The contribution of retinal and extraretinal signals to manual tracking movements

We have assessed the contribution made by retinal and extraretinal signals when subjects used their hand to track targets moving at constant velocities. Comparisons were made between responses produced under the following conditions: (1) with full vision of the hand and unrestricted movement of the eyes, (2) without vision of the hand or (3) while visually fixating a stationary LED. Target velocity was varied in a pseudo-random order across trials. In each condition response latency decreased as target velocity was increased. There was a 24 ms increase in latency when vision of the hand was removed or eye movements were restricted. Under normal conditions, subjects were able to accurately catch up to and match target velocity with their hand. When vision of the hand was removed, subjects lagged behind the target but were able to match target velocity. This deficit was eliminated when vision of the hand was made available for the beginning of the response. When subjects were required to visually fixate they could catch up to the target with their hand, but subsequently produced a steady state hand velocity that was greater than target velocity. When the LED was positioned such that the target started in the peripheral visual field, the overestimation of target velocity was evident from the beginning of the response: subjects produced initial accelerations with their hand that were significantly greater than in normal conditions. Finally, normal responses were produced when subjects were required to visually pursue a second target that moved at the same speed and in the same direction as the main target. When the velocities of these two targets differed, subjects produced hand movements that were initially more appropriate for the target being visually pursued. Together these results suggest that vision of the hand and how it is initially positioned relative to the target is necessary to catch up to the target; whereas the extraretinal signal concerned with eye velocity is required to produce an accurate steady state hand velocity.     

Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control

Summary 1. The control of pointing arm movements in the absence of visual guidance was investigated in unpracticed human subjects. The right arm grasped a lever which restricted the movement of the right index fingertip to a horizontal arc, centered between the axes of eye rotation. A horizontal panel directly above the arm prevented visual feedback of the movement. Visual stimuli were presented in discrete positions just above panel and fingertip. A flag provided visual feedback on fingertip position before each pointing movement (Exp. A and B), or before a movement sequence (Exp. C). 2. When subjects pointed from straight ahead to eccentric stimulus positions (Exp. A), systematic and variable pointing errors were observed; both kinds of errors increased with stimulus eccentricity. When subjects pointed from 30 deg left to stimuli located further right (Exp. B), errors increased with stimulus position to the right. Taken together, these findings suggest that pointing accuracy depends not primarily on stimulus position, but rather on required movement amplitude. 3. When subjects performed sequences of unidirectional movements (Exp. C), systematic and variable errors increased within the sequence. A quantitative analysis revealed that this increase can be best described as an accumulation of successive pointing errors. 4. We conclude that both findings, error increase with amplitude, and accumulation of successive errors, when considered together strongly support the hypothesis that amplitude, rather than final position, is the controlled variable of the investigated movements.     

Ocular perturbations and retinal/extraretinal information: the coordination of saccadic and manual movements

Two experiments were conducted to examine the interactions between the ocular and manual systems during rapid goal-directed movements. A point-light array was used to generate Müller-Lyer configuration target endpoints (in-Müller, out-Müller, ’X’) for 30 cm aiming movements. Vision (of the limb and target), eye position, and the concurrence of eye movement were varied to manipulate the availability of retinal and extraretinal information. In addition, the Müller-Lyer endpoints were used to generate predictable biases in accuracy of these information channels. Although saccadic amplitude was consistently biased, manual bias in response to illusory targets only occurred in trials with concurrent eye movement and elimination of retinal target information on limb movement initiation; covariation of eye and hand displacement was also most prevalent in these trials. Contrary to previous findings, there was no temporal relation between eye and hand movements. In addition to any role in coordinated eye-hand action, the availability of vision of both the limb and target again had strong performance benefits for rapid manual aiming. Received: 14 August 1998 / Accepted: 8 March 1999     

