A dissociation between visual and motor workspace inhibits generalization of visuomotor adaptation across the limbs

We have previously shown that the pattern of interlimb transfer following visuomotor adaptation depends on whether the two arms share task-space at a given workspace location: when the two arms adapted to a novel visuomotor rotation in unshared, lateral workspaces, transfer of movement direction information occurred symmetrically (i.e., from dominant to nondominant arm, and vice versa). When the two arms shared the same task-space, however, transfer of the same information became asymmetric (i.e., only from dominant to nondominant arm). In the present study, I investigated the effect of a conflict between visual and proprioceptive information of task-space on the pattern of interlimb transfer, by dissociating visual and motor workspaces. I hypothesized that the pattern of interlimb transfer would be determined by the way the motor control system uses available sensory information, and predicted that depending on whether the system relied more on vision or proprioception, transfer would occur either symmetrically or asymmetrically. Surprisingly, the results indicated that despite substantial adaptation to a novel visuomotor rotation, no transfer occurred across the arms when the visual and motor workspaces were dissociated in space. Based on this finding, I suggest that when a conflict exists between visual and proprioceptive information with respect to the sharing of the given task-space by the two arms, it interferes with executive decisions made by the motor control system in determining hand dominance at a given workspace, which results in a lack of transfer across the arms.     

Acquisition and generalization of visuomotor transformations by nonhuman primates

The kinematics of straight reaching movements can be specified vectorially by the direction of the movement and its extent. To explore the representation in the brain of these two properties, psychophysical studies have examined learning of visuomotor transformations of either rotation or gain and their generalization. However, the neuronal substrates of such complex learning are only beginning to be addressed. As an initial step in ensuring the validity of such investigations, it must be shown that monkeys indeed learn and generalize visuomotor transformations in the same manner as humans. Here, we analyze trajectories and velocities of movements as monkeys adapt to either rotational or gain transformations. We used rotations with different signs and magnitudes, and gains with different signs, and analyzed transfer of learning to untrained movements. The results show that monkeys can adapt to both types of transformation with a time course that resembles human learning. Analysis of the aftereffects reveals that rotation is learned locally and generalizes poorly to untrained directions, whereas gain is learned more globally and can be transferred to other amplitudes. The results lend additional support to the hypothesis that reaching movements are learned locally but can be easily rescaled to other magnitudes by scaling the peak velocity. The findings also indicate that reaching movements in monkeys are planned and executed very similarly to those in humans. This validates the underlying presumption that neuronal recordings in primates can help elucidate the mechanisms of motor learning in particular and motor planning in general.     

Transfer of sensorimotor adaptation between different movement categories

We examined whether task-dependent modulation was evident in a motor learning paradigm. Subjects performed reaching movements before, during, and after exposure to a novel force perturbation while adopting either a spatial goal, "continue towards the target", or an effort goal, "keep your effort profile the same". Before the perturbation, the hand trajectories were moderately straight and accurate regardless of the task. However, during and immediately after the perturbation, the reaches exhibited unambiguous task-dependent differences in both the initial and terminal periods of the reach. With the spatial goal, subjects showed terminal compensations to the force-induced displacements indicative of feedback control. In addition, feedforward control was evident in the smaller path deviations with continued exposure and the initial path aftereffects when the perturbation was removed. In contrast, when adopting an effort goal, subjects showed large and chronically deviated endpoints from the perturbation indicating an absence of feedback compensation. They also showed no feedforward adaptation during repeated exposure or visible aftereffects when the perturbation was removed. Therefore, both feedforward and feedback control mechanisms show task-dependent modulation in a motor learning paradigm.     

Long-lasting aftereffects of prism adaptation in the monkey

The errors in target-reaching that are produced by laterally displacing vision with wedge prisms decrease with trials (prism adaptation). When the prisms are removed, errors in the opposite direction are observed (aftereffect). We investigated the size of the aftereffect 24 h and 72 h after a monkey had adapted to a visual displacement (30 mm), with rapid reaching movements. The aftereffect more than half of the size of the displacement was observed when the effect was tested immediately after the monkey had been exposed to the displacement for 50 trials. In contrast, the aftereffect was not observed at 24 h even when the monkey had been exposed to the displacement for 250 trials. However, when the monkey had been exposed for 500 trials, significant aftereffects more than half of the size of the displacement were observed at 24 h and 72 h. When both arms were adapted to opposite prism displacements, the long-lasting aftereffect was further shown to be specific for the arm used during the exposure. The results indicate that the aftereffects of prism adaptation last for at least 3 days, though more than 200 trials of additional repetition are required to consolidate the short-term effects into long-lasting ones.     

