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.     

Listing's law for eye,head and arm movements and their synergistic control

Summary We have recorded eye, head, and upper arm rotations in five healthy human subjects using the three-dimensional search coil technique. Our measurements show that the coordination of eye and head movements during gaze shifts within ± 25 deg relative to the forward direction is organized by restricting the rotatory trajectories of the two systems to almost parallel planes. These so-called Listing planes for eye-in-space and head-in-space rotations are workspace-oriented, not body-fixed. Eye and head trajectories in their respective planes are closely related in direction and amplitude. For pointing or grasping, the rotatory trajectories of the arm are also restricted to a workspace-oriented Listing plane. During visually guided movements, arm follows gaze, and the nine-dimensional rotatory configuration space for eye-head-arm-synergies (three degrees of freedom for each system) is reduced to a two-dimensional plane in the space of quaternion vectors.     

The coordination of eye,head, and arm movements during reaching at a single visual target

Summary The time of occurrence of eye, head, and arm movements directed at the same visual target was measured in five human subjects. The latency of activation of the corresponding neck and arm muscles was also measured. It appears that although the overt movements are sequentially ordered (starting with the eye movement, then the head and finally the arm) the EMG discharges are synchronous with respect to the eye movement onset. In addition, eye movement latency appears definitely (though weakly) correlated with either neck or arm EMG latencies. Neck and arm EMG latencies are also mutually correlated. These results indicate a clustering of segmental motor programs for target oriented actions.Supported by INSERM (Unité 94)     

General coordination of shoulder,elbow and wrist dynamics during multijoint arm movements

Studies of multijoint arm movements have demonstrated that the nervous system anticipates and plans for the mechanical effects that arise from motion of the linked limb segments. The general rules by which the nervous system selects appropriate muscle activities and torques to best deal with these intersegmental effects are largely unknown. In order to reveal possible rules, this study examined the relationship of muscle and interaction torques to joint acceleration at the shoulder, elbow and wrist during point-to-point arm movements to a range of targets in the horizontal plane. Results showed that, in general, dynamics differed between the joints. For most movements, shoulder muscle torque primarily determined net torque and joint acceleration, while interaction torque was minimal. In contrast, elbow and wrist net torque were determined by a combination of muscle and interaction torque that varied systematically with target direction and joint excursion. This "shoulder-centered pattern" occurred whether subjects reached targets using straight or curved finger paths. The prevalence of a shoulder-centered pattern extends findings from a range of arm movement studies including movement of healthy adults, neurological patients, and simulations with altered interaction effects. The shoulder-centered pattern occurred for most but not all movements. The majority of the remaining movements displayed an "elbow-centered pattern," in which muscle torque determined initial acceleration at the elbow and not at the shoulder. This occurred for movements when shoulder excursion was <50% of elbow excursion. Thus, both shoulder- and elbow-centered movements displayed a difference between joints but with reversed dynamics. Overall, these findings suggest that a difference in dynamics between joints is a general feature of horizontal plane arm movements, and this difference is most commonly reflected in a shoulder-centered pattern. This feature fits well with other general shoulder-elbow differences suggested in the literature on arm movements, namely that: (a) agonist muscle activity appears more closely related to certain joint kinematics at the shoulder than at the elbow, (b) adults with neurological damage display less disruption of shoulder motion than elbow motion, and (c) infants display adult-like motion first in the shoulder and last at the wrist.     

Role of the cerebellar flocculus region in the coordination of eye and head movements during gaze pursuit

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive ( approximately 43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.     

Coordination of fast eye and arm movements in a tracking task

Summary Eye and arm movements to single and double-step target displacements were studied to investigate whether or not the motor systems of the eye and arm share common command signals from the internal representation, which specify a) when a movement is initiated and b) the end position of a movement. The correlation between the time of onset of eye and arm movements was significant for single-step and double-step target displacements into the same direction. However, it was small and not significant for double-step target displacements into opposite directions if the time interval between first and second target displacement was 75 or 100 ms. This indicates that the command signal which specifies when a movement is started is different for both systems. However, the reconstructed signal in the internal representation, which specifies the end position of movements, is rather similar for eye and arm movements which seems to point to a common command signal. This result was corroborated by experiments in which eye and arm were found to jump always to the same target in the condition that two different targets were presented simultaneously.     

