Effects of passive heat stress and recovery on human cognitive function: An ERP study

Hiroki Nakata; Ryusuke Kakigi; Manabu Shibasaki

doi:10.1371/journal.pone.0254769

Peer Review History

Original SubmissionOctober 23, 2020
15 Dec 2020 Decision Letter - Daqing Guo, Editor PONE-D-20-33346 Effects of passive heat stress and recovery on human cognitive function: An ERP study PLOS ONE Dear Dr. Shibasaki, 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 Jan 25 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: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled '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, Daqing Guo Academic Editor PLOS ONE Additional Editor Comments: This manuscript needs to be significantly improved before it can be accepted for publication in 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. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. Please see the following video for instructions on linking an ORCID iD to your Editorial Manager account: https://www.youtube.com/watch?v=_xcclfuvtxQ [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: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: In this study the authors explore the effects of passive heat stress and recovery on the human cognitive function with Flanker tasks, involving congruent and incongruent stimuli. The results showed the reaction time (RT) was shortened during Heat rather than Pre and Recovery, and the peak amplitudes of the P300 component in ERPs were significantly smaller during Heat than during Pre, suggesting that hyperthermia alters the human cognitive function. However, I would have below comments for authors to improve the work. 1. In the abstract, there was unclear description on cognitive function, such as “… indicating a recuperated cognitive function…”, “These results suggest that hyperthermia alters the human cognitive function…”. Human cognitive function involves multiple factors, such as attention, memory, decision and so on. 2. In the introduction, “Several non-invasive recording methods have been used to investigate the human cognitive function.”, what’s the non-invasive recording methods? Please give more description. 3. In the last paragraph of the introduction, it looks like the section of discussion, please adjust the paragraph and provide more background introduction. 4. “Sixteen subjects (thirteen males and three females; mean age 21.4 ± 1.0 years) participated in this study”，it reflected the mismatch in the factor of gender. Whether the gender difference has an impact on the effects of passive heat stress and recovery on human cognitive function? Please give more explain. 5. How long does the Flanker task last, and how many trials in total does the task consist of for each subject? 6. In the section of EEG recordings, there only were 5 electrodes, and need make sure the quality of EEG data, what is the impedance of the five electrodes across the whole EEG experiment? And provide the detailed information. 7. In the section Discussion, the logic needs to be strengthened, and provide more supporting materials to support the finding “The effectiveness of cooling on impaired cognitive function in hyper-thermic individuals”. Reviewer #2: Concentrating on the effect of hyperthermia on human cognition, the authors conducted the Flanker tasks to investigate the differences of ERP and behaviors across different conditions. They found the varied measurements across multiple factors, although these results seem sound, concerns should be resolved by authors before considering for publication. 1. Although the authors mentioned the aim of their study, more information should be given for their novelty and purpose for hyperthermia and related ERP study. 2. Have the authors considered the gender effect on their results, since only three females were included in their study. 3. Since the authors said the ’incompatible’ setting was used in Flanker task, for congruent and incongruent conditions, how the subjects responded to these varied stimuli. 4. Only five channels were recorded, if the authors tried any referencing techniques during their data preprocessing. 5. For statistics, how did the authors perform the multiple comparison correction for ERP and behavior measurements? 6. If it is necessary to present the results for SD of RT when introducing their results. 7. How could the authors explain the confusing results of shorter RT and latency but decreased P300 amplitude for HEAT condition. 8. If it is suitable to using the Flanker task to index the task difficulty, the authors should give some explanation. 9. As depicted, more electrodes would be needed to clarify the brain mechanism accounting for effect of hyperthermia on P300, since our brain works as a large-scale complex network, and concentrating on P300 network, many related works have been implemented, such as F. Li, et al., Scientific Reports, 2015, 5: 15129; W. Peng, et al., PLoS One, 2012, 7(4):e34163 ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review?** For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. Attachments Attachment Submitted filename: Comments.docx https://doi.org/10.1371/journal.pone.0254769.r001
Revision 1
