PONE-D-23-13216Task-relevant object shape properties act as poor but viable cues for the attribution of motor errors to external objectsPLOS ONE

Dear Dr. Modchalingam,

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PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: No

Reviewer #3: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This study examined an object transporting task using the right arm in an immersive virtual-reality environment and examined the following two questions:

1) Is the extrinsic cue (object shape in this study) sufficient to allow for associated motor errors to be attributed to the object itself rather than the hand?

2) Does increasing task relevancy (associating two object shapes with different directions of visuomotor perturbation) allow for forming distinct motor memories for different extrinsic cues?

To test the first question, the authors conducted the Single Learning experiment. They asked whether learning of a 30-degree visuomotor rotation with a single object can be transferred to a new object with a different shape. The results showed that the learning effect fully transferred to the new object, suggesting that object shape is not a sufficient contextual cue to promote motor error assignment. On the other hand, the adaptation effect did not transfer sufficiently to the untrained hand regardless of the congruence or incongruence of the object shape. This suggests that intrinsic cues to movements, like used hands, may be helpful for context switching during motor learning.

To test the second question, they conducted the Dual Learning experiment. Two objects with different shapes were associated with two opposite visuomotor rotations to test if they could simultaneously learn the two distinct perturbations. The results showed that the subjects could not fully learn the two rotations. A small learning effect was partially observed, but due to the explicit strategy. Based on these results, the authors concluded that task-relevant visual properties of objects are insufficient for motor memory switching.

In motor neuroscience, the question of what information provides the context cues for motor memory switching is of great importance and has been extensively debated. As the authors mention, intrinsic cues to movements are known to be possible contextual information for the simultaneous formation of different motor memories. On the other hand, concerning the extrinsic cue on which this study focuses, it has been considered that it does not allow memory switching, except in some studies (e.g., Osu et al., 2004).

This study is novel in at least two respects. First, their task design gives higher task relevance to the extrinsic cue (object shape). The goal receptacle for the spherical object was a cylinder, and for the cubic object, a box. It has yet to be sufficiently investigated if increasing the task relevancy of such extrinsic cues may facilitate memory switching. Second, while most previous studies have used more conventional laboratory environments with robotic manipulandum, the authors tested the question under more realistic conditions in an immersive virtual-reality environment. Motor research using HMDs has been increasing in recent years, but the effects of virtual reality environments still need to be thoroughly investigated. Thus, this experimental data has a novelty and will be a valuable accumulation of knowledge for the field.

The introduction is well-written. The discussion of the results also makes sense. On the other hand, there are several issues regarding the description of the methodology and the robustness of the analysis and results. Specifically, I would like to mention the following points.

Major concerns

1) Methods: Please add a more detailed description of the experimental protocols. I think there was no description about how many trials each phase consisted of in each experiment.

2) Results: The medians of the three receptacle positions in the first and last trial-set were used in the statistical analysis. I recommend using the average, as the magnitude of the errors may depend on the receptacle position.

3) Results: I would like to know how robust the results of Experiment-2 are. The change in the hand angle thorough the experiment looks very small. The authors used only the first and last trial-set (three trials for each trial-set) to be analyzed. Please analyze using the first and last three trial-sets, as many studies often take the average of about ten trials.

4) Results: For Fig3D, the significant change in hand angle from baseline was observed only for the CCW rotation. The authors considered this change may be due to explicit (Fig. 3E). However, if the behavioral change during the Dual Learning experiment is due to an explicit process, why is there no change in CW? Also, the explicit process is believed to allow for quick and large behavioral changes. In contrast, why is the observed behavioral change so small if the explicit process works? The authors need to discuss these two points.

5) Result of Fig3D: Related to the fourth point, the authors mention that, although it may result from explicit strategy, the participants could utilize the object shape cues to change their movements depending on the context for the opposing visuomotor rotations. However, considering that only the CCW rotation led to a significant movement change in Fig. 3E, it is possible to think that it exhibited the learning for one context and the failure to learn for the other rather than showing different adaptive changes for the two contexts. This possibility should also be discussed.

Minor concerns

6) Methods: The receptacles were located 45, 90, and 180 degrees from the object's spawn location. The 45 and 180-degree target locations are asymmetric with respect to the 90-degree target, and only the 180-degree location is far from the other two locations. Please explain why these three positions were chosen.

7) Results: Please report whether or not there was any difference in the results between the three receptacle positions.

8) Discussion: In the last sentence (lines 449-450): "our findings suggest that task-relevant object-shape cues may not be sufficient to create new context-dependent internal models for motor control but rather update existing models.” The logic is unclear to me. What evidence from your results supports this argument? Could you please further explain on this point?

