Interlimb transfer of visuomotor rotations: independence of direction and final position information

Previous findings from our laboratory support the idea that the dominant arm is more proficient than the non-dominant arm in coordinating intersegmental dynamics for specifying trajectory direction and shape during multijoint reaching movements. We also showed that adaptation of right and left arms to novel visuomotor rotations was equivalent, suggesting that this process occurs upstream to processes that distinguish dominant and non-dominant arm performance. Because of this, we speculate that such visuomotor adaptations might transfer to subsequent performance during adaptation with the other arm. We now examine whether opposite arm training to novel visuomotor rotations transfers to affect adaptation using the right and left arms. Two subject groups, RL and LR, each comprising seven right-handed subjects, adapted to a 30 degrees counterclockwise rotation in the visual display during a center-out reaching task performed in eight directions. Each group first adapted using either the right (RL) or left (LR) arm, followed by opposite arm adaptation. In order to assess transfer, we compared the same side arm movements (either right or left) following opposite arm adaptation to those performed prior to opposite arm adaptation. Our findings indicate unambiguous transfer of learning across the arms. Different features of movement transferred in different directions: Opposite arm training improved the initial direction of right arm movements under the rotated visual condition, whereas opposite arm training improved the final position accuracy, but not the direction of left arm movements. These findings confirm that transfer of training was not due to a general cognitive strategy, since such an effect should influence either hand equally. These findings support the hypothesis that each arm controller has access to information learned during opposite arm training. We suggest that each controller uses this information differently, depending on its proficiency for specifying particular features of movement. We discuss evidence that these two aspects of control are differentially mediated by the right and left cerebral hemispheres.     

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.     

The efficacy of colour cues in facilitating adaptation to opposing visuomotor rotations

We investigated visuomotor adaptation using an isometric, target-acquisition task. Following trials with no rotation, two participant groups were exposed to a random sequence of 30° clockwise (CW) and 60° counter-clockwise (CCW) rotations, with (DUAL-CUE), or without (DUAL-NO CUE), colour cues that enabled each environment (non-rotated, 30° CW and 60° CCW) to be identified. A further three groups experienced only 30° CW trials or only 60° CCW trials (SINGLE rotation groups) in which each visuomotor mapping was again associated with a colour cue. During training, all SINGLE groups reduced angular deviations of the cursor path during the initial portion of the movements, indicating feedforward adaptation. Consistent with the view that the adaptation occurred automatically via recalibration of the visuomotor mapping (Krakauer et al. 1999), post-training aftereffects were observed, despite colour cues that indicated that no rotation was present. For the DUAL-CUE group, angular deviations decreased with training in the 60° trials, but were unchanged in the 30° trials, while for the DUAL-NO CUE group angular deviations decreased for the 60° CW trials but increased for the 30° CW trials. These results suggest that in a dual adaptation paradigm a colour cue can permit delineation of the two environments, with a subsequent change in behaviour resulting in improved performance in at least one of these environments. Increased reaction times within the training block, together with the absence of aftereffects in the post-training period for the DUAL-CUE group suggest an explicit cue-dependent strategy was used in an attempt to compensate for the rotations.     

Estimation of temporal resolution of object identification in human vision

The purpose of the study was to estimate the temporal processing capacity of human object identification under different stimulus conditions. Objects, either facial images or characters, were shown in a rapid sequence on a computer display using a rapid serial visual presentation (RSVP) method. One of the images was a target and the other images were distracters. The task of the observer was to identify the target. A staircase algorithm was used to determine the threshold frequency of image presentation in the RSVP sequence. The threshold frequency was determined as a function of image contrast, size, and mean luminance. The results showed that the threshold frequency, around 10 Hz for faces (100 ms per face) and about 25 Hz for characters (40 ms per character), was independent of contrast and size at medium and high contrast values, medium and large sizes, and high luminances, but decreased at very low contrasts or small sizes and medium or low levels of luminance. Computer simulations with a model, in which temporal integration limited perceptual speed, suggest that the experimentally found difference in processing time for faces and characters is not due to the physical differences of these stimulus types, but it seems that face-specific sites in the brain process facial information slower than object-specific areas process character information. Contrast, size, and luminance affect the signal-to-noise ratio and the temporal characteristics of low-level neural signal representation. Thus, the results suggest that at low contrasts, low luminances and small sizes, the processing speed of object identification is limited by low-level factors, while at high contrasts and luminances, and at large sizes, processing speed is limited by high-order processing stages. Processing speed seems to depend on stimulus type so that for faces processing is slower than for characters.     

