Implicit motor adaptation patterns in a redundant motor task manipulating a stick with both hands

Reviewer #1 (Public Review):

Summary/Strengths:

This manuscript describes a stimulating contribution to the field of human motor control. The complexity of control and learning is studied with a new task offering a myriad of possible coordination patterns. Findings are original and exemplify how baseline relationships determine learning.

Weaknesses:

A new task is presented: it is a thoughtful one, but because it is a new one, the manuscript section is filled with relatively new terms and acronyms that are not necessarily easy to rapidly understand.

First, some more thoughts may be devoted to the take-home message. In the title, I am not sure manipulating a stick with both hands is a key piece of information. Also, the authors appear to insist on the term 'implicit', and I wonder if it is a big deal in this manuscript and if all the necessary evidence appears in this study that control and adaptation are exclusively implicit. As there is no clear comparison between gradual and abrupt sessions, the authors may consider removing at least from the title and abstract the words 'implicit' and 'implicitly'. Most importantly, the authors may consider modifying the last sentence of the abstract to clearly provide the most substantial theoretical advance from this study.

It seems that a substantial finding is the 'constraint' imposed by baseline control laws on sensorimotor adaptation. This seems to echo and extend previous work of Wu, Smith et al. (Nat Neurosci, 2014): their findings, which were not necessarily always replicated, suggested that the more participants were variable in baseline, the better they adapted to a systematic perturbation. The authors may study whether residual errors are smaller or adaptation is faster for individuals with larger motor variability in baseline. Unfortunately, the authors do not present the classic time course of sensorimotor adaptation in any experiment. The adaptation is not described as typically done: the authors should thus show the changes in tip movement direction and stick-tilt angle across trials, and highlight any significant difference between baseline, early adaptation, and late adaptation, for instance. I also wonder why the authors did not include a few no-perturbation trials after the exposure phase to study after-effects in the study design: it looks like a missed opportunity here. Overall, I think that showing the time course of adaptation is necessary for the present study to provide a more comprehensive understanding of that new task, and to re-explore the role of motor variability during baseline for sensorimotor adaptation.

The distance between hands was fixed at 15 cm with the Kinarm instead of a mechanical constraint. I wonder how much this distance varied and more importantly whether from that analysis or a force analysis, the authors could determine whether one hand led the other one in the adaptation.

I understand the distinction between task- and end-effector irrelevant perturbation, and at the same time results show that the nervous system reacts to both types of perturbation, indicating that they both seem relevant or important. In line 32, the errors mentioned at the end of the sentence suggest that adaptation is in fact maladaptive. I think the authors may extend the Discussion on why adaptation was found in the experiments with end-effector irrelevant and especially how an internal (forward) model or a pair of internal (forward) models may be used to predict both the visual and the somatosensory consequences of the motor commands.

Reviewer #2 (Public Review):

Summary:

The authors have developed a novel bimanual task that allows them to study how the sensorimotor control system deals with redundancy within our body. Specifically, the two hands control two robot handles that control the position and orientation of a virtual stick, where the end of the stick is moved into a target. This task has infinite solutions to any movement, where the two hands influence both tip-movement direction and stick-tilt angle. When moving to different targets in the baseline phase, participants change the tilt angle of the stick in a specific pattern that produces close to the minimum movement of the two hands to produce the task. In a series of experiments, the authors then apply perturbations to the stick angle and stick movement direction to examine how either tip-movement (task-relevant) or stick-angle (task-irrelevant) perturbations affect adaptation. Both types of perturbations affect adaptation, but this adaptation follows the baseline pattern of tip-movement and stick angle relation such that even task-irrelevant perturbations drive adaptation in a manner that results in task-relevant errors. Overall, the authors suggest that these baseline relations affect how we adapt to changes in our tasks. This work provides an important demonstration that underlying solutions/relations can affect the manner in which we adapt. I think one major contribution of this work will also be the task itself, which provides a very fruitful and important framework for studying more complex motor control tasks.

Strengths:

Overall, I find this a very interesting and well-written paper. Beyond providing a new motor task that could be influential in the field, I think it also contributes to studying a very important question - how we can solve redundancy in the sensorimotor control system, as there are many possible mechanisms or methods that could be used - each of which produces different solutions and might affect the manner in which we adapt.

Weaknesses:

I would like to see further discussion of what the particular chosen solution implies in terms of optimality.

The underlying baseline strategy used by the participants appears to match the path of minimum movement of the two hands. This suggests that participants are simultaneously optimizing accuracy and minimizing some metabolic cost or effort to solve the redundancy problem. However, once the perturbations are applied, participants still use this strategy for driving adaptation. I assume that this means that the solution that participants end up with after adaptation actually produces larger movements of the two hands than required. That is - they no longer fall onto the minimum hand movement strategy - which was used to solve the problem. Can the authors demonstrate that this is either the case or not clearly? These two possibilities produce very different implications in terms of the results.

If my interpretation is correct, such a result (using a previously found solution that no longer is optimal) reminds me of the work of Selinger et al., 2015 (Current Biology), where participants continue to walk at a non-optimal speed after perturbations unless they get trained on multiple conditions to learn the new landscape of solutions. Perhaps the authors could discuss their work within this kind of interpretation. Do the authors predict that this relation would change with extensive practice either within the current conditions or with further exploration of the new task landscape? For example, if more than one target was used in the adaptation phase of the experiment?

On the other hand, if the adaptation follows the solution of minimum hand movement and therefore potentially effort, this provides a completely different interpretation.

Overall, I would find the results even more compelling if the same perturbations applied to movements to all of the targets and produced similar adaptation profiles. The question is to what degree the results derive from only providing a small subset of the environment to explore.

Reviewer #3 (Public Review):

Summary:

This study explored how the motor system adapts to new environments by modifying redundant body movements. Using a novel bimanual stick manipulation task, participants manipulated a virtual stick to reach targets, focusing on how tip-movement direction perturbations affected both tip movement and stick-tilt adaptation. The findings indicated a consistent strategy among participants who flexibly adjusted the tilt angle of the stick in response to errors. The adaptation patterns are influenced by physical space relationships, guiding the motor system's choice of movement patterns. Overall, this study highlights the adaptability of the motor system through changes in redundant body movement patterns.

Strengths:

This paper introduces a novel bimanual stick manipulation task to investigate how the motor system adapts to novel environments by altering the movement patterns of our redundant body.

Weaknesses:

The generalizability of the findings is quite limited. It would have been interesting to see if the same relationships were held for different stick lengths (i.e., the hands positioned at different start locations along the virtual stick) or when reaching targets to the left and right of a start position, not just at varying angles along one side. Alternatively, this study would have benefited from a more thorough investigation of the existing literature on redundant systems instead of primarily focusing on the lack of redundancy in endpoint-reaching tasks. Although the novel task expands the use of endpoint robots in motor control studies, the utility of this task for exploring motor control and learning may be limited.