Goal-directed modulation of stretch reflex gains is reduced in the non-dominant upper limb.

Most individuals experience their dominant arm as being more dexterous than the non-dominant arm, but the neural mechanisms underlying this asymmetry in motor behaviour are unclear. Using a delayed-reach task, we have recently demonstrated strong goal-directed tuning of stretch reflex gains in the dominant upper limb of human participants. Here, we used an equivalent experimental paradigm to address the neural mechanisms that underlie the preparation for reaching movements with the non-dominant upper limb. There were consistent effects of load, preparatory delay duration and target direction on the long latency stretch reflex. However, by comparing stretch reflex responses in the non-dominant arm with those previously documented in the dominant arm, we demonstrate that goal-directed tuning of short and long latency stretch reflexes is markedly weaker in the non-dominant limb. The results indicate that the motor performance asymmetries across the two upper limbs are partly due to the more sophisticated control of reflexive stiffness in the dominant limb, likely facilitated by the superior goal-directed control of muscle spindle receptors. Our findings therefore suggest that fusimotor control may play a role in determining performance of complex motor behaviours and support existing proposals that the dominant arm is better supplied than the non-dominant arm for executing more complex tasks, such as trajectory control.

Congruent visual cues speed dynamic motor adaptation.

Motor adaptation to novel dynamics occurs rapidly using sensed errors to update the current motor memory. This adaption is strongly driven by proprioceptive and visual signals that indicate errors in the motor memory. Here, we extend this previous work by investigating whether the presence of additional visual cues could increase the rate of motor adaptation, specifically when the visual motion cue is congruent with the dynamics. Six groups of participants performed reaching movements while grasping the handle of a robotic manipulandum. A visual cue (small red circle) was connected to the cursor (representing the hand position) via a thin red bar. After a baseline, a unidirectional (3 groups) or bidirectional (3 groups) velocity-dependent force field was applied during the reach. For each group, the movement of the red object relative to the cursor was either congruent with the force field dynamics, incongruent with the force field dynamics, or constant (fixed distance from the cursor). Participants adapted more to the unidirectional force fields than to the bidirectional force field groups. However, across both force fields, groups in which the visual cues matched the type of force field (congruent visual cue) exhibited higher final adaptation level at the end of learning than the control or incongruent conditions. In all groups, we observed that an additional congruent cue assisted the formation of the motor memory of the external dynamics. We then demonstrate that a state estimation-based model that integrates proprioceptive and visual information can successfully replicate the experimental data.NEW & NOTEWORTHY We demonstrate that adaptation to novel dynamics is stronger when additional online visual cues that are congruent with the dynamics are presented during adaptation, compared with either a constant or incongruent visual cue. This effect was found regardless of whether a bidirectional or unidirectional velocity-dependent force field was presented to the participants. We propose that this effect might arise through the inclusion of this additional visual cue information within the state estimation process.

Assistive Loading Promotes Goal-Directed Tuning of Stretch Reflex Gains.

Voluntary movements are prepared before they are executed. Preparatory activity has been observed across the CNS and recently documented in first-order neurons of the human PNS (i.e., in muscle spindles). Changes seen in sensory organs suggest that independent modulation of stretch reflex gains may represent an important component of movement preparation. The aim of the current study was to further investigate the preparatory modulation of short-latency stretch reflex responses (SLRs) and long-latency stretch reflex responses (LLRs) of the dominant upper limb of human subjects. Specifically, we investigated how different target parameters (target distance and direction) affect the preparatory tuning of stretch reflex gains in the context of goal-directed reaching, and whether any such tuning depends on preparation duration and the direction of background loads. We found that target distance produced only small variations in reflex gains. In contrast, both SLR and LLR gains were strongly modulated as a function of target direction, in a manner that facilitated the upcoming voluntary movement. This goal-directed tuning of SLR and LLR gains was present or enhanced when the preparatory delay was sufficiently long (>250 ms) and the homonymous muscle was unloaded [i.e., when a background load was first applied in the direction of homonymous muscle action (assistive loading)]. The results extend further support for a relatively slow-evolving process in reach preparation that functions to modulate reflexive muscle stiffness, likely via the independent control of fusimotor neurons. Such control can augment voluntary goal-directed movement and is triggered or enhanced when the homonymous muscle is unloaded.

