Motor learning and transfer: from feedback to feedforward control

AbstractPrevious work has demonstrated that when learning a new motor task, the nervous system modifies feedforward (ie. voluntary) motor commands and that such learning transfers to fast feedback (ie. reflex) responses evoked by mechanical perturbations. Here we show the inverse, that learning new feedback responses transfers to feedforward motor commands. Sixty human participants (34 females) used a robotic exoskeleton and either 1) received short duration mechanical perturbations (20 ms) that created pure elbow rotation or 2) generated self-initiated pure elbow rotations. They did so with the shoulder joint free to rotate (normal arm dynamics) or locked (altered arm dynamics) by the robotic manipulandum. With the shoulder unlocked, the perturbation evoked clear shoulder muscle activity in the long-latency stretch reflex epoch (50-100ms post-perturbation), as required for countering the imposed joint torques, but little muscle activity thereafter in the so-called voluntary response. After locking the shoulder joint, which alters the required joint torques to counter pure elbow rotation, we found a reliable reduction in the long-latency stretch reflex over many trials. This reduction transferred to feedforward control as we observed 1) a reduction in shoulder muscle activity during self-initiated pure elbow rotation trials and 2) kinematic errors (ie. aftereffects) in the direction predicted when failing to compensate for normal arm dynamics, even though participants never practiced self-initiated movements with the shoulder locked. Taken together, our work shows that transfer between feedforward and feedback control is bidirectional, furthering the notion that these processes share common neural circuits that underlie motor learning and transfer.

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Shared internal models for feedforward and feedback control of arm dynamics in non-human primates

10.1101/2020.04.05.026757 ◽

2020 ◽

Author(s):

Rodrigo S. Maeda ◽

Rhonda Kersten ◽

J. Andrew Pruszynski

Keyword(s):

Feedback Control ◽

Muscle Activity ◽

Shoulder Joint ◽

Feedforward Control ◽

Neural Mechanisms ◽

Shoulder Muscle ◽

Intersegmental Dynamics ◽

Systematic Reduction ◽

Elbow Motion ◽

Feedback Responses

AbstractPrevious work has shown that humans account for and learn novel properties or the arm’s dynamics, and that such learning causes changes in both the predictive (i.e., feedforward) control of reaching and reflex (i.e., feedback) responses to mechanical perturbations. Here we show that similar observations hold in old-world monkeys (macaca fascicularis). Two monkeys were trained to use an exoskeleton to perform a single-joint elbow reaching and to respond to mechanical perturbations that created pure elbow motion. Both of these tasks engaged robust shoulder muscle activity as required to account for the torques that typically arise at the shoulder when the forearm rotates around the elbow joint (i.e., intersegmental dynamics). We altered these intersegmental arm dynamics by having the monkeys generate the same elbow movements with the shoulder joint either free to rotate, as normal, or fixed by the robotic manipulandum, which eliminates the shoulder torques caused by forearm rotation. After fixing the shoulder joint, we found a systematic reduction in shoulder muscle activity. In addition, after releasing the shoulder joint again, we found evidence of kinematic aftereffects (i.e., reach errors) in the direction predicted if failing to compensate for normal arm dynamics. We also tested whether such learning transfers to feedback responses evoked by mechanical perturbations and found a reduction in shoulder feedback responses, as appropriate for these altered arm intersegmental dynamics. Demonstrating this learning and transfer in non-human primates will allow the investigation of the neural mechanisms involved in feedforward and feedback control of the arm’s dynamics.

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Generalizing movement patterns following shoulder fixation

Journal of Neurophysiology ◽

10.1152/jn.00696.2019 ◽

2020 ◽

Vol 123 (3) ◽

pp. 1193-1205 ◽

Cited By ~ 3

Author(s):

Rodrigo S. Maeda ◽

Julia M. Zdybal ◽

Paul L. Gribble ◽

J. Andrew Pruszynski

Keyword(s):

Muscle Activity ◽

Shoulder Joint ◽

Internal Model ◽

Movement Patterns ◽

Partial Reduction ◽

Forearm Rotation ◽

General Internal ◽

Shoulder Muscle ◽

Intersegmental Dynamics ◽

Partial Learning

Generalizing newly learned movement patterns beyond the training context is challenging for most motor learning situations. Here we tested whether learning of a new physical property of the arm during self-initiated reaching generalizes to new arm configurations. Human participants performed a single-joint elbow reaching task and/or countered mechanical perturbations that created pure elbow motion with the shoulder joint free to rotate or locked by the manipulandum. With the shoulder free, we found activation of shoulder extensor muscles for pure elbow extension trials, appropriate for countering torques that arise at the shoulder due to forearm rotation. After locking the shoulder joint, we found a partial reduction in shoulder muscle activity, appropriate because locking the shoulder joint cancels the torques that arise at the shoulder due to forearm rotation. In our first three experiments, we tested whether and to what extent this partial reduction in shoulder muscle activity generalizes when reaching in different situations: 1) different initial shoulder orientation, 2) different initial elbow orientation, and 3) different reach distance/speed. We found generalization for the different shoulder orientation and reach distance/speed as measured by a reliable reduction in shoulder activity in these situations but no generalization for the different elbow orientation. In our fourth experiment, we found that generalization is also transferred to feedback control by applying mechanical perturbations and observing reflex responses in a distinct shoulder orientation. These results indicate that partial learning of new intersegmental dynamics is not sufficient for modifying a general internal model of arm dynamics. NEW & NOTEWORTHY Here we show that partially learning to reduce shoulder muscle activity following shoulder fixation generalizes to other movement conditions, but it does not generalize globally. These findings suggest that the partial learning of new intersegmental dynamics is not sufficient for modifying a general internal model of the arm’s dynamics.

