Minimal impact of chronic proprioceptive loss on implicit sensorimotor adaptation and perceived movement outcome.

Implicit sensorimotor adaptation keeps our movements well calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual realignment model, implicit adaptation ceases when the perceived movement outcome-a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision-is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who experience deafferentation (i.e., individuals with impaired proprioception and touch). We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived movement outcomes throughout the experiment. Surprisingly, both implicit adaptation and perceived movement outcome were minimally impacted by chronic deafferentation, posing a challenge to the perceptual realignment model of implicit adaptation.NEW & NOTEWORTHY We tested six individuals with chronic somatosensory deafferentation on a novel task that isolates implicit sensorimotor adaptation and probes perceived movement outcome. Strikingly, both implicit motor adaptation and perceptual movement outcome were not significantly impacted by chronic deafferentation, posing a challenge for theoretical models of adaptation that involve proprioception.

Spatio-temporal modulation of cortical activity during motor deadaptation depends on the feedback of task-related error.

Motor adaptations are responsible for recalibrating actions and facilitating the achievement of goals in a constantly changing environment. Once consolidated, the decay of motor adaptation is a process affected by available sensory information during deadaptation. However, the cortical response to task error feedback during the deadaptation phase has received little attention. Here, we explored changes in brain cortical responses due to feedback of task-related error during deadaptation. Twelve healthy volunteers were recruited for the study. Right hand movement and EEG were recorded during repetitive trials of a hand reaching movement. A visuomotor rotation of 30° was introduced to induce motor adaptation. Volunteers participated in two experimental sessions organized in baseline, adaptation, and deadaptation blocks. In the deadaptation block, the visuomotor rotation was removed, and visual feedback was only provided in one session. Performance was quantified using angle end-point error, averaged speed, and movement onset time. A non-parametric spatiotemporal cluster-level permutation test was used to analyze the EEG recordings. During deadaptation, participants experienced a greater error reduction when feedback of the cursor was provided. The EEG responses showed larger activity in the left centro-frontal parietal areas during the deadaptation block when participants received feedback, as opposed to when they did not receive feedback. Centrally distributed clusters were found for the adaptation and deadaptation blocks in the absence of visual feedback. The results suggest that visual feedback of the task-related error activates cortical areas related to performance monitoring, depending on the accessible sensory information.

A lateralized motor network in order to understand adaptation to visuomotor rotation.

Objective.The functional asymmetry between the two brain hemispheres in language and spatial processing is well documented. However, a description of difference in control between the two hemispheres in motor function is not well established. Our primary objective in this study was to examine the distribution of control in the motor hierarchy and its variation across hemispheres.Approach.We developed a computation model termed the bilateral control network and implemented the same in a neural network framework to be used to replicate certain experimental results. The network consists of a simple arm model capable of making movements in 2D space and a motor hierarchy with separate elements coding target location, estimated position of arm, direction, and distance to be moved by the arm, and the motor command sent to the arm. The main assumption made here is the division of direction and distance coding between the two hemispheres with distance coded in the non-dominant and direction coded in the dominant hemisphere.Main results.With this assumption, the network was able to show main results observed in visuomotor adaptation studies. Importantly it showed decrease in error exhibited by the untrained arm while the other arm underwent training compared to the corresponding naïve arm's performance-transfer of motor learning from trained to the untrained arm. It also showed how this varied depending on the performance variable used-with distance as the measure, the non-dominant arm showed transfer and with direction, dominant arm showed transfer.Significance.Our results indicate the possibility of shared control between the two hemispheres. If indeed found true, this result could have major significance in motor rehabilitation as treatment strategies will need to be designed in order to account for this and can no longer be confined to the arm contralateral to the affected hemisphere.

Implicit reward-based motor learning.