20 Jan 2021 Author Response Response to Editorial Office This manuscript needs to be significantly improved before it can be accepted for publication in 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. We revised our manuscript meeting PLOS ONE's style requirements. 2. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. We added the ORCiD ID for the corresponding author (Manabu Shibasaki) in the title page. Response to Reviewer #1 Reviewer #1: In this study the authors explore the effects of passive heat stress and recovery on the human cognitive function with Flanker tasks, involving congruent and incongruent stimuli. The results showed the reaction time (RT) was shortened during Heat rather than Pre and Recovery, and the peak amplitudes of the P300 component in ERPs were significantly smaller during Heat than during Pre, suggesting that hyperthermia alters the human cognitive function. However, I would have below comments for authors to improve the work. 1. In the abstract, there was unclear description on cognitive function, such as “… indicating a recuperated cognitive function…”, “These results suggest that hyperthermia alters the human cognitive function…”. Human cognitive function involves multiple factors, such as attention, memory, decision and so on. We revised these parts (from page 2, line 47 to page 3, line 58): “However, the peak amplitudes of the P300 component in ERPs, which involved selective attention, expectancy, and memory updating, were significantly smaller during Heat than during Pre, suggesting the impairment of neural activity in cognitive function. Notably, the peak amplitudes of the P300 component were higher during Recovery than during Heat, indicating that the impaired neural activity had recovered after sufficient whole-body cooling. An indicator of the stimulus classification/evaluation time (peak latency of P300) and the RT were shortened during Heat stress, but such shortening was not noted after whole-body cooling. These results suggest that hyperthermia affects the human cognitive function, reflected by the peak amplitude and latency of the P300 component in ERPs during the Flanker tasks,” 2. In the introduction, “Several non-invasive recording methods have been used to investigate the human cognitive function.”, what’s the non-invasive recording methods? Please give more description. We revised this part (page 4, lines 93-96): “Several non-invasive recording methods have been used to investigate the human cognitive function, such as functional magnetic resonance imaging (fMRI), functional near-infrared spectroscopy (fNIRS), and transcranial magnetic stimulation (TMS).” 3. In the last paragraph of the introduction, it looks like the section of discussion, please adjust the paragraph and provide more background introduction. We revised this part, as suggested (page 6, lines 129-145): “Thus, we chose “visual” Flanker tasks, which were used to examine the neural systems that resolve the conflict among response options [12]. In these tasks, a central target stimulus is presented simultaneously with distractor stimuli (flankers) and subjects are requested to respond according to the target and ignore the flankers. In general, the reaction time (RT) is shorter with Congruent stimuli than Incongruent stimuli [13, 14], indicating different levels of task difficulty [13, 14]. The second involves recovery after heat stress. As mentioned above, a short period of whole-body cooling after heat stress and face/head cooling during heat stress did not lead to full recovery of the peak amplitude of P300 [9, 10]. In addition, after a thorough literature research, we failed to identify any study examining the recovery process after heat stress by P300. Providing scientific evidence to support recovery from hyperthermia might be important to develop a methodology in our daily life and sports activities. Thus, we should examine whether sufficient whole-body cooling recovers the cognitive function reflected by the P300 component in ERPs.” 4. “Sixteen subjects (thirteen males and three females; mean age 21.4 ± 1.0 years) participated in this study”, it reflected the mismatch in the factor of gender. Whether the gender difference has an impact on the effects of passive heat stress and recovery on human cognitive function? Please give more explain. Thank you for this suggestion. We added the explanation in limitations of the present study (page 20, lines 466-474): “Finally, the present study recorded the data from thirteen males and three females, but did not investigate gender differences in the effects of passive heat stress and recovery on the human cognitive function. It is well-known that there are gender differences in thermoregulatory responses [31, 32]. In this study, we controlled the subjects’ internal temperature with a water-perfused suit, which minimized individuals’ thermoregulatory capacity. Therefore, any gender difference in thermoregulatory responses might affect the cognitive function during the process of recovery from hyperthermia. Further studies are needed to clarify this.” 5. How long does the Flanker task last, and how many trials in total does the task consist of for each subject? We added the explanation (from page 8, line 196 to page 9, line 203): “A run comprised 160 stimuli (i.e., 8 min), which included 40 stimuli for the left congruent arrowhead, 40 stimuli for the right congruent arrowhead, 40 stimuli for the left incongruent arrowhead, and 40 stimuli for the right incongruent arrowhead. The probability of all stimuli was equal, being presented in a random order. Inter-stimulus interval was fixed. Pre, Heat, and Recovery sessions included 160 stimuli, respectively. In a practice run, subjects were instructed to perform the Flanker tasks with 40 stimuli before recording the Pre session.” 