Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autism

Elena V. Orekhova; Viktoriya O. Manyukhina; Ilia A. Galuta; Andrey O. Prokofyev; Dzerassa E. Goiaeva; Tatiana S. Obukhova; Kirill A. Fadeev; Justin F. Schneiderman; Tatiana A. Stroganova

doi:10.1371/journal.pone.0281531

Peer Review History

Original SubmissionOctober 20, 2022
8 Dec 2022 Decision Letter - Mehdi Adibi, Editor PONE-D-22-28959Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autismPLOS ONE Dear Dr. Orekhova, 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. The reviewer were mostly positive. There are some minor changes, esp. in the figures, for instance Fig 1 and 2 may include some raw data or event related activity in time domain which will help to make sense of the observed spectral changes. Fig 1a, middle panel is not clear. Also important info on the figure conventions and panels are missing in the captions. For instance, Figure 6 includes many panels (columns) and can be improved by including titles to the panels, and referring back to them in the text. Please submit your revised manuscript by Jan 22 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'. 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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, Mehdi Adibi, Ph.D., M.Sc., B.Sc. Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. 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. You indicated that you had ethical approval for your study. In your Methods section, please ensure you have also stated whether you obtained consent from parents or guardians of the minors included in the study or whether the research ethics committee or IRB specifically waived the need for their consent. 3. Thank you for stating the following in the Acknowledgments Section of your manuscript: "We would like to thank children and their families for participation in this study. This study was supported by Russian Science Foundation (project #22-25-00419)." We note that you have provided funding information that is not currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: "This study was supported by Russian Science Foundation (project # 22-25-00419, to EVO)." Please include your amended statements within your cover letter; we will change the online submission form on your behalf. 4. 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. Additional Editor Comments: Dear Editors, The reviewer comments were mostly positive, I have also reviewed the manuscript. There is only a few points by one of the reviewers, and I agree that requires some adjustment to in the figures to include experimental procedure and raw data and averaged waveform and event related activity prior to spectral analyses. This will help to visualise and characterise the sort of changes in the activity (time domain) that may contribute to spectral changes. this can be integrated in fig 1 and 2. In figure 1a, panels can be named individually, the panel in the middle is confusing. Figure captions at times do not provide enough information about the plots. For instance, panels (columns) in Fig 6. [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: Yes 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 focus of the present study, titled “Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autism” from Orekhova et al., was the relationship between stimulation-related modulations of MEG gamma oscillations and perception of visual motion in children with ASD. Considering how for some children with ASD, it is difficult to tolerate MEG and MRI data collection procedures, this work can give useful data. After reading this work I have no specific requests for the authors and I consider the work done so far good for publication. Reviewer #2: 1.To unravel the role of surround inhibition in V1 vs top-down modulation of V1 the authors investigated the role of putative neural inhibitory deficits in atypical motion perception in children with ASD by exploring velocity-related modulation of the visual GR, using two separate sets of high-contrast drifting gratings, presented in two separate experiments (psychophysical and MEG). Experiments suggests that the poor directional sensitivity to small moving gratings observed in some autistic children is secondary to more basic, inhibition-related processes that influence directional tuning of the receptive fields in the V1. Authors conducted the experiments in a rigorous way and explained every step in a clear way, indicating also the limitation of this study. In the material and methods authors indicated that only TD and ASD boys were employed, I just suggest to explain in a brief sentence, why girls are not included (male to female ratio in ASD). Even if well explained in the text, I suggest to add a more detailed description also in figure legend 1. 2. the statistical analysis has been performed appropriately and rigorously. 3. all data underlying the findings described in their manuscript are fully available. 4. the manuscript is presented in an intelligible fashion and it is written in standard English. ****** 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: No 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. Attachments Attachment Submitted filename: PONE-D-22-28959_review_report.docx https://doi.org/10.1371/journal.pone.0281531.r001
Revision 1
10 Jan 2023 Author Response Responses to Editor’s comments The reviewer were mostly positive. There are some minor changes, esp. in the figures, for instance Fig 1 and 2 may include some raw data or event related activity in time domain which will help to make sense of the observed spectral changes. Fig 1a, middle panel is not clear. Also important info on the figure conventions and panels are missing in the captions. For instance, Figure 6 includes many panels (columns) and can be improved by including titles to the panels, and referring back to them in the text. We are grateful to the Editor and Reviewers for the positive evaluation of our work. As suggested, we revised figure 1 by including the raw data. We also made captions over all the panels, which, we hope, made the content easier to understand. Since Figure 2 presents information similar to that in Figure 1b (right-hand panels), we believe that the inclusion of raw data in this figure may be redundant. We marked all panels in figure 6 by letters of the alphabet and refer to them in the text. Responses to Reviewer’s comments Reviewer #1: The focus of the present study, titled “Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autism” from Orekhova et al., was the relationship between stimulation-related modulations of MEG gamma oscillations and perception of visual motion in children with ASD. Considering how for some children with ASD, it is difficult to tolerate MEG and MRI data collection procedures, this work can give useful data. After reading this work I have no specific requests for the authors and I consider the work done so far good for publication. We are grateful to the reviewer for the positive evaluation of our work. Reviewer #2: We are grateful to the reviewer for taking the time to review our manuscript and provide comments. 1. In the material and methods authors indicated that only TD and ASD boys were employed, I just suggest to explain in a brief sentence, why girls are not included (male to female ratio in ASD). We added the following text to the Methods section (lines 141-145): We limited our sample to males because the ratio of males to females among people with ASD is very high (~4/1) [51], and the relatively small sample size of our study would not have allowed us to analyze female participants with ASD as a separate group. On the other hand, the putative differences in neural excitability between males and females with ASD [52] preclude combining them into a single sample. 2. Even if well explained in the text, I suggest to add a more detailed description also in figure legend 1. Thank you for this suggestion. We added more information to the legend. Fig 1. Overview of the data collection and analysis pipelines. (a) Psychophysical experiment. Large or small gratings moving left or right were presented for a short period of time. The subject had to indicate the direction of motion by pressing the corresponding button. In case of a wrong response the exposure time increased, while in case of two correct responses in a row it decreased (‘one-up—two-down staircase’). The minimum time required for the subject to detect direction of motion (i.e. duration threshold) of small and large gratings was defined as the average exposure time at all but the first two ‘reversals’ of the corresponding staircase. (b) MEG experiment. The subject was presented with circular gratings drifting toward the center at different speeds. Brain activity corresponding to baseline and visual stimulation intervals was localized using LCMV beamforming. Stimulation-related changes in gamma power (gamma response) were calculated as (stimulation-baseline)/baseline. The peak frequency and power of gamma response (GR) were analyzed at ‘maximal sources’ in the visual cortex. For a detailed description of the experimental procedures and analysis, see the Methods section. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0281531.r002
26 Jan 2023 Decision Letter - Mehdi Adibi, Editor Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autism PONE-D-22-28959R1 Dear Dr. Orekhova, 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 for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, 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, Mehdi Adibi, Ph.D., M.Sc., B.Sc. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0281531.r003
Formally Accepted
3 Feb 2023 Acceptance Letter - Mehdi Adibi, Editor PONE-D-22-28959R1 Gamma oscillations point to the role of primary visual cortex in atypical motion processing in autism Dear Dr. Orekhova: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. 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 plosone@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. Mehdi Adibi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0281531.r004

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