Altering the visuomotor gain

Two experiments investigated the effects of providing nonveridical knowledge of the results (KR) in a visuomanual task in which participants pointed to briefly (200 ms) presented targets without seeing their hand. By showing after each trial the movement endpoint displaced radially with respect to its true position, we were able to alter progressively the gain of the visuomanual loop. In experiment 1, the KR was provided only for transversal movements and for one target distance, but the effect generalized to all directions and all distances. Moreover, it also generalized to the other hand that had never been biased. In experiment 2, nonveridical KR was supplied for movements along the two major diagonals which require sharply different muscle synergies. The transfer to other directions and to the other hand was equally substantial. It is argued that the results support the vector coding hypothesis, which holds that the input to the motor execution stage is supplied by specifying independently the amplitude and the direction of the vector from the initial to the final position in an extrinsic frame of reference. We also discuss the possible brain structures involved in the biasing action of the KR. Electronic Publication     

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.

On-line corrections for visuomotor errors

This study was designed to determine how visual feedback mediates error corrections during reaching. We used visuomotor rotations to dissociate a cursor, representing finger position, from the actual finger location. We then extinguished cursor feedback at different distances from the start location to determine whether corrections were based on error extrapolation from prior cursor information. Results indicated that correction amplitude varied with the extent of cursor feedback. A second experiment tested specific aspects of error information that might mediate corrections to visuomotor rotations: rotation angle, distance between the finger and cursor positions and the duration of cursor exposure. Results showed that corrections did not depend on the amplitude of the rotation angle or the amount of time the cursor was shown. Instead, participants corrected for the cursor–finger distance, at the point where cursor feedback was last-seen. These findings suggest that within-trial corrections and inter-trial adaptation might employ different mechanisms.     

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.     

An event-related potential evoked by movement planning is modulated by performance and learning in visuomotor control

Based on a previous exploratory study, the functionality of event-related potentials related to visuomotor processing and learning was investigated. Three pursuit tracking tasks (cursor control either mouse, joystick, or bimanually) revealed the greatest tracking error and greatest learning effect in the bimanual task. The smallest error without learning was found in the mouse task. Error reduction reflected visuomotor learning. In detail, target–cursor distance was reduced continuously, indicating a better fit to a changed direction, whereas response time remained at 300 ms. A central positive ERP component with an activity onset 100 ms after a directional change of the target and most likely generated in premotor areas could be assigned to response planning and execution. The magnitude of this component was modulated by within-and-between-task difficulty and size of the tracking error. Most importantly, the size of this component was sensitive to between-subject performance and increased with visuomotor learning. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Degree of handedness affects intermanual transfer of skill learning

