Peer Review History
Original SubmissionApril 13, 2021 |
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PONE-D-21-12218 Early alpha/beta oscillations reflect the gradual formation of face-related expectations in the brain PLOS ONE Dear Dr. Roehe, 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 Jul 06 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript:
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Academic Editor PLOS ONE Additional Editor Comments: The manuscript was reviewed by two reviewers. While the reviewers were positive about the overall study, there are several major concerns along with some minor issues raised by the reviewers. The authors need to address all those comments and revise the manuscript before it can be accepted for publication. 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 2. Please change "female” or "male" to "woman” or "man" as appropriate, when used as a noun (see for instance https://apastyle.apa.org/style-grammar-guidelines/bias-free-language/gender). 3. 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If you are unable to obtain consent from the subject of the photograph, you will need to remove the figure and any other textual identifying information or case descriptions for this individual. [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: No Reviewer #2: No ********** 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 have tried to explore the neural correlates (ERPs and EEG power) underlying face related expectations by presenting participants with two image categories- expected and random; predicted images are followed by the expected images about which the participants learn apriori in the training session. Even though the authors do not find much difference in their behaviour in response to the two image categories, they do find some interesting modulations in N170, alpha/beta and gamma band activity during and prior to the presentation of the expected images compared to random images. Overall the study is well conducted but has some major concerns which are listed below as comments. Major comments 1. This is a gender discrimination study, yet the participant pool has a gender bias, 23 females and 10 males. What is the rationale for this selection? Out of excluded if there are any males, then situation is even more biased! 2. It has not been mentioned in the methods how the line noise was removed from the EEG data. Also, for EEG recordings the online reference and ground electrodes were FCz and FPz, respectively. How were the reference and ground chosen? If they are the system defaults, how were the data from these electrodes interpreted? 3. The results of the article show enhancement in alpha/beta power with face related expectations. This is particularly shown by a positive correlation (Fig.5) between peak alpha/beta power (2500-3000 ms) and left-lateralized modulation of N170. It has been shown by several researchers that N170 is just not face-specific but is rather elicited in response to prediction errors. Studies have shown that N170 was larger in amplitude for unpredictable versus predictable stimulus onsets, irrespective of the object category. Please see to the following articles P. Johnston, J. Robinson, A. Kokkinakis, S. Ridgeway, M. Simpson, S. Johnson, J. Kaufman, A.W. Young Temporal and spatial localization of prediction-error signals in the visual brain Biol. Psychol., 125 (2017), pp. 45-57 Thierry, G., Martin, C. D., Downing, P., and Pegna, A. J. (2007). Controlling for interstimulus perceptual variance abolishes N170 face selectivity. Nat. Neurosci. 10, 505–511. doi: 10.1038/nn1864 Can the authors say these effects would not exist for expectations related to non-face stimuli? 4. The N170 modulation was mostly left lateralized seen specifically at P7/TP7 whereas the alpha/beta enhancement was bilateral. A correlation between the two supports the hypothesis that processes of expectation are reflected in increased alpha/beta activity, which makes the processing of expected stimuli more efficient and consequently reduces the amplitude of N170. What would the authors comment on the topographical inconsistency of these two measures in terms of brain regions processing the expectedness of faces? 5. In the TFA specially for studying GBA, the low pass filter has been set to 1000 Hz. However in humans, high gamma only upto ~90 Hz can be recorded through EEG beyond which the high frequency oscillations (which cannot be recorded through EEG as they are mostly of sub-cortical origin) are contaminated with noise which should be filtered out for any time-frequency analysis. 6. The authors claim that their findings propose an approximate timeframe throughout which consistent traces of enhanced alpha/beta power illustrate the development of face-related expectations which peaks at around 2500-3000ms after the onset of the predictive image. This can be due to the expectedness of the expected face or very well be due to just any other stimulus following the predictive face/image (in case some other stimulus instead of the expected image was randomly paired with the predictive image) because the inter-stimulus duration was fixed (~2500ms) which after repeated trials raises expectation for the subsequent stimuli after fixed intervals. How do the authors delineate these two possibilities? 7. If authors can make a figure to connect the brain mechanisms (N170, alpha/beta, gamma) and predictive processes – somewhat of a summary, that would immensely help following the Discussion. 8. No data or codes link was submitted for review, which seems to be PLOS one policy Minor points 1. Subplots of Fig 3B are incomprehensible. 