Memory pointing in children and adults: dissociations in the maturation of spatial and temporal movement parameters

In previous studies a systematic directional error (the “motor oblique effect”) was found in 2D memory pointing movements of healthy adults. In this study we extend these observations to observe that healthy children displayed the same motor oblique effect. In contrast other spatial and temporal movement parameters (mean amplitude error, square directional and amplitude error, latency and the time to maximum velocity) changed with increasing age. Memory delay increased the square directional and amplitude error independent of age. Finally failure of movement inhibition during the delay was more frequent in children compared to adults. These results favor the hypothesis that the motor oblique effect related to perceptual processing biases is constant from childhood while other movement parameters are modulated by age reflecting the continuing optimization of motor control from childhood to adulthood. The dissociation of memory and age effects suggests that motor working memory is already mature in young children.     

"Motor oblique effect": perceptual direction discrimination and pointing to memorized visual targets share the same preference for cardinal orientations

In previous studies we observed a pattern of systematic directional errors when humans pointed to memorized visual target locations in two-dimensional (2-D) space. This directional error was also observed in the initial direction of slow movements toward visual targets or movements to kinesthetically defined targets in 2-D space. In this study we used a perceptual experiment where subjects decide whether an arrow points in the direction of a visual target in 2-D space and observed a systematic distortion in direction discrimination known as the "oblique effect." More specifically, direction discrimination was better for cardinal directions than for oblique. We then used an equivalent measure of direction discrimination in a task where subjects pointed to memorized visual target locations and showed the presence of a motor oblique effect. We finally modeled the oblique effect in the perceptual and motor task using a quadratic function. The model successfully predicted the observed direction discrimination differences in both tasks and, furthermore, the parameter of the model that was related to the shape of the function was not different between the motor and the perceptual tasks. We conclude that a similarly distorted representation of target direction is present for memorized pointing movements and perceptual direction discrimination.     

The effects of increasing memory load on the directional accuracy of pointing movements to remembered targets

The directional accuracy of pointing arm movements to remembered targets in conditions of increasing memory load was investigated using a modified version of the Sternbergs context-recall memory-scanning task. Series of 2, 3 or 4 targets (chosen randomly from a set of 16 targets around a central starting point in 2D space) were presented sequentially, followed by a cue target randomly selected from the series excluding the last one. The subject had to move to the location of the next target in the series. Correct movements were those that ended closer to the instructed target than any other target in the series while all other movements were considered as serial order errors. Increasing memory load resulted in a large decrease in the directional accuracy or equivalently in the directional information transmitted by the motor system. The constant directional error varied with target direction in a systematic fashion reproducing previous results and suggesting the same systematic distortion of the representation of direction in different memory delay tasks. The constant directional error was not altered by increasing memory load, contradicting our hypothesis that it might reflect a cognitive strategy for better remembering spatial locations in conditions of increasing uncertainty. Increasing memory load resulted in a linear increase of mean response time and variable directional error and a non-linear increase in the percentage of serial order errors. Also the percentage of serial order errors for the last presented target in the series was smaller (recency effect). The difference between serial order and directional spatial accuracy is supported by neurophysiological and functional anatomical evidence of working memory subsystems in the prefrontal cortex.This work was supported by internal funding from Aeginition University Hospital     

Amplitude and direction errors in kinesthetic pointing

We investigated the accuracy with which, in the absence of vision, one can reach again a 2D target location that had been previously identified by a guided movement. A robotic arm guided the participants hand to a target (locating motion) and away from it (homing motion). Then, the participant pointed freely toward the remembered target position. Two experiments manipulated separately the kinematics of the locating and homing motions. Some robot motions followed a straight path with the bell-shaped velocity profile that is typical of natural movements. Other motions followed curved paths, or had strong acceleration and deceleration peaks. Current motor theories of perception suggest that pointing should be more accurate when the homing and locating motion mimics natural movements. This expectation was not borne out by the results, because amplitude and direction errors were almost independent of the kinematics of the locating and homing phases. In both experiments, participants tended to overshoot the target positions along the lateral directions. In addition, pointing movements towards oblique targets were attracted by the closest diagonal (oblique effect). This error pattern was robust not only with respect to the manner in which participants located the target position (perceptual equivalence), but also with respect to the manner in which they executed the pointing movements (motor equivalence). Because of the similarity of the results with those of previous studies on visual pointing, it is argued that the observed error pattern is basically determined by the idiosyncratic properties of the mechanisms whereby space is represented internally.     

