Peer Review History
Original SubmissionJune 28, 2019 |
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Transfer Alert
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PONE-D-19-18265 On the development of sleep states in the first weeks of life PLOS ONE Dear Dr. Schabus, Thank you for submitting your manuscript to PLOS ONE. Your paper was overall well received and definitely has merit. Still, some important issues need to be addressed. Also please note that one reviewer had already submitted their review before receiving your data. As I wrote you per email, please make an extra effort in annotating the data, and in providing instructions for the complete reproducibility of your results. We would appreciate receiving your revised manuscript by Aug 30 2019 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:
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, Daniele Marinazzo Academic Editor PLOS ONE Journal Requirements: 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 1. Please amend the subsection category “[FOR JOURNAL STAFF USE ONLY]” for your manuscript. Unfortunately, this is not a valid category. At this time, please choose one or more subsections that best represent the topic(s) of your study. 2. We note that you have stated that you will provide repository information for your data at acceptance. Should your manuscript be accepted for publication, we will hold it until you provide the relevant accession numbers or DOIs necessary to access your data. If you wish to make changes to your Data Availability statement, please describe these changes in your cover letter and we will update your Data Availability statement to reflect the information you provide. [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: I Don't Know 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: No 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: Overall the paper is well organised, clear, straight to the point and easy to understand. I only have few minor comments that the authors may consider to keep into account for a revised version of the ms. I would avoid the term "well-sized sample" when defining the number of newborns included in the study, at least if the authors did not perform any analysis to define the sample size. The authors report that the MSPE was calculated for non-overlapping 30s segments. Do the authors investigated the possible time-window effect? How much the reported results may depend on this "arbitrary" choice? The authors state that "To provide equal number of observation for each subject and for each sleep stage MSPE (or PSD) values were averaged first across EEG channels, and next across a random sample of 10 epochs". If I understand correctly, the authors started with a 128 channels EEG and ended with features extracted from the "average" of 6 EEG channels. Isn't this a bit odd? May the authors comment on this? I would avoid to define "marginally significant" an interaction with p=.086. At least, if they do not consider "marginally no significant" the p-values equal to 0.02... Probably, the - only - residual main concern (but fully disclosed by the author in the limitations section) is related with the lacking of a double (manual) scoring. Reviewer #2: Wielek et al. (1) describe the power and multiscale permutation entropy features of babies’ wake, REM and non-REM states as a function of early development and (2) automatically classify those stages with such features. They validate the automatic classification using manual labeling techniques. Characterizing developmental changes in the spectral and complex signatures that differentiate various arousal/sleep states is highly relevant both to developmental science as well as cognitive neuroscience, as is knowledge regarding the practical utility of automatically predicting sleep stages on the basis of these features. The use of spectral and entropy features is well motivated and the associated references are well chosen. Wielek et al. find that across all channels, fast permutation entropy increased from REM to REM and wake, whereas the opposite pattern was observed at slow scales. Furthermore, entropy during sleep decreased with early development, whereas no power or entropy changes were observed during wake. Changes in entropy were not equally observed in different power bins and entropy (mostly from frontal and physiological channels) better recovered the manual sleep stage labels than spectral power. NREM and wake states could be recovered with little confusion, aligning with the observed entropy gradient across arousal states. Most of the manuscript is clearly framed and motivated, while results are presented in a clear fashion. Nonetheless, I found some of the results difficult to interpret due to methodological and conceptual limitations, which I will describe in more detail below. Given the relevance of the topic, I would recommend the acceptance of this manuscript conditional on changes made referring to the points below. Major points 1. One general limitation of the approach by Wielek et al. is that it relies on an accurate manual scoring, which the authors sufficiently note in the text. Due to the centrality of accurate scoring, I was surprised that the paper did not describe changes in sleep stages between sessions in more detail and discuss whether and how their results deviate from previous work looking at early development and sleep. Under the assumption that manual sleep scoring is the gold standard, manually labeled sleep stages should already offer insight into development, although I could surprisingly not find results pertaining to e.g. the relative duration of classes. 