Binary feedback, providing information solely about task success or failure, can be sufficient to drive motor learning. While binary feedback can induce explicit adjustments in movement strategy, it remains unclear if this type of feedback also induces implicit learning. We examined this question in a center-out reaching task by gradually moving an invisible reward zone away from a visual target to a final rotation of 7.5° or 25° in a between-group design. Participants received binary feedback, indicating if the movement intersected the reward zone. By the end of the training, both groups modified their reach angle by about 95% of the rotation. We quantified implicit learning by measuring performance in a subsequent no-feedback aftereffect phase, in which participants were told to forgo any adopted movement strategies and reach directly to the visual target. The results showed a small, but robust (2-3°) aftereffect in both groups, highlighting that binary feedback elicits implicit learning. Notably, for both groups, reaches to two flanking generalization targets were biased in the same direction as the aftereffect. This pattern is at odds with the hypothesis that implicit learning is a form of use-dependent learning. Rather, the results suggest that binary feedback can be sufficient to recalibrate a sensorimotor map.

Sensory prediction error drives subconscious motor learning outside of the laboratory.

Sensorimotor adaptation is supported by at least two parallel learning systems: an intentionally controlled explicit strategy and an involuntary implicit learning system. Past work focused on constrained reaches or finger movements in laboratory environments has shown subconscious learning systems to be driven in part by sensory prediction error (SPE), i.e., the mismatch between the realized and expected outcome of an action. We designed a ball rolling task to explore whether SPEs can drive implicit motor adaptation during complex whole body movements that impart physical motion on external objects. After applying a visual shift, participants rapidly adapted their rolling angles to reduce the error between the ball and the target. We removed all visual feedback and told participants to aim their throw directly toward the primary target, revealing an unintentional 5.06° implicit adjustment to reach angles that decayed over time. To determine whether this implicit adaptation was driven by SPE, we gave participants a second aiming target that would "solve" the visual shift, as in the study by Mazzoni and Krakauer (Mazzoni P, Krakauer JW. J Neurosci 26: 3642-3645, 2006). Remarkably, after rapidly reducing ball-rolling error to zero (due to enhancements in strategic aiming), the additional aiming target caused rolling angles to deviate beyond the primary target by 3.15°. This involuntary overcompensation, which worsened task performance, is a hallmark of SPE-driven implicit learning. These results show that SPE-driven implicit processes, previously observed within simplified finger or planar reaching movements, actively contribute to motor adaptation in more complex naturalistic skill-based tasks.NEW & NOTEWORTHY Implicit and explicit learning systems have been detected using simple, constrained movements inside the laboratory. How these systems impact movements during complex whole body, skill-based tasks has not been established. Here, we demonstrate that sensory prediction errors significantly impact how a person updates their movements, replicating findings from the laboratory in an unconstrained ball-rolling task. This real-world validation is an important step toward explaining how subconscious learning helps humans execute common motor skills in dynamic environments.

Strategy-based motor learning decreases the post-movement ß power.

Motor learning depends on the joint contribution of several processes including cognitive strategies aiming at goal achievement and prediction error-driven implicit adaptation. Understanding this functional interplay and its clinical implications requires insight into the individual learning processes, including at a neural level. Here, we set out to examine the impact of learning a cognitive strategy, over and above implicit adaptation, on the oscillatory post-movement ß rebound (PMBR), which typically decreases in power following (visuo)motor perturbations. Healthy participants performed reaching movements towards a target, with online visual feedback replacing the view of their moving hand. The feedback was sometimes rotated, either relative to their movements (visuomotor rotation) or invariant to their movements (and relative to the target; clamped feedback), always for two consecutive trials interspersed between non-rotated trials. In both conditions, the first trial with a rotation was unpredictable. On the second trial, the task was either to re-aim, and thereby compensate for the rotation experienced in the first trial (visuomotor rotation; Compensate condition), or to ignore the rotation and keep on aiming at the target (clamped feedback; Ignore condition). After-effects did not differ between conditions, indicating that the amount of implicit learning was similar, while large differences in movement direction in the second rotated trial between conditions indicated that participants successfully acquired re-aiming strategies. Importantly, PMBR power following the first rotated trial was modulated differently in the two conditions. Specifically, it decreased in both conditions, but this effect was larger when participants had to acquire a cognitive strategy and prepare to re-aim. Our results therefore suggest that the PMBR is modulated by cognitive demands of motor learning, possibly reflecting the evaluation of a behaviourally significant goal achievement error.

