Peer Review History
| Original SubmissionApril 30, 2020 |
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PONE-D-20-12674 Disentangling listening effort and memory load beyond behavioural evidence PLOS ONE Dear Dr. Zhang, 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 30 2020 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:
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Claude Alain 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. Please amend either the title on the online submission form (via Edit Submission) or the title in the manuscript so that they are identical. 3. Please provide additional details regarding participant consent. In the Methods section, please ensure that you have specified (1) whether consent was informed and (2) what type you obtained (for instance, written or verbal). If your study included minors, state whether you obtained consent from parents or guardians. If the need for consent was waived by the ethics committee, please include this information. 4. Please ensure that you have outlined how you recorded data on pupil diameter in your Methods section. Additional Editor Comments (if provided): [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: 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: Review on Zhang et al. “Disentangling listening effort and memory load beyond behavioural evidence” In this work, the authors aim to characterize the effect of listening effort and memory load on pupil diameter using a dual-task paradigm. They reported the behavioural and pupillometry result from one experiment, where subjects were instructed to repeat a word immediately after its representation. Listening effort was manipulated by varying the SNR of the word. Memory load was manipulated by having an additional task where subjects also needed to memorise 10 words in a row and recall these 10 words after the 10th word. After the response, subjects self-reported their subjective rating of effort. Most of their findings were consistent with previous studies or very much expected: (1) the memory recall performance decreased in the more difficult listening condition (i.e. the word is hard to hear), (2) larger pupil dilation associated with harder-to-hear words due to the greater listening effort and associated with words in the dual-task due to the greater cognitive load, (3) larger pupil dilation should be associated with response (verbally produce the word), especially in the more difficult listening condition. (4) higher subjective effort rating in harder conditions. The authors were surprised by the fact that although the absolute pupil diameter was larger in the dual-task over the 10-word trial, one of the pupil metrics, peak pupil diameter (=max pupil diameter – pre-trial baseline), decreased since the second word. From this, they claim that the involvement of extra cognitive load interferes with the effect of listening effort on pupil diameter and this is possibly due to the fatigue. Overall, I found the study well-designed and the data carefully analysed. I particularly like the dual-task paradigm used here, which is quite elegant; the two conditions both involve same acoustic stimuli (i.e. word) and basic task (i.e. recognize and repeat the word) but differ only in the need of maintaining the memory of words. This makes this study distinct from the past studies (as authors mentioned around line 514). This makes the comparison of pupil data neat and clear. The paradigm is also of great potential as it is very close to the real-life listening situation: listeners to recognize the word in noise, reproduce the word accurately, and occasionally remember the word for future recall. ***Major concerns*** 1. The possibly most important finding of this study is the fact the PPD (peak pupil diameter) tends to be smaller in the last few words in the repeat-to-recall condition. The authors were very surprised by this result and tried to interpret it by comparing with the previous listening effort studies like Zekveld et al, 2019. However, the explanation the authors offered in the discussion was extensive but not satisfying. It has been well-known that PPD is not only related to the effort or load but also strongly related to its baseline; the larger the baseline, the smaller the PPD. Figure 4b clearly showed that the large baseline is the case. Thus, a simple explanation for this result is that pupil simply saturated in the repeat with recall condition and the pupil simply cannot expand further in the presence of additional words and responses. If this is the case, the result is not surprising at all. To exclude this possibility, the authors should consider running further analysis (e.g. regress out the effect of baseline from PPD) or conducting additional experiments to show that pupil still CAN dilate further in the repeat with recall condition. If these cannot be done, the authors should at least discuss it in the discussion. The saturation could be not only due to the mechanical limitation of the muscles controlling the pupil diameter, but also because pupil diameter is strongly correlated with the norepinephrine activity in the LC system. Since the authors are aware of the link between pupil diameter and LC-NE system as this was briefly mentioned in Introduction (line 36), they should also take this into account in the discussion. 