Intermanual transfer of skill learning has often been used as a paradigm to study functional specialization and hemispheric interactions in relation to handedness. This literature has not evaluated whether degree of handedness impacts learning and intermanual transfer. Because handedness scores are related to factors that might influence intermanual transfer, such as engagement of the ipsilateral hemisphere during movement (Dassonville et al. in Proc Natl Acad Sci USA 94:14015–14018, 1997) and corpus callosum volume (Witelson in Science 229:665–668, 1985; Brain 112:799–835, 1989), we tested whether degree of handedness is correlated with transfer magnitude. We had groups of left and right handed participants perform a sensorimotor adaptation task and a sequence learning task. Following learning with either the dominant or nondominant hand, participants transferred to task performance with the other hand. We evaluated whether the magnitude of learning and intermanual transfer were influenced by either direction and/or degree of handedness. Participants exhibited faster sensorimotor adaptation with the right hand, regardless of whether they were right or left handed. In addition, less strongly left handed individuals exhibited better intermanual transfer of sensorimotor adaptation, while less strongly right handed individuals exhibited better intermanual transfer of sequence learning. The findings suggest that involvement of the ipsilateral hemisphere during learning may influence intermanual transfer magnitude.     

Spatial representation of overlearned arbitrary visuomotor associations

Our movements can be guided directly by spatial information, but also more flexibly through arbitrary rules. We have recently shown that as arbitrary visuomotor mappings became overlearned, they come to rely not only on fronto-striatal circuits, but also on the posterior parietal cortex (PPC). Since this region supports multiple reference frames for hand movements, the question arose whether overlearned visuomotor associations could come to rely on a spatial framework, similar to spatially guided movements. Alternatively, overlearned visuomotor associations could be non-spatial in nature. In this study we investigate the characteristics of the movement representations supporting arbitrary visuomotor mappings by assessing how performance of extensively trained arbitrary visuomotor associations depends on the effector used to provide the response. After extensive training on a set of arbitrary visuomotor associations, subjects were asked to perform the same task in one of two novel settings that varied either the spatial or the motor relationship between visual instructions and finger movements. We found that the change in spatial configuration resulted in a larger amount of interference on the performance of the original mappings than the configuration change in motor coordinates. This result suggests that the visual stimuli became arbitrarily coupled to locations in space and not directly to the finger movements. We infer that overlearned arbitrary visuomotor associations are represented in spatial coordinates, in an effector-independent framework. This result raises the possibility that the previously reported involvement of the posterior parietal cortex in overlearned visuomotor behavior reflects the transition from an arbitrary visuomotor mapping into a spatially based stimulus-location-response mapping. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Dissociable contributions of motor-execution and action-observation to intermanual transfer

We examined the suggestion that some of the processes subserving learning through action-observation and motor-execution are different because sensory motor reafference is not available while the limb is at rest in the former condition. We confirmed the action-observation and motor-execution groups learned equally the absolute time and relative time constraints associated with a movement sequence timing task. However, data from mirror (same motor commands as those in practice) and non-mirror (same visual spatial coordinates as those in practice) intermanual transfer tests showed a clear dissociation in performance following these forms of practice. While positive transfer was exhibited by both groups in the non-mirror condition, there was a significant decrement in relative time performance in the mirror condition only after action-observation. These findings confirm that some of the processes underpinning these forms of motor learning are not somatotopic. Indeed, while motor and visual representations are developed during motor-execution, the absence of sensorimotor reafference during action-observation enables relative time to be represented in visual spatial coordinates only. These behavioural effects for intermanual transfer are discussed with reference to activity in supplementary motor area.     

Modulation of frontal and parietal neuronal activity by visuomotor learning. An ERP analysis of implicit and explicit pursuit tracking tasks

The present study investigated changes in frontal and parietal activity related to visuomotor learning. Improvement in task performance should be achieved by a transition from feedback control to feedforward control. Event-related potential (ERP) activity related to visual feedback analysis of successful error corrections was expected to decrease at parietal scalp locations. (Pre-) motor activity related to the execution of directional changes should increase and begin earlier.     

