. Two additional experiments were carried out with single photon emission computed tomography using ^99mTc-hexamethylpropyleneamine oxime as tracer, and a slight, relative decrease in counts was noted in the right hemisphere during rotation of the head to the right. These results would strongly suggest that unilateral increases and decreases in T _ty could have been caused by one-sided decreases and increases, respectively, in blood flow to the brain and/or the tympanic membrane, induced by a vasomotor reflex involving vestibular stimulation.