2. As mentioned before, this paradigm is very neat and of great potential. The authors have already manipulated the level of listening effort using different levels of SNRs. However, the paradigm lacks the manipulation of cognitive load/memory load while it can be simply done. One way to manipulate the memory load is to vary the number of the words required to recall, for example, 5/10/15 words to recall. This will add an additional but necessary dimension to the existing study, otherwise it’s not able to disentangle the effect of listening effort on pupil diameter and that of memory load on pupil diameter, which is actually stated in the title of this paper. This additional experiment with varying memory load should also provide some answers to the questions stated in (1) whether the pupil is saturated in the repeat with recall condition. 3. [Line 549] A minor concern related to this part is that Zekvel et al., 2019 might not be the best study to compare with. The paradigm used in the current study requires listeners to sustain attention over a much longer period; 10 words in total including the sound presentation, the word reproduction, and the word type-in by the experimenter might take almost 30 seconds. I would recommend the authors to take a look at recent pupillometry publications using a sound signal with a similar length. 4. [line 122] The authors need to justify how this sample size was determined. 5. [line 240] How was PPD computed here? Was it extracted from each trial and then averaged within each subject? Or was PPD directly extracted from each subject’s average pupil diameter response? 6. [line 248] Similar question (5) applies to peak latency. 7. [Line 387] The stat test shows a significant difference in the second time window. However, by looking at Figure 5b the error bar of Forgotten and Correct largely overlaps and makes this test result unconvincing. Could the authors run a time-series stat analysis on the pupil data (like the analysis used in Figure 3a, Zhao et al. 2019 Trends in Hearing) to double-check whether the significance is true and if so when the significant interval starts? 8. [line 410] Please state the method of the correlation. e.g. Spearman or Pearson? ***Other comments*** 1. [Fig.5] Please use different colours for different conditions’ shaded area. The current colour and pattern makes it hard to tell which area belongs to which condition. 2. [Fig.5] How are these time windows determined? 3. [Figure 6] The solid curve looks over-smoothed compared to its shaded area. Comparing the relationship between the shaded area and the solid curve in Figure 5, the shaded area in Figure 6 are extremely spiky. Maybe additional smooth was accidentally applied to the group average? If so, the authors should justify the difference in the analysis pipeline. 4. [line 394] Possibly I misunderstood the content, but could the authors please provide more details or make it clearer: how is the mean pupil diameter computed here? Over which time window? Also, to support the statement this line, could you also plot the mean pupil diameter against the number stated words and test the correlation like Figure 7? 5. [line 417] Nice to see that the authors noticed the relationship between these metrics with the age as ageing is a known factor in pupil diameter. As the authors stated “Note that these correlations should be considered with caution due to no corrections” I was expecting to see these results with the age being regressed out. 6. [line 472] “the recall task probably because it was more interesting and rewarding”. It’s unclear how the recall task can be rewarding here. Did the authors apply a special bonus to the repeat with recall condition? Reviewer #2: I think this is a pretty good paper, in principle. The work seems to have been well done, and it addresses some very interesting and timely questions. That said, I found the original manuscript relatively difficult to read, not because of any problems with language but because I think it needs one more thorough revision now that the authors have successfully thought through all of their ideas - there are good ideas in here, but they're jumbled up still, and hard to find. Thus, most of my suggestions relate to writing and organization. Abstract When stating “different signal to noise ratios” please state what these are. Otherwise it makes no sense to state that “ (PPD) was bigger in the 0dB versus other conditions” because we have no idea whether those were all negative, or all positive, or by how much compared to 0 dB. It’s not clear to me from the abstract how baseline PPD can follow a growth pattern. I assume this means across trials or perhaps across words within a trial, but that is not clear. If PPD increased, how did it them decrease? This whole paragraph could be rewritten more clearly. No need to refer to “concur with the recent literature” in the abstract. IT's a statement that is too vague to be useful. 