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Trunk Angle Modulates Feedforward and Feedback Control during Single-Limb Squatting

Journal of Functional Morphology and Kinesiology ◽

10.3390/jfmk6040082 ◽

2021 ◽

Vol 6 (4) ◽

pp. 82

Author(s):

Kristin A. Johnson ◽

Shojiro Nozu ◽

Richard K. Shields

Keyword(s):

Motor Control ◽

Feedback Control ◽

Muscle Activity ◽

Feedforward Control ◽

Cruciate Ligament ◽

Dynamic Performance ◽

Ligament Injury ◽

Long Latency ◽

Long Latency Reflexes ◽

Feedback Responses

Trunk positioning and unexpected perturbations are high-risk conditions at the time of anterior cruciate ligament injury. The influence of trunk positioning on motor control responses to perturbation during dynamic performance is not known. We tested the influence of trunk position on feedforward and feedback control during unexpected perturbations while performing a novel single-limb squatting task. We also assessed the degree that feedforward control was predictive of feedback responses. In the flexed trunk condition, there were increased quadriceps (p < 0.026) and gluteus medius long-latency reflexes (p < 0.001) and greater quadriceps-to-hamstrings co-contraction during feedforward (p = 0.017) and feedback (p = 0.007) time bins. Soleus long-latency reflexes increased more than 100% from feedforward muscle activity regardless of trunk condition. Feedforward muscle activity differentially predicted long-latency reflex responses depending on the muscle (R2: 0.47–0.97). These findings support the concept that trunk positioning influences motor control responses to perturbation and that feedback responses may be invariant to the feedforward control strategy.

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Explicit feedback and instruction do not change shoulder muscle activity reduction after shoulder fixation

10.1101/2020.03.25.008466 ◽

2020 ◽

Cited By ~ 1

Author(s):

Rodrigo S. Maeda ◽

Julia M. Zdybal ◽

Paul L. Gribble ◽

J. Andrew Pruszynski

Keyword(s):

Muscle Activity ◽

Shoulder Joint ◽

The Third ◽

Task Instructions ◽

Visual Biofeedback ◽

Shoulder Muscle ◽

Intersegmental Dynamics ◽

Elbow Movement ◽

Human Participants ◽

And Task

AbstractGenerating pure elbow rotation requires contracting muscles at both the shoulder and elbow joints to counter torques that arise at the shoulder when the forearm rotates (i.e., intersegmental dynamics). Previous work has shown that human participants learn to reduce their shoulder muscle activity if the same elbow movement is performed after the shoulder joint is mechanically locked, which is appropriate because locking the shoulder joint eliminates the torques that arise at the shoulder when the forearm rotates. However, this learning is slow (i.e., it unfolds over hundreds of trials) and incomplete (i.e., shoulder activity is not fully eliminated). Here we investigated whether and how the addition of explicit strategies and biofeedback modulate this type of learning. Three groups of human participants (N = 55) performed voluntary pure elbow rotations using a robotic exoskeleton that permits shoulder and elbow rotation in a horizontal plane. Participants did the task with the shoulder free to move (baseline), then with the shoulder joint locked by the robotic manipulandum (adaptation), and then with the shoulder free to move again (post-adaptation). The first group of participants performed this protocol and received no instructions about what to do after their shoulder was locked. The second group of participants received visual feedback about their shoulder muscle activity after each movement and was instructed to reduce their shoulder activity to zero. The third group of participants also received visual biofeedback, but it was removed part way through the experiment. We found that, although all groups learned, the rate and magnitude of learning was not reliably different across the groups. Taken together, our results suggest that learning new arm dynamics, unlike other motor learning paradigms, unfolds independent of explicit instructions, biofeedback and task instructions.