Adaptation and generalization in acceleration-dependent force fields

Any passive rigid inertial object that we hold in our hand, e.g., a tennis racquet, imposes a field of forces on the arm that depends on limb position, velocity, and acceleration. A fundamental characteristic of this field is that the forces due to acceleration and velocity are linearly separable in the intrinsic coordinates of the limb. In order to learn such dynamics with a collection of basis elements, a control system would generalize correctly and therefore perform optimally if the basis elements that were sensitive to limb velocity were not sensitive to acceleration, and vice versa. However, in the mammalian nervous system proprioceptive sensors like muscle spindles encode a nonlinear combination of all components of limb state, with sensitivity to velocity dominating sensitivity to acceleration. Therefore, limb state in the space of proprioception is not linearly separable despite the fact that this separation is a desirable property of control systems that form models of inertial objects. In building internal models of limb dynamics, does the brain use a representation that is optimal for control of inertial objects, or a representation that is closely tied to how peripheral sensors measure limb state? Here we show that in humans, patterns of generalization of reaching movements in acceleration-dependent fields are strongly inconsistent with basis elements that are optimized for control of inertial objects. Unlike a robot controller that models the dynamics of the natural world and represents velocity and acceleration independently, internal models of dynamics that people learn appear to be rooted in the properties of proprioception, nonlinearly responding to the pattern of muscle activation and representing velocity more strongly than acceleration.     

Straight ahead acts as a reference for visuomotor adaptation

One can adapt movement planning to compensate for a mismatch between vision and action. Previous research with prismatic lenses has shown this adaptation to be accompanied with a shift in the evaluation of one’s body midline, suggesting an important role of this reference for successful adaptation. This interpretation leads to the prediction that rotation adaptation could be more difficult to learn for some directions than others. Specifically, we hypothesized that targets seen to the right of the body midline but for which a rotation imposes a movement to its left would generate a conflict leading to a bias in movement planning. As expected, we observed different movement planning biases across movement directions. The same pattern of biases was observed in a second experiment in which the starting position was translated 15 cm to the right of the participants’ midline. This indicates that the “straight ahead” direction, not one’s midline, serves as an important reference for movement planning during rotation adaptation.

Greater reliance on impedance control in the nondominant arm compared with the dominant arm when adapting to a novel dynamic environment

This study investigated differences in adaptation to a novel dynamic environment between the dominant and nondominant arms in 16 naive, right-handed, neurologically intact subjects. Subjects held onto the handle of a robotic manipulandum and executed reaching movements within a horizontal plane following a pseudo-random sequence of targets. Curl field perturbations were imposed by the robot motors, and we compared the rate and quality of adaptation between dominant and nondominant arms. During the early phase of the adaptation time course, the rate of motor adaptation between both arms was similar, but the mean peak and figural error of the nondominant arm were significantly smaller than those of the dominant arm. Also, the nondominant limb’s aftereffects were significantly smaller than in the dominant arm. Thus, the controller of the nondominant limb appears to have relied on impedance control to a greater degree than the dominant limb when adapting to a novel dynamic environment. The results of this study imply that there are differences in dynamic adaptation between an individual’s two arms.     

Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study

There are several invariant features of pointto-point human arm movements: trajectories tend to be straight, smooth, and have bell-shaped velocity profiles. One approach to accounting for these data is via optimization theory; a movement is specified implicitly as the optimum of a cost function, e.g., integrated jerk or torque change. Optimization models of trajectory planning, as well as models not phrased in the optimization framework, generally fall into two main groups-those specified in kinematic coordinates and those specified in dynamic coordinates. To distinguish between these two possibilities we have studied the effects of artificial visual feedback on planar two-joint arm movements. During self-paced point-to-point arm movements the visual feedback of hand position was altered so as to increase the perceived curvature of the movement. The perturbation was zero at both ends of the movement and reached a maximum at the midpoint of the movement. Cost functions specified by hand coordinate kinematics predict adaptation to increased curvature so as to reduce the visual curvature, while dynamically specified cost functions predict no adaptation in the underlying trajectory planner, provided the final goal of the movement can still be achieved. We also studied the effects of reducing the perceived curvature in transverse movements, which are normally slightly curved. Adaptation should be seen in this condition only if the desired trajectory is both specified in kinematic coordinates and actually curved. Increasing the perceived curvature of normally straight sagittal movements led to significant (P<0.001) corrective adaptation in the curvature of the actual hand movement; the hand movement became curved, thereby reducing the visually perceived curvature. Increasing the curvature of the normally curved transverse movements produced a significant (P<0.01) corrective adaptation; the hand movement became straighter, thereby again reducing the visually perceived curvature. When the curvature of naturally curved transverse movements was reduced, there was no significant adaptation (P>0.05). The results of the curvature-increasing study suggest that trajectories are planned in visually based kinematic coordinates. The results of the curvature-reducing study suggest that the desired trajectory is straight in visual space. These results are incompatible with purely dynamicbased models such as the minimum torque change model. We suggest that spatial perception-as mediated by vision-plays a fundamental role in trajectory planning.     