11 speech recognition is similar to what? 48-52 weird change of tense in the middle of this sentence. (“needs to decode… pondering…”) 93+ I think the section on LISTENING condition should be a separate paragraph. Also, I’m not sure it makes sense to go into this much detail about the study before the methods section. Right now, I’m left wanting to know more – for example, was the SNR variation blocked or was it randomized within trials? So either more info is needed here, or possibly less. 95-97 this sentence seems out of place (“The effect of SNR …”) 98-99 the issue of pupil traces for recalled vs. not recalled tokens seems quite a bit different from the topics that have been discussed so far. This is a big issue in the memory literature, and you probably need to take a look as some of that to restructure your introduction to better reflect this emphasis and the scientific context in which it fits. 105 I’d leave out “according to past studies” – you’re doing your own work here. 109-113 This prediction needs to be broken up, and perhaps re-thought. If baseline PD is expected to increase with memory load then it’s not obvious to me that PPD will also increase – if you’re raising the floor over the course of the 10 items in the trial, does it make sense to assume that the peak from that increasingly higher floor will *also* be increasing? Also, How do you think the increased memory load-related increasing baseline will interact with the previously mentioned decrease in PD as a function of time-on-task? 114-116 It is not clear whether this “rise” in PD is referring to the appearance of the pupil diameter trace in the course of a single stimulation, or over the course of a 10-word trial, or over the course of the entire experiment. The issue of time needs to be MUCH clearer throughout the paper. 121-126 It’s common to provide a gender breakdown for participants. But, more importantly, it’s incredibly important to identify the number of participants run in French and the number run in English. This could be a very significant factor and should probably be included in the final analysis [it is analyzed, so definitely mention it here]. 128-138 How many words in all? How many lists per condition? This is starting to seem like a rather incomplete Stimuli section. 127-134 Please break down durations by language. Ideally, please list all words in the supplementary materials. Was there any attempt to balance the intelligibility of the different word lists? If not, word list might need to be a factor in the eventual model as well. Also, a reference to “Fournier” words is needed, I don't know what those. 147 Was the calibration done with a pure tone, or with the speech stimuli and (if speech) then with or without noise (and if with noise, then at what SNR level)? 150 I presume “at 14 dB” means “at 14 dB SNR” but that should be made clear 159 what is the significance of the (0.5s) in this line and the (1s) in the next line? From the procedures section, it’s still not clear whether SNR was constant for a given set of words, or block of trials, or randomized (either across words within a trial, which would be admittedly strange) or across trials. Also, the ordering of TASK and LISTENING condition combinations is not specified. 162 Adjustment of the Target level in a constant noise level means that in the highest SNR condition the Target was 14 dB louder than in the 0 dB condition, right? This seems like an extreme difference, even without the presence of noise. What was the noise level alone? More importantly, what was the level of the signal in the QUIET condition – the same as that in the 0dB condition, or the 14 dB condition, or something else? Given that autonomic responses can be influenced by absolute level, what procedures were implemented to ensure that the differences observed were not simply due to differences in overall signal level? 169 Were there procedures for dealing with homophones? Were the transcribers well-versed in the set of words being used? Could the experimenter/transcriber see the intended word? 175 what was the time delay before the word RECALL appeared? 184 Was a “block” one set of 10 words, or 3? 189-192 Please provide degrees of freedom for the t-tests. 203 missing “were” before “retained” (or change to “remained”) 1.4.1+ It would be easier to understand the statistical analyses if you would provide the actual model, either in lme4 syntax (easy to do in this case) or in standard mathematical notation. This is quite common nowadays and could be put into supplementary materials if space is an issue. 232 What does “aggregated per word” mean? Averaged? Also, in this context, it is confusing to say “per word” if you actually mean (as I think you do) “per word position” (i.e. 1-10). Aggregating “per word” seems impossible if listeners never heard the same word twice as implied in the methods section. 236 Please clarify – these were the “aggregated” traces, right? 