Real sounds influence postural stability in people with vestibular loss but not in healthy controls

Anat V. Lubetzky; Maura Cosetti; Daphna Harel; Marlee Sherrod; Zhu Wang; Agnieszka Roginska; Jennifer Kelly

doi:10.1371/journal.pone.0317955

Peer Review History

Original SubmissionSeptember 16, 2024
8 Dec 2024 Decision Letter - Renato S. Melo, Editor PONE-D-24-39333Real Sounds Influence Postural Stability in People with Vestibular Loss but Not in Healthy ControlsPLOS ONE Dear Dr. Lubetzky, 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 submit your revised manuscript by Jan 22 2025 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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The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. [Note: HTML markup is below. Please do not edit.] 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: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 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 ****** 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 ****** 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: The manuscript compares the effects of auditory stimuli (no sound, white noise, and real-life environmental sounds—subway trains passing by in a station) on postural control in two visual conditions, static and dynamic (in an immersive contextual scene), simulating a real-life context in a virtual environment, in patients with unilateral vestibular loss and healthy controls. The testing was conducted on a foam surface with eyes open. The authors hypothesized that hearing real-life sounds would influence postural control in patients with vestibular deficits, as the vestibular system is a primary contributor to balance. They concluded that auditory stimuli, particularly contextually-relevant sounds, led to increased postural sway in vestibular patients but not in healthy controls during a standing balance task. While the methodology appears sound overall, I have several major concerns that need to be addressed for the manuscript to be fully convincing. Major Comments - The authors did not adequately justify their findings based on known anatomical and physiological mechanisms. There are evidences on the integration of vestibular, auditory, and somatosensory inputs during postural control (Minino et al. 2023, Ann. Biomed. Eng., Review). The auditory system contributes to balance by providing spatial cues and better perception of the three-dimensional surrounding space. However, the manuscript lacks sufficient discussion on the links between auditory stimuli with vestibular function, particularly in the context of stance on an unstable surface (foam). - More importantly, the study’s design introduces a dual-task paradigm, as participants are required to maintain postural control while processing auditory information. Cognitive involvement, such as attention and memory, plays a significant role in dual-task performance. Patients with vestibular hypofunction generally require greater cognitive resources to maintain postural stability due to their compromised sensory input. In dual-task situations, attention is divided between postural control and another concurrent task (in this case, auditory processing). This division of attention is known to impair postural control, especially in patients with vestibular deficits, who cannot fully allocate sufficient cognitive resources to both tasks. The authors did not address this aspect, which is crucial for interpreting their findings. Therefore, the manuscript should discuss the cognitive demands imposed by real-life sound stimuli and how this may exacerbate postural instability in vestibular patients. Minor Comments: - The participant information in Table 1 is typically presented in the Method section. I suggest removing the table and including the details in the text. - The manuscript does not clarify whether there are significant statistical differences in demographic data between the patient and control groups. This should be included for transparency. - These figures appear to repeat the data already reported in Table 3. To avoid redundancy, I recommend either removing the figures or presenting additional insights beyond the table data. - In the figures, data are reported as means, with bars likely indicating standard deviations. Please confirm and clarify this in the figure legends. - Significant differences in the data should be clearly marked with appropriate symbols in the figures. - The age range of participants is mentioned for the first time in the Discussion section, and only for the healthy control group. This information should be included in the Method section and reported for both the patient and control groups. Reviewer #2: A well desisgned study. Minor comments Replace ' Sample elegibilty criteria' by 'Elgibity criteria' or 'Inclusion and Exclusion Criteria' in the title of Table 1 and corresponding text. Change Table 2 heading as Descriptive statistics ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Mansoureh Adel Ghahraman Reviewer #2: No ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0317955.r001
Revision 1
18 Dec 2024 Author Response Summary of Revisions Ref: PONE-D-24-39333 Title: Real Sounds Influence Postural Stability in People with Vestibular Loss but Not in Healthy Controls Journal: PLOS ONE Dear Prof. Melo fellow referees, We thank you for a thorough, detailed, constructive and very helpful review. We have made all of the corrections, and revised the manuscript according to your suggestions. We used track-changes font to highlight those changes made in the manuscript in response to the comments within the manuscript itself. In addition, below is a point-by-point list detailing how each of the major comments was addressed. Sincerely, The Authors ************************************************************* Reviewer #1: The manuscript compares the effects of auditory stimuli (no sound, white noise, and real-life environmental sounds—subway trains passing by in a station) on postural control in two visual conditions, static and dynamic (in an immersive contextual scene), simulating a real-life context in a virtual environment, in patients with unilateral vestibular loss and healthy controls. The testing was conducted on a foam surface with eyes open. The