Dissociating visual and kinesthetic coordinates during pointing movements

Goal-directed movements imply that the visual coordinates in which the localisation of the goal is coded are transformed into proprioceptive coordinates in which the arm movement is coded. The two systems of coordinates are normally superimposed. Using a virtual reality device attached to the subject's head, we have created a situation where these systems were dissociated from each other. The virtual environment involved virtual visual targets and an image of the subject's hand reconstructed from the output of a data glove wore by the subject's right hand. When the subject's head was rotated, the visual targets and the image of the hand rotated by the same amount. Movements of the real hand were thus in conflict with those of the reconstructed hand, which appeared to err in the direction of head rotation. Pointing movements directed at five targets (0°, 26° and 52° on each side) were studied for five different head positions (0°, 45° and 80° to the right and to the left). The results showed a significant pointing bias towards head position, except for the left-most targets in the right head rotations. Constant errors in azimuth were proportional to the amount of head rotation. When the head was rotated to the right, constant errors in azimuth were greater during pointing towards right than left targets. Similarly, they were greater for left than for right stimuli when the head was rotated to the left. Errors in amplitude were not influenced by the direction nor the amount of head rotation. Finally, a decrease in the directional bias took place within blocks of trials. These results indicate that head position signals are used during the process of transforming motor coordinates from the visual to the pro-prioceptive system of reference.     

Misdirections in slow goal-directed arm movements and pointer-setting tasks

Summary Information about the direction of the virtual line between two positions in space (directional information) is used in many decision-making and motor tasks. We investigated how accurately directional information is processed by the brain. Subjects performed two types of task. In both tasks they sat at a table. In the first task they had to move their hand slowly and accurately from an initial position 40 cm in front of them to visually presented targets at a distance of 30 cm from the initial position (movement task). We analysed the initial movement direction. In the second task subjects had to position pointers in the direction of the targets as accurately as they could (perceptive task). We found that in the movement task the subjects started the movements to most targets in a direction that deviated consistently from the direction of the straight line between initial position and target position. The maximum deviation ranged from 5–10° for the various subjects. The mean standard deviation was 4°. In the perceptive task the subjects positioned the pointer in similarly deviating directions. Furthermore, we found that the maximum deviation in the pointer direction depended on the length of the pointer: the smaller the pointer, the larger the consistent deviations in the pointer direction. The shortest pointer showed deviations comparable to the deviations found in the movement task. These findings suggest that the deviations in the two tasks stem from the same source.     

Adjustments of fast goal-directed movements in response to an unexpected inertial load

Summary Subjects made fast goal-directed elbow flexion movements against an inertial load. Target distance was 8 or 16 cm, randomly chosen. To exert a force in the direction of the movement subjects had to activate flexors of both shoulder and elbow, but shoulder flexors did not change appreciably in length during the movement. In 20% of the trials the inertial load was increased or decreased without knowledge of the subjects. Until 90–110 ms after the onset of the agonist muscle activity (about 65–85 ms after the start of movement) EMG activity was very similar in all conditions tested. The changes that occured in the EMG from that moment on were effectively a later cessation of the agonist activity and a later start of the antagonist activity if the load was increased unexpectedly. If the load was reduced unexpectedly, the agonist activity ceased earlier and the antagonist activity began earlier. The latency at which EMGs started to change was the same for muscles around shoulder and elbow, for agonists and antagonists and for both distances. All adjustments had the same latency (37 ms) relative to the point where the angular velocity of the elbow in the unexpectedly loaded movements differed by 0.6 rad/s from the expected value. We discuss why simple reflex- or servo-mechanisms cannot account for the measured EMG changes. We conclude that appropriate adjustments of motor programmes for fast goal-directed arm movements start within 40 ms of the detection of misjudgment of load.     

The relative contribution of retinal and extraretinal signals in determining the accuracy of reaching movements in normal subjects and a deafferented patient

This experiment investigated the relative extent to which different signals from the visuo-oculomotor system are used to improve accuracy of arm movements. Different visuo-oculomotor conditions were used to produce various retinal and extraretinal signals leading to a similar target amplitude: (a) fixating a central target while pointing to a peripheral visual target, (b) tracking a target through smooth pursuit movement and then pointing to the target when its excursion ceased, and (c) pointing to a target reached previously by a saccadic eye movement. The experiment was performed with a deafferented subject and control subjects. For the deafferented patient, the absence of proprioception prevented any comparison between internal representations of target and limb (through proprioception) positions during the arm movement. The deafferented patient's endpoint therefore provided a good estimate of the accuracy of the target coordinates used by the arm motor system. The deafferented subject showed relatively good accuracy by producing a saccade prior to the pointing, but large overshooting in the fixation condition and undershooting in the pursuit condition. The results suggest that the deafferented subject does use oculomotor signals to program arm movement and that signals associated with fast movements of the eyes are better for pointing accuracy than slow ramp movements. The inaccuracy of the deafferented subject when no eye movement is allowed (the condition in which the controls were the most accurate) suggests that, in this condition, a proprioceptive map is involved in which both the target and the arm are represented.     