Mechanisms underlying interlimb transfer of visuomotor rotations

We previously reported that opposite arm training improved the initial direction of dominant arm movements, whereas it only improved the final position accuracy of non-dominant arm movements. We now ask whether each controller accesses common, or separate, short-term memory resources. To address this question, we investigated interlimb transfer of learning for visuomotor rotations that were directed oppositely [clockwise (CW)/counterclockwise (CCW)] for the two arms. We expected that if information obtained by initial training was stored in the same short-term memory space for both arms, opposite arm training of a CW rotation would interfere with subsequent adaptation to a CCW rotation. All subjects first adapted to a 30° rotation (CW) in the visual display during reaching movements. Following this, they adapted to a 30° rotation in the opposite direction (CCW) with the other arm. In contrast to our previous findings for interlimb transfer of same direction rotations (CCW/CCW), no effects of opposite arm adaptation were indicated in the initial trials performed. This indicates that interlimb transfer is not obligatory, and suggests that short-term memory resources for the two limbs are independent. Through single trial analysis, we found that the direction and final position errors of the first trial of movement, following opposite arm training, were always the same as those of naive performance. This was true whether the opposite arm was trained with the same or the opposing rotation. When trained with the same rotation, transfer of learning did not occur until the second trial. These findings suggest that the selective use of opposite arm information is dependent on the first trial to probe current movement conditions. Interestingly, the final extent of adaptation appeared to be reduced by opposite arm training of opposing rotations. Thus, the extent of adaptation, but not initial information transfer, appears obligatorily affected by prior opposite arm adaptation. According to our findings, it is plausible that the initiation and the final extent of adaptation involve two independent neural processes. Theoretical implications of these findings are discussed. Electronic Publication     

Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks

OBJECTIVE: (1) To verify whether the prefrontal cortex (PFC) is specifically involved in visuomotor sequence learning as opposed to other forms of motor learning and (2) to establish the role of executive functions in visuomotor sequence learning. BACKGROUND: Visuomotor skill learning depends on the integrity of the premotor and parietal cortex; the prefrontal cortex, however, is essential when the learning of a sequence is required. METHODS: We studied 25 patients with PFC lesions and 86 controls matched for age and educational level. Participants performed: (1) a Pursuit Tracking Task (PTT), composed of a random tracking task (perceptual learning) and a pattern tracking task (explicit motor sequence learning with learning indicated by the decrease in mean root square error across trial blocks), (2) a 12-item sequence version of a serial reaction time task (SRTT) with specific implicit motor sequence learning indicated by the rebound increase in response time when comparing the last sequence block with the next random block, and (3) a neuropsychological battery that assessed executive functions. RESULTS: PFC patients were impaired in sequence learning on the pattern tracking task of the PTT and on the SRTT as compared to controls, but performed normally on the PTT random tracking task. Learning on the PTT did not correlate with learning on the SRTT. PTT performance correlated with planning functions while SRTT performance correlated with working memory capacity. CONCLUSIONS: The PFC is specifically involved in explicit and implicit motor sequence learning. Different PFC regions may be selectively involved in such learning depending on the cognitive demands of the sequential task.     

Coordination in childhood: modifications of visuomotor representations in 6- to 11-year-old children

This research investigated the development of visuomotor coordination in childhood, more specifically the conversion of visual information into motor sequences. Three groups of children (aged 6, 8 and 11 years) and a group of adults performed pointing movements without direct feedback from their arm displacements. Visual information, provided by a video camera, was disturbed by rotations of 0 degree, 45 degrees, 90 degrees, 135 degrees or 180 degrees. Six-year-old children showed poor accuracy for 180 degrees rotations. These results suggest that the youngest children use unidirectional representations to convert visual information into motor sequences. At 8 years of age, children showed a shift from unidirectional to bidirectional representations, as reflected by reduced errors for 180 degrees rotations. Eleven-year-old children and adults showed the same type of representations, i.e., bidirectional. However, as reflected by their slower movement time and slower modifications in temporal accuracy across trials, the oldest children have not yet reached maturation in their adaptive process when compared to adults.     

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.     

