Destruction of ERP responses to deviance in an auditory oddball paradigm in amyloid infusion mice with memory deficits

Bowon Kim; Jisu Shin; YoungSoo Kim; Jee Hyun Choi

doi:10.1371/journal.pone.0230277

Peer Review History

Original SubmissionNovember 21, 2019
5 Jan 2020 Decision Letter - Dong-Gyu Jo, Editor PONE-D-19-32332 Destruction of ERP responses to deviance in an auditory oddball paradigm in amyloid infusion mice with memory deficits PLOS ONE Dear Dr. Choi, 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. We would appreciate receiving your revised manuscript by Feb 19 2020 11:59PM. When you are 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. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols 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). This letter should be uploaded as separate file and labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out. We look forward to receiving your revised manuscript. Kind regards, Dong-Gyu Jo, Ph.D Academic Editor PLOS ONE Journal Requirements: 1. When submitting your revision, we need you to address these additional requirements. 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 http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. To comply with PLOS ONE submissions requirements, in your Methods section, please provide additional information on the animal research and ensure you have included details on (1) methods of sacrifice, (2) methods of anesthesia and/or analgesia, and (3) efforts to alleviate suffering. Please ensure that you have provided this information for all parts of your study, including the icv injections. 3. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. Please see the following video for instructions on linking an ORCID iD to your Editorial Manager account: https://www.youtube.com/watch?v=_xcclfuvtxQ 4. Thank you for stating the following in your Competing Interests section: I have read the journal's policy and the authors of this manuscript have the following competing interests Please complete your Competing Interests on the online submission form to state any Competing Interests. If you have no competing interests, please state "The authors have declared that no competing interests exist.", as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now This information should be included in your cover letter; we will change the online submission form on your behalf. Please know it is PLOS ONE policy for corresponding authors to declare, on behalf of all authors, all potential competing interests for the purposes of transparency. PLOS defines a competing interest as anything that interferes with, or could reasonably be perceived as interfering with, the full and objective presentation, peer review, editorial decision-making, or publication of research or non-research articles submitted to one of the journals. Competing interests can be financial or non-financial, professional, or personal. Competing interests can arise in relationship to an organization or another person. Please follow this link to our website for more details on competing interests: http://journals.plos.org/plosone/s/competing-interests 5. Thank you for stating the following financial disclosure: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. a) Please provide an amended Funding Statement that declares all the funding or sources of support received during this specific study (whether external or internal to your organization) as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now. b) Please state what role the funders took in the study. If any authors received a salary from any of your funders, please state which authors and which funder. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." Please include your amended statements within your cover letter; we will change the online submission form on your behalf. [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 authors conducted an auditory oddball test on the Alzheimer’s disease mouse model with infusing amyloid-beta intra-ventricle. They present data showing amyloid beta eliminated the difference of ERP signature, and showing the difference of MMN in A-beta group for the first time. They suggest this study may provide a markers of sensory memory in mouse AD model. This manuscript describes a technically sound data and the experiments conducted rigorously. The conclusion is well drawn from data. This manuscript can be re-evaluate to publish after some minor revisions performed. Minor revision 1. affiliation has typo. 2. line7, ‘Alzheimer’s mouse model’ may change to “Alzheimer’s disease mouse model” 3. line 138, “method3” may be typo. 4. line 204, “studies27” may be type. 5. line 210, character “beta” is missing 6. recommend to be edited by native speaker. Reviewer #2: The manuscript reports an interesting study of an Aβ infusion mouse model of Alzheimers Disease (AD). They investigate behavioural measures of spatial memory using the Y-maze task and electrophysiological measures of sensory memory using the oddball paradigm comparing deviant and standard responses. They report impaired performance of the AD mouse model on the Y- maze task as well as evidence that deviant responses in the oddball paradigm and perhaps mismatch like response are also reduced in the AD mice compared with the control mice. 1. The manuscript is clearly written, however this could be developed further in particular to tie together the interaction of the abeta oligomers with the likely interaction point at the level of the neuron that is then assayed by the electrophysiological tests – and how this correlates with assaying. 2. Was any work done to corroborate the distribution of the Abeta oligomers are ICV (whether within this study of previously)? 3. How do the concentrations and timings and electrophysiological findings correlate or differ from work done using abeta oligomer incubations in brain slice (rodent), or biopsy derived human material? This is important in the overall experimental rationale. ****** 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 to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0230277.r001
Revision 1