1 trace per subject per word-position? Also, given that the actual words were presumably of different durations, I think using absolute time (i.e. in seconds) is a bad idea, because it could blur effects that are related to the duration of the word. You might consider normalizing all times before any averaging is done. Or fit a curve to each individual trace and then compute the peak and the latency from that, then do averages over those values. 243-26 I like the comparison between the “block baseline” and the “word position baseline”. 252-291 I find it a little confusing (and quite demanding on my working memory) to present all statistical analyses prior to any results. I think this section would be helped by using sub-headings and, again, by providing the actual models in either lme4 syntax or as an equation. Alternatively, these paragraphs could be put as the initial paragraph of the respective results (sub)sections. 265-282 I think the discussion of the second time window suggests that what you really should be doing is looking at the entire pupil diameter curve from the onset of the word-position to 1.5s after its offset. See Winn & Moore (2018) for a really clever way of breaking such long(ish) traces down for analysis. Figure 2 a minor point, but it seems needlessly complicated to present the results with different Y axes representing essentially the same thing - % correct words repeated vs. Average number of words remembered (presumably out of 10?) 323-418 The results section is incredibly hard to read. Please revise to put things into complete sentences. It’s not just about presenting a bunch of equations here, you need to organize them in such a way that the reader can understand what you’re talking about. At this point I can’t really. Please give values (i.e. don’t just tell me baseline PD was bigger in one level than another, tell me what the value was for each level). It’s confusing to read that baseline pupil diameter was “bigger than 14 dB” (line 332) when to my knowledge we don’t typically measure pupil diameter in decibels. Yes, I can figure out what you mean, but this is currently written as it might be written in a lab notebook, for personal consumption, not as it should be written for scientific communication. And in some cases, it’s opaque: in line 335, is the (0.2 mm) referring to the absolute diameter, or the amount by which it is bigger? Even at the end “due to no corrections” is practically txting the results… Also, I think the trend analyses could be discussed separately. Basically, right now it seems as if you're more or less just listing the results of all the tests you did, maybe in chronological order or perhaps loosely organized (?) according to dependent measure. Please consider some way of organizing the results in a way that facilitates the reader’s understanding of why you conclude what you will eventually conclude or, at a minimum, that reflects the issues that you determined were relevant to investigate as described in the introduction. Ideally, the results section should be presented in the same order as the discussion section, which should walk the reader through the data toward the eventual theoretical claims that you want to make (and which should reflect the relative importance of topics as discussed in the introduction). Right now I honestly can’t figure out what data point(s) are particularly relevant or irrelevant, it just sort of devolved into a giant mass of statistical tests presented without obvious organization. [Discussion section is also a bit confusing - mostly due to digressions, though] Figures 3 & 4 Looking at the traces in Figures 3a and 4a it seems apparent to me that peak pupil dilation may not be a useful metric here. Except in the first word position there really isn’t much of a *peak* of any sort visible in 4a. And you can see that when those word positions get averaged together (for the images in 3a) any potential peakedness disappears. So why not use average PD or something like that? I think that would tell the story at least as well, and would be less subject to potentially weird micro-effects such as the weird flip of the black and red dots in positions 5, 8, and 9 of figure 4c. Also, the Y axis of 3c and 4c should somehow indicate that this is change from baseline. In general, I’d recommend considering a very different way of doing this analysis, perhaps along the lines of Winn & Moore (2018). 340 should this be 3b or 4b? 432-443 references needed here to Pichora-Fuller et al. 1995, Surprenant (1999, 2007). 