Prism adaptation with delayed visual error signals in the monkey

Errors in reaching produced by displacing the visual field with wedge prisms decrease with trials, even when the error is not revealed until the completion of the movement. To examine how much additional delay in visual feed-back the monkey can compensate for, the effects of delaying the visual error signals were studied by presenting the terminal visual images after one of five delays, ranging from 0 to 500 ms. Adaptation was fastest when the delay was 0 or 10 ms, decreased significantly with a delay as small as 50 ms and approached zero when the delay was 500 ms. The size of the after-effect decreased with the delay accordingly. The results indicate that prism adaptation in the monkey critically depends on the availability of visual information within 50 ms of completion of the movement. Comparing the results with those for humans, we suggest that monkey and human share a mechanism of adaptation with a short time window of 50 ms, but the monkey lacks another mechanism of adaptation that allows a visual delay of 500 ms or more in humans.     

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     

Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements

Summary The visual properties of 77 dorsolateral pontine nucleus (DLPN) cells were studied in two alert monkeys. In 41 cells, presentation of a moving random dot background pattern, while the monkeys fixated a stationary spot, elicited modulations in discharge rate that were related either to (i) the velocity of background motion in a specific direction or to (ii) only the direction of background movement. Thirty-six DLPN cells exhibited responses to small, 0.6–1.7 deg, visual stimuli. Nine such cells exhibited non-direction selective receptive fields that were eccentric from the fovea. During fixation of a stationary bluish spot, the visual responses of 27 DLPN cells to movement of a small, white test spot were characterized by two components: (1) as the test spot crossed the fovea in a specific direction, transient velocity-related increases in discharge rate occurred and (2) a maintained, smaller increase in activity was observed for the duration of test spot movement in the preferred direction. This DLPN activity associated with small visual stimuli was also observed during smooth-pursuit eye movements when, due to imperfect tracking, retinal image motion of the target produced slip in the same direction. These preliminary results suggest that the DLPN could supply the smooth-pursuit system with signals concerning the direction and velocity of target image motion on the retina.This study was supported by NSF Grant BNS-8107111, NIH Grant R01 EY04552-01, and the Smith-Kettlewell Eye Research Foundation Dedication. This paper is dedicated to Dr. Kitsuya Iwama, Emeritus Professor of Osaka University Medical School, on his retirement. The first author is grateful for the inspiration and guidance that Dr. Iwama provided during the early part of the author's education in neurophysiology.     

Interaction of extraretinal eye position signals in a double-step saccade task: psychophysical estimation

The time course of extraretinal eye position signals (EEPSs) for visually guided saccades made successively with a short intersaccadic interval was estimated on the basis of perceptual errors in localizing a visual target flashed between the two saccades. The EEPSs for the first and the second saccades were shown to interact in a specific way when the intersaccadic interval was short. The pattern of interaction depended on the direction of the second saccade. It is suggested that when the second saccade was made in the opposite direction to the first saccade, the EEPS for the first saccade was interrupted before its completion in preparation for the onset of the second saccade. When the two saccades were made in the same direction, the EEPS for the first saccade developed more quickly than in a single-saccade condition. the results are discussed in relation to the findings of recent neurophysiological studies.     

Adaptation of sound localization induced by rotated visual feedback in reaching movements

A visuo-motor adaptation task was used to investigate the effects of this adaptation on the auditory-motor representation during reaching movements. We show that, following exposure to a rotated screen cursor-hand relationship, the movement paths during auditory conditions exhibited a similar pattern of aftereffects as those observed during movements to visual targets, indicating that the newly formed model of visuo-motor transformations for hand movement was available to the auditory-motor network for planning the hand movements. This plasticity in human sound localization does not require active cross-modal experience, and retention tests indicated that the newly formed internal model does not reside primarily within the central auditory system as suggested in past studies examining the plasticity of sound localization to distorted spatial vision.     