Stability of inverted pendulum reveals transition between predictive control and impedance control in grip force modulation.

During object manipulation, our sensorimotor sys-tem needs to represent the objects dynamics in order to better control it. This is especially important in the case of grip force control where small forces can cause the object to slip from our fingers, and excessive forces can cause fatigue or even damage the object. While the tradeoff between these two constraints is clear for stable objects, such as lifting a soda can, it is less clear how the sensorimotor system adjusts the grip force for unstable objects. For this purpose, we measured the change in the grip force of individual human participants while they stabilize five different lengths of an inverted pendulum. These lengths set different dynamics of the pendulum, ranging in their degree of controllability. We observed two main states during such manipulation, a marginally stable state of the pendulum and a stabilization state in which participants acted to stabilize the system. While during the stabilization state participants increased their applied grip force, for the stable state we observed a mixed behaviour. For small and less controllable pendulums, grip force increased while for larger pendulums, participants could modulate the the grip force according to the anticipated load forces. Based on these results, we suggest that the pendulum dynamics change the control strategy between predictive control and impedance control.

Motor Learning in Response to Different Experimental Pain Models Among Healthy Individuals: A Systematic Review.

Learning new movement patterns is a normal part of daily life, but of critical importance in both sport and rehabilitation. A major question is how different sensory signals are integrated together to give rise to motor adaptation and learning. More specifically, there is growing evidence that pain can give rise to alterations in the learning process. Despite a number of studies investigating the role of pain on the learning process, there is still no systematic review to summarize and critically assess investigations regarding this topic in the literature. Here in this systematic review, we summarize and critically evaluate studies that examined the influence of experimental pain on motor learning. Seventeen studies that exclusively assessed the effect of experimental pain models on motor learning among healthy human individuals were included for this systematic review, carried out based on the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement. The results of the review revealed there is no consensus regarding the effect of pain on the skill learning acquisition and retention. However, several studies demonstrated that participants who experienced pain continued to express a changed motor strategy to perform a motor task even 1 week after training under the pain condition. The results highlight a need for further studies in this area of research, and specifically to investigate whether pain has different effects on motor learning depending on the type of motor task.

Active strategies for multisensory conflict suppression in the virtual hand illusion.

The perception of our body in space is flexible and manipulable. The predictive brain hypothesis explains this malleability as a consequence of the interplay between incoming sensory information and our body expectations. However, given the interaction between perception and action, we might also expect that actions would arise due to prediction errors, especially in conflicting situations. Here we describe a computational model, based on the free-energy principle, that forecasts involuntary movements in sensorimotor conflicts. We experimentally confirm those predictions in humans using a virtual reality rubber-hand illusion. Participants generated movements (forces) towards the virtual hand, regardless of its location with respect to the real arm, with little to no forces produced when the virtual hand overlaid their physical hand. The congruency of our model predictions and human observations indicates that the brain-body is generating actions to reduce the prediction error between the expected arm location and the new visual arm. This observed unconscious mechanism is an empirical validation of the perception-action duality in body adaptation to uncertain situations and evidence of the active component of predictive processing.

Nanomesh pressure sensor for monitoring finger manipulation without sensory interference.

Monitoring of finger manipulation without disturbing the inherent functionalities is critical to understand the sense of natural touch. However, worn or attached sensors affect the natural feeling of the skin. We developed nanomesh pressure sensors that can monitor finger pressure without detectable effects on human sensation. The effect of the sensor on human sensation was quantitatively investigated, and the sensor-applied finger exhibits comparable grip forces with those of the bare finger, even though the attachment of a 2-micrometer-thick polymeric film results in a 14% increase in the grip force after adjusting for friction. Simultaneously, the sensor exhibits an extreme mechanical durability against cyclic shearing and friction greater than hundreds of kilopascals.