Components of sensorimotor adaptation in young and elderly subjects

Previous studies have found that sensorimotor adaptation to visual distortions is degraded in seniors compared with younger subjects, whereas after-effects on removal of the distortion are age-independent. The latter finding was interpreted as evidence that adaptive recalibration is not affected by old age, and that the observed degradation is therefore due to impairment of strategic control. However, after-effects are not a reliable measure of recalibration, because they can be artificially inflated by perseveration, a characteristic symptom in old age. The present work therefore introduces a test of recalibration which is insensitive to perseveration. Twelve young and twelve old subjects executed center-out pointing movements while visual feedback about their fingertip was either veridical (baseline), 60-deg rotated (adaptation), or absent (after-effect).They also executed tracking movements toward an unpredictably moving object before and after the pointing task. Seniors adapted less than younger subjects but their after-effects were not degraded. More importantly, transfer of adaptation from a pointing to a tracking task was not degraded in seniors. The latter outcome documents, in a more compelling fashion than previous work, that recalibration in the elderly is not impaired, and that the observed deficit of adaptation is therefore most probably because of impaired strategic control. This conclusion is supported by two additional findings: compared with young subjects our seniors performed less well on a cognitive screening test and acquired no explicit knowledge about the nature of the imposed visual distortion.     

Dual adaptation to two opposing visuomotor rotations when each is associated with different regions of workspace

Studies examining dual adaptation to opposing novel environments have yielded contradictory results, with previous evidence supporting both successful dual adaptation and interference leading to poorer adaptive performance. Whether or not interference is observed during dual adaptation appears to be dependent on the method used to allow the performer of the task to distinguish between two novel environments. This experiment tested if colour cues, a separation in workspace, and presentation schedule, could be used to distinguish between two opposing visuomotor rotations and enable dual adaptation. Through the use of a purpose designed manipulandum, each visuomotor rotation was either presented in the same region of workspace and associated with colour cues (Group 1), different regions of workspace in addition to colour cues (Groups 2 and 3) or different regions of workspace only (Groups 4 and 5). We also assessed the effectiveness of the workspace separation with both randomised and alternating presentation schedules (Groups 4 and 5). The results indicated that colour cues were not effective at enabling dual adaptation when each of the visuomotor rotations was associated with the same region of workspace. When associated with different regions of workspace, however, dual adaptation to the opposing rotations was successful regardless of whether colour cues were present or the type of presentation schedule.     

Performance differences in visually and internally guided continuous manual tracking movements

Control of familiar visually guided movements involves internal plans as well as visual and other online sensory information, though how visual and internal plans combine for reaching movements remain unclear. Traditional motor sequence learning tasks, such as the serial reaction time task, use stereotyped movements and measure only reaction time. Here, we used a continuous sequential reaching task comprised of naturalistic movements, in order to provide detailed kinematic performance measures. When we embedded pre-learned trajectories (those presumably having an internal plan) within similar but unpredictable movement sequences, participants performed the two kinds of movements with remarkable similarity, and position error alone could not reliably identify the epoch. For such embedded movements, performance during pre-learned sequences showed statistically significant but trivial decreases in measures of kinematic error, compared to performance during novel sequences. However, different sets of kinematic error variables changed significantly between learned and novel sequences for individual participants, suggesting that each participant used distinct motor strategies favoring different kinematic variables during each of the two movement types. Algorithms that incorporated multiple kinematic variables identified transitions between the two movement types well but imperfectly. Hidden Markov model classification differentiated learned and novel movements on single trials based on the above kinematic error variables with 82 ± 5% accuracy within 244 ± 696 ms, despite the limited extent of changes in those errors. These results suggest that the motor system can achieve markedly similar performance whether or not an internal plan is present, as only subtle changes arise from any difference between the neural substrates involved in those two conditions.     

Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning

There is increasing evidence supporting the notion that the contribution of sleep to consolidation of motor skills depends on the nature of the task used in practice. We compared the role of three post-training conditions in the expression of delayed gains on two different motor skill learning tasks: finger tapping sequence learning (FTSL) and visuomotor adaptation (VMA). Subjects in the DaySleep and ImmDaySleep conditions were trained in the morning and at noon, respectively, afforded a 90-min nap early in the afternoon and were re-tested 12 h post-training. In the NightSleep condition, subjects were trained in the evening on either of the two learning paradigms and re-tested 12 h later following sleep, while subjects in the NoSleep condition underwent their training session in the morning and were re-tested 12 h later without any intervening sleep. The results of the FTSL task revealed that post-training sleep (day-time nap or night-time sleep) significantly promoted the expression of delayed gains at 12 h post-training, especially if sleep was afforded immediately after training. In the VMA task, however, there were no significant differences in the gains expressed at 12 h post-training in the three conditions. These findings suggest that “off-line” performance gains reflecting consolidation processes in the FTSL task benefit from sleep, even a short nap, while the simple passage of time is as effective as time in sleep for consolidation of VMA to occur. They also imply that procedural memory consolidation processes differ depending on the nature of task demands. J. Doyon and M. Korman contributed equally.     

Error generalization as a function of velocity and duration: human reaching movements

Our sensory-motor control system has a remarkable ability to adapt to novel dynamics during reaching movements and generalizes this adaptation to movements made in different directions, positions and even speeds. The degree and pattern of this generalization are of great importance in deducing the underlying mechanisms that govern our motor control. In this report we expand our knowledge on the generalization between movements made at different speeds. We wished to determine the pattern of generalization between different speed and duration movements on a trial-by-trial basis. In addition, we tested three hypotheses for the pattern of generalization. The first hypothesis was that the generalization was maximum for the speed of the movement just made with a linear decrease in generalization as one moves away from that preferred speed. The second was that the generalization is always highest for the fastest speed movements and linearly decreases with speed. The last hypothesis came from our preliminary results, which suggested that the generalization plateaus. Human subjects made targeted reaching movements at four different maximum speeds (15, 35, 55 and 75 cm/s) presented in pseudorandom order to one spatial target (15 cm extent) while holding onto a robotic manipulandum that produced a viscous curl field. Catch trials (trial where the curl field was unexpectedly removed) were used to probe the generalization between the four speed/durations on a movement-by-movement basis. We found that the pattern of generalization was linear between the first three speed categories (15–55 cm/s), but plateaued after the 55 cm/s category. We compared the subjects’ results with a simulated adaptive controller that used a population code by combining the output of basis elements. These basis elements encoded limb velocity and associated this with a force expectation at that velocity. We found that using a basis set of Gaussians the adaptive controller produced movements that generalized in virtually the exact manner as the subjects, as we have previously demonstrated for movements made to different spatial targets. Thus, the human internal model may employ such a population code.     

Context-specific adaptation of saccade gain

Previous studies established that vestibular reflexes can have two adapted states (e.g., gain) simultaneously, and that a context cue (e.g., vertical eye position) can switch between the two states. The present study examined this phenomenon of context-specific adaptationfor horizontal saccades, using a variety of contexts. Our overall goal was to assess the efficacy of different context cues in switching between adapted states. A standard double-step paradigm was used to adapt saccade gain. In each experiment, we asked for a simultaneous gain decrease in one context and gain increase in another context, and then determined if a change in the context would invoke switching between the adapted states. Horizontal eye position worked well as a context cue: saccades with the eyes deviated to the right could be made to have higher gains while saccades with the eyes deviated to the left could be made to have lower gains. Vertical eye position was less effective. This suggests that the more closely related a context cue is to the response being adapted, the more effective it is. Roll tilt of the head, and upright versus supine orientations, were somewhat effective in context switching; these paradigms contain orientation of gravity with respect to the head as part of the context.     

Force adaptation transfers to untrained workspace regions in children

When humans perform goal-directed arm movements under the influence of an external damping force, they learn to adapt to these external dynamics. After removal of the external force field, they reveal kinematic aftereffects that are indicative of a neural controller that still compensates the no longer existing force. Such behavior suggests that the adult human nervous system uses a neural representation of inverse arm dynamics to control upper-extremity motion. Central to the notion of an inverse dynamic model (IDM) is that learning generalizes. Consequently, aftereffects should be observable even in untrained workspace regions. Adults have shown such behavior, but the ontogenetic development of this process remains unclear. This study examines the adaptive behavior of children and investigates whether learning a force field in one hemifield of the right arm workspace has an effect on force adaptation in the other hemifield. Thirty children (aged 6-10 years) and ten adults performed 30 degrees elbow flexion movements under two conditions of external damping (negative and null). We found that learning to compensate an external damping force transferred to the opposite hemifield, which indicates that a model of the limb dynamics rather than an association of visited space and experienced force was acquired. Aftereffects were more pronounced in the younger children and readaptation to a null-force condition was prolonged. This finding is consistent with the view that IDMs in children are imprecise neural representations of the actual arm dynamics. It indicates that the acquisition of IDMs is a developmental achievement and that the human motor system is inherently flexible enough to adapt to any novel force within the limits of the organism's biomechanics.     