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The influence of startReact on long-latency reflexive muscle activation during the transition from posture to movement

10.1101/180554 ◽

2017 ◽

Author(s):

Claire F. Honeycutt ◽

Vengateswaran J. Ravichandran ◽

Eric J. Perreault

Keyword(s):

Muscle Activity ◽

Stretch Reflex ◽

Muscle Activation ◽

Strong Influence ◽

Time Window ◽

Motor Tasks ◽

Motor Pathways ◽

Long Latency ◽

Startreact Effect ◽

The Continuum

AbstractMany motor tasks involve transitions from posture to movement such as shifting from holding an object to setting it on a surface. Although many movements are voluntary processes, they are facilitated through motor pathways that span the continuum between reflexive and voluntary control. The mechanisms driving the long-latency stretch reflex (LLSR) have remained hotly contested. Recently, startReact has been shown to influence the fast muscular response to perturbations (Ravichandran et. al. 2013). The objective of this study was to evaluate how the LLSR and startReact impact the muscular response during the transition from posture to movement. We hypothesized that both the LLSR and startReact would be involved throughout the transition from posture to movement; however there would be a clear transition from LLSR dominance during posture to startReact dominance near/during movement. We tested this hypothesis using perturbations of elbow posture at various times before a fast ballistic extension movement. We found clear evidence that both the LLSR and startReact components were influenced changes in the late long-latency time window. The results provide insights on how the nervous system regulates involuntary responses to perturbations during the transition from maintenance of arm posture to movement.New and NoteworthyWe recently demonstrated that the startReact effect, the startled release of a planned movement, can influence the muscular response during the LLSR. Here we observe how the influence of startReact can change from the transition from posture (no/little influence) to movement (strong influence). While not all paradigms trigger a startReact effect, this work demonstrates that when present startRect can have a profound effect on the overall muscle activity - even obscuring the traditional LLSR response.

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Factors which Modify the Short and Long Latency Components of the Stretch Reflex in the Human Forearm

Motor Control ◽

10.1007/978-1-4615-7508-5_8 ◽

1987 ◽

pp. 43-50

Author(s):

R. G. Lee ◽

R. Hayashi ◽

W. Becker

Keyword(s):

Stretch Reflex ◽

Long Latency ◽

Human Forearm

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Neurophysiological changes in the visuomotor network after practicing a motor task

Journal of Neurophysiology ◽

10.1152/jn.00020.2018 ◽

2018 ◽

Vol 120 (1) ◽

pp. 239-249 ◽

Cited By ~ 10

Author(s):

James E. Gehringer ◽

David J. Arpin ◽

Elizabeth Heinrichs-Graham ◽

Tony W. Wilson ◽

Max J. Kurz

Keyword(s):

Motor Learning ◽

Motor Planning ◽

Motor Task ◽

Force Production ◽

Oscillatory Activity ◽

Matching Task ◽

Force Output ◽

Motor Action ◽

Visuomotor Transformations ◽

Target Matching

Although it is well appreciated that practicing a motor task updates the associated internal model, it is still unknown how the cortical oscillations linked with the motor action change with practice. The present study investigates the short-term changes (e.g., fast motor learning) in the α- and β-event-related desynchronizations (ERD) associated with the production of a motor action. To this end, we used magnetoencephalography to identify changes in the α- and β-ERD in healthy adults after participants practiced a novel isometric ankle plantarflexion target-matching task. After practicing, the participants matched the targets faster and had improved accuracy, faster force production, and a reduced amount of variability in the force output when trying to match the target. Parallel with the behavioral results, the strength of the β-ERD across the motor-planning and execution stages was reduced after practice in the sensorimotor and occipital cortexes. No pre/postpractice changes were found in the α-ERD during motor planning or execution. Together, these outcomes suggest that fast motor learning is associated with a decrease in β-ERD power. The decreased strength likely reflects a more refined motor plan, a reduction in neural resources needed to perform the task, and/or an enhancement of the processes that are involved in the visuomotor transformations that occur before the onset of the motor action. These results may augment the development of neurologically based practice strategies and/or lead to new practice strategies that increase motor learning. NEW & NOTEWORTHY We aimed to determine the effects of practice on the movement-related cortical oscillatory activity. Following practice, we found that the performance of the ankle plantarflexion target-matching task improved and the power of the β-oscillations decreased in the sensorimotor and occipital cortexes. These novel findings capture the β-oscillatory activity changes in the sensorimotor and occipital cortexes that are coupled with behavioral changes to demonstrate the effects of motor learning.

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Reflex Responses Induced by Tooth Unloading

Journal of Neurophysiology ◽

10.1152/jn.2000.84.2.1088 ◽

2000 ◽

Vol 84 (2) ◽

pp. 1088-1092 ◽

Cited By ~ 29

Author(s):

Kemal S. Türker ◽

Melissa Jenkins

Keyword(s):

Local Anesthetic ◽

Muscle Activity ◽

Masseter Muscle ◽

Horizontal Direction ◽

Reflex Response ◽

Maxillary Incisor ◽

Static Force ◽

Incisor Tooth ◽

Long Latency ◽

Unloading Reflex

The reflex response of the masseter muscle to the rapid unloading of a single maxillary incisor tooth was studied. Unloading of a static force of 2 N in the horizontal direction resulted in a short-latency excitation, inhibition, and long-latency excitation of masseter muscle activity occurring at latencies of approximately 13, 20, and 40 ms, respectively, with a corresponding change in bite force occurring slightly later in each case. Following the blocking of periodontal input by the injection of local anesthetic around the stimulated tooth, inhibitory responses were abolished. Therefore, it is concluded that the observed masseteric inhibition was caused by the unloading of periodontal mechanoreceptors and thus that these receptors may contribute to the jaw unloading reflex.

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