Asymmetry in kinematic generalization between visual and passive lead-in movements are consistent with a forward model in the sensorimotor system.

In our daily life we often make complex actions comprised of linked movements, such as reaching for a cup of coffee and bringing it to our mouth to drink. Recent work has highlighted the role of such linked movements in the formation of independent motor memories, affecting the learning rate and ability to learn opposing force fields. In these studies, distinct prior movements (lead-in movements) allow adaptation of opposing dynamics on the following movement. Purely visual or purely passive lead-in movements exhibit different angular generalization functions of this motor memory as the lead-in movements are modified, suggesting different neural representations. However, we currently have no understanding of how different movement kinematics (distance, speed or duration) affect this recall process and the formation of independent motor memories. Here we investigate such kinematic generalization for both passive and visual lead-in movements to probe their individual characteristics. After participants adapted to opposing force fields using training lead-in movements, the lead-in kinematics were modified on random trials to test generalization. For both visual and passive modalities, recalled compensation was sensitive to lead-in duration and peak speed, falling off away from the training condition. However, little reduction in force was found with increasing lead-in distance. Interestingly, asymmetric transfer between lead-in movement modalities was also observed, with partial transfer from passive to visual, but very little vice versa. Overall these tuning effects were stronger for passive compared to visual lead-ins demonstrating the difference in these sensory inputs in regulating motor memories. Our results suggest these effects are a consequence of state estimation, with differences across modalities reflecting their different levels of sensory uncertainty arising as a consequence of dissimilar feedback delays.

A Technique for Measuring Visuomotor Feedback Contributions to the Control of an Inverted Pendulum.

We developed a new technique to measure the contributions of rapid visuomotor feedback responses to the stabilization of a simulated inverted pendulum. Human participants balanced an inverted pendulum simulated on a robotic manipulandum. At a random time during the balancing task, the visual representation of the tip of the pendulum was shifted by a small displacement to the left or right while the motor response was measured. This response was either the exerted force against a fixation position, or the motion to re-stabilize the pendulum in the free condition. Our results demonstrate that rapid involuntary visuomotor feedback responses contribute to the stabilization of the pendulum.

Feedback Delay Changes the Control of an Inverted Pendulum.

We recently developed a simulated inverted pendulum in order to examine human sensorimotor control strategies for stabilization. This simulated system allows us to manipulate the visual and haptic feedback independently from the physical dynamics of the task. Here we examine the effect of sensory delay in a balancing task. Human participants attempted to balance an inverted pendulum (simulated on a robotic manipulandum) with three different added delays (25, 50, and 75 ms), where the same delay was added to both the visual and haptic feedback. Increasing sensory delays decreased the ability of the participants to stabilize the pendulum. Investigation into the online control of the pendulum showed that with longer delays participants reduced their movement frequency but increased the amplitudes of their corrections.

LQG framework explains performance of balancing inverted pendulum with incongruent visual feedback.

Successful manipulation of objects requires forming internal representations of the object dynamics. To do so, the sensorimotor system uses visual feedback of the object movement allowing us to estimate the object state and build the representation. One way to investigate this mechanism is by introducing a discrepancy between the visual feedback about the object's movement and the actual movement. This causes a decline in the ability to accurately control the object, shedding light about possible factors influencing the performance. In this study, we show that an optimal feedback control framework can account for the performance and kinematic characteristics of balancing an inverted pendulum when visual feedback of pendulum tip did not represent the actual pendulum tip. Our model suggests a possible mechanism for the role of visual feedback on forming internal representation of objects' dynamics.

Controller Gains of an Inverted Pendulum are Influenced by the Visual Feedback Position.