Reviewer #2: This paper examines if and how object shape might be used consolidate context-dependent motor plans. In the experimental protocol, an association is made between object shape/target (e.g. cube with square receptacle) and the deviation of the visually perceived movement trajectory in a virtual environment. Performance was evaluated using the “heading angle”, a measure based on the angular deviation from a straight line to the target at 3cm along the 10cm movement trajectory. This heading angle was used to represent initial directional error, prior to corrections based on feedback. Clamped trials where visually perceived position of the end effector along the movement trajectory was fixed (based upon displacement from departure point) were used to evaluate the post effect.

Based upon the results, movement adaptation did not appear to be retained when participants used their opposite hand during the clamped trials. At the same time, movement adaptation appeared present when the object was changed whilst using the same hand. The interpretation is that participants attribute errors to the hand being used rather than the object which is transported. This finding is a little curious as it seems that the hand was never affected during the reach stage (per results line 277 and 309), only during the transportation stage when the hand interacts with the object. This peculiarity does not seem to be addressed in the discussion.

Overall, there are many pleasing aspects of this study. Generally speaking, I found the paper well-written and easy to follow. The inclusion of Bayes factors for gauging the likelihood of the null hypotheses was very helpful. Despite this, I have a non-trivial concern regarding the methodological approach. The main variable used here (heading angle) is based on the angular deviation from a straight line early in the movement trajectory. It appears that the underlying assumption is that movement trajectories for this task should be straight. However, I don’t feel that this holds for the experimental conditions examined. In effect, the use of a cube shaped object with a square shaped receptacle implies a significant task constraint, in that the object must be aligned to the form of the receptacle upon placement. As a consequence, the movement trajectory will likely differ to that which would be used for point to point reaching. A person could exploit different postural configurations through the upper limb (shoulder, elbow, wrist, finger) in order to remain close to a linear pathway, although even this will be constrained by the position of the target in the peripersonal space. It is more likely that they would choose a curvilinear path with comfortable joint configuration (as we tend to do when we take a mug by the handle).

It appears that the authors attempted to make some adjustments for this issue. They report that individual postures according to target location were controlled for by subtracting HA angles at baseline from HA angles in the training (experimental) phase (see line 223). Still, I remain unconvinced by this approach. I feel that the best solution would have been examining the 6-DOF position of the rectangular object along with the upper limb kinematics (in particular the wrist). Of course, I would of course be much less concerned if the deposit zone was more simply a larger 2D drop off zone, implying much less stringent spatial constraints. The specific receptacle presented to subjects is highly specific, adjusted in dimensions (including depth) to accommodate for the visually perceived object. As it stands, the results indeed show statistically significant differences in heading angle between the objects with different shapes (p=0.0153, BF10 = 3.14; line 328). With these elements in mind, my concern is that the study design and dependent variable used in this study are questionable. Given this, I would not recommend accepting this paper.

Reviewer #3: This paper presented a study in which the authors examined the extent to which object shape cues can be used to support context-specific motor adaptation to visuomotor rotations. Overall, the design is sound and the presentation is mostly fine. I have a few concerns about the clarity of the experimental protocol and how the results should be interpreted.

Major

1. The authors argue that the object shape in this experiment is ‘task-relevant’. However, I think this may require more discussion. In my opinion, the object shape is task-relevant in a same way as object color, which is only associative to visuomotor rotation. But in every-day life, object shape could be more ‘task-relevant’ as it could provide information about task dynamics (e.g., weight, weigh distribution, functional goal, etc.). Therefore, while I agree with the findings, I am skeptical about the generalizability of the results to a broader consideration of what ‘object shape’ could provide as contextual cues. There were a few sentences in the last paragraph about this limitation, but I think this point should be emphasized to avoid misunderstanding of the results. I would also recommend the authors reconsider the use of ‘task-relevant’ in the title.

2. What does ‘exclude strategies’ mean exactly and how did the subjects interpret it?

Minor

1. It was not clear what the number of trials was for the experiments (fig. 1). I assume Training 1 had 180 trials, but how about Training 2, Test, and Aligned? Also, how many clamp trials? Please clarify.

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

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Movement-goal relevant object shape properties act as poor but viable cues for the attribution of motor errors to external objects

PONE-D-23-13216R1

Dear Dr. Modchalingam,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kind regards,

Shenbing Kuang, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #3: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #3: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #3: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: I thank the authors for the revised version of the manuscript. I found responses to previous concerns satisfactory. I have one last concern regarding Fig 3 for the Dual learning experiment.

In Fig 3A, as described in Methods, the authors used normalized HAs to align the direction of the HA change to two opposing visuomotor rotations. A change in the positive direction indicates that the HA changed to compensate for the rotation in each condition. In Fig 3C and D, I am wondering if the authors are using normalized HAs? If so, negative values in CCW indicate that learning performance got worse. This is relevant to the conclusion, so please be sure to provide an explanation for this in the text.

I would also like to see what the learning curve looks like using non-normalized HAs for each of the opposing rotations, and I would suggest that the authors present the figure in supplementary results.

Reviewer #3: (No Response)

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Reviewer #1: No

Reviewer #3: No

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