2. The dual aims of this manuscript (1: describing entropy & PSD changes with arousal states and age; 2: decoding such states) are not perfectly intersected. For example, decoding of sleep stages appears to be maximal from frontal channels, but the description of entropy & PSD features is done on the average across all channels. Therefore, both parts of the manuscript appear rather segmented. Scoring is described as difficult due to artifacts. This would also affect the features used for manual labeling. Sleep stage scoring appears to be driven primarily by physiological as well as frontal channels that are highly prone to muscular contributions, suggesting that automatic sleep stage scoring may be driven primarily by philological channels as well as frontal channels that are highly prone to muscular contribution. Thus, decoding accuracy may derive to a large part also from non-neural sources, which fundamentally constrains arguments related to ‘cortical development’ This should be more clearly stated and discussed in the manuscript as it challenges the interpretation as stemming from neural sources. 3. More generally, the mechanistic interpretation of the observed entropy effects is difficult here, due to the potential nonlinear contributions to the measure. In contrast to the observed differences in entropy and limited modulation of rhythmic features, much of the discussion focusses on rhythmic signatures. This may relate at least in part to the way these binned values are calculated. A global power normalization is uncommon and produces effects that are very difficult to interpret. Due to the 1/f distribution of the power spectrum, even high frequency power will always be normalized to the predominant low-frequency power. This is readily observed also from the plots (see Figure 4, 1-3Hz has relative power around 90%, whereas beta power is in the range of 5%.) This is especially problematic, as the normalization is applied regardless of sleep stage, which presumably consist of different rations of low-to-high-frequency content. Unequal distributions of sleep stages as observed in the present data may therefore create unequal baselines. It’s further not clear how this normalization would ‘facilitate comparison between session’ (l. 196 f.) as session differences could be expressed in different baselines. Concerns regarding normalization choices could be alleviated by presenting average PSD spectra for the individual sleep stages as has been done in Figure S6 for entropy. 4. Linked to the relevance of considering the entire spectrum rather than narrow bands/bins, preliminary evidence suggests that sleep stages may be differentiated by the slope of the arrhythmic 1/f spectrum (Lendner et al., 2019, bioRxiv). Notably, fast scale entropy is often directly related to 1/f slopes (Bruce et al., 2009, Waschke et al., 2017, Vakorin & McIntosh, 2012), suggesting that a similar link may also exist in the present data. [On a side note, this link of a single scale to a multiscale property such as the 1/f spectrum questions to some extent the notion that prior approaches used ‘temporally more unspecific entropy measures’ (l. 443).] High convergence between these measures would provide more information about the interpretation of fine-scale permutation entropy here. 5. A big advantage of this dataset appears to be the longitudinal (vs. cross-sectional) nature of the design, which was surprisingly not overtly noted. On the negative side, there does not appear to be a habituation session. The session effect could thus at least in part also reflect a retest effect due to habituation effects, which should be noted. Minor points -L. 30: ‘the baby’s brain signal complexity (and spectral power) revealed huge developmental changes in sleep in the first 5 weeks of life’. As no effect size measures were provided and effects visually are rather constrained, I would refrain from using the word ‘huge’ here. The same goes for statements such as ‘massive drop’ (l. 458). -L. 100ff.: ‘a big practical advantage is that entropy-based features, such as permutation -entropy, are typically more robust against common EEG artifacts as compared to spectral measures (Bandt et al., 2002)]’. This statement and reference are questionable. The reference merely shows that nonlinear features can be robustly identified even in the presence of noise. But no comparison to spectral features is provided. Furthermore, strong noise would also impact permutation entropy, especially if it is strong enough to limit manual labeling as suggested by the authors. -The section on Participants and EEG should add a description of the criteria for starting and stopping the approx. 