Visuomotor Adaptation of Lower Extremity Movements During Virtual Ball-Kicking Task.

Sophisticated soccer players can skillfully manipulate a ball with their feet depending on the external environment. This ability of goal-directed control in the lower limbs has not been fully elucidated, although upper limb movements have been studied extensively using motor adaptation tasks. The purpose of this study was to clarify how the goal-directed movements of the lower limbs is acquired by conducting an experiment of visuomotor adaptation in ball-kicking movements. In this study, healthy young participants with and without experience playing soccer or futsal performed ball-kicking movements. They were instructed to move a cursor representing the right foot position and shoot a virtual ball to a target on a display in front of them. During the learning trials, the trajectories of the virtual ball were rotated by 15° either clockwise or counterclockwise relative to the actual ball direction. As a result, participants adapted their lower limb movements to novel visuomotor perturbation regardless of the soccer playing experience, and changed their whole trajectories not just the kicking position during adaptation. These results indicate that the goal-directed lower limb movements can be adapted to the novel environment. Moreover, it was suggested that fundamental structure of visuomotor adaptation is common between goal-directed movements in the upper and lower limbs.

Asymmetrical transfer of adaptation between reaching and tracking: implications for feedforward and feedback processes.

Reaching and manual tracking are two very common tasks for studying human sensorimotor processes. Although these motor tasks rely both on feedforward and feedback processes, emphasis is more on feedforward processes for reaching and feedback processes for tracking. The extent to which feedforward and feedback processes are interrelated when being updated is not settled yet. Here, using reaching and tracking as proxies, we examined the bidirectional relationship between the update of feedforward and feedback processes. Forty right-handed participants were asked to move a joystick so as to either track a target moving rather unpredictably (pursuit tracking) or to make fast pointing movements toward a static target (center-out reaching task). Visuomotor adaptation was elicited by introducing a 45° rotation between the joystick motion and the cursor motion. Half of the participants adapted to rotation first via reaching movements and then with pursuit tracking, whereas the other half performed both tasks in opposite order. Group comparisons revealed a strong asymmetrical transfer of adaptation between tasks. Namely, although nearly complete transfer of adaptation was observed from reaching to tracking, only modest transfer was found from tracking to reaching. A control experiment (n = 10) revealed that making target motion fully predictable did not impact the latter finding. One possible interpretation is that the update of feedforward processes contributes directly to feedback processes, but the update of feedback processes engaged in tracking can be performed in isolation. These results suggest that reaching movements are supported by broader (i.e. more universal) mechanisms than tracking ones.NEW & NOTEWORTHY Reaching and manual tracking are thought to rely differently on feedforward and feedback processes. Here, we show that although nearly complete transfer of visuomotor adaptation occurs from reaching to tracking, only minimal transfer is found from tracking to reaching. Even though the update of feedforward processes (key for reaching) proved directly useful to feedback processes (key for tracking), the strong asymmetrical transfer suggests that feedback control can be updated independently from feedforward adaptation.

Prolonged Feedback Duration Does Not Affect Implicit Recalibration in a Visuomotor Rotation Task.