Response of cat retinal ganglion cells to motion of visual texture

Summary Responses of retinal ganglion cells to motion of large fields of visual texture were recorded in the lightly anaesthetised, immobilized cat. Brisk sustained and brisk transient, on- or off-centre, units gave a modulated response to texture motion. The pattern of temporal modulation of the response was dependent upon the particular configuration (sample) of texture crossing the receptive field. The magnitude of the response depended on the size of the receptive field centre. For all units, whether sustained or transient the magnitude of response to a textured field of fixed angular subtense declined as centre-diameter increased from 0.9 deg. For brisk units the response magnitude levelled off for centre sizes smaller than 0.9 deg. Responses to texture were confined spatially to the region of the receptive field, and the overall characteristics of this response were due to interactions between the centre and surround mechanisms of the receptive field. In brisk transient units, no evoked response was evident when texture motion was confined to regions well away from the receptive field of the unit, i.e. no periphery or shift effect could be demonstrated. The results support previous suggestions that the differential sensitivity to texture motion evident in cortical neurones must be due to intra-cortical processing.Supported by Project Grant G978/558/N from the Medical Research Council     

A developmental study of retinal afferents and visual responses in the cat pretectum

Summary Neuronal responses in the pretectum (PT) were analyzed in 4–16 week old kittens after visual and electrical stimulation and compared with adult responses from a previous study. All three retinal fiber types projecting to the adult PT could be electrically activated in kittens from 4 weeks on. There was a dramatic reduction of response latencies to electric shocks to retinal afferents applied at the optic chiasm (OX) and optic tract (OT) in postsynaptic cells as a function of age, involving X-, Y-, and Wfibers. At four through six weeks postnatally the reduction in latency was found to be due to enhanced signal transmission at the axonal terminal region. Latency reduction continued after six weeks of life due to sharp increases in conduction velocity of the afferent fibers. Different steps in the maturation of visual response specifity were found for neurons of different functional types. Possible relationships are discussed between the development of neuronal responses of pretectal cells and the maturation of oculomotor behavior.     

Differential influence of the visual framework on end point accuracy and trajectory specification of arm movements

In this study the influence of visual scene on both arm end point accuracy and spatial path kinematics was evaluated. Eight subjects, immersed in a virtual environment, were required to point to one of ten targets located at two distances and in five directions. Targets were presented in frameworks of different complexity. The simplest framework was constituted by a uniform background, the most complex framework was constituted by a perspective-arranged grid. In the other two conditions it consisted of lines having a direction parallel to either the subject's sagittal or frontal body axis. Movements were executed without vision of both target and framework. The results showed that pointing movements were hypometric in all conditions. No difference in end point localization was observed between movements executed after presentation of the simplest and the most complex scenes. However, hypometria significantly increased when the scene was formed by lines parallel to the subject's sagittal axis. Visual information on the scene was also used to specify hand path parameters. Trajectory curvature increased with decreasing complexity of the framework. Correspondingly, the pointing kinematics varied. Taken together, these results suggest that visual analysis of cues surrounding the target can influence both target localisation and hand path planning. However, scene complexity is directly related only to determining trajectory curvature. We conclude that planning an arm movement consists of at least two processes: target localisation and hand path specification. Environmental visual cues forming the scene are taken into account differently during the two processes.     

Impairment of extraretinal eye position signals after central thalamic lesions in humans

Accuracy of four different types of memory-guided saccades was studied in two patients with a small central thalamic lesion, probably involving the region of the internal medullary lamina (IML), and in a control group. In the first paradigm, the eyes and head remained immobile between the time of the presentation of the visual target to be remembered and the memory-guided saccade. In the other three paradigms, the eyes were displaced during the same period (before the memory-guided saccade) by either visually-guided saccades, a smooth pursuit eye movement or a body movement (with vestibulo-ocular reflex suppression). Therefore, in these three paradigms, the initial eye displacement required the use of extraretinal eye position to produce accurate memory-guided saccades. Compared with the control group, the two patients had normal accuracy in the first memory-guided saccade paradigm, in which there was no initial eye displacement, but markedly impaired saccade accuracy in the other three paradigms. These results suggest that the cortical areas triggering saccades did not receive correct extraretinal eye position signals. They are consistent with an impairment of the efference copy, which could be distributed to the cortical ocular motor areas by the IML.     