6. In the section of EEG recordings, there only were 5 electrodes, and need make sure the quality of EEG data, what is the impedance of the five electrodes across the whole EEG experiment? And provide the detailed information. We added the explanation (page 10, lines 236-239): “All electrodes were detached after ERP recordings in Pre and Heat sessions, respectively, to avoid the effect of sweat on the EEG paste. Just before ERP recordings in Heat and Recovery sessions, all electrodes were again attached.” 7. In the section Discussion, the logic needs to be strengthened, and provide more supporting materials to support the finding “The effectiveness of cooling on impaired cognitive function in hyper-thermic individuals”. Thank you for this constructive comment. We revised this section (from page 17, line 391 to page 19, line 440). Response to Reviewer #2 Concentrating on the effect of hyperthermia on human cognition, the authors conducted the Flanker tasks to investigate the differences of ERP and behaviors across different conditions. They found the varied measurements across multiple factors, although these results seem sound, concerns should be resolved by authors before considering for publication. 1. Although the authors mentioned the aim of their study, more information should be given for their novelty and purpose for hyperthermia and related ERP study. Thank you for this suggestion. We revised the Introduction section (page 6, lines 129-145): “Thus, we chose “visual” Flanker tasks, which were used to examine the neural systems that resolve the conflict among response options [12]. In these tasks, a central target stimulus is presented simultaneously with distractor stimuli (flankers) and subjects are requested to respond according to the target and ignore the flankers. In general, the reaction time (RT) is shorter with Congruent stimuli than Incongruent stimuli [13, 14], indicating different levels of task difficulty [13, 14]. The second involves recovery after heat stress. As mentioned above, a short period of whole-body cooling after heat stress and face/head cooling during heat stress did not lead to full recovery of the peak amplitude of P300 [9, 10]. In addition, after a thorough literature research, we failed to identify any study examining the recovery process after heat stress by P300. Providing scientific evidence to support recovery from hyperthermia might be important to develop a methodology in our daily life and sports activities. Thus, we should examine whether sufficient whole-body cooling recovers the cognitive function reflected by the P300 component in ERPs.” 2. Have the authors considered the gender effect on their results, since only three females were included in their study. Thank you for this suggestion. Reviewer #1 also pointed out the same problem. We added the explanation in limitations of the present study (page 20, lines 466-474): “Finally, the present study recorded the data from thirteen males and three females, but did not investigate gender differences in the effects of passive heat stress and recovery on the human cognitive function. It is well-known that there are gender differences in thermoregulatory responses [31, 32]. In this study, we controlled the subjects’ internal temperature with a water-perfused suit, which minimized individuals’ thermoregulatory capacity. Therefore, any gender difference in thermoregulatory responses might affect the cognitive function during the process of recovery from hyperthermia. Further studies are needed to clarify this.” 3. Since the authors said the ’incompatible’ setting was used in Flanker task, for congruent and incongruent conditions, how the subjects responded to these varied stimuli. We added the explanation (page 8, lines 188-194): “For example, when the central arrowhead was directed to the left, the subjects were instructed to press a button with their left thumb. However, after being trained in the compatible setting, subjects were requested to respond in a direction opposite to the target arrowhead, called an ‘incompatible’ setting. For example, when the central arrowhead was directed to the left, the subjects were instructed to press a button with their right thumb.” 4. Only five channels were recorded, if the authors tried any referencing techniques during their data preprocessing. Reviewer #1 also pointed out the same problem. We added the explanation (page 10, lines 230-231): “Each scalp electrode was referenced to linked earlobes, which were mathematically calculated and averaged for reference.” 