authors hypothesized that hearing real-life sounds would influence postural control in patients with vestibular deficits, as the vestibular system is a primary contributor to balance. They concluded that auditory stimuli, particularly contextually-relevant sounds, led to increased postural sway in vestibular patients but not in healthy controls during a standing balance task. While the methodology appears sound overall, I have several major concerns that need to be addressed for the manuscript to be fully convincing. Major Comments - The authors did not adequately justify their findings based on known anatomical and physiological mechanisms. There are evidences on the integration of vestibular, auditory, and somatosensory inputs during postural control (Minino et al. 2023, Ann. Biomed. Eng., Review). The auditory system contributes to balance by providing spatial cues and better perception of the three-dimensional surrounding space. However, the manuscript lacks sufficient discussion on the links between auditory stimuli with vestibular function, particularly in the context of stance on an unstable surface (foam). Thank you for this comment. These connections are now added to the introduction (paragraph 1) to better set the stage for this scientific inquiry as well as to the discussion (paragraph 3). - More importantly, the study’s design introduces a dual-task paradigm, as participants are required to maintain postural control while processing auditory information. Cognitive involvement, such as attention and memory, plays a significant role in dual-task performance. Patients with vestibular hypofunction generally require greater cognitive resources to maintain postural stability due to their compromised sensory input. In dual-task situations, attention is divided between postural control and another concurrent task (in this case, auditory processing). This division of attention is known to impair postural control, especially in patients with vestibular deficits, who cannot fully allocate sufficient cognitive resources to both tasks. The authors did not address this aspect, which is crucial for interpreting their findings. Therefore, the manuscript should discuss the cognitive demands imposed by real-life sound stimuli and how this may exacerbate postural instability in vestibular patients. We added a discussion paragraph (paragraph 3) to address this point. Thank you! Minor Comments: - The participant information in Table 1 is typically presented in the Method section. I suggest removing the table and including the details in the text. Done. - The manuscript does not clarify whether there are significant statistical differences in demographic data between the patient and control groups. This should be included for transparency. This was added to Table 1. - These figures appear to repeat the data already reported in Table 3. To avoid redundancy, I recommend either removing the figures or presenting additional insights beyond the table data. We believe that illustrating the results increases clarity for the readers. At the same time, any reader wishing to compare results, conduct a power analysis or report it in a review would need the exact estimates. That being said, given your suggestion, we moved Table 3 to an Appendix. - In the figures, data are reported as means, with bars likely indicating standard deviations. Please confirm and clarify this in the figure legends. The data in the figures are model estimated marginal means and their 95% confidence intervals. This is now explained in the figure captions. - Significant differences in the data should be clearly marked with appropriate symbols in the figures. Given the complexity of the models (main effect of group, visual load, and interactions separately for each auditory condition), we believe that including symbols in the figures would complicate the visualization whereas the P values reported in the text allow the reader to understand all the comparisons that we made per model. In addition, adding symbols to the figures would provide information regarding an arbitrary cutoff (0.05) whereas when the exact P values allow the readers to make their own judgement. We strongly believe that to be best statistical practice. - The age range of participants is mentioned for the first time in the Discussion section, and only for the healthy control group. This information should be included in the Method section and reported for both the patient and control groups. Done. Reviewer #2: A well designed study. Minor comments Replace ' Sample eligibility criteria' by 'Eligibly criteria' or 'Inclusion and Exclusion Criteria' in the title of Table 1 and corresponding text. The table was removed as per Reviewer 1’s request. The information is now presented in the text under the sub-hearing ‘eligibility criteria’. Change Table 2 heading as Descriptive statistics Done. Attachments Attachment Submitted filename: Summary of Revisions.docx https://doi.org/10.1371/journal.pone.0317955.r002
8 Jan 2025 Decision Letter - Renato S. Melo, Editor Real Sounds Influence Postural Stability in People with Vestibular Loss but Not in Healthy Controls PONE-D-24-39333R1 Dear Dr. Lubetzky, 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. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Renato S. Melo, PhD 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) ******** 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: (No Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: (No Response) ****** 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: (No Response) ****** 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: (No Response) ****** 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: (No Response) ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Mansoureh Adel Ghahraman ******** https://doi.org/10.1371/journal.pone.0317955.r003
Formally Accepted
10 Jan 2025 Acceptance Letter - Renato S. Melo, Editor PONE-D-24-39333R1 PLOS ONE Dear Dr. Lubetzky, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. If we can help with anything else, please email us at customercare@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Renato S. Melo Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0317955.r004

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