9 Feb 2020 Author Response Reviewer #1 1. affiliation has typo. We deleted the typo. 2Division of Bio-Medical Science & Technology, KIST School, Korea University of Science and Technology, Seoul, Republic of Koreaparentheses 2Division of Bio-Medical Science & Technology, KIST School, Korea University of Science and Technology, Seoul, Republic of Korea 2. line7, ‘Alzheimer’s mouse model’ may change to “Alzheimer’s disease mouse model” We changed the sentence as you suggested. an Aβ-infused Alzheimer’s mouse model an Aβ-infused Alzheimer’s disease mouse model 3. line 138, “method3” may be typo. It was a style error for referencing. We corrected the error. method3 was changed to method [4]. 4. line 204, “studies27” may be type. studies27 was changed to studies [27] 5. line 210, character “beta” is missingWe fixed the error. A�- was changed to Aβ- Reviewer #2: 1. The manuscript is clearly written, however this could be developed further in particular to tie together the interaction of the abeta oligomers with the likely interaction point at the level of the neuron that is then assayed by the electrophysiological tests – and how this correlates with assaying. [Reply] We agree with the reviewer’s opinion of adding value by collimating the pathological and electrophysiological changes by A infusion. Since the pathological data can be obtained after the experiment, it would be desirable to record EEG as close as possible to the injection time point. But the 4-week delay in EEG recording was inevitable to reach sufficient mouse welfare and health conditions required for obtaining reliable EEG responses. For instance, differential ERP is known to be reduced in inattentive or fatigued or unhealthy animals. Hence, we endowed animals 3 weeks before implantation surgery and another week before recording, for full recovery from infusion and implantation surgery, respectively. We believe that the Aβ oligomer injection influences the central nervous system in a devastating way. It is known that Aβ infusion induces an irreversible change in brain tissue: Cardinal features of Aβ infusion include synapse loss, tau hyperphosphorylation, astrocyte and microglial activation, and most importantly, neurofibrillary tangle formation, which is irreversible (Forny-Germano et al., J Neurosci, 2014). Our study shows an irreversible influence of ICV injection fingerprinted in the ERP results, which has a translational value because of its availability for cross-species comparison between human patients and the mouse model. 2. Was any work done to corroborate the distribution of the Abeta oligomers are ICV (whether within this study of previously)?[Reply] We have reported a brain section-level evidence of A infusion in brain tissue in our previous methodology paper (Kim et al., J. Vis. Exp., 2016). However, the propagation of infusion effect over time through various brain regions has not been studied yet. We expect that the devastating effect of A infusion will not be restricted to the injection site since it affected differential ERP, engaging both bottom-up and top-down cortical circuits. 3. How do the concentrations and timings and electrophysiological findings correlate or differ from work done using abeta oligomer incubations in brain slice (rodent), or biopsy derived human material? This is important in the overall experimental rationale. [Reply] We appreciate this comment. As far as we know, a direct comparison between biopsy-derived human material and brain slice of infusion model has not yet been reported. Notwithstanding, the Aβ-ICV injection model has been widely investigated with variations of Aβ aggregate species, Aβ isomers, injection numbers, and base animal models accompanied by behavior tests. However, it is hard to find complete datasets of pathology and behaviors in terms of timing and concentration. Nonetheless, several research articles (cited in our manuscript) used similar experimental conditions to ours (~ 2 ug concentration, one-month delay after injection in observation). Here are the corresponding papers. Scientific Reports (2015) 5, 11708 reports that memory deficits and synaptoxicity of mice became gradually worse over 3 and 40 days since the single injection of Aβ(1-42) 3 ug. Journal of neuroscience research (2010) 88, 2923-2932 reports long-term potentiation changes with fear conditioning and CaN activity results by CV injection of Aβ oligomers in lower amounts than those of our experimental design. Neuroscience letter (1994) 170, 63-66 reports behavioral alterations in water-maze by varied concentrations of Aβ monomers in lower amounts than those of our experimental design. Attachments Attachment Submitted filename: PLoSONE_abeta_rev_letter_fin.docx https://doi.org/10.1371/journal.pone.0230277.r002
26 Feb 2020 Decision Letter - Dong-Gyu Jo, Editor Destruction of ERP responses to deviance in an auditory oddball paradigm in amyloid infusion mice with memory deficits PONE-D-19-32332R1 Dear Dr. Choi, We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements. Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication. Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. 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 enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and 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. With kind regards, Dong-Gyu Jo, 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: All comments have been addressed Reviewer #2: All comments have been addressed ******** 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: Yes Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: 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 #1: Yes Reviewer #2: 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 #1: Yes Reviewer #2: 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 #1: (No Response) Reviewer #2: Authors have addressed all concerns and provide additional information that support the conclusion of their study. ****** 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: No Reviewer #2: No https://doi.org/10.1371/journal.pone.0230277.r003
Formally Accepted
2 Mar 2020 Acceptance Letter - Dong-Gyu Jo, Editor PONE-D-19-32332R1 Destruction of ERP responses to deviance in an auditory oddball paradigm in amyloid infusion mice with memory deficits Dear Dr. Choi: I am 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 notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, 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. For any other questions or concerns, please email plosone@plos.org. Thank you for submitting your work to PLOS ONE. With kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Dong-Gyu Jo Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0230277.r004

Open letter on the publication of peer review reports

PLOS recognizes the benefits of transparency in the peer review process. Therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. Reviewers remain anonymous, unless they choose to reveal their names.

We encourage other journals to join us in this initiative. We hope that our action inspires the community, including researchers, research funders, and research institutions, to recognize the benefits of published peer review reports for all parts of the research system.

Learn more at ASAPbio .