5. For statistics, how did the authors perform the multiple comparison correction for ERP and behavior measurements? We performed the Bonferroni post-hoc multiple-comparison to identify the specific differences among sessions, but did not adjust the comparison correction. We added the explanation (from page 11, line 267 to page 12, line 277): “For all repeated-measures factors, we tested whether Mauchly’s sphericity assumption was violated. If the result of Mauchly’s test was significant and the assumption of sphericity was violated, Greenhouse-Geisser adjustment was used to correct sphericity by altering the degrees of freedom using a correction coefficient epsilon. When a significant effect of Session was identified, the Bonferroni post-hoc multiple-comparison was adjusted to identify the specific differences among sessions. When a significant effect of Stimulus was identified, the post-hoc paired-t-test was adjusted to identify the specific difference between Congruent and Incongruent stimuli. We did not adjust the multiple comparison correction for all data.” 6. If it is necessary to present the results for SD of RT when introducing their results. Thank you for this helpful comment. We added the explanation on the results for SD of RT in many parts of Discussion sections. 7. How could the authors explain the confusing results of shorter RT and latency but decreased P300 amplitude for HEAT condition. We revised the Discussion section (from page 18, line 424 to page 19, line 440): “We considered that acceleration of RT and the latency of P300 and small response variability were related to specific effective connectivity in neural networks with an increasing internal temperature, which differs from the theory of structural connectivity [see a review, 27]. Kao et al. [28] recently reported that the peak amplitude of P300 in Flanker tasks was reduced, and that the peak latencies of P300 and RT were shortened after high-intensity interval training on a treadmill. Since the modulation of P300 was very similar to our findings, their data might be related to the effects of an increasing body temperature as well as the exercise of running on a treadmill. We hypothesized that the effects of an increasing body temperature on P300 differed between the amplitude and latency, paradoxically. Indeed, a study using multi-channel EEG recording showed that the resting-state network topology was significantly correlated with the amplitude of P300, but not the latency [29]. This study suggests that the amplitude and latency of P300 is related to different neural mechanisms, networks, and/or functional connectivity in the whole brain.” 8. If it is suitable to using the Flanker task to index the task difficulty, the authors should give some explanation. We added the Introduction section to explain the task difficulty in the Flanker task (page 6, lines 129-135): “Thus, we chose “visual” Flanker tasks, which were used to examine the neural systems that resolve the conflict among response options [12]. In these tasks, a central target stimulus is presented simultaneously with distractor stimuli (flankers) and subjects are requested to respond according to the target and ignore the flankers. In general, the reaction time (RT) is shorter with Congruent stimuli than Incongruent stimuli [13, 14], indicating different levels of task difficulty [13, 14].” 9. As depicted, more electrodes would be needed to clarify the brain mechanism accounting for effect of hyperthermia on P300, since our brain works as a large-scale complex network, and concentrating on P300 network, many related works have been implemented, such as > F. Li, et al., Scientific Reports, 2015, 5: 15129; W. Peng, et al., PLoS One, 2012, 7(4):e34163 Thank you for this suggestion. We added the explanation in Discussion (from page 18, line 433 to page 19, line 440): “We hypothesized that the effects of an increasing body temperature on P300 differed between the amplitude and latency, paradoxically. Indeed, a study using multi-channel EEG recording showed that the resting-state network topology was significantly correlated with the amplitude of P300, but not the latency [29]. This study suggests that the amplitude and latency of P300 is related to different neural mechanisms, networks, and/or functional connectivity in the whole brain.” Limitations of the present study (from page 19, line 458 to page 20, line 462): “Our ERP methods involving recordings from five electrodes did not directly clarify the brain regions associated with the reduced amplitude of P300 or the accelerated latency of P300. Therefore, multi-channel ERP recording would be needed to investigate the generator mechanisms, neural networks, and functional connectivity of P300.” Attachments Attachment Submitted filename: Response to Reviewers0119.docx https://doi.org/10.1371/journal.pone.0254769.r002