Motor planning of arm movements is direction-dependent in the gravity field

In the present study we analyzed kinematic and dynamic features of arm movements in order to better elucidate how the motor system integrates environmental constraints (gravity) into motor planning and control processes. To reach this aim, we experimentally manipulated the mechanical effects of gravity on the arm while maintaining arm inertia constant (i.e. the distribution of the mass around the shoulder joint). Six subjects performed single-joint arm movements (rotation around the shoulder joint) in both sagittal (upward, U, versus downward, D) and horizontal (left, L, versus right, R) planes, at different amplitudes and from different initial positions. Under these conditions, shoulder gravitational torques (SGTs) significantly varied when arm movements were performed in the sagittal but not in the horizontal plane. Contrary to SGTs, arm inertia remained constant and similar for both horizontal and sagittal planes since subjects performed arm movements with only one degree of freedom. All subjects, whatever the movement direction, appropriately scaled shoulder joint kinematic parameters according to movement amplitude. Furthermore, peak velocity and movement duration were equivalent for both horizontal and sagittal planes. Interestingly, some kinematic parameters significantly differed according to U/D but not L/R directions. Specifically, acceleration duration was greater for D than U movements, while the opposite was true for peak acceleration. Consequently, although vertical and horizontal arm movements shared a general common strategy (i.e. scaling law), the kinematic asymmetries between U and D arm movements, especially those that reflect central planning process (i.e. peak acceleration), indicated different motor intentions regarding the direction of the upcoming movement. These findings indicate that the interaction of the arm with the dynamics of the environment is internally represented during the generation of arm trajectories.     

Role of the cat substantia nigra pars reticulata in eye and head movements I. Neural activity

Summary 1. Single unit activity was recorded in the Substantia Nigra pars reticulata (SNpr) of cats trained to orient their gaze toward visual and/or auditory targets. 2. Cells in the SNpr have a steady high rate of spontaneous activity ranging from 35 to 120 spikes per second. The neurons respond to sensory stimuli or in relation to saccadic eye movements with a decrease or a cut-off of the spontaneous discharge. 3. Among 109 cells recorded in the SNPR 60 were responsive to visual stimuli (mean latency = 118 ms). Most of the receptive fields which were plotted were large encompassing part of the ipsilateral field. 4. Thirty nine (39) cells were responsive to auditory stimuli (mean latency = 81 ms). A majority of these cells showed a better response for stimuli located in the contralateral hemifield. 5. In a few cells, the sensory responses were modulated by the subsequent orienting behavior of the animals. 6. Thirty one (31) cells showed a response in relation to saccades. These units typically stopped discharging between 50 and 300 ms prior to the onset of the saccade. 39% of these units also responded in relation to spontaneous saccades in the dark. 61% of the saccadic cells also responded to sensory stimuli in the absence of saccades. Six (6) cells were found to respond to active head movements. 7. These results are discussed in the framework of the role that the basal ganglia might have in the selection of the sensory stimuli that trigger orienting behaviors.     

The coordination of eye, head, and hand movements in a natural task

Relatively little is known about movements of the eyes, head, and hands in natural tasks. Normal behavior requires spatial and temporal coordination of the movements in more complex circumstances than are typically studied, and usually provides the opportunity for motor planning. Previous studies of natural tasks have indicated that the parameters of eye and head movements are set by global task constraints. In this experiment, we explore the temporal coordination of eye, head, and hand movements while subjects performed a simple block-copying task. The task involved fixations to gather information about the pattern, as well as visually guided hand movements to pick up and place blocks. Subjects used rhythmic patterns of eye, head, and hand movements in a fixed temporal sequence or coordinative structure. However, the pattern varied according to the immediate task context. Coordination was maintained by delaying the hand movements until the eye was available for guiding the movement. This suggests that observers maintain coordination by setting up a temporary, task-specific synergy between the eye and hand. Head movements displayed considerable flexibility and frequently diverged from the gaze change, appearing instead to be linked to the hand trajectories. This indicates that the coordination of eye and head in gaze changes is usually the consequence of a synergistic linkage rather than an obligatory one. These temporary synergies simplify the coordination problem by reducing the number of control variables, and consequently the attentional demands, necessary for the task. Electronic Publication     

Spatial object representation and its use in planning eye movements

The eye movements we make to look at objects require that the spatial information contained in the objects image on the retina be used to generate a motor command. This process is known as sensorimotor transformation and has been generally addressed using simple point targets. Here, we investigate the sensorimotor transformation involved in planning double saccade sequences directed at one or two objects. Using both visually guided saccades toward stationary objects and objects subjected to intrasaccadic displacements, and memory-guided saccades, we found that the coordinate transformations required to program the second saccade were different for saccades aimed at a new target object and saccades that scanned the same object. While saccades aimed at a new object were updated on the basis of the actual eye position, those that scanned the same object were performed with a fixed amplitude, irrespective of the actual eye position. Our findings demonstrate that different abstract representations of space are used in sensory-to-motor transformations, depending on what action is planned on the objects.     