Hand and joint paths during reaching movements with and without vision

 This study examines whether the kinematics of pointing movements are altered by the sensory systems used to select spatial targets and to guide movement. Hand and joint paths of visually guided reaching movements of human subjects were compared with two non-visual conditions where only proprioception was available: (1) movements of the same subjects with blindfolds, and (2) movements by congenitally blind subjects. While hand-path curvatures were overall quite small, sighted subjects wearing a blindfold showed a statistical increase in hand-path curvature compared with their visually guided movements. Blindfolded subjects also showed greater hand-path curvature than blind subjects. These increases in hand-path curvature for blindfolded subjects did not always lead to a decrease in joint-path curvature. While there were differences between blind subjects and sighted subjects using vision for some movement directions, there was no systematic difference between these two groups. The magnitude of joint-path curvature showed much greater variation than hand-path curvature across the movement directions. We found variation in joint-path curvature to be correlated to two factors, one spatial and one geometrical. For all subject groups, joint-path curvature tended to be smaller for sagittal-plane movements than for transverse or diagonal movements. As well, we found that the magnitude of joint-path curvature was also related to the relative motion at each joint. Joint-path curvature tended to increase when movements predominantly involved changes in shoulder angle and was minimal when movements predominantly involved elbow motion. The consistently small curvatures of hand trajectory across blind and sighted subjects emphasize the powerful tendency of the motor system to generate goal-directed reaching movements with relatively straight hand trajectories, even when deprived of visual feedback from very early in life. Received: 16 July 1997 / Accepted: 20 May 1998     

No automatic pilot for visually guided aiming based on colour

It has been claimed that visually guided limb movements are automatically corrected in response to a change in target location but not when the same change in target is cued through a colour switch (Pisella et al. 2000). These findings were based solely on limb endpoint data. Here we examine the kinematic trajectory of the hand during the entire movement. Participants pointed rapidly to a target object that could change position either by changing spatial location, or by switching colour with a second object. Participants performed in two instructional conditions: a "go" condition to index intentional movements and a "stop" condition in which failures to stop pointing indexed automatic limb guidance. Kinematic analysis indicated efficient intentional pointing in both location and colour change conditions. However, only targets that changed spatial location elicited involuntary limb modifications and these occurred within 150 ms of the change. This conclusion held even after baseline differences in the efficiency of processing colour-defined targets were taken into account, thereby strengthening the claim of a strongly automatic pilot for visually guided limb movements.     

Preparatory activity in motor cortex reflects learning of local visuomotor skills

In humans, learning to produce correct visually guided movements to adapt to new sensorimotor conditions requires the formation of an internal model that represents the new transformation between visual input and the required motor command. When the new environment requires adaptation to directional errors, learning generalizes poorly to untrained locations and directions, indicating that such learning is local. Here we replicated these behavioral findings in rhesus monkeys using a visuomotor rotation task and simultaneously recorded neuronal activity. Specific changes in activity were observed only in a subpopulation of cells in the motor cortex with directional properties corresponding to the locally learned rotation. These changes adhered to the dynamics of behavior during learning and persisted between learning and relearning of the same rotation. These findings suggest a neural mechanism for the locality of newly acquired sensorimotor tasks and provide electrophysiological evidence for their retention in working memory.     

The brain uses efference copy information to optimise spatial memory

Does a motor response to a target improve the subsequent recall of the target position or can we simply use peripheral position information to guide an accurate response? We suggest that a motor plan of the hand can be enhanced with actual motor and efference copy feedback (GoGo trials), which is absent in the passive observation of a stimulus (NoGo trials). To investigate this effect during eye and hand coordination movements, we presented stimuli in two formats (memory guided or visually guided) under three modality conditions (eyes only, hands only (with eyes fixated), or eyes and hand together). We found that during coordinated movements, both the eye and hand response times were facilitated when efference feedback of the movement was provided. Furthermore, both eye and hand movements to remembered locations were significantly more accurate in the GoGo than in the NoGo trial types. These results reveal that an efference copy of a motor plan enhances memory for a location that is not only observed in eye movements, but also translated downstream into a hand movement. These results have significant implications on how we plan, code and guide behavioural responses, and how we can optimise accuracy and timing to a given target.     

