PONE-D-22-16057Effect of Geometric Distortion Correction on Thickness and Volume Measurements of Cortical Parcellations in 3D T1w gradient echo sequencesPLOS ONE

Dear Dr. Thaler,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. In particular, Reviewer 2 raised significant concerns about the lack of ground truth in some experiments, a lack of details in the methods and results, and the overall impact of the results. Certainly, transparency and consistency of procedures are cornerstones of science, but beyond reinforcing these notions, the reviewer wondered if additional recommendations regarding best practices in applying distortion correction in imaging studies could be derived from the results. 

Please submit your revised manuscript by Nov 03 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Dzung Pham

Academic Editor

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: Yes

Reviewer #2: No

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

Reviewer #1: Yes

Reviewer #2: No

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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

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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

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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: Well written paper, with some minor English issues (see below)

Not very innovative, standar statistics and existing public software tools were used for evaluation of the effects of different methods for distorion correction. You could describe some the non-linearity models. No mathematical formalisms are presented, just mentioning and citing known analysis techniques.

Please enhance the quality of figures 2 and 3; the text is very blurred; I also recommend maximizing contrast by using black for the font.

Some corrections:

Page 2, line 22

lateraloccipital and postcentral

lateral occipital and postcentral

THIS IS PREFERRED, "postcentral" is fine

Please make this correction in all the document

Page 15, line 18

Of note, it was reported by Jovicich

? what do you mean by "Of note"? ask help form an English.spoken person

page 17 line 13

captured in or study

included in our study <- you refer to sources of distortion, the use of "capture" is incorrect.

Reviewer #2: This paper looks at the effect of gradient non-linearities corrections on 3D T1-w magnetic resonance (MR) images. Specifically, the paper compares the estimates from the output of the Freesurfer processing pipeline such as brain volumes and regional cortical thickness from images with and without correction of non-linearities (DC, as per authors). There is a lot of work in the paper, and I found the figures to be essential to the understanding of the manuscript.

Introduction

I found the introduction lacking fundamental details. The literature has significant contributions trying to address gradient non-linearities and their impact to the reconstructed images. They present the source, the physics behind their correction and potential improvements while their limitations. The authors site only three papers that address image distortions corrections. However, these only describe some of the problems including multi-site data and these are not included in the introduction. I recommend expanding to add a short review of others’ findings.

The authors state that numerous factors can affect the images. A little naming of them is needed in the introduction. Furthermore, the authors indicate that these factors can be easily adjusted in a single site study. I don’t believe the statement is true. There are factors that are not related to the technology used, unavoidable changes to the technology, errors from the coils, factors associated with the participant, the physiology (such as flow, susceptibility), and positioning in the scanner. What are the inherent errors of perfect data? Multiple of these factors are not able to be corrected. Rudrapatna et al. demonstrated that motion influences the non-linearities corrections. I believe some of these should be introduce in the introduction

The paper tests the use versus the non-use of a motion correction technique. However, which of these two approaches is correct or more accurate is not known. There is no ground true when scanning humans. Have the authors considered using phantom and what are the limitations of such approach? What is the novelty of this technique compared to others. There are multiple correction techniques, what differentiates this DC algorithm from others? There is a need to explain the correction technique, the expectations of the correction and the therefore elaborate a hypothesis. What problem is this paper really targeting? The hypothesis should be quantifiable and should state the reasoning to the change of using the DC technique. A significant change does not really indicate that there is a cause-consequence that drives a hypothesis.

Materials

Brain morphology is dependent on the age and gender of the participants. The demographics of this study are highly variable. A more detailed information will help understand the changes seen in the results. The study is based on one scanner, one software version, one protocol version, one correction technique. How long did it take to get the 36 subjects scanned? There are intricate changes to the technology that can biased the results here presented. Did anything else change? More detailed information is needed.