Similar planning strategies for whole-body and arm movements performed in the sagittal plane

The present paper looks for kinematic similarities between whole-body and arm movements executed in the sagittal plane. Eight subjects performed sit-to-stand (STS) and back-to-sit (BTS) movements at their preferred speed in the sagittal plane. Kinematics analysis focused on shoulder motion revealed that STS was composed of a straight, forward displacement followed by a curved, upward displacement while BTS was characterized by a curved, downward and straight, backward displacement. Curvature of the upward displacement was significantly greater than the downward one. Analysis of shoulder-velocity profiles showed that movement duration was significantly longer for BTS compared with STS and that the shape of the velocity profiles changed when subjects performed an STS compared with a BTS movement. Velocity profiles of the upward and downward displacements also differed; the relative acceleration duration (acceleration duration divided by movement duration during the vertical motion) was smaller for the upward compared with the downward displacement. The present results are in accordance with previous findings concerning the execution of vertical arm movements and suggest that the CNS uses similar motor plans for the performance of arm and whole-body movements in the sagittal plane.     

Integration of visual and somatosensory target information in goal-directed eye and arm movements

 In this study, we compared separate and coordinated eye and hand movements towards visual or somatosensory target stimuli in a dark room, where no visual position information about the hand could be obtained. Experiment 1 showed that saccadic reaction times (RTs) were longer when directed to somatosensory targets than when directed to visual targets in both single- and dual-task conditions. However, for hand movements, this pattern was only found in the dual-task condition and not in the single-task condition. Experiment 1 also showed that correlations between saccadic and hand RTs were significantly higher when directed towards somatosensory targets than when directed towards visual targets. Importantly, experiment 2 indicated that this was not caused by differences in processing times at a perceptual level. Furthermore, hand-pointing accuracy was found to be higher when subjects had to move their eyes as well (dual task) compared to a single-task hand movement. However, this effect was more pronounced for movements to visual targets than to somatosensory targets. A schematic model of sensorimotor transformations for saccadic eye and goal-directed hand movements is proposed and possible shared mechanisms of the two motor systems are discussed. Received: 15 June 1998 / Accepted: 21 September 1998     

Clavicle, a neglected bone: morphology and relation to arm movements and shoulder architecture in primates

In spite of its importance for movements of the upper limbs, the clavicle is an infrequently studied shoulder bone. The present study compares clavicular morphology among different extant primates. Methods have included the assessment of clavicular curvatures projected on two perpendicular planes that can be assessed overall as cranial and dorsal primary curvatures. Results showed that in cranial view, three morphologies can be defined. One group exhibited an external curvature considerably more pronounced than the internal one (Gorilla, Papio); a second group was characterized by an internal curvature much more pronounced than the external one (Hylobates, Ateles); and a third group contained those with the two curvatures equally pronounced (Pan, Homo, Pongo, Procolobus, Colobus). Clavicle curvatures projected on the dorsal plane could be placed into four groups. The first group is characterized by two curvatures, an inferior and a superior (Apes, Spider monkeys). The second included monkeys, whose clavicles have an inferior curvature much more pronounced than the superior one. The third group includes only Hylobates, whose clavicles possess only the superior curvature. The last group includes only modern humans, whose clavicles show only the inferior curvature, which is less pronounced than that which exists in monkeys. Curvatures in cranial view relate information regarding the parameters of arm elevation while those in dorsal view offer insights into the position of the scapula related to the thorax. The use of clavicular curvature analysis offers a new dimension in assessment of the functional morphology of the clavicle and its relationship to the shoulder complex.     

Electrical stimulation of the frontal eye field in a monkey produces combined eye and head movements

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.     