Neural activity correlated with the preparation and execution of visually guided arm movements in the cingulate motor area of the monkey

Recent anatomical and physiological studies have suggested that parts of the cingulate cortex are involved in the control of movement. These areas have been collectively termed the cingulate motor area (CMA). Currently almost nothing is known, however, about how neurons in the CMA actually participate in the control of movement. Therefore, we investigated the role of cells in the dorsal and ventral banks of the CMA (CMAd and CMAv, respectively) in the preparation and execution of visually guided arm movements. We recorded the activity of neurons while a monkey performed a visually guided, two-dimensional instructed delay task. A monkey was required to operate a joystick that moved a cursor from a centrally located hold target to one of four peripheral targets. Neurons were classified as exhibiting preparatory activity if the neural discharge during the postinstruction delay period was significantly higher than the preinstruction activity. Neurons were classified as exhibiting movement activity if the neural discharge was significantly elevated around the time of the movement. Of the 115 task-related neurons studied, 18 (16%) exhibited only preparatory activity, 48 (42%) exhibited only movement activity, and 49 (43%) exhibited both preparatory and movement activity. Neurons were further classified in terms of their directional tuning. For 51% of neurons with preparatory activity, that activity was directional. A significantly larger proportion of movement-related activity was directional (78%). For neurons with both directional preparatory and movement activity, the preferred directions were highly correlated (r=0.83). The median onset of movement activity was 10 ms before the beginning of movement (range -200 to 200 ms). The patterns and directionality of task-related activity of CMA neurons observed in this study are similar to those previously reported for other cortical motor areas. Together, these data provide preliminary evidence that neurons in CMAd and CMAv play a role in both the preparation and execution of visually guided arm movements.     

l-Dopa induces under-damped visually guided motor responses in Parkinson’s disease

Parkinson’s disease preferentially affects internally generated movements, e.g., movements recalled from memory, while externally cued movements are relatively preserved. However, l-dopa may have effects on visually guided movements as well as error-related processing. Fourteen Parkinson’s disease (PD) subjects (on and off l-dopa medication) as well as ten normal controls performed a tracking task using a joystick. During discrete 30 s blocks, the visual feedback of the actual tracking errors were attenuated, amplified or unaltered. Second order dynamical system models, with the desired trajectory as the input and the actual motor performance as the output, were used to characterize the motor performance by the each subject under each condition. Although the overall root-mean-square tracking error did not significantly differ between groups, the nature of the motor performance differed significantly across groups. A clear dissociation was made between manipulations of error feedback—which altered the natural frequency of the models—and the effects of l-dopa, which affected damping. Compared to normal controls, PD subjects were significantly overdamped before medication and underdamped after medication. We interpret our results as being suggestive of l-dopa normalization of compensatory overactive cerebellar activity in PD.     

Touch responses made to remembered and visual target locations in the dark: a human psychophysical study

Saccadic eye movements made to remembered locations in the dark show a distinct up-shift in macaque monkey, and slight upward bias in humans (Gnadt et al. 1991). This upward bias created in the visual spatial mapping of a saccade may be translated downstream in a hand/touch movement. This error could possibly reveal (a) information about the frames of reference used in each scenario and (b) the sources of this error within the brain. This would suggest an early planning stage if they are shared, or a later stage if the errors are distinct. Methods: Eight human subjects performed touch responses to a touch screen monitor to both visual and remembered target locations. The subjects used a high-resolution touch-screen monitor, a bite bar and chin-rest for restricting head movements during responses. All target locations were 20° vectors from the central starting position in horizontal, vertical and oblique planes of motion. Results: Subjects were accurate to both visual and remembered target locations with little variance. Subject means showed no significant differences between control and memory trials; however, a distinct asymmetry was observed between cardinal and oblique planes during memory trials. Subjects consistently made errors to oblique locations during touches made to the remembered location that was not evident in control conditions. This error pattern revealed a strong hypermetric tendency for oblique planes of touches made to a remembered location.     

Fixation offset facilitates saccades and manual reaching for single but not multiple target displays

Turning off a fixation point, typically for 200 ms, before the onset of a peripheral target substantially reduces saccadic reaction times. This facilitatory effect generated by an inserted temporal gap between fixation offset and the target appearance is called the “gap” effect [J Opt Soc Am 57:1030–1033, 1967]. We show that the gap reduces the initial latency of both saccades and manual pointing in single and multiple target displays. Yet, in multiple target displays, the gap increased the movement duration because eye or hand movements were frequently misdirected toward distractors so that the trajectory had to be corrected. Thus, in spite of the shortened latency, the total time for trial completion was not shortened in multiple target displays, whereas it was reduced in single target displays. This selective gap effect for a single target was not restricted to goal-directed motor tasks because perceptual discrimination tasks, where no motor response is required, also demonstrated the gap effect only for single target displays. Our results suggest that the gap may facilitate attentional disengagement, but it does not help target selection in motor and perceptual discrimination tasks, where the allocation of attention to the target is required.     

Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment

To execute visually guided reaching movements, the central nervous system (CNS) must transform a desired hand trajectory (kinematics) into appropriate muscle-related commands (dynamics). It has been suggested that the CNS might face this challenging computation by using internal forward models for the dynamics. Previous work in humans found that new internal models can be acquired through experience. In a series of studies in monkeys, we investigated how neurons in the motor areas of the frontal lobe reflect the movement dynamics and how their activity changes when monkeys learn a new internal model. Here we describe the results for the supplementary motor area (SMA-proper, or SMA). In the experiments, monkeys executed visually guided reaching movements and adapted to an external perturbing force field. The experimental design allowed dissociating the neuronal activity related to movement dynamics from that related to movement kinematics. It also allowed dissociating the changes related to motor learning from the activity related to motor performance (kinematics and dynamics). We show that neurons in SMA reflect the movement dynamics individually and as a population, and that their activity undergoes a variety of plastic changes when monkeys adapt to a new dynamic environment.     

Visual control of reaching movements without vision of the limb

The spatial and temporal organization of hand and eye movements were studied in normal human subjects as they pointed toward small visual targets. The experiment was designed to assess the role of information about target position in correcting the trajectory of the hand when view of the hand was not available. To accomplish this, the duration of target presentation was systematically varied across blocks of trials. The results of this experiment showed that pointing movements were about 3 times more accurate when the target was present throughout the entire pointing movement, than when the target disappeared shortly after the hand movement had begun. These data indicate that pointing movements made without view of the limb are not purely preprogrammed but instead, are corrected during their execution. These modifications to the motor program are smoothly integrated into the ongoing movement and must depend upon comparing visual information about the position of the target with nonvisual information about the position of the limb. The source of this non-visual information was not directly established in the present experiment but presumably must be derived from kinesthetic reafferences and/or efference copy.     

Direct evidence for the contribution of the superior colliculus in the control of visually guided reaching movements in the cat

The production of visually guided reaching movements relies on a large neural network. Based on indirect experimental evidence, it has been suggested that the superior colliculus, a subcortical centre known for its key role in controlling rapid orienting gaze shifts, also belongs to this network. The aim of the present study was to investigate the role of the cat superior colliculus (SC) in the control of visually guided reaching movements. To address this issue, we studied the effect of SC electrical stimulation on forelimb reaching movements in two cats trained to catch a piece of food. Electrical stimulation delivered just after the movement onset yielded a consistent perturbation of the movement trajectory of the forelimb extremity. This perturbation followed stimulation onset by 56 ± 11 ms on average, and consisted of a deviation of the spatial path and a deceleration of the movement. The forelimb perturbation was elicited in the absence of concomitant gaze or head displacement in 52% of the stimulation trials. Forelimb perturbations were followed by in-flight adjustments so that reaching movements reliably ended on the target. The present results constitute the first behavioural evidence for a contribution of the cat SC to the control of visually guided forelimb movements.     

The time course of online trajectory corrections in memory-guided saccades

Recent investigations have revealed the kinematics of horizontal saccades are less variable near the end of the trajectory than during the course of execution. Converging evidence indicates that oculomotor networks use online sensorimotor feedback to correct for initial trajectory errors. It is also known that oculomotor networks express saccadic corrections with decreased efficiency when responses are made toward memorized locations. The present research investigated whether repetitive motor timekeeping influences online feedback-based corrections in predictive saccades. Predictive saccades are a subclass of memory-guided saccades and are observed when one makes series of timed saccades. We hypothesized that cueing predictive saccades in a sequence would facilitate the expression of trajectory corrections. Seven participants produced a number of single unpaced, visually guided saccades, and also sequences of timed predictive saccades. Kinematic and trajectory variability were used to measure the expression of online saccadic corrections at a number of time indices in saccade trajectories. In particular, we estimated the minimum time required to implement feedback-based corrections, which was consistently 37 ms. Our observations demonstrate that motor commands in predictive memory-guided saccades can be parameterized by spatial working memory and retain the accuracy of online trajectory corrections typically associated with visually guided behavior. In contrast, untimed memory-guided saccades exhibited diminished kinematic evidence for online corrections. We conclude that motor timekeeping and sequencing contributed to efficient saccadic corrections. These results contribute to an evolving view of the interactions between motor planning and spatial working memory, as they relate to oculomotor control.     