The methods sections should have enough information to allow others to reproduce the experiment. This is a requirement for transparency and reproducibility of any scientific publication. I think there are many sections that can be improved, and more information is needed.

• On the DC technique to further assess the results. This include the algorithm itself and the software version and others.

• The acquisition process, not just only the T1-w. length to acquire 36 participants, coil, landmarking, motion correction, etc.

• Freesurfer v7.1 is known to provide inaccurate parcellations of the brain, compared to previous versions. It often overestimates the temporal and parietal cortex. This refers to the robustness of the Freesurfer pipeline. Have the authors encounter these issues? Was there any mitigation action to correct the template transformations? Did the pipeline behave similarly between the nDC and the DC corrected data? Did all the transformations work accurately? How was this evaluated?

• The estimate of the isocentre needs an explanation. What was the purpose or intent for its estimate. The paragraph as listed does not indicate the intention of the estimate use.

• CCC is considered similar to ICC. How was it calculated, there are multiple ICC estimates depending on the data (see Koo 2016). When reporting ICC, the confidence intervals should also be reported. These determine if the ICC is excellent, good, or poor.

• LME model: given that the hypothesis is measuring difference, I understand the model used to fit the difference between the 2 images. However, where all the fixed effect used in the model simultaneously or one at the time? The explanation needs more information on the purpose of the modeling. The LME was not used to model the data, but it was used to measure factors that could influence the difference in the estimates. Results indicate a somewhow different use of the model. How was the p -value estimated? Was it a simple ANOVA between 2 different model? Which factors were used and why? If you use volume and thickness, are you expecting edge voxels to influence the results? In addition, given the variability in the demographics of the cohort used in the study, why were age and gender not used as factors as well?

Results:

Initially I found the results interesting and was surprised to see the region dependency of the estimates. It can be expected from the algorithm, and its special dependency in the correction technique. However, physiological variability can also lead to distortions that the algorithm can either not be able to or inaccurate try to correct. This is dependent of the DC algorithm.

As I looked further, I found some confusing information

• I recognized this is a small cohort. There is no information on how the difference, or the estimates were distributed across participants. Are these normally distributed? If not, is the t-test and LME model appropriate or is there a need for non-parametric test?

• Figure 2 and 3: they report % change. Percentage normalized to which value? I think the formula of the difference % [nDC-DC]/??? should be present in the axis to help their interpretation. This normalization can also bias the results. It is currently sorted based in most negative change to most positive change. When sorted based on anatomical region, were other information that could be inferred? Like most regions in the frontal lobe have statistically significant changes based on the t-test and why? What drives the changes in some regions compared to others.

• Table 1: If the 95% CI for the difference and therefore associated with Figue 2 and 3? For example, Caudalmiddlefrontal, it is not statistically significance different (t-test) in the volume, however, the variability in the difference estimates is high and crosses zero. Are there outliers, a particular participant driving this variability, is it a cohort variability? Further explanation is needed. The text speaks of summary values, which are usually good as a start point, but needs further detailed description of some examples.

• Figure 4, what drive the low CCC values? Is it the within variability of the measures?

Discussion

The discussion section describes the need to report the type of data (nDC or DC) used in the estimates to infer changes. I agree with the authors that this is relevant and important and should always be described in a paper. Again, this aligns with the importance of transparency and reproducibility of published data. However, in cross-sectional, particularly at a single centre, if all data are treated in the same manner, the biases due to non-linear gradients can be considered similar to all participants if collected within a short time frame. Furthermore, you might not be affected by the correction, considering that this is not better than non-corrected data, if not applied at all. However, the biases due to anatomical variability and others are still present. In longitudinal data there are other sources of errors that can affect your measure more than non-linear gradients.

The authors highlight the importance of the changed seen and compared those to anatomical changes over time in different pathologies reported in the literature. In the review, caution should be considered and group results by similarly managed data. Each study had chosen a processing pipeline and sometimes papers cannot be compared even less grouped together. I agree with the authors that head positioning is an important and unavoidable factor. How can the effect of this be minimized?

