bioRxiv Science⌕ Search

Biology subjects

Maeda, R. S.

Publications and source records attributed to Maeda, R. S..

6 recordsLinked to original sources

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

Previous work has shown that humans account for and learn novel properties or the arms 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 arms dynamics.

neuroscience↗

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

Generating 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.

neuroscience↗

Motor learning and transfer: from feedback to feedforward control

Previous 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.

neuroscience↗

Sensory information from a slipping object elicits a rapid and automatic shoulder response

Humans have the remarkable ability to hold, grasp, and manipulate objects. Previous work has reported rapid and coordinated reactions in hand and shoulder muscles in response to external perturbations to the arm during object manipulation; however, little is known about how somatosensory feedback of an object slipping in the hand influences responses of the arm. We built a hand-held device to stimulate the sensation of slipping at all five fingertips. The device was integrated into an exoskeleton robot that supported it against gravity. The setup allowed us to decouple somatosensory stimulation in the fingers from forces applied to the arm-- two variables that are highly interdependent in real-world scenarios. Fourteen participants performed three experiments in which we measured their arm feedback responses during slip stimulation. Slip stimulations were applied horizontally, in one of two directions, and participants were either instructed to follow the slip direction, or to move the arm in the opposite direction. Participants showed responses within [~]67 ms of slip onset when following the direction of slip, but significantly slower responses when instructed to move in the opposite direction. Arm responses were modulated by the speed but not the distance of the slip. Finally, when slip stimulation was combined with mechanical perturbations to the arm, we found that sensory information from the fingertips significantly modulated the shoulder feedback response. Overall, the results demonstrate the existence of a rapid feedback system that stabilizes hand-held objects.\n\nNEW & NOTHEWORTHYWe tested whether the sensation of an object slipping from the fingers modulates shoulder feedback responses. We found rapid shoulder feedback responses when participants were instructed to follow the slip direction with the arm. Shoulder responses following mechanical joint perturbations were also potentiated when combined with slipping. These results demonstrate the existence of fast and automatic feedback responses in the arm in reaction to sensory input to the fingertips that maintain grip on hand-held objects.

neuroscience↗

Generalizing movement patterns following shoulder fixation

A common goal of motor learning is generalizing newly learned movement patterns beyond the training context. Here we tested whether learning a new physical property of the arm during self-initiated reaching generalizes to new arm configurations. One hundred human participants performed a single-joint elbow reaching task and/or countered mechanical perturbations that created pure elbow motion. Participants did so with the shoulder joint either free to rotate or locked by the robotic manipulandum. With the shoulder free, we found activation of shoulder extensor muscles for pure elbow extension trials, as required to counter the interaction torques that arise at the shoulder due to forearm rotation. After locking the shoulder joint, we found a substantial reduction in shoulder muscle activity that developed slowly over many trials. This reduction is appropriate because locking the shoulder joint cancels the interaction torques that arise at the shoulder to do forearm rotation and thus removes the need to activate shoulder muscles. In our first three experiments, we tested whether this reduction generalizes when reaching is self-initiated in (1) a different initial shoulder orientation, (2) a different initial elbow orientation and (3) for a different reach distance/speed. We found reliable generalization across initial shoulder orientation and reach distance/speed but not for initial elbow orientation. In our fourth experiment, we tested whether generalization is also transferred to feedback control by applying mechanical perturbations and observing reflex responses in a distinct shoulder orientation. We found robust transfer to feedback control.\n\nNew & NoteworthyHere we show that learning to reduce shoulder muscles activity following shoulder fixation generalizes to other movement conditions but does not generalize globally, indicating that the nervous system does not implement such learning by modifying a general internal model of arm dynamics.\n\nDisclosuresThe authors declare no conflict of interest.

neuroscience↗

Compensating for intersegmental dynamics across the shoulder, elbow and wrist joints during feedforward and feedback control

Moving the arm is complicated by mechanical interactions that arise between limb segments. Such intersegmental dynamics cause torques applied at one joint to produce movement at multiple joints and, in turn, the only way to create single joint movement is by applying torques at multiple joints. Here, we investigated whether the nervous system accounts for intersegmental limb dynamics across the shoulder, elbow, and wrist joints during self-initiated reaching and when countering external mechanical perturbations. Our first experiment tested whether the timing and amplitude of shoulder muscle activity accounts for interaction torques produced during single-joint elbow movements from different elbow initial orientations and over a range of movement speeds. We found that shoulder muscle activity reliably preceded movement onset and elbow agonist activity, and was scaled to compensate for the magnitude of interaction torques arising because of forearm rotation. Our second experiment tested whether elbow muscles compensate for interaction torques introduced by single-joint wrist movements. We found that elbow muscle activity preceded movement onset and wrist agonist muscle activity, and thus the nervous system predicted interaction torques arising because of hand rotation. Our third and fourth experiments tested whether shoulder muscles compensate for interaction torques introduced by different hand orientations during self-initiated elbow movements and when countering mechanical perturbations that caused pure elbow motion. We found that the nervous system predicted the amplitude and direction of interaction torques, appropriately scaling the amplitude of shoulder muscle activity during self-initiated elbow movements and rapid feedback control. Taken together, our results demonstrate that the nervous system robustly accounts for intersegmental dynamics, and that the process is similar across the proximal to distal musculature of the arm as well as between feedforward (i.e., self-initiated) and feedback (i.e., reflexive) control.\n\nNEW & NOTEWORTHYIntersegmental dynamics complicate the mapping between applied joint torques and the resulting joint motions. Here, we provide evidence that the nervous system robustly predicts these intersegmental limb dynamics across the shoulder, elbow and wrist joints during reaching and when countering external perturbations.

neuroscience↗