A new paradigm to investigate the roles of head and eye movements in the coordination of whole-body movements

Although previous studies have demonstrated the existence of coordinated eye and head movements during gaze shifts, none has studied the temporal and spatial characteristics of the various body segments during gaze transfers that require whole body movements. Without this information it is not possible to determine the extent of the interaction between the oculomotor control system and the motor control systems responsible for moving other body parts. Presented here is a detailed analysis of the timing and kinematic characteristics of participants (N=5) eye, head, upper body and feet during rotation of their body to align with light cues positioned at eccentric locations (45, 90, and 135°, left and right of centre). For all rotation amplitudes there was a clear sequence of body segment orientation (eye, head, upper body and feet) consistent with previous studies of locomotor steering and significant correlations between the onset latency times of the eyes and all body segments. There were also significant correlations between temporally aligned kinematic profiles of the feet and the eye in space for all movement amplitudes. The extent of correlation was significantly lower for displacement profiles of the feet versus head and of the feet versus upper body. These findings demonstrate substantial eye-foot coordination during a novel whole-body rotation paradigm and provide evidence that the output of the motor systems responsible for moving the feet is heavily influenced by the motor systems responsible for generating and coordinating eye and head movements to peripheral targets.     

Role of agonist and antagonist muscles in fast arm movements in man

Summary Fast goal-directed voluntary movements of the human upper extremity are known to be associated with three distinct bursts of EMG activity in antagonistic muscles. The role of each burst (AG1, ANT, AG2) in controlling motion is not fully understood, largely because overall limb response is a complex function of the entire sequence of bursts recorded during experimental trials. In order to investigate the role of each burst of muscle activity in controlling motion, we studied fast voluntary arm movements and also developed two simulation techniques, one employing a mathematical model of the limb and the other using electrical stimulation of human arm muscles. These techniques show that two important movement parameters (peak displacement, time to reach peak displacement) are non-linear functions of the magnitude of the antagonist input (torque and stimulation voltage, respectively, in our two simulations). In the fastest movements, the agonist muscle is primarily responsible for the distance moved, while the antagonist muscle provides an effective means of reducing movement time. The third component of the triphasic pattern moderates the antagonist braking forces and redirects the movement back to the target.     

Role of the cat substantia nigra pars reticulata in eye and head movements II. Effects of local pharmacological injections

Summary 1. Guided and reflex eye movements were studied in cats trained to make orienting saccades toward visual and auditory targets. Injections of a GABA-agonist (Muscimol) or GABA-antagonists (Bicuculline and Picrotoxin) were made in the Substantia Nigra pars reticulata (SNpr). 2. Bicuculline and Picrotoxin, whether unilaterally or bilaterally injected had no effect on the posture nor the oculomotor performance of the animals. Neck muscle activity remained symmetrical. 3. Unilateral injections of Muscimol produced oro-facial akinesia, reduction of the number of eye movements, contralateral head turning, visual neglect mostly (but not only) for ipsilateral visual space. Balance between the gains of the vestibulo-ocular reflex (VOR) in the two directions of movement was changed. Gain was decreased for the ipsilateral rotation. The optokinetic nystagmus (OKN) was not affected. Contralateral neck muscles were hypertonic. 4. After bilateral injections of Muscimol, the cats did not orient. The VOR was normal when the injections induced no postural asymmetry. Hypertony was bilateral. 5. Implications of these results for the role of the basal ganglia in motor control are discussed. We suggest that in Parkinson's disease the fixed inhibitory drive of the SNpr on the tectum and on the thalamus is disrupted.     

Oculo-manual tracking of visual targets in monkey: role of the arm afferent information in the control of arm and eye movements

Summary The study was aimed at defining the role of hand (and arm) kinaesthetic information in coordination control of the visuo-oculo-manual tracking system. Baboons were trained to follow slow-moving and stepping visual targets either with the eyes alone or with the eyes and a lever moved by the forelimb about the vertical axis. A LED was attached to the lever extremity. Four oculo-manual tracking condidtions were tested and compared to eye-alone tracking: Eye and hand tracking of a visual target presented on a screen, eye tracking of the hand, and eye tracking of an imaginary target actively moved by the arm. The performance of the animals evaluated in terms of latency, and velocity and position precision for both eye and hand movements was seen to be equivalent to that of humans in similar situations. After dorsal root rhizotomy (C1-T2) the animals were unable to produce slow arm motion in response to slow-moving targets. Instead, they produced successions of ballistic-like motions whose amplitude decreased as retraining proceeded. In addition, the animals could not longer respond with smooth pursuit eye movements to an imaginary target actively displaced by the animal's forelimb. It was concluded that the absence of ocular smooth pursuit after lesion results from the disruption of a signal derived from arm kinaesthetic information and addresses to the oculomotor system. This signal is likely to be used in the control of coordination between arm and eye movements during visuo-oculo-manual tracking tasks. One cause of the animal's inability to achieve slow arm movement in response to slow target motion is thought to be due to a lesion-induced alteration of the spinal common pathway dynamics which normally integrate the velocity signal descending from the arm movement command system.