I find it difficult to relate the discussion to the proposed hypothesis. Can the hypothesis really be proven if not all regions are affected similarly? Are there edge-effects or outliers in the ROIs used? If so, how was this evaluated and corrected for?

How does the physiology affect the DC algorithm?

Minor comments

• Use of acronyms such as MR and MRI, while known, should always be introduced. Same for DC.

• Introduction: line 8 should be single site or single centre, and not single-side.

• Introduction: Page 5 line 1, confusing, needs references and further explanation.

• Figure1: please overlay with some transparency, hard to see the differences.

• Discussion: page 14 line 09 I would use dementia, as it is a spectrum. Also, it is Parkinson’s disease and there is a full stop after it that should be a comma.

• Discussion: page 14 line 22: This can lead… is repeated from 2 sentences before.

• Discussion: page 15 line 22 should say cortical areas, not areals

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Reviewer #1: No

Reviewer #2: No

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PONE-D-22-16057R1Effect of Geometric Distortion Correction on Thickness and Volume Measurements of Cortical Parcellations in 3D T1w Gradient Echo SequencesPLOS ONE

Dear Dr. Thaler,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. In particular, some important clarifications in the methods were requested by the reviewer. 

Please submit your revised manuscript by Apr 01 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Dzung Pham

Academic Editor

PLOS ONE

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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 #3: (No Response)

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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 #3: Yes

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

Reviewer #3: Yes

**********

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 #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 #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 #3: This paper investigates the effects of distortion correction on thickness and volume measurements from 3D T1w MR images using FreeSurfer and a commercially available distortion correction algorithm. Adequate data were acquired and processed to support the objective of this study. Careful proofreading, more elaboration, and better presentation of the results are needed.

***Introduction

In the sentence “…scanner system upgrades or movement”, what movement? Scanner movement?

***Materials and Methods

"No additional motion correction was applied." --> "No motion correction was applied."

More details about the distortion correction algorithm are needed. Siemens provides two options (2D or 3D) for distortion correction. Which one was used? A brief description of the correction algorithm, which can be obtained from Siemens scientists/staff, will be helpful for readers to be aware of the differences between readers’ algorithms and the algorithm in this work.

Were any filters used?

*FreeSurfer cortical thickness and volume

Figure 1: It is very hard to visualize blue and purple. While it is good to inspect the whole brain, having close-up or zoomed-in views is needed to appreciate the differences between DC and nDC. For example, see figure 4 in https://pubmed.ncbi.nlm.nih.gov/31666530/. Showing the ROIs with most pronounced differences in thickness and volume measurements would be helpful. For example, precentral and paracentral ROIs.

Use either isocenter or isocentre.

It seems that the last paragraph in this section is to explain how the distance was calculated. In sentence “Isocenter coordinates for each patient were derived from the origin of the anatomical coordinate system that were transferred to the respective image coordinate system”, what is the isocenter in this sentence? Is it the magnetic isocenter mentioned in Statistics?

In “The isocentre … then used to calculate the distance for each FreeSurfer parcel from the isocenter. “, what are the two isocenters? Were they the magnetic isocenter that was mentioned later. Please clarify.

How was the distance calculated?

***Results

*Cortical thickness and volume

Since Table 1 is a busy table, adding horizontal gridlines will improve its readability. Further, it may be helpful to add a column on the left to assign a number to each ROI/row. Then use the numbers as y labels in Figures 2 and 3, whose y labels in the current format are too busy/blurry to read. Doing so will greatly improve the visualization of the figures. More comments about Figs 2 and 3 below.

In the title of Table 1:

The sentence “A p-value <0.05 was considered statistically significant” appeared in Statistics already and thus is redundant. It may be better to revise the last three sentences as two: “Significant differences (p < 0.05) are highlighted in bold. The false discovery rate (FDR) was used to correct for multiple comparisons.”