Participation of the cerebellar dentate nucleus in the control of a goal-directed movement in monkeys

Summary Experiments carried out on seven adult baboons were addressed at specifying the participation of the cerebellar dentate nucleus (DN) in the control of duration and accuracy of a goal-directed movement. The visuo-motor task used in this experiment involved trained pointing movement towards stationary target.The monkeys trained to point with the index finger to a target light were required to perform stereotyped movements of constant amplitude and direction, or movements with variable amplitude and direction. Duration of response execution was measured by movement time and accuracy by terminal spatial errors. We analysed the effects of excluding the DN on the arm ipsilateral or contralateral to the partially inactivated nucleus.Two techniques have been used to impair the DN activity: in three monkeys the structure was reversibly cooled with a chronically implanted thermode; in four others partial electrolytic destruction of the DN was performed.In the arm ipsilateral to the lesioned DN we observed modifications of movement times, appearance of systematic errors with increased dispersion. Contralateral effects were restricted to movement times. Changes in movement times and spatial errors were studied over time (4 months) in permanently lesioned animals. Only the spatial dispersion presented a total recovery.These data show that the DN is concerned with the control of speed and accuracy during the execution of visually triggered movements in monkeys. Moreover comparison of results concerning ipsilateral and contralateral effects of DN dysfunction on movement times and errors, and evidence of different time course of recovery in these variables, suggest a differential control exerted by the DN on speed and accuracy of goal directed movements.This work was in part supported by CNRS Grants and INSERM Grants (ATP 80.79.112, CRL 75.4.346.6)     

Internalizing agency of self-action: perception of one's own hand movements depends on an adaptable prediction about the sensory action outcome

Extensive work on learning in reaching and pointing tasks has demonstrated high degrees of plasticity in our ability to optimize goal-directed motor behavior. However, studies focusing on the perceptual awareness of our own actions during motor adaptation are still rare. Here we present the first simultaneous investigation of sensorimotor adaptation on both levels, i.e., action and action perception. We hypothesized that self-action perception relies on internal predictions about the sensory action outcome that are updated in a way similar to that of motor control. Twenty human subjects performed out-and-back pointing movements that were fed back visually. Feedback was initially presented in spatiotemporal correspondence with respect to the actual finger position, but later rotated by a constant angle. When distorted feedback was applied repetitively, subjects' perceived pointing direction shifted in the direction of the trajectory rotation. A comparable perceptual reinterpretation was observed in control trials without visual feedback, indicating that subjects learned to predict the new visual outcome of their actions based on nonvisual, internal information. The perception of the world, however, remained unchanged. The changes in perception of one's own movements were accompanied by adaptive changes in motor performance of the same amount, i.e., a secondary motor compensation opposite to the direction of the imposed visual rotation. Our results show that the perception of one's own actions depends on adaptable internal predictions about the sensory action outcome, allowing us to attribute new sensory consequences of our actions to our own agency. Furthermore, they indicate that the updated sensory prediction can be used to optimize motor control.     

Perceptual distortion contributes to the curvature of human reaching movements

Unconstrained point-to-point human arm movements are generally gently curved, a fact which has been used to assess the validity of models of trajectory formation. In this study we examined the relationship between curvature perception and movement curvature for planar sagittal and transverse arm movements. We found a significant correlation (P<0.0001, n=16) between the curvature perceived as straight and the curvature of actual arm movements. We suggest that subjects try to make straight-line movements, but that actual movements are curved because visual perceptual distortion makes the movements appear to be straighter than they really are. We conclude that perceptual distortion of curvature contributes to the curvature seen in human point-to-point arm movements and that this must be taken into account in the assessment of models of trajectory formation.     

Reference frame conversions for repeated arm movements

The aim of this study was to further understand how the brain represents spatial information for shaping aiming movements to targets. Both behavioral and neurophysiological studies have shown that the brain represents spatial memory for reaching targets in an eye-fixed frame. To date, these studies have only shown how the brain stores and updates target locations for generating a single arm movement. But once a target's location has been computed relative to the hand to program a pointing movement, is that information reused for subsequent movements to the same location? Or is the remembered target location reconverted from eye to motor coordinates each time a pointing movement is made? To test between these two possibilities, we had subjects point twice to the remembered location of a previously foveated target after shifting their gaze to the opposite side of the target site before each pointing movement. When we compared the direction of pointing errors for the second movement to those of the first, we found that errors for each movement varied as a function of current gaze so that pointing endpoints fell on opposite sides of the remembered target site in the same trial. Our results suggest that when shaping multiple pointing movements to the same location the brain does not use information from the previous arm movement such as an arm-fixed representation of the target but instead mainly uses the updated eye-fixed representation of the target to recalculate its location into the appropriate motor frame.