Perception action interaction: the oblique effect in the evolving trajectory of arm pointing movements

In previous studies, we provided evidence for a directional distortion of the endpoints of movements to memorized target locations. This distortion was similar to a perceptual distortion in direction discrimination known as the oblique effect so we named it the “motor oblique effect”. In this report we analyzed the directional errors during the evolution of the movement trajectory in memory guided and visually guided pointing movements and compared them with directional errors in a perceptual experiment of arrow pointing. We observed that the motor oblique effect was present in the evolving trajectory of both memory and visually guided reaching movements. In memory guided pointing the motor oblique effect did not disappear during trajectory evolution while in visually guided pointing the motor oblique effect disappeared with decreasing distance from the target and was smaller in magnitude compared to the perceptual oblique effect and the memory motor oblique effect early on after movement initiation. The motor oblique effect in visually guided pointing increased when reaction time was small and disappeared with larger reaction times. The results are best explained using the hypothesis that a low level oblique effect is present for visually guided pointing movements and this effect is corrected by a mechanism that does not depend on visual feedback from the trajectory evolution and might even be completed during movement planning. A second cognitive oblique effect is added in the perceptual estimation of direction and affects the memory guided pointing movements. It is finally argued that the motor oblique effect can be a useful probe for the study of perception–action interaction.     

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.     

Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man

Application of a small (around 1 mA), constant electric current between the mastoid processes (galvanic stimulation) of a standing subject produces enhanced body sway in the approximate direction of the ear behind which the anode is placed. We examined the electromyographic (EMG) responses evoked by such stimulation in the soleus and in the triceps brachii muscles. For soleus, subjects stood erect, with their eyes closed, leaning slightly forward. The head was turned approximately 90° to the right or left relative to the feet. In averaged records (n=40), current pulses of 25 ms or longer modulated the EMG in a biphasic manner: a small early component (latency 62±2.4 ms, mean ± SEM) was followed by a larger late component (latency 115±5.2ms) of opposite sign, which was appropriate to produce the observed body sway. The early component produced no measurable body movement. Lengthening the duration of the stimulus pulse from 25 to 400 ms prolonged the late component of the response but had little effect on the early component. Short- and long-latency EMG responses were also evoked in the triceps brachii muscle if subjects stood on a transversely pivoted platform and had to use the muscle to maintain their balance in the anteroposterior plane by holding a fixed handle placed by the side of their hip. The latency of the early component was 41±2.6 ms; the latency of the late component was 138±4.3 ms and was again of appropriate sign for producing the observed body sway. Galvanic stimulation evoked no comparable responses in either triceps brachii or soleus muscles if these muscles were not being used posturally. The responses were most prominent if vestibular input provided the dominant source of information about postural stability, and were much smaller if subjects lightly touched a fixed support or opened their eyes. The difference in latency between the onset of the early component of the response in arm and leg muscles suggests that this part of the response uses a descending pathway which conducts impulses down the spinal cord with a velocity comparable with that of the fast conducting component of the corticospinal tract. The late component of the EMG response occurs earlier in the leg than the arm. We suggest that it forms part of a patterned, functional response which is computed independently of the early component.     

Proprioceptive guidance and motor planning of reaching movements to unseen targets

The ability to make accurate reaching movements toward proprioceptively defined target locations was studied in seven normal subjects who were trained to reach to five different targets in a horizontal plane, with no vision of hand or target. The task consisted of moving a handle from a fixed origin to each target location, fast and accurately. Target locations were learned in training sessions that utilized acoustic cuing. Most movements were rapid, with a bell-shaped velocity profile. The error in target reproduction, which constituted the difference between the position consciously identified as the correct target location and the real target location, was calculated in each trial. This was compared with the error in preprogrammed reaching, which constituted the difference between the point in space where the initial fast movement toward the target ended and the target location. The absence of significant differences between these two error types indicated that the transformation from an internal representation of target location into a motor program for reaching to it did not introduce an additional reaching error. Learning of target locations was done only with the right hand, yet, reaching of both hands was tested. This allowed a comparison between the subjects' ability to utilize a transformed spatial code (reaching with the untrained hand) and their ability to use a direct sensory-motor code (reaching with the trained hand). While transformation of the spatial code was found to reduce it's accuracy, utilization of this code in motor programming again did not appear to introduce an additional error.