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This work was supported by grants IN225414, IN200817, and IT201123 from the Universidad Nacional Autónoma de México (DGAPA-PAPIIT), with TF as recipient. 

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Partly

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously? -->?>

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available??>

The PLOS Data policy

Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English??>

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1:  This study investigated whether healthy older adults with excessive theta absolute power (AP) in their EEG, considered at risk for cognitive impairment, show reduced performance on highly demanding cognitive tasks. The researchers compared performance on the Visual Short-Term Memory Binding Test (VSTMBT) and the Loewenstein-Acevedo Scale for Semantic Interference and Learning (LASSI-II) between older adults with and without excessive theta AP. The results showed that no significant differences were found between the risk group (excessive theta AP) and control group on any test scores from the VSTMBT or LASSI-II. The degree of excessive theta AP did not predict performance on these highly demanding cognitive tasks.

There were no significant differences in performance when comparing high-risk, low-risk, and control groups. Traditional neuropsychological tests also showed no significant differences between groups.

The authors conclude that older adults with excessive theta AP do not exhibit impaired performance in highly demanding cognitive contexts, despite being at electroencephalographic risk of developing cognitive impairment in the future.

The study addresses an important gap in the literature by examining the relationship between EEG-based biomarkers of cognitive impairment risk and sensitive neuropsychological tests.

The use of both traditional and novel, highly demanding cognitive tests provides a comprehensive assessment. The inclusion of multiple criteria for defining risk groups adds robustness to the analysis. However, to my point of view, there are still some limitations need to be further addressed:

The statistical approaches, including permutation testing,PCA and multiple comparison corrections, are appropriate and robust. However, the sample size is relatively small, which may limit statistical power to detect subtle differences.

The cross-sectional design prevents conclusions about the predictive value of excessive theta AP for future cognitive decline.

The lack of significant differences between groups is intriguing and warrants further investigation. The authors' discussion of cognitive reserve as a potential explanation is appropriate.

It would be valuable to consider other factors that might influence the relationship between EEG markers and cognitive performance, such as lifestyle factors or genetic risk.

Overall, this is a well-conducted study that makes a valuable contribution to the field of cognitive aging and EEG biomarkers. While the negative findings are yielded, the authors are suggested to provide more detailed results interpretation with important insights and directions for future research.

Reviewer #2:  Peer reviewed by Jacob A. Eder., PhD,

For manuscript submission and further recommendations for conciseness of the scope of study.

PLOS ONE

No evidence of reduced capacity during highly demanding cognitive tasks in healthy

older adults at electroencephalographic risk of cognitive impairment

--Manuscript Draft—

PONE-D-24-42123

Article Type: Research Article

Full Title: No evidence of reduced capacity during highly demanding cognitive tasks in healthy

older adults at electroencephalographic risk of cognitive impairment

Short Title: Electroencephalographic risk of cognitive impairment and cognition

Corresponding Author: Thalía Fernández, Ph.D.

Universidad Nacional Autonoma de Mexico

Querétaro, Querétaro MEXICO

The manuscript demonstrates methodological rigor suitable for PLOS ONE publication standards, based on its design, analysis, and scope of inquiry into EEG biomarkers and cognitive assessment outcomes. The study implements a longitudinal and correlational approach, examining EEG-based markers in tandem with high-demand cognitive assessments to assess risk factors associated with cognitive decline in older adults—a population that often falls within the scope of neurodegenerative studies.

The participant inclusion criteria are meticulously outlined, encompassing individuals within the specified age range who meet neuropsychological benchmarks indicative of healthy cognitive function. Through the application of electroencephalography (EEG) with a specific focus on theta power as a predictive biomarker, the methodology aligns with established neurophysiological protocols. Notably, the use of non-invasive EEG as a predictive tool allows for a nuanced exploration of cognitive reserve and decline, serving as a non-intrusive alternative to cerebrospinal biomarkers, which carry significant procedural risks and costs.

From a neuropsychological perspective, the use of high-cognitive-demand tests—namely, the Visual Short-Term Memory Binding Test (VSTMBT) and the Loewenstein-Acevedo Scale for Semantic Interference and Learning (LASSI-II)—demonstrates an attempt to unveil cognitive decline undetectable by conventional neuropsychological assessments. Both assessments are neuropsychometrically validated tools sensitive to early cognitive dysfunction, and their inclusion reflects an understanding of the need for advanced diagnostic tools in clinical neuropsychology.

Statistical analysis is executed with precision through permutation-based testing, principal component analysis (PCA), and regression modelling, providing a robust framework to address the potential predictive value of theta power. Corrective measures for multiple comparisons, including false discovery rate (FDR) adjustments, reflect a statistical approach that minimizes Type I error risk, thereby strengthening the validity of the findings.