30 min recordings were. -L151f.: “Segments with artifacts were rejected based on simple power spectral density (PSD) thresholds” oNo information is available regarding what these thresholds were. -L93: “such as Fast Fourier”. The full title of ‘Fast Fourier Transform’ would be necessary here. -I found particular aspects of the statistical procedure questionable. First, all data are averaged across EEG channels and then 10 random samples were selected to equate epoch amounts. Here, some sort of random re-sampling (e.g. bootstrapping) should be considered. Regarding the averaging procedure, Figure S4 provides an interesting contrast of frontal and occipital channels. Such a contrast makes sense given that the decoding analysis suggests a stronger representation of sleep stage information at frontal channels. However, no statistics appear to be used, especially no statistics support the claim that the ‘difference between REM and WAKE at week-5 is more pronounced at the frontal channels’ (lines 690ff.). In Figure S1, inference on which stage decoding is improved between features appears to lack statistics. -Regarding the power results, effects are observed in the beta and delta band. These bands are infamous for muscle artifact contamination in EEG recordings and some strong outliers are present in the data. The possible influence of artifacts should at least be discussed, although it would be even better to supplement such discussion with power spectra of the data. -The presentation of individual data points is appreciated. However, this reveals that some conditions include clear outliers (e.g. Slow entropy NREM; especially relevant as much of the discussion focusses on the potential relevance of delta oscillations). These should be controlled for in the statistical analysis. -Figure 1D is supposed to schematically display that permutation entropy at different levels of coarse-graining can differentiate between different sleep stages. It is unclear how these three exemplary traces were chosen, what the error associated with them is etc. Even for a schematic example, this is misleading for inference purposes. Why not plot MSPE values in addition to power values as depicted in plot C? Or accumulate across all time points within sleep stages to get estimates with an indication of the associated error. -The bars in the upper plots of Figure 5 are missing labels. -The provided Figures were of a noticeably low resolution. High-quality vector images would be more appealing for final publication. -‘This confirms that not all changes in EEG complexity are reflected by changes in power’ (l. 449 ff.). This is a very strong statement that cannot be backed up by the data. Differences in the power spectrum (e.g., 1/f slopes) other than the bins tested could also covary with age and sleep stage. -‘In our case however, this difference in signal-to-noise ratio has been counterbalanced by the sleep specific entropy decrease from week-2 to week-5, which manifests itself as decreased performance in classifying NREM (week-5 training, week-2 test).’ (l. 520 ff.). It is unclear to my why these two observations are claimed to be related? Fast scale entropy appears to decrease during sleep with age both for NREM and REM sleep. Why would this exclusively affect the classification of NREM? -‘This confirms that developmental changes’ (l. 524). Very strong, and in my view unsupported strength of the conclusion. Better go with ‘suggest’ etc. -‘whereas stage wake may be (oscillatory-wise) already widely developed’ (l. 525 f.). To the extent that the power measures here can be interpreted as ‘oscillatory’, the results suggest that also the sleep stages are already widely developed as no pairwise session effects were observed for any frequency bin in any sleep stage. -The current manuscript still contains grammatical errors. Please consider carefully assessing the manuscript again and correcting those in a revision. omight render rather low reproducibility (89); cf. yield oduring quite sleep (116); cf. quiet oThe classifier is later called as MSPE-based (189). owe restrict our (260); cf. restricted oat fast scale (311); cf. a fast scale/ fast scales o… ********** 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. |
Revision 1 |
PONE-D-19-18265R1 On the development of sleep states in the first weeks of life PLOS ONE Dear Dr. Schabus, Thank you for submitting your revised manuscript to PLOS ONE. Your way of addressing the issues emerging upon the first submission was overall very appreciated. A few points, detailed in the reviews below, remain to be clarified before we can accept this paper in PLOS One. We would appreciate receiving your revised manuscript by Nov 09 2019 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:
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, Daniele Marinazzo Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] 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: (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: Yes Reviewer #2: Partly ********** 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: I have not further comments. All my previous comments have been addressed. The manuscript is technically sound and clearly presented. Reviewer #2: Many thanks to the authors for the revision of the manuscript. The changes addressed many of my previous concerns and the current manuscript presents the data and their limitations more clearly. In addition, the available data documentation appears clear, although I did not run any of the scripts. There are a few points that I would still like to see addressed, including some changes introduces in the current revision. With such minor revisions, I would recommend publication in PLOS ONE. - A more thorough discussion of decoding sleep stages from physiological channels is still missing. While the potential influence of physiological noise on the interpretation of frontal EEG recordings has been adequately noted in multiple places, the decoding results warrant a specific discussion. I recommend noting that development of sleep patterns is not only associated with neural, but also with physiological changes (e.g., eye movement output) and that these features may be crucial markers for the manually labeled sleep stages. With the provided data, it appears wrong for readers to infer that neural differences are driving classification results and this should be made explicit. - “On average 5-weeks old newborns spend a higher percentage of total time (19%) in NREM sleep as compared with 2-weeks old babies (11.5%). […] A significantly larger proportion of participants showed NREM during week-5 (66%) as compared to week-2 (35%) […] Using paired-samples (by including only those subjects that actually show given sleep-state in both sessions), we found no significant effects differences in the median duration of classes from week-2 to week-5”. Were pair-wise statistics performed on the initial (overall) data? If these differences are significant, wouldn’t the inference be that cross-sectionally, NREM sleep increases, but not longitudinally within person? If so, this should be noted as much of the discussion ascribes the observed neural effects to an increase in NREM sleep and an associated increase in slow waves. - Thank you for adding information on when the recordings were taken. I am still a bit unclear about the exact recording setup. Were mothers asked to perform nursery rhymes as acoustic stimulation every approx. 5 min? More information on this would be appreciated. The fact that the data were not recorded during continuous night-time sleep should also be repeated in the Introduction and Discussion section to avoid misunderstandings. - Figure S9 is unclear to me. Why are the PSD curves repeated for each bin when they are identical? I am also not sure what the Figure is telling me about the presented bins as no statistical comparison is made here. This is complicated by the fact that value ranges are largely unreadable. - The discussion of sleep spindle development and anticorrelated entropy is much clearer now. Given this discussion, it would be interesting to know whether spectral differences between sessions were inter-individually anticorrelated with differences in entropy, i.e., whether spectral features relate to observed entropy effects. - 163: ‘Percentile thresholding’. 95% percentile? - 224: ‘individual amount’. I’d recommend ‘inter-individual differences. - 286: ‘paired-samples’. Specific that those are ‘paired-samples t-tests’. - 347: “Note that only NREM shows differences in the PSD spectra between age groups and the developing 9–14 Hz peak exclusively observed at week-5 of age.” Differences in the alpha peak are hard to see and are more obvious at occipital channels (Figure S5). A log-log scaling in addition with error bars may aid visualization. - 359: “reveled” vs. ‘revealed’ - 376: “We found an increase in oscillatory activity from week-2 to week-5”. I would recommend to change this to spectral power, as this does not appear to be a narrowband, i.e. oscillatory, effect. Also, the addition of error bars to Figure 4 would be beneficial. - 471: Starting the discussion with “Please note that” appears unnecessarily defensive and should be dropped. - 745: “Given the rapid cap placement and movement of babies at this early age we would refrain from over-interpreting these results.” This is a puzzling statement to me, at least in its current phrasing. Are the authors concerned that cap positioning strongly varied across time points and babies? Then all of the other results in the manuscript would be equally questionable as the inferences assume that the selected channels are in comparable locations. ********** 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 [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. |
Revision 2 |
On the development of sleep states in the first weeks of life PONE-D-19-18265R2 Dear Dr. Schabus, 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, Daniele Marinazzo Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: |
Formally Accepted |
PONE-D-19-18265R2 On the development of sleep states in the first weeks of life Dear Dr. Schabus: 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. Daniele Marinazzo Academic Editor PLOS ONE |
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