Visuomotor rotations are frequently used to study cognitive processes underlying motor adaptation. Explicit aiming strategies and implicit recalibration are two of these processes. A large body of literature indicates that both processes are in fact dissociable and mainly independent components that can be measured using different manipulations in visuomotor rotation tasks. Visual feedback is a crucial element in these tasks, and it therefore plays an important role when assessing explicit re-aiming and implicit recalibration. For instance, researchers have found timing of visual feedback to affect the contribution of implicit recalibration to learning: if feedback is shown only at the end of the movement (instead of continuously), implicit recalibration decreases. Similarly, participants show lower levels of implicit recalibration if visual feedback is presented with a delay (instead of immediately). We thus hypothesized that the duration of feedback availability might also play a role. The goal of this study was thus to investigate the effect of longer versus shorter feedback durations on implicit recalibration in human participants. To this end, we compared three feedback durations in a between-subject design: 200, 600, and 1200 ms. Using a large sample size, we found differences between groups to be quite small, to the point where most differences indicated statistical equivalence between group means. We therefore hypothesize that feedback duration, when only endpoint feedback is presented, has a negligible effect on implicit recalibration. We propose that future research investigate the effect of feedback duration on other parameters of adaptation, so as proprioceptive recalibration and explicit re-aiming.

Using EEG to study sensorimotor adaptation.

Sensorimotor adaptation, or the capacity to flexibly adapt movements to changes in the body or the environment, is crucial to our ability to move efficiently in a dynamic world. The field of sensorimotor adaptation is replete with rigorous behavioural and computational methods, which support strong conceptual frameworks. An increasing number of studies have combined these methods with electroencephalography (EEG) to unveil insights into the neural mechanisms of adaptation. We review these studies: discussing EEG markers of adaptation in the frequency and the temporal domain, EEG predictors for successful adaptation and how EEG can be used to unmask latent processes resulting from adaptation, such as the modulation of spatial attention. With its high temporal resolution, EEG can be further exploited to deepen our understanding of sensorimotor adaptation.

Composition and decomposition of visuomotor maps during manual tracking.

Adapting hand movements to changes in our body or the environment is essential for skilled motor behavior, as is the ability to flexibly combine experience gathered in separate contexts. However, it has been shown that when adapting hand movements to two different visuomotor perturbations in succession, interference effects can occur. Here, we investigate whether these interference effects compromise our ability to adapt to the superposition of the two perturbations. Participants tracked with a joystick, a visual target that followed a smooth but an unpredictable trajectory. Four separate groups of participants (total n = 83) completed one block of 50 trials under each of three mappings: one in which the cursor was rotated by 90° (ROTATION), one in which the cursor mimicked the behavior of a mass-spring system (SPRING), and one in which the SPRING and ROTATION mappings were superimposed (SPROT). The order of the blocks differed across groups. Although interference effects were found when switching between SPRING and ROTATION, participants who performed these blocks first performed better in SPROT than participants who had no prior experience with SPRING and ROTATION (i.e., composition). Moreover, participants who started with SPROT exhibited better performance under SPRING and ROTATION than participants who had no prior experience with each of these mappings (i.e., decomposition). Additional analyses confirmed that these effects resulted from components of learning that were specific to the rotational and spring perturbations. These results show that interference effects do not preclude the ability to compose/decompose various forms of visuomotor adaptation.NEW & NOTEWORTHY The ability to compose/decompose task representations is critical for both cognitive and behavioral flexibility. Here, we show that this ability extends to two forms of visuomotor adaptation in which humans have to perform visually guided hand movements. Despite the presence of interference effects when switching between visuomotor maps, we show that participants are able to flexibly compose or decompose knowledge acquired in previous sessions. These results further demonstrate the flexibility of sensorimotor adaptation in humans.

Taking aim at the perceptual side of motor learning: exploring how explicit and implicit learning encode perceptual error information through depth vision.