Although this study’s results do not show significant cognitive differences between the groups in either the high-demand or conventional assessments, the findings contribute to the body of literature by challenging the sensitivity of EEG-based markers to predict cognitive deterioration in cognitively healthy older adults. This conclusion aligns with the notion of cognitive reserve, suggesting that neurodegeneration may not immediately manifest behaviourally in individuals with compensatory cognitive mechanisms. Further investigation could explore the potential protective role of higher education levels, which might contribute to these individuals' apparent cognitive resilience.

In summary, the study exemplifies adherence to PLOS ONE’s publication criteria, utilizing quantifiable, reproducible, and rigorous techniques. The limitations acknowledged by the authors, such as the educational bias and restricted generalizability, are pertinent and recommend avenues for subsequent research to employ broader, demographically diverse sampling to validate these findings. This study thus establishes a foundation for expanding the application of EEG biomarkers in predictive neuropsychological assessments of age-related cognitive decline.

The study, while methodologically sound, would benefit from addressing several key areas to strengthen its contributions to neuropsychological and neurophysiological literature on age-related cognitive decline. Expanding upon these areas in future research would enhance both the study’s impact and its applicability within broader clinical and research contexts. The following recommendations are advised:

1. Broader Biomarker Integration:

The study currently relies solely on theta power as the electroencephalographic marker, which, while valuable, may not capture the full range of neurodegenerative processes linked to cognitive impairment. Integrating additional EEG frequency bands (e.g., alpha, delta, beta) could provide a more comprehensive profile of neurophysiological function, particularly in preclinical populations. Furthermore, incorporating other biomarkers, such as cerebrospinal fluid (CSF) amyloid-beta and tau levels, or neuroimaging markers like PET scans for amyloid or tau deposition, would enable a multi-modal approach that could cross-validate EEG findings and strengthen predictive accuracy.

2. Longitudinal Monitoring:

Although, this study provides a snapshot of cognitive and EEG measures, longitudinal monitoring over extended periods would reveal whether excessive theta power correlates with cognitive decline over time in the same individuals. Such an approach would enhance understanding of the temporal dynamics of theta power and its potential role as an early marker for neurocognitive disorders. Tracking changes in theta activity and cognitive performance over intervals (e.g., every six months to one year) would help delineate the predictive timeline for cognitive impairment in aging populations.

3. Diverse and Representative Sample:

This study’s sample shows an educational bias toward highly educated participants, potentially contributing to a heightened cognitive reserve that could mitigate detectable neuropsychological impairment. Future studies should aim for a sample that includes a diverse range of educational backgrounds, as well as socio-demographic diversity, to improve the generalizability of findings. It would be particularly informative to examine whether theta power’s predictive value varies across individuals with different baseline cognitive reserves.

4. Use of Additional Cognitive Assessments:

While the Visual Short-Term Memory Binding Test (VSTMBT) and Loewenstein-Acevedo Scale for Semantic Interference and Learning (LASSI-II) are suitable for assessing high-cognitive demand and are sensitive to subtle deficits, a broader neuropsychological battery would capture a wider array of cognitive functions potentially affected by neurodegenerative processes. Including tests that assess executive functions, attention, and processing speed—such as the Stroop Task, Trail Making Test, and Wisconsin Card Sorting Test—could reveal more nuanced cognitive impairments associated with excessive theta power. Additionally, the use of computerized cognitive assessments could facilitate finer-grained analysis of reaction times and error patterns, yielding a more detailed cognitive profile.

5. Exploration of Compensatory Mechanisms and Cognitive Reserve:

The study suggests that high educational attainment may serve as a proxy for cognitive reserve, potentially enabling individuals to maintain cognitive performance despite neurophysiological alterations. Further exploration of compensatory mechanisms through functional neuroimaging (e.g., fMRI or MEG during task performance) could clarify the neural correlates of cognitive reserve in older adults with excessive theta power. Identifying brain regions or networks that exhibit compensatory activation patterns would deepen the understanding of how cognitive reserve mitigates the effects of neurophysiological decline and could aid in developing targeted interventions.

6. Enhanced EEG Protocols and Dynamic Testing Conditions:

Given that EEG was recorded in a resting state, it may not fully capture task-specific neural activity variations that emerge during cognitive engagement. Employing task-based EEG recordings, particularly during high-cognitive-demand tasks like the VSTMBT and LASSI-II, would yield data on event-related potentials (ERPs) and dynamic EEG responses associated with cognitive performance. ERPs, particularly within theta, alpha, and gamma frequencies, could reveal task-specific deficits not apparent in resting-state EEG and provide a more detailed understanding of cognitive processing under demanding conditions.

7. Data Sharing and Open Access:

In line with open science practices, making EEG datasets and cognitive performance scores publicly available (where ethical and permissible) would enable independent verification and meta-analytic integration of findings across studies. While the data availability statement mentions restrictions on the LASSI-II data, public accessibility of non-restricted datasets (e.g., EEG data and VSTMBT scores) would facilitate further research and contribute to building a cumulative evidence base for EEG markers in cognitive impairment.