In Figures 2 and 3, y labels are too blurry to read. The information of the two figures is similar to/derived from Table 1. While it is nice to visualize the ranking of ROIs in terms of differences, it is more relevant to visualize the dependence of difference on distance, which is directly related to geometric distortion. Therefore, I suggest to add the following figures: mean-percentage-difference vs distance plots for thickness and volume measurements. Include 3 curves in each figure: mean-percentage-difference vs x, y, and z.

There is a formula/equation in the caption of Figures 2 and 3. It can be moved to be and described better in the section “FreeSurfer cortical thickness and volume”.

In Figure 4, use “Concordance correlation coefficient” is more descriptive/explicit than “CCC”. X labels are blurry.

***Discussion

“… were not included in or study” --> “… were not included in our study”

“For the mixed linear model” --> “For the linear mixed model”

To calculate p values for linear mixed model, please check “Evaluating significance in linear mixed-effects models in R” (https://link.springer.com/article/10.3758/s13428-016-0809-y).

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Reviewer #3: No

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PONE-D-22-16057R2Effect of Geometric Distortion Correction on Thickness and Volume Measurements of Cortical Parcellations in 3D T1w Gradient Echo SequencesPLOS ONE

Dear Dr. Thaler,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please clearly indicate the distortion correction setting within the manuscript in the Materials and Methods section. To verify this setting on Siemens dicom files, this can usually be found in the Image Type dicom tag (0008,0008) and is indicated by ND for no distortion correction, DIS2D for 2D distortion correction, or DIS3D for 3D distortion correction. Alternatively, packages like GDCM can also be used to examine the Siemens private header under "sDistortionCorrFilter.ucMode". A value of 1 indicates no distortion correction, 2 indicates 2D, 4 indicates 3D. This setting is important to fully understand the implications of this study (cf. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8971027 and  https://pubmed.ncbi.nlm.nih.gov/16757858/).

Please submit your revised manuscript by May 12 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

• A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
• A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Dzung Pham

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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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 #3: (No Response)

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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 #3: Yes

**********

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

Reviewer #3: Yes

**********

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 #3: Yes

**********

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 #3: Yes

**********

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 #3: acquired within 5m55s -> acquired in 5m55s

As mentioned previously, please specify 2D or 3D correction used for the study. And discuss/mention possible differences between the 2D and 3D corrections or lack of comparing the two may be a limitation of this study in discussion/limitations.

It is nice to compare images with and without geometry correction in Figs 1A-D.

In Figs 1C and D, if possible please add arrows to point out the regions/edges that show the effects of the correction.

Labels E and F in Fig 1 are missing.

As pointed out by the statement "The distortion effects were most prominent in the central region but difficult to detect visually" in Fig 1 caption, is it possible to have close-up views of an off-isocenter region of E and F to show purple and blue regions better?

For Fig 4, my previous suggestion of using label IDs does not seem to be much helpful. In order to improve the readability of this figure, please consider to move the ID/label to close to left and right alternately of the error bars. Doing so, a larger font size can be used. e.g. following is a cartoon version of the aforementioned arrangement:

4.Entorhinal |---------O---------|

|-------------------------O-----------------------------| 8.Insula

And use "Cortical ROIs" as the label for y axis.

In Fig 5, all labels should be in black, instead of gray. These labels are a bit blurry. Font size of X labels need to be increased to be readable.

Supplemental Fig 1 and 2 show that percentage differences in cortical thickness and volume are minimal at a location ~(125,125,125) mm away from the scanner isocenter. This is counter-intuitive. At isocenter, gradient is 0 and B0 is more uniform, shouldn't geometric distortion be less influential? Please clarify.

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Reviewer #3: No

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Effect of Geometric Distortion Correction on Thickness and Volume Measurements of Cortical Parcellations in 3D T1w Gradient Echo Sequences

PONE-D-22-16057R3

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