15 Mar 2021 Decision Letter - Guillaume Thierry, Editor PONE-D-20-33346R1 Effects of passive heat stress and recovery on human cognitive function: An ERP study PLOS ONE Dear Dr. Shibasaki, 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. First, allow me to introduce myself as the new editor handling your paper, as requested by the editorial office of PlosONE. Since I was not involved in the review process of your manuscript from the start, I have requested an evaluation from a third expert, to make sure that issues that might have been missed in the first round of reviews have been rechecked. I am pleased to say that the feedback on your paper is overall very positive, as is my own evaluation. The study is very interesting and the data and analyses provided are overall convincing. As you will see, the two reviewers who originally reviewed your paper have now recommended acceptance and require no other changes to the paper. Reviewer 3, however, has some concerns that would need to be addressed before I can recommend your paper for publication in PlosONE. At the moment, and unless the revisions requested bring up a critical issue in the next round, I expect to be in a position to make a final decision on your submission without requiring another round of external reviews. Whilst points 1 and 2 raised by the reviewer 3 are mainly interpretative and methodological, which should be quite straightforward to address, point 3 is more delicate. I invite you to address the remaining issues raised by Reviewer 3 carefully and submit your revised paper at your earliest convenience. Please submit your revised manuscript by Apr 29 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: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled '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, Guillaume Thierry, Ph.D. Academic Editor PLOS ONE Journal Requirements: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. [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: All comments have been addressed Reviewer #3: (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: (No Response) Reviewer #2: Yes Reviewer #3: Partly ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: (No Response) Reviewer #2: Yes Reviewer #3: 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: (No Response) Reviewer #2: Yes Reviewer #3: 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: (No Response) Reviewer #2: Yes Reviewer #3: 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 authors have made substantial changes to the manuscript to respond to my previously comments. I have no other comments. Reviewer #2: All of my concerns have been resolved by authors, and I do not have any further comments. Thanks for the authors' work. Reviewer #3: The manuscript reports analyses of ERP data before, during, and after participants underwent a heat stress challenge paradigm. These data must have been demanding to acquire and the authors are to be congratulated on this. I have a few points I would like them to respond to, a few substantive issues followed by more minor points: 1. The changes to cognitive function during heat stress and recovery are framed as impairments in the discussion, but the actual task performance, in terms of RT and consistency, is improved, while accuracy appears similar across conditions (perhaps a ceiling effect?). Yes the P300 was smaller in amplitude, but I don’t think that is evidence of impairment in of itself. This needs some attention in the Discussion. 2. I don’t see any mention of artefact correction or rejection – were all trials used? If EEG data quality differed between conditions, that could plausibly drive effects in component amplitudes – are you able to assess how likely that is to be a problem? 3. Related to the above point, you mention that electrodes were detached between conditions to minimise sweat artefacts. Can you reassure me that this dealt with this, as this does seem like a potentially important issue? 4. The theoretical relevance of changes to variability of RTs is not discussed. Minor issues 1. Breaking the introduction into more paragraphs might make it a bit more reader friendly. 2. Page 7 – ‘The man body mass and height…’ – Should ‘man’ read ‘mean’? 3. Page 8 – ‘the 2nd ERP was recorded after…’ – I would change to ‘ERP session was’ or ‘ERPs were’. Likewise for ‘the 3rd ERP 4. Page 12 – ‘Significance was set at p < 0.05.’ – ‘significance’ should read ‘alpha’ ****** 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 Reviewer #3: Yes:** Christopher W N Saville [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. https://doi.org/10.1371/journal.pone.0254769.r003
Revision 2
23 Mar 2021 Author Response Response to Reviewer #3 The manuscript reports analyses of ERP data before, during, and after participants underwent a heat stress challenge paradigm. These data must have been demanding to acquire and the authors are to be congratulated on this. I have a few points I would like them to respond to, a few substantive issues followed by more minor points: 1. The changes to cognitive function during heat stress and recovery are framed as impairments in the discussion, but the actual task performance, in terms of RT and consistency, is improved, while accuracy appears similar across conditions (perhaps a ceiling effect?). Yes the P300 was smaller in amplitude, but I don’t think that is evidence of impairment in of itself. This needs some attention in the Discussion. We added the explanation in the Discussion (page 19, lines 437-455): “The interpretation of these results requires special attention. We considered that acceleration of RT and the latency of P300 and smaller SD of RT (response variability) were related to specific effective connectivity in neural networks with an increasing internal temperature, which differs from the theory of structural connectivity [see a review, 30]. Kao et al. [31] recently reported that the peak amplitude of P300 in Flanker tasks was reduced, and that the peak latencies of P300 and RT were shortened after high-intensity interval training on a treadmill. Since the modulation of P300 and RT were very similar to our findings, their data might be related to the effects of an increasing body temperature as well as the exercise of running on a treadmill. We hypothesized that the effects of an increasing body temperature on P300 differed between the amplitude and latency, paradoxically. Indeed, a study using multi-channel EEG recording showed that the resting-state network topology was significantly correlated with the amplitude of P300, but not the latency [32]. This study suggests that the amplitude and latency of P300 is related to different neural mechanisms, networks, and/or functional connectivity in the whole brain. In future studies, these parameters should be analyzed during passive heat stress.” 