Motor learning in visuomotor adaptation tasks results from both explicit and implicit processes, each responding differently to an error signal. Although the motor output side of these processes has been extensively studied, the visual input side is relatively unknown. We investigated if and how depth perception affects the computation of error information by explicit and implicit motor learning. Two groups of participants made reaching movements to bring a virtual cursor to a target in the frontoparallel plane. The Delayed group was allowed to reaim and their feedback was delayed to emphasize explicit learning, whereas the camped group received task-irrelevant clamped cursor feedback and continued to aim straight at the target to emphasize implicit adaptation. Both groups played this game in a highly detailed virtual environment (depth condition), leveraging a cover task of playing darts in a virtual tavern, and in an empty environment (no-depth condition). The delayed group showed an increase in error sensitivity under depth relative to no-depth. In contrast, the clamped group adapted to the same degree under both conditions. The movement kinematics of the delayed participants also changed under the depth condition, consistent with the target appearing more distant, unlike the Clamped group. A comparison of the delayed behavioral data with a perceptual task from the same individuals showed that the greater reaiming in the depth condition was consistent with an increase in the scaling of the error distance and size. These findings suggest that explicit and implicit learning processes may rely on different sources of perceptual information.NEW & NOTEWORTHY We leveraged a classic sensorimotor adaptation task to perform a first systematic assessment of the role of perceptual cues in the estimation of an error signal in the 3-D space during motor learning. We crossed two conditions presenting different amounts of depth information, with two manipulations emphasizing explicit and implicit learning processes. Explicit learning responded to the visual conditions, consistent with perceptual reports, whereas implicit learning appeared to be independent of them.

Interlimb differences in visuomotor and dynamic adaptation during targeted reaching in children.

While a number of studies have focused on movement (a)symmetries between the arms in adults, less is known about movement asymmetries in typically developing children. The goal of this study was to examine interlimb differences in children when adapting to novel visuomotor and dynamic conditions while performing a center-out reaching task. We tested 13 right-handed children aged 9-11 years old. Prior to movement, one of eight targets arranged radially around the start position was randomly displayed. Movements were made either with the right (dominant) arm or the left (nondominant) arm. The children participated in two experiments separated by at least one week. In one experiment, subjects were exposed to a rotated visual display (30° about the start circle); and in the other, a 1 kg mass (attached eccentrically to the forearm axis). Each experiment consisted of three blocks: pre-exposure, exposure and post-exposure. Three measures of task performance were calculated from hand trajectory data: hand-path deviation from the straight target line, direction error at peak velocity and final position error. Results showed that during visuomotor adaptation, no interlimb differences were observed for any of the three measures. During dynamic adaptation, however, a significant difference between the arms was observed at the first cycle during dynamic adaptation. With regard to the aftereffects observed during the post-exposure block, direction error data indicate considerably large aftereffects for both arms during visuomotor adaptation; and there was a significant difference between the arms, resulting in substantially larger aftereffects for the right arm. Similarly, dynamic adaptation results also showed a significant difference between the arms; and post hoc analyses indicated that aftereffects were present only for the right arm. Collectively, these findings indicate that the dominant arm advantage for developing an internal model associated with a novel visuomotor or dynamic transform, as previously shown in young adults, may already be apparent at 9 to 11-year old children.

Methods matter: Your measures of explicit and implicit processes in visuomotor adaptation affect your results.

Visuomotor rotations are frequently used to study the different processes underlying motor adaptation. Explicit aiming strategies and implicit recalibration are two of these processes. Various methods, which differ in their underlying assumptions, have been used to dissociate the two processes. Direct methods, such as verbal reports, assume explicit knowledge to be verbalizable, where indirect methods, such as the exclusion, assume that explicit knowledge is controllable. The goal of this study was thus to directly compare verbal reporting with exclusion in two different conditions: during consistent reporting and during intermittent reporting. Our results show that our two conditions lead to a dissociation between the measures. In the consistent reporting group, all measures showed similar results. However, in the intermittent reporting group, verbal reporting showed more explicit re-aiming and less implicit adaptation than exclusion. Curiously, when exclusion was measured again, after the end of learning, the differences were no longer apparent. We suspect this may reflect selective decay in implicit adaptation, as has been reported previously. All told, our results clearly indicate that methods of measurement can affect the amount of explicit re-aiming and implicit adaptation that is measured. Since it has been previously shown that both explicit re-aiming and implicit adaptation have multiple components, discrepancies between these different methods may arise because different measures reflect different components.

Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands.

Intermittent exposure to a sensorimotor perturbation, such as a visuomotor rotation, is known to cause a directional bias on the subsequent movement that opposes the previously experienced perturbation. To date, it is unclear whether the parietal cortex is causally involved in this postperturbation movement bias. In a recent electroencephalogram study, Savoie et al. (2018) observed increased parietal activity in response to an intermittent visuomotor perturbation, raising the possibility that the parietal cortex could subserve this change in motor behavior. The goal of the present study was to causally test this hypothesis. Human participants (N = 28) reached toward one of two visual targets located on either side of a fixation point, while being pseudorandomly submitted to a visuomotor rotation. On half of all rotation trials, single-pulse transcranial magnetic stimulation (TMS) was applied over the right (N = 14) or left (N = 14) parietal cortex 150 ms after visual feedback provision. To determine whether TMS influenced the postperturbation bias, reach direction was compared on trials that followed rotation with (RS + 1) and without (R + 1) TMS. It was hypothesized that interfering with parietal activity would reduce the movement bias following rotated trials. Results revealed a significant and robust postrotation directional bias compared with both rotation and null rotation trials. Contrary to our hypothesis, however, neither left nor right parietal stimulation significantly impacted the postrotation bias. These data suggest that the parietal areas targeted here may not be critical for perturbation-induced motor output changes to emerge.

Task Errors Drive Memories That Improve Sensorimotor Adaptation.

Traditional views of sensorimotor adaptation (i.e., adaptation of movements to perturbed sensory feedback) emphasize the role of automatic, implicit correction of sensory prediction errors. However, latent memories formed during sensorimotor adaptation, manifest as improved relearning (e.g., savings), have recently been attributed to strategic corrections of task errors (failures to achieve task goals). To dissociate contributions of task errors and sensory prediction errors to latent sensorimotor memories, we perturbed target locations to remove or enforce task errors during learning and/or test, with male/female human participants. Adaptation improved after learning in all conditions where participants were permitted to correct task errors, and did not improve whenever we prevented correction of task errors. Thus, previous correction of task errors was both necessary and sufficient to improve adaptation. In contrast, a history of sensory prediction errors was neither sufficient nor obligatory for improved adaptation. Limiting movement preparation time showed that the latent memories driven by learning to correct task errors take at least two forms: a time-consuming but flexible component, and a rapidly expressible, inflexible component. The results provide strong support for the idea that movement corrections driven by a failure to successfully achieve movement goals underpin motor memories that manifest as savings. Such persistent memories are not exclusively mediated by time-consuming strategic processes but also comprise a rapidly expressible but inflexible component. The distinct characteristics of these putative processes suggest dissociable underlying mechanisms, and imply that identification of the neural basis for adaptation and savings will require methods that allow such dissociations.SIGNIFICANCE STATEMENT Latent motor memories formed during sensorimotor adaptation manifest as improved adaptation when sensorimotor perturbations are reencountered. Conflicting theories suggest that this "savings" is underpinned by different mechanisms, including a memory of successful actions, a memory of errors, or an aiming strategy to correct task errors. Here we show that learning to correct task errors is sufficient to show improved subsequent adaptation with respect to naive performance, even when tested in the absence of task errors. In contrast, a history of sensory prediction errors is neither sufficient nor obligatory for improved adaptation. Finally, we show that latent sensorimotor memories driven by task errors comprise at least two distinct components: a time-consuming, flexible component, and a rapidly expressible, inflexible component.

Combined action observation and motor imagery facilitates visuomotor adaptation in children with developmental coordination disorder.