On-line vs. off-line utilization of peripheral visual afferent information to ensure spatial accuracy of goal-directed movements

Manual aiming movements are often initiated when one gazes at the target, while the hand is seen in peripheral vision. The objective of the present study was to determine whether vision of ones hand in peripheral vision and/or central vision as it progresses towards the target can be used to modulate the direction and the extent components of the initial movement impulse. Participants performed video aiming movements while vision of the cursor they were moving was permitted for its whole trajectory, 40° to 15° of visual angle, 15° to 0° of visual angle, or not visible at all. Movements were to be completed within prescribed movement times varying between 300 ms and 900 ms. The results did not reveal endpoint accuracy or variability differences between the 40°–15° and the 15°–0° visual feedback conditions. Both conditions yielded lower endpoint bias and variability than the no-vision condition from early on after movement initiation. This indicates that the visual afferent information available in the 40°–15° and the 15°–0° visual feedback conditions could be used to better plan upcoming movements than the no vision condition. From these data, it appears very unlikely that different portions of the retina are specialized for processing different movement attributes as has been suggested in the past (Paillard 1980; Paillard and Amblard 1985). Both the peripheral and central retina are apt at detecting on-line extent and direction errors in ones movement. In addition, the data cast serious doubts on the widely accepted proposition that the movement initial impulse is essentially ballistic.     

Striatal neuronal activity during the initiation and execution of hand movements made in response to visual and vibratory cues

Summary Recordings were obtained from 146 neurons in the neostriatum of rhesus monkeys while they performed wrist movements in response to visual and vibratory cues. Of these, 75 putamen and 29 caudate neurons exhibited changes in firing rate that were temporally related to the onset of the wrist movements and that began prior to movement onset. This premovement activity (PMA) usually was directionally specific, in that the magnitude or direction of change in firing rates was different during flexion trials as compared to trials involving wrist extension. PMA onset usually preceded movement onset by more than 100 ms and in most instances preceded the average onset of task-related changes in electromyographic (EMG) activity in muscles of the wrist and forelimb. For most neurons. the changes in neuronal activity that began prior to movement were maintained during movement execution. However, approximately one-third of the neurons that exhibited PMA changed their firing rate in the opposite direction, relative to their PMA and to their baseline rate of activity, once the movement began. Several other neurons either exhibited PMA only or they altered their discharge rates during movement execution but did not exhibit PMA. These observations suggest that, despite the close temporal relationship between the onset of PMA and the onset of wrist movement, the neuronal mechanisms mediating the PMA may differ from those that occur during movement execution. The PMA onset of neostriatal neurons occurred earlier in visually cued than in vibratory cued trials. These differences were statistically significant only for flexion trials, however, in which movements were made against a load and in the same direction as the palmar vibratory stimulus. For trials involving wrist extension, PMA onsets for visually cued as compared with vibratory cued trials were not statistically different. These findings contrast with data obtained previously from somatosensory cortical neurons during performance of the same behavioral task. On average, PMA in the putamen began earlier, relative to movement onset, than it did in the somatosensory cortex. Moreover, in the somatosensory cortex, PMA onset occurred earlier in vibratory cued than in visually cued trials, irrespective of movement direction (Nelson 1988; Nelson and Douglas 1989). For putamen neurons, but not for caudate or cortical neurons, the onset of PMA also occurred significantly earlier during extension trials than flexion trials, irrespective of the modality of the go-cue. These modality-dependent and direction-dependent differences in the PMA onset of neostriatal neurons may reflect the responsiveness of these neurons to somatosensory inputs (e.g., load conditions and vibratory stimulation) that were associated with the behavioral task. These data confirm observations made by other investigators that a substantial proportion of neurons in the putamen exhibit movement-related changes in discharge rate that are initiated prior to task-related changes in EMG activity, and they further suggest that this PMA may be initiated sufficiently early to influence even the earliest task-related activity of cortical neurons.     

The influence of motion signals in hand movements

It has been shown that motion after-effects (MAE) may affect the perceived position of moving objects and, more recently, that MAE signals can also affect pursuit eye movements: smooth pursuit eye movements are favoured by the illusory motion percept that is caused by motion adaptation. Here we investigated the relationship between MAE and arm movements. The objective of our research was: (1) to analyze possible effects of MAE when the arm tracks the changing position of a moving object, and (2) to investigate the influence of MAE on pointing movements to both static and moving targets. Our results show that the (unseen) hand position was trailing the target much less when target and MAE direction was the same. At the end of manual pursuit, subjects caught up with the moving target. However, when target direction was opposite the MAE, subjects’ hands moved more slowly, causing larger lags between the target and the hand position (Experiment 1). In Experiment 2, we found a similar effect of motion signals when subjects pointed to a moving target but found no effect of MAE when pointing to a static object (Experiment 3). We conclude that the effect of motion signals is only revealed when we need to update the changing position of a target.