2. Either put figures with captions in the text together, or keep them in the end with references. The fig caption in text and, figures in the end is very difficult to read. Reviewer #2: This is a particularly well designed and interesting study by Roche and colleagues to understand the origination and development implicit expectation using EEG. Recent evidence further suggests that both pre-stimulus neuronal oscillations and peri-stimulus event-related potentials are reliable biomarkers of implicit expectations arising from statistical learning paradigms. Employing such a paradigm in gender-classification task based on face stimuli they investigated attenuation of ERP signals, Pre-stimulus Alpha/Beta oscillations and Post-stimulus GBA determine the temporal constraints of face-related expectation formation. While I found the research questions are all relevant and methods employed here are technically accurate and the overall narrative also presented well, I do have the following questions, suggestions and comments. Introduction # In my opinion, a more challenging issue I find for all these perceptual paradigms is how much perception of familiar or surprising occurrences are devoid of memory processing. There has to some involvement of component of memory specifically when the participants get trained in what kind of occurrences are expected versus not. Due to this training, they form a representation in memory of those perceptual prototype. Hence, I wonder how much of the face related expectation is aided by the service of memory and if you could dissociate what neurophysiological correlates are driven particularly by perceptual prediction and expectation versus memory component. Indeed you write about habituation and memory effects and repetition suppression effects in the discussion section. # One of the major issues of this work that I find is I am not too sure if I completely understand how the broader question asked and the overarching goal and hypothesis of this study design is any different from what has been investigated in some of the earlier works to address the following, How low-frequency neuronal oscillations act as carriers of sensory evidence and top-down predictions, respectively (von Stein and Sarnthein 2000; Bastos et al. 2012). In other words, whether slow pre stimulus alpha oscillations in task-relevant brain regions are stronger in the presence of predictions, whether they influence early categorization processes, and whether this interplay indeed boosts perception in general. https://pubmed.ncbi.nlm.nih.gov/26142463/ It would be crucial to delineate what separates out this study from the previous ones to be able to appreciate more the importance and exclusiveness of the findings. # In lines 76-78, authors write that “The insight that the projection of prediction errors is mediated by high gamma frequency (60 – 100Hz) synchronisation, which requires a greater energetic cost than lower frequencies [8,9]”, This statement is understandable but how does that shines light on the underlying processes shaping variability of ERPs is not clear. Perhaps, you could consider revising this statement. # Also, please explain why lesser Cognitive resource would suggest diminished ERPs. Is there already worked out inverse relationship between no. of Cognitive Resource and amplitude/power of ERP response or vice versa. Could please cite appropriate reference to justify this relationship? # The opposite such as amplified ERPs are evident for arbitrary or surprising occurrences. This is of course similar to what you expect for familiar versus unfamiliar stimuli or novel stimuli which is not consolidated yet in the memory. However, those which are already consolidated via prior experience/learning are already very familiar (e.g., expected faces) and should give similar to repetition suppression effect (repeated exposure). similarly, for surprising faces one should expect very similar effect as oddball stimuli. I would appreciate if you could you provide some of your reasoning against this comment? # Authors write “Drawing upon this, it seems apparent that somewhat unexpected events are predominantly distinguishable from expected occurrences by enhanced gamma-band activity (GBA).” There could be multiple interpretation of enhanced gamma-band activity. One specific reason you mention is supported by few recent studies which suggest that enhanced GBA could be involved in encoding and updating internal representation. However, thinking loud along the line of reasoning you have outlined in the Introduction I wonder whether this also has anything to do with deployment of larger number of cognitive resources while processing somewhat unexpected events. If you could kindly comment on this. Materials and methods # You do not have a gender balanced sample for this study. I am wondering whether that has any impact on the gradual built up of implicit expectation and top-down prediction of expected face occurrences. Previous studies have shown that in the primary visual cortex while decoding faces and expressions, women showed a more bilateral functioning than men and there are some gender differences while processing neutral and affective faces. There are also difference that are found in the EEG N1 response as well as during oddball N170 amplitude response. Could you please provide your reasoning? # The authors hypotheses regarding the enhancement Alpha/Beta power pre-stimulus as top down prediction of expected faces. I am wondering why hypothesize about amplitude/power and why not phase of pre stimulus Alpha/Beta. I would imagine phase of pre stimulus Alpha may also play a crucial role. Also, this change in pre stimulus Alpha power could just reflect the ongoing background excitability which has a biophysical basis and has got nothing to do with any prediction about the faces. Please comment on this. # In lines 214-215, authors have mentioned about the selection of pre-post durations, however, not provided any details with regards to what is the basis of this selection. The authors write, “-200ms pre- to 600ms post-stimulus onset for ERPs. The 200ms prior to stimulus onset served as a baseline. For the TFA, data was epoched from -2000ms to approx. 