461-506 I really struggled with this discussion. I think the long and detailed references to the noise reduction work are distracting and superfluous. So lines 436-455 could be reduced to just lines 451-455. Also, this discussion brings up the question of what, exactly, pupil dilation tells us. Arguably, it could provide information about the overall level of engagement of cognitive resources (I think that’s what the baseline measurement is supposed to get at, here) in these two conditions, as well as the moment-by-moment allocation of those resources during part of a task (encoding, repetition, recall). Given that you *have* pupil dilation data, I think this needs to be addressed somehow, before going into details of what dual task paradigms may or may not tell us. And, finally, what do you conclude? I appreciate that there are multiple possible interpretations, but you've thought about this far more than most. Could you lead the reader from this apparent bafflement into something that we can be more satisfied with? 488 Could you examine age differences in your data? What would you predict to see either in terms of behavior or pupil dilation if people are prioritizing things differently? 490 what does it mean that the recall paradigm is from previous studies? Which recall paradigm? 498 Define SWIR acronym. 509 What second hypothesis? There are so many hypotheses swirling around by now I’ve lost track of which one is which. Please restate. 519 these references did not all use the same speech perception task. Clarify. 523 You don’t really have data showing any greater effort of your task over other tasks. 540 The lack of position effect is extremely unusual for a serial recall task and needs to be discussed in much more detail. It should also be presented in the results. This is one of those memory effects that is so basic it’s taught in intro psych textbooks... I would very much like to see a graph of word recognition and recall by word position. I have great difficulty imaging that there wasn’t some kind of recency effect at least, if not also a primacy effect, with a 10-item list to be recalled. 585-621 It seems to me that the best explanation for smaller growth of the PPD is that the baseline is increasing. So the limit (probably physiological, based on light levels) is imposed not in terms of how much the pupil can dilate, but in terms of how much of a dilation it will reach. In other words, illumination, which you held constant, may have imposed an upper limit on pupil dilation, such that as the baseline creeps up with increasing memory load in the recall condition, or creeps down with increasing habituation in the repeat-only condition, you get the difference between the two gradually shrinking (in the recall condition) or increasing (in the repeat only condition). 623-626 Word choice seems problematic. What does it mean to “hold predictive power” or to be “responsive for recall performance”? Say what you want to say in a simple way. References that should be incorporated into a revision Goldinger, S. D., & Papesh, M. H. (2012). Pupil dilation reflects the creation and retrieval of memories. Current directions in psychological science, 21(2), 90-95. Kucewicz, M. T., Dolezal, J., Kremen, V., Berry, B. M., Miller, L. R., Magee, A. L., ... & Worrell, G. A. (2018). Pupil size reflects successful encoding and recall of memory in humans. Scientific reports, 8(1), 1-7. Miller, A. L., Gross, M. P., & Unsworth, N. (2019). Individual differences in working memory capacity and long-term memory: The influence of intensity of attention to items at encoding as measured by pupil dilation. Journal of Memory and Language, 104, 25-42. Pichora‐Fuller, M. K., Schneider, B. A., & Daneman, M. (1995). How young and old adults listen to and remember speech in noise. The Journal of the Acoustical Society of America, 97(1), 593-608. Surprenant, A. M. (1999). The effect of noise on memory for spoken syllables. International Journal of Psychology, 34(5-6), 328-333. Surprenant, A. M. (2007). Effects of noise on identification and serial recall of nonsense syllables in older and younger adults. Aging, Neuropsychology, and Cognition, 14(2), 126-143. Winn, M. B., & Moore, A. N. (2018). Pupillometry reveals that context benefit in speech perception can be disrupted by later-occurring sounds, especially in listeners with cochlear implants. Trends in hearing, 22, 2331216518808962. ********** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Sijia Zhao Reviewer #2: Yes: Alexander L. Francis [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". 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PONE-D-20-12674R1 Disentangling listening effort and memory load beyond behavioural evidence: Pupillary response to listening effort during a concurrent memory task PLOS ONE Dear Dr. Zhang, Thank you for submitting your manuscript to PLOS ONE. Your revised manuscript has been reviewed by the original reviewer. One is satisfied with your revision while the other request further clarification. 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 Dec 03 2020 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:
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Claude Alain 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: (No Response) 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: Partly Reviewer #2: Yes ********** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No 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: The revised version of the manuscript gained on clarity and furthermore improved in its readability. I have read the authors’ responses and I am happy with most of them. However, two of my major concerns —which are also actually the most important major concerns of my first review— still require authors’ response. I also checked the raw pupil data the authors uploaded. It’s great, however, it’s unclear if each row represents a time sample. To make the analysis reproducible, could you please also add the time coordinate for each entry? —————— # MAJOR CONCERN #1: ## REVIEWER 1 IN ROUND 1: 1. The possibly most important finding of this study is the fact the PPD (peak pupil diameter) tends to be smaller in the last few words in the repeat-to-recall condition. The authors were very surprised by this result and tried to interpret it by comparing with the previous listening effort studies like Zekveld et al, 2019. However, the explanation the authors offered in the discussion was extensive but not satisfying. It has been well-known that PPD is not only related to the effort or load but also strongly related to its baseline; the larger the baseline, the smaller the PPD. Figure 4b clearly showed that the large baseline is the case. Thus, a simple explanation for this result is that pupil simply saturated in the repeat with recall condition and the pupil simply cannot expand further in the presence of additional words and responses. If this is the case, the result is not surprising at all. To exclude this possibility, the authors should consider running further analysis (e.g. regress out the effect of baseline from PPD) or conducting additional experiments to show that pupil still CAN dilate further in the repeat with recall condition. If these cannot be done, the authors should at least discuss it in the discussion. The saturation could be not only due to the mechanical limitation of the muscles controlling the pupil diameter but also because pupil diameter is strongly correlated with the norepinephrine activity in the LC system. Since the authors are aware of the link between pupil diameter and LC-NE system as this was briefly mentioned in Introduction (line 36), they should also take this into account in the discussion. ## Authors: We thank the reviewer’s contribution to this interpretation of the results. We agree that baseline and PPD are correlated mathematically because (X-Y) and Y will always be correlated by R2=0.5, assuming X and Y completely random. And past literatures have also demonstrated this correlation. However, the exact relation between baseline and PPD during a hearing or cognitive task depends on the underlying cause. For instance, the effect of old age induces smaller baseline and smaller PPD due to physiological constraints and changes of activity in peripheral and/or central nervous system (Piquado et al., 2010; Kuchinsky et al., 2016; Wang et al., 2018). Lower luminance induces bigger baseline but smaller PPD due to the ‘gripping’ of parasympathetic system (Wang et al., 2018). Therefore, it is unclear what direction this relation between PPD and baseline should be in a task with concurrent listening and cognitive demands. What is surprising in our results is that we initially hypothesised that PPD might increase with more difficult SNR and more items to retain in the memory, but we see instead that the pupil dilation ‘capped’ during the listening section (before the word recall section). However, looking at the baseline dynamics let us understand partially the cause of the ‘capping’. This highlights the importance to look both at the PPD and baseline in future experiments that involves more ecologically realistic tests. We share with Reviewer 1 the desire to further disentangle baseline from PPD by either regressing out the effect of baseline or showing that pupil can still dilate further in repeat with recall condition. The first approach, however, is problematic as long as we do not understand the exact conditions where base and PPD are negatively correlated from conditions where they may be positively correlated (whether this is seen within or across subjects). So, we opted for the second approach: while a sort of pupil saturation was present during the listening and encoding section from 1st to 10th word, the pupil increased at the onset of recall on average by 0.3mm! Reviewer 1 did not realize this finding, so we made it more explicit in the article: the ceiling of the pupil during the recall blocks cannot be due to mechanical limitation of the muscles controlling the pupil diameter, because right at the end of the block, the pupil diameter rose considerably, an effect equivalent to six times the average PPD at the 10th word. Therefore, it is clear that the pupil ceiling during listening and encoding was not at all due to mechanical constraints but originated from cognitive resource allocation strategy. The best interpretation we can offer – and that we discussed – is that listeners would reserve their resources during the 1st to 10th word in order to retrieve the words during the recall section. ## REVIEWER 1 IN ROUND 2: Sorry for being very fussy about this. This has been surprisingly