EEG correlates of coordinate processing during intermanual transfer

Goal-directed movements require mapping of target information to patterns of muscular activation. While visually acquired information about targets is initially encoded in extrinsic, object-centered coordinates, muscular activation patterns are encoded in intrinsic, body-related coordinates. Intermanual transfer of movements previously learned with one hand is accomplished by the recall of unmodified extrinsic coordinates if the task is performed in original orientation. Intrinsic coordinates are retrieved in case of mirror-reversed orientation. In contrast, learned extrinsic coordinates are modified during the mirror movement and intrinsic coordinates during the originally oriented task. To investigate the neural processes of recall and modification, electroencephalogram (EEG) recording was employed during the performance of a figure drawing task previously trained with the right hand in humans. The figure was reproduced with the right hand (Learned-task) and with the left hand in original (Normal-task) and mirror orientations (Mirror-task). Prior to movement onset, beta-power and alpha- and beta-coherence decreased during the Normal-task as compared with the Learned-task. Negative amplitudes over fronto-central sites during the Normal-task exceeded amplitudes manifested during the Learned-task. In comparison to the Learned-task, coherences between fronto-parietal sites increased during the Mirror-task. Results indicate that intrinsic coordinates are processed during the pre-movement period. During the Normal-task, modification of intrinsic coordinates was revealed by cerebral activation. Decreased coherences appeared to reflect suppressed inter-regional information flow associated with utilization of intrinsic coordinates. During the Mirror-task, modification of extrinsic coordinates induced activation of cortical networks.     

The role of proprioception and attention in a visuomotor adaptation task

The role of proprioception in the control and adaptation of visuomotor relationships is still unclear. We have studied a deafferented subject, IW, and control subjects in a task in which they used single joint elbow extension to move to a visual target, with visual feedback of the terminal position provided by a cursor displayed in the plane of their movements. We report the differences in movement accuracy between the deafferented subject and controls in the normal task and when challenged with a cognitive load, counting backwards. All subjects were less accurate when counting; this was a small effect for the controls (<10% change) but much greater for the deafferented subject (>60% change). We also examined changes in movement kinematics when the instructed amplitude was altered via a changed gain between final arm position and presentation of the feedback cursor. The deafferented subject maintained temporal movement parameters stable and altered amplitude by scaling force (i.e. changed peak velocity), whereas the controls scaled both movement velocity and duration. Finally, we compared the subjects' adaptation of movement amplitude after a period of exposure to the changed visuomotor gain. The deafferented subject was able to adapt, but his adaptation was severely impaired by the counting task. These results suggest that proprioception is not an absolute requirement for adaptation to occur. Instead, proprioception has a more subtle role to play in the adjustment to visuomotor perturbations. It has an important role in the control of reaching movements, while in the absence of proprioception, attention appears necessary to monitor movements.     

Intermanual transfer of proximal and distal motor engrams in humans

We studied intermanual motor transfer for right-to-left or left-to-right direction of transfer between either proximal or distal upper extremity muscle groups. The influence of previously acquired motor engrams (original learning, OL) on learning efficiency of the contralateral side (transfer learning, TL) was examined in 26 right-handed healthy subjects. The task consisted of the drawing of meaningless figures. During TL, OL figures had to be reproduced as vertical mirror reversals. Data revealed a benefit for right-to-left but not left-to-right direction of transfer for time to complete a figure as well as a left-to-right transfer benefit for spatial motor precision. Furthermore, a benefit for intermanual transfer of training between proximal but not distal muscle groups was found when movement time to complete a figure was evaluated. Of special interest was the observation of a disadvantage due to prior contralateral learning for performance at right distal effectors. The asymmetrical transfer benefits with respect to side are in line with previous findings and support the proficiency model and the cross-actiation model. Results further showed that intermanual transfer of training might differ with respect to muscle group involvement and suggest that, although primarily facilitating, previous opposite hand training may lead to inhibitory influences on subsequent contralateral reproduction.Part of this study was presented to the International Neuropsychological Society meeting in Angers, 1994