In this study we experimentally test and model the control behavior of human participants when controlling inverted pendulums of different dynamic lengths, and with visual feedback of varying congruence to these dynamic lengths. Participants were asked to stabilize the inverted pendulum of L = 1 m and L = 4 m, with visual feedback shown at various distances along the pendulum. We fit a family of linear models to the control input (cart velocity) applied by participants. We further tested the models by predicting this control input for a pendulum with dynamic length L = 2 m and comparing the prediction to the experimental data. We show that the sum of proportional error correction and a term inversely proportional to visual feedback gain can well describe the control in human participants.

A Simulated Inverted Pendulum to Investigate Human Sensorimotor Control.

Sensorimotor control regulates balance and stability as well as adaptation to the external environment. We introduce the use of a simulated inverted pendulum to study human sensorimotor control, demonstrating that this system introduces similar control challenges to human subjects as a physical inverted pendulum. Participants exhibited longer stabilization of the system as the pendulum length between the hand and the center of mass increased while the required control input varied in a non-monotonic, yet predictable manner. Finally, we show that the experimental results can be modelled as a PD controller with a time delay of $\tau = 140$ ms, matching the human visuomotor delay. Our results provide evidence of the importance of vision in a control of unstable systems and serve as a proof of concept of a simulated inverted pendulum.

Influence of Visual Feedback on the Sensorimotor Control of an Inverted Pendulum.

We examine the visual influence of stabilization in human sensorimotor control using a simulated inverted pendulum. As the inverted pendulum is fully simulated, we are able to manipulate the visual feedback independently from the dynamics during the motor control task. Human subjects performed a balancing task of an upright pendulum on a robotic manipulandum in two different visual feedback conditions. First we examined how subjects perform a task where the visual feedback is congruent with the pendulum dynamics. Second we tested how subjects performed when the physical dynamics were fixed but the visual feedback of the pendulum length was modulated. Subjects exhibited deficits in the control of the pendulum when haptic and visual feedback did not match, even when the visual feedback provided more sensitive information about the state of the pendulum. Overall we demonstrate the importance of accurate feedback regarding task dynamics for stabilization.

Rapid visuomotor feedback gains are tuned to the task dynamics.

Adaptation to novel dynamics requires learning a motor memory, or a new pattern of predictive feedforward motor commands. Recently, we demonstrated the upregulation of rapid visuomotor feedback gains early in curl force field learning, which decrease once a predictive motor memory is learned. However, even after learning is complete, these feedback gains are higher than those observed in the null field trials. Interestingly, these upregulated feedback gains in the curl field were not observed in a constant force field. Therefore, we suggest that adaptation also involves selectively tuning the feedback sensitivity of the sensorimotor control system to the environment. Here, we test this hypothesis by measuring the rapid visuomotor feedback gains after subjects adapt to a variety of novel dynamics generated by a robotic manipulandum in three experiments. To probe the feedback gains, we measured the magnitude of the motor response to rapid shifts in the visual location of the hand during reaching. While the feedback gain magnitude remained similar over a larger than a fourfold increase in constant background load, the feedback gains scaled with increasing lateral resistance and increasing instability. The third experiment demonstrated that the feedback gains could also be independently tuned to perturbations to the left and right, depending on the lateral resistance, demonstrating the fractionation of feedback gains to environmental dynamics. Our results show that the sensorimotor control system regulates the gain of the feedback system as part of the adaptation process to novel dynamics, appropriately tuning them to the environment.NEW & NOTEWORTHY Here, we test whether rapid visuomotor feedback responses are selectively tuned to the task dynamics. The responses do not exhibit gain scaling, but they do vary with the level and stability of task dynamics. Moreover, these feedback gains are independently tuned to perturbations to the left and right, depending on these dynamics. Our results demonstrate that the sensorimotor control system regulates the feedback gain as part of the adaptation process, tuning them appropriately to the environment.

Temporal Evolution of Spatial Computations for Visuomotor Control.