1500ms, time-locked to stimulus onset.” Any comment on what exactly guided your selection of a specific pre stimulus duration as we know from previous studies that the choice of pre stimulus duration can have significant impact on the outcome of power changes and involvement of specific frequency band of interest. Hence, what frequency bands subserve the prediction process is very much sensitive to the choice of those parameters e.g., pre stimulus duration. Results # Kindly explain why a title as “Early alpha/beta oscillations reflect the gradual formation of face-related expectations in the brain” deemed appropriate. Is it really gradual over the entire period of pre stimulus duration or is it an accelerated process just before the onset of the expected image? It seems to be the latter based on the following results unless I did not follow these results correctly. A significant positive relationship was, however, observed between the modulation of alpha/beta power underlying the final peak (8-30Hz; 2500 – 3000ms) and the modulation of the N170 (Spearman’s rho = .46, p = .021, 95% 381 CI [0.14 0.69]; Fig 5). Discussion I enjoyed reading the discussion section. However, I could not resist myself repeating my last comment again. Discussion section actually begins with what was my last comment for the previous section. It seems to me a more appropriate title hiding in the statement below, “Predictable visual events are often met by implicit expectations to allow the brain to reserve cognitive resources.” Authors should certainly clarify which one of the two is more appropriate interpretation here the gradual development and built up of predictions prior to expected stimulus onset or an accelerated process showing tendency towards conserving cognitive resources in the process of predictions of expected outcome. # In lines 426-427 I suggest please provide some relevant references when you are discussing right lateralized habituation effects. “These habituation effects or memory-driven modulations were found to be predominantly right-lateralised.” (reference please) Is this memory-driven modulations of N170 ERPs predominantly right-lateralised irrespective of gender in face related expectation. Related to my earlier question about selected sampling. # I think the authors cited and covered references which are most relevant to their findings based on ERPs, pre stimulus brain activity, GBA. However, I would like to point out that the recent studies suggest frequently reported negative relationship between pre-stimulus α/Beta power and stimulus detection or behavioural performance may be explained by changes in detection criterion. I am wondering whether there is something similar is happing here for example Pre stimulus power change in Alpha/Beta is driven by the state of neural excitability (brain states of individual participants), rather than top-down prediction of expected occurrences. Could you please comment on this. Related to my earlier question on background excitability. # The authors write in line 512 One could question why this pre-stimulus enhancement in alpha/beta power fluctuates instead of being a stable and continual increase in power leading right up to the presentation of expected targets. I do have the same question and also related to my previous question of gradual bult up of expectation versus final peak increase before the presentation of expected targets. You have already provided an elaborate and solid reasoning in lines 515-521. But still curious whether this transient enhancement of power in the Alpha/Beta band should be considered at all for the entire inter-stimulus duration of 3 seconds as you have mentioned is too long a duration. Somehow, It seems these individual peaks are fundamentally functionally distinct and more meaningful pre stimulus anticipatory power change is occurring over a relatively short-interval of time frames with regards to significant functional attenuation the amplitude of ERPs to the presentation of expected targets. Hence, the clear role of these three peaks at least the first two and in particular, the middle one is not so clear after all. The waxing and waning of pre stimulus Amplitude/power change over certain time intervals and windows could be purely based on the change in background excitability and brain states. I could also anticipate substantial inter individual and inter-trial differences in the processes of how expectations reflected in increased alpha/beta activity, which makes processing of expected stimuli more efficient for some participants and consequently reduces the amplitude of the N170 but not necessarily with the same efficiency and reduction for others. ********** 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. 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Revision 1 |
Early alpha/beta oscillations reflect the formation of face-related expectations in the brain PONE-D-21-12218R1 Dear Dr. Roehe, 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, Mukesh Dhamala, Ph. D. Academic Editor PLOS ONE Additional Editor Comments (optional): We accept the work for publication, but ask the authors to consider doing a minor revision of the manuscript following the comment of Reviewer 1. 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: I appreciate that the authors have carefully undertaken the revisions following my previous comments. I have a minor issue related to point 6 of the first round review. In Abstract there is a statement “A particularly interesting finding was the early onset of alpha/beta power enhancement which peaked immediately after the depiction of the predictive face; meaning, three seconds prior to the presentation of an expected image. Hence, our findings propose an approximate timeframe throughout which consistent traces of enhanced alpha/beta power illustrate the early prioritisation of top-down processes to facilitate the development of implicitly cued face-related expectations.” This statement needs to toned down/ rephrased because the 3 second time-scale is resulting from a choice of a specific stimulus and not true for any face related expectations presented in an arbitrary time scale. Reviewer #2: (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: Arpan Banerjee Reviewer #2: No |
Formally Accepted |
PONE-D-21-12218R1 Early alpha/beta oscillations reflect the formation of face-related expectations in the brain Dear Dr. Roehe: 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. Mukesh Dhamala Academic Editor PLOS ONE |
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