2. I don’t see any mention of artefact correction or rejection – were all trials used? If EEG data quality differed between conditions, that could plausibly drive effects in component amplitudes – are you able to assess how likely that is to be a problem? We added the explanation in Materials and Methods section (page 10, lines 235-237): “Artifacts or noise caused by blinking or sweating were excluded on-line. If the number averaged was less than 35 for each stimulus, additional trials were performed.” 3. Related to the above point, you mention that electrodes were detached between conditions to minimise sweat artefacts. Can you reassure me that this dealt with this, as this does seem like a potentially important issue? Thank you for constructive comment. We added the discussion on this issue (page 17, lines 390-399): “In addition, the reduced amplitude of P300 might be related to electrical noise due to sweating during passive heat stress. However, as mentioned above, to avoid the effect of sweat on the EEG paste, we reattached all electrodes just before ERP recordings in Heat and Recovery sessions. Our previous study using the same procedure as in the present study showed that the amplitudes of some components in somatosensory evoked potentials (SEPs) reduced during passive heat stress, but other components did not [22, 23]. If the presence of sweat influences the SEP waveforms, all SEP components should be distorted. Therefore, we considered that sweat had a reduced effect on the amplitude of P300 in the present study.” 4. The theoretical relevance of changes to variability of RTs is not discussed. We added the discussion (from page 18, line 430 to page 19, line 455). Minor issues 1. Breaking the introduction into more paragraphs might make it a bit more reader friendly. We revised the introduction section. 2. Page 7 – ‘The man body mass and height…’ – Should ‘man’ read ‘mean’? Revised (page 7, line 155): “The mean body mass and height of the subjects were 71.7 ± 11.3 kg, and 170.5 ± 6.3 cm, respectively.” 3. Page 8 – ‘the 2nd ERP was recorded after…’ – I would change to ‘ERP session was’ or ‘ERPs were’. Likewise for ‘the 3rd ERP Revised (page 8, line 175): “ERPs were recorded after the external ear canal temperature” Revised (page 8, line 180): “ERPs were recorded (Recovery session) (Fig 1A).” 4. Page 12 – ‘Significance was set at p < 0.05.’ – ‘significance’ should read ‘alpha’ Revised (page 12, line 281): “All statistical analyses were conducted with α = 0.05.” Attachments Attachment Submitted filename: Response to ReviewersPONE-D-20-33346R1.docx https://doi.org/10.1371/journal.pone.0254769.r004
5 Jul 2021 Decision Letter - Thalia Fernandez, Editor Effects of passive heat stress and recovery on human cognitive function: An ERP study PONE-D-20-33346R2 Dear Dr. Shibasaki, 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, Thalia Fernandez, Ph.D. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed Reviewer #3: (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: Yes Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: N/A Reviewer #3: 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: No Reviewer #3: 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 Reviewer #3: 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 authors have made substantial changes to the manuscript to respond to my previously comments. I have no further comments. Reviewer #2: Thanks for the authors hard-working, no further comments for this work, so I suggest the publication of this work. Reviewer #3: Thank you for addressing my comments. However, the conclusions section still claims that cognition is impaired. Both by use of the word 'impairment' and by talking about recovery after cooling. I am not convinced the data support this characterisation so ask suggest the authors to either amend the conclusions or make the case why they think their data support a claim of impairment. Otherwise I am happy with the manuscript. ****** 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 Reviewer #3: Yes:** Christopher W N Saville https://doi.org/10.1371/journal.pone.0254769.r005
Formally Accepted
12 Jul 2021 Acceptance Letter - Thalia Fernandez, Editor PONE-D-20-33346R2 Effects of passive heat stress and recoveryon human cognitive function: An ERP study Dear Dr. Shibasaki: 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. Thalia Fernandez Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0254769.r006

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