Goal-directed reaching movements are guided by visual feedback from both target and hand. The classical view is that the brain extracts information about target and hand positions from a visual scene, calculates a difference vector between them, and uses this estimate to control the movement. Here we show that during fast feedback control, this computation is not immediate, but evolves dynamically over time. Immediately after a change in the visual scene, the motor system generates independent responses to the errors in hand and target location. Only about 200 ms later, the changes in target and hand positions are combined appropriately in the response, slowly converging to the true difference vector. Therefore, our results provide evidence for the temporal evolution of spatial computations in the human visuomotor system, in which the accurate difference vector computation is first estimated by a fast approximation.

Fractionation of the visuomotor feedback response to directions of movement and perturbation.

Recent studies have highlighted the modulation and control of feedback gains as support for optimal feedback control. While many experiments contrast feedback gains across different environments, only a few have demonstrated the appropriate modulation of feedback gains from one movement to the next. Here we extend previous work by examining whether different visuomotor feedback gains can be learned for different directions of movement or perturbation directions in the same posture. To do this we measure visuomotor responses (involuntary motor responses to shifts in the visual feedback of the hand) during reaching movements. Previous work has demonstrated that these feedback responses can be modulated depending on the statistical distributions of the environment. Specifically, feedback gains were upregulated for task-relevant environments and downregulated for task-irrelevant environments. Using these two statistical distributions, the first experiment examined whether these feedback responses could be independently modulated for the same limb posture for two directions of movement (same limb posture but on either an inward or outward movement), while the second examined whether the feedback responses could modulate, within a single movement, to perturbations to the left or right of the reach. Both experiments demonstrated that visuomotor feedback responses could be learned independently such that the response was appropriate for the environment. This work demonstrates that feedback gains can be simultaneously tuned (upregulated and downregulated) depending on the state of the body and the environment. The results indicate the degree to which feedback responses can be fractionated in order to adapt to the world.

Selection and control of limb posture for stability.

Impedance control can be used to stabilize the limb against both instability and unpredictable perturbations. Limb posture influences motor noise, energy usage and limb impedance as well as their interaction. Here we examine whether subjects use limb posture as part of a mechanism to regulate limb stability. Subjects performed stabilization tasks while attached to a two dimensional robotic manipulandum which generated a virtual environment. Subjects were instructed that they could perform the stabilization task anywhere in the workspace, while the chosen postures were tracked as subjects repeated the task. In order to investigate the mechanisms behind the chosen limb postures, simulations of the neuro-mechanical system were performed. The results indicate that posture selection is performed to provide energy efficiency in the presence of force variability.

Visuomotor feedback gains upregulate during the learning of novel dynamics.

At an early stage of learning novel dynamics, changes in muscle activity are mainly due to corrective feedback responses. These feedback contributions to the overall motor command are gradually reduced as feedforward control is learned. The temporary increased use of feedback could arise simply from the large errors in early learning with either unaltered gains or even slightly downregulated gains, or from an upregulation of the feedback gains when feedforward prediction is insufficient. We therefore investigated whether the sensorimotor control system alters feedback gains during adaptation to a novel force field generated by a robotic manipulandum. To probe the feedback gains throughout learning, we measured the magnitude of involuntary rapid visuomotor responses to rapid shifts in the visual location of the hand during reaching movements. We found large increases in the magnitude of the rapid visuomotor response whenever the dynamics changed: both when the force field was first presented, and when it was removed. We confirmed that these changes in feedback gain are not simply a byproduct of the change in background load, by demonstrating that this rapid visuomotor response is not load sensitive. Our results suggest that when the sensorimotor control system experiences errors, it increases the gain of the visuomotor feedback pathways to deal with the unexpected disturbances until the feedforward controller learns the appropriate dynamics. We suggest that these feedback gains are upregulated with increased uncertainty in the knowledge of the dynamics to counteract any errors or disturbances and ensure accurate and skillful movements.