under-addressed in the literature. As you are aware of it now, please properly discuss it in the manuscript and point out that, although it’s less exciting, it is a reasonable explanation of your result. (1) I am not convinced by the authors' rejection to regress out the baseline from PPD on a trial basis. As shown in the first paragraph of their response, the authors clearly understood the concern about the correlation between baseline and PPD. As such correlation potentially exist and explains the key result, it should be carefully examined and reported, because it potentially “fully” not just “partially” explains the key finding here. No matter it’s a positive or negative correlation, no matter it’s within- or across- subjects. (2) The authors’ response to my second approach is not satisfying either. Remember, the key finding here is the PPD (peak pupil diameter) tends to be smaller in the last few words in the repeat-to-recall condition. The authors need to examine if this is due to the pupillary saturation in the last few words. In other words, the authors need to show that in the last few words, the pupil can still dilate more flexibly just like in other conditions. The dilation from 1st to 10th word (as shown in figure 4b) does not solve the concern at all. Actually, based on figure 4b, the baseline reached a plateau between 4.0-4.1mm after the 6th word, strongly suggesting that the saturation is the case. (3) Moreover, I am not convinced by the authors’ statement that “The best interpretation we can offer – and that we discussed – is that listeners would reserve their resources during the 1st to 10th word to retrieve the words during the recall section.” This statement is strong, but the link between “small PPD in the last few words” and “reserving the resource” is weak to me. Please elaborate on it. —————— # MAJOR CONCERN #2 ## REVIEWER 1 IN ROUND 2: 5. [line 240] How was PPD computed here? Was it extracted from each trial and then averaged within each subject? Or was PPD directly extracted from each subject’s average pupil diameter response? ## AUTHORS: We thank Reviewer 1 for this comment, which we have repeatedly heard while presenting these results at conferences. It is a matter of constant debate. For sentences, the pupil dilation is more stable than it is for individual words, and thus arguably, one might want to extract PPD directly from individual sentences. We found that this did not apply well to individual words. So, we opted for the PPD taken from the averaged traces. We firstly performed the baseline correction to subtract the baseline of each trial from the pupil trace. Then traces were aligned by the onset of the response prompt and aggregated per listener per condition. PPD was then calculated at this aggregated level, instead of the trial level. This method was chosen in aligned with past studies and ensured PPD was more robust (Zekveld et al., 2010; Zekveld et al., 2013; Zekveld et al., 2014). We have re-organised the method and result sections to clarify the detailed procedure (line280). ## REVIEWER 1 IN ROUND 2: Thanks. (1) could you clarify what you meant by “this did not apply well to individual words”? How did you determine that method doesn’t apply well? (2) although it’s ok to choose this method as it has been consistently used by Zekveld lab since 2010, it does not mean that in 2020 we, the pupillometry field, should still ONLY reply on this simple method. So, to demonstrate that your result is robust and replicable, please at least report the result with the trial level PPD in supplementary materials. 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: Sijia Zhao Reviewer #2: Yes: Alexander L. Francis [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. |
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Disentangling listening effort and memory load beyond behavioural evidence: Pupillary response to listening effort during a concurrent memory task PONE-D-20-12674R2 Dear Dr. Zhang, Thank you for the revision of your manuscript and for your patience in awaiting our response. For some reason, I could not reach one of the reviewers anymore, although s/he agreed to review the manuscript. I now decided to not wait any longer. 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, Claude Alain Academic Editor PLOS ONE Additional Editor Comments (optional): Thank you for the revision of your manuscript and for your patience in awaiting our response. For some reason, I could not reach one of the reviewers anymore. I now decided to not wait any longer and am pleased to tell you that your work has now been accepted for publication in PLoS ONE. Reviewers' comments: |
| Formally Accepted |
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PONE-D-20-12674R2 Disentangling listening effort and memory load beyond behavioural evidence: Pupillary response to listening effort during a concurrent memory task Dear Dr. Zhang: 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. Claude Alain Academic Editor PLOS ONE |
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