The internal modelling deficit (IMD) hypothesis suggests that motor control issues associated with Developmental Coordination Disorder (DCD) are the result of impaired predictive motor control. In this study, we examined the benefits of a combined action observation and motor imagery (AO + MI) intervention designed to alleviate deficits in internal modelling and improve eye-hand coordination during a visuomotor rotation task. Twenty children with DCD were randomly assigned to either an AO + MI group (who watched a video of a performer completing the task whilst simultaneously imagining the kinaesthetic sensations associated with action execution) or a control group (who watched unrelated videos involving no motor content). Each group then attempted to learn a 90° visuomotor rotation while measurements of completion time, eye-movement behaviour and movement kinematics were recorded. As predicted, after training, the AO + MI group exhibited quicker completion times, more target-focused eye-movement behaviour and smoother movement kinematics compared to the control group. No significant after-effects were present. These results offer further support for the IMD hypothesis and suggest that AO + MI interventions may help to alleviate such deficits and improve motor performance in children with DCD.

Combining Action Observation and Motor Imagery Improves Eye-Hand Coordination during Novel Visuomotor Task Performance.

In this study, we compared the effectiveness of concurrent action observation and motor imagery (AO + MI), observing with the intent to imitate (active observation; AO), and passive observation (PO) training interventions for improving eye-hand coordination. Fifty participants were assigned to five groups [AO + MI, AO, PO, physical practice (PP); control] and performed a visuomotor rotation task, whilst eye movements were recorded. Each participant then performed 20 task trials in a training intervention before repeating the visuomotor rotation task in a post-test. As expected, PP produced the greatest improvement in task performance and eye-hand coordination. However, in comparison to the control group, AO + MI training produced a statistically significant increase in both task performance and eye-hand coordination, but no such improvements were found following AO or PO.

Activity in Primary Motor Cortex Related to Visual Feedback.

Neural modulation in primate motor cortex exhibits complex patterns. We found that modulation during reaching could be separated into discrete temporal epochs. To determine if these epochs are driven by behavioral events, monkeys performed variations of a center-out reaching task. Monkeys viewed a computer cursor matched to hand position and a radial target at 1 of 16 locations. In some trials, they performed a visuomotor rotation (the cursor moved at an angle to the hand). After adaptation, encoding changes for single units are temporally structured: adaptation could affect one temporal component of a unit's response but not another. In half the normal and perturbed trials, we removed visual feedback before movement. Adaptation-sensitive firing components toward the end of movement are often weak or absent during reaches without feedback. These results show that temporal structure in motor cortical activity is driven by behavior, with a discrete component related to visual feedback.

Eye Movements during Visuomotor Adaptation Represent Only Part of the Explicit Learning.

Visuomotor rotations are learned through a combination of explicit strategy and implicit recalibration. However, measuring the relative contribution of each remains a challenge and the possibility of multiple explicit and implicit components complicates the issue. Recent interest has focused on the possibility that eye movements reflects explicit strategy. Here we compared eye movements during adaptation to two accepted measures of explicit learning: verbal report and the exclusion test. We found that while reporting, all subjects showed a match among all three measures. However, when subjects did not report their intention, the eye movements of some subjects suggested less explicit adaptation than what was measured in an exclusion test. Interestingly, subjects whose eye movements did match their exclusion could be clustered into the following two subgroups: fully implicit learners showing no evidence of explicit adaptation and explicit learners with little implicit adaptation. Subjects showing a mix of both explicit and implicit adaptation were also those where eye movements showed less explicit adaptation than did exclusion. Thus, our results support the idea of multiple components of explicit learning as only part of the explicit learning is reflected in the eye movements. Individual subjects may use explicit components that are reflected in the eyes or those that are not or some mixture of the two. Analysis of reaction times suggests that the explicit components reflected in the eye movements involve longer reaction times. This component, according to recent literature, may be related to mental rotation.