8. Consideration of Potential Confounding Factors:

Factors such as cardiovascular health, diet, and sleep quality—known to impact both EEG measures and cognitive function—are not accounted for in the current analysis. Future studies should consider controlling for or assessing these variables, as they could interact with theta power and cognitive performance. Screening for cardiovascular markers, diet quality, or incorporating self-reported sleep assessments could account for potential confounding effects and provide a more refined understanding of theta power’s relationship with cognitive health.

9. Investigating Non-Linear and Interaction Effects:

The current analysis appears to focus on linear relationships between theta power and cognitive performance. Wherever, cognitive decline may not exhibit a strictly linear association with theta power, particularly in populations with high cognitive reserve. Future research could investigate non-linear models or explore interactions between theta power and other demographic or neuropsychological variables (e.g., age, education level, and baseline cognitive performance) to uncover complex patterns that linear models may miss.

10. Developing a Predictive Model with Machine Learning:

Machine learning (ML) techniques, such as random forests or support vector machines, could be employed to develop predictive models using the study’s EEG and neuropsychological data. ML approaches can handle multi-dimensional data and potentially identify latent patterns across theta power, cognitive test scores, and demographic variables, which could improve predictive precision. ML algorithms may thus offer a practical solution for clinicians to assess cognitive risk factors using EEG data, integrating it into a tool for early-stage dementia risk assessment.

Collectively, these recommendations would elevate the study's contributions to the field, offering a more comprehensive understanding of the interplay between EEG biomarkers, cognitive reserve, and neuropsychological assessment in older adults. By addressing these suggestions, future research would refine EEG-based cognitive risk assessment tools, aligning with broader clinical and scientific initiatives for the early detection of neurodegenerative disorders.

RECOMMENDATIONS TO CONSIDER BEFORE PUBLICATION FINALISATION

Based on the thorough examination of this study, the manuscript demonstrates a high level of methodological rigor and scientific integrity, making it a strong candidate for publication. Wherever, while the study aligns well with the standards of PLOS ONE, appropriately and professionally incorporating specific revisions before submission could enhance the manuscript’s robustness and potential impact. Here is a summary of suggestions to consider:

1. Expanded Biomarker Assessment: While theta power is valuable, adding a discussion on the limitations of relying on a single EEG band as a marker and suggesting future studies include additional biomarkers would present a more comprehensive analysis. Mentioning plans to integrate multi-modal biomarker approaches, even if not implemented here, would position this work within the broader context of cognitive impairment research.

2. Longitudinal Perspective Emphasis: Reinforcing the potential of a longitudinal follow-up in a future study, particularly considering theta power's predictive window, would give readers a sense of the study’s next logical steps. While this is currently a cross-sectional study, emphasizing the importance of observing cognitive and theta power changes over time would underscore its contribution to the field and encourage replication studies.

3. Task-Based EEG Recommendation: The manuscript would benefit from acknowledging the limitation of using resting-state EEG alone and suggesting task-based EEG or event-related potential (ERP) testing in future studies. Briefly discussing how task-based EEG might reveal distinct neural activity patterns associated with cognitive effort could add depth to the methodological context.

4. Broader Sample Demographics: Addressing the educational homogeneity of the sample more directly, with an acknowledgment of its potential impact on cognitive reserve, could enhance transparency. Proposing a more demographically diverse sample in future studies, as a brief note in the limitations, would also demonstrate attentiveness to generalizability issues.

5. Confounding Variables: A short discussion on the influence of confounding factors such as diet, cardiovascular health, or sleep quality, while not feasible within the current scope, would provide context for the findings and inform future studies seeking to disentangle EEG changes specific to cognitive impairment from those influenced by lifestyle factors.

If these suggestions are integrated concisely, the manuscript will present a well-rounded perspective that addresses the current findings while inviting future exploration. Overall, the paper is near ready for submission, but these minor adjustments would strengthen its reception and significance within the field.

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what does this mean? ). If published, this will include your full peer review and any attached files.

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Reviewer #1: Yes:  Bochao Lin

Reviewer #2: Yes:  Jacob A. Eder, PhD

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Attachments

Attachment

Submitted filename: PLOS PONE-D-24-42123 Peer Review_Eder.pdf

No evidence of reduced capacity during highly demanding cognitive tasks in healthy older adults at electroencephalographic risk of cognitive impairment

PONE-D-24-42123R1

Dear Dr. Fernández,

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.

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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,

Giulia Prete

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers are very satisfied with the revisions made. I carefully revised the manuscript myself and I believe it adds important evidence in this research field. Thus, I am happy to support the publication of the manuscirpt in ots present form and I would like to thank very much the expert Reviewers for the time spent in their revisions, and the Authors who ully considered the suggestions received. As you can see below, Reviewer 2 only recommends to further specify future research directions: I leave it to the authors to decide whether and how to implement this point. 

Reviewer's Responses to Questions

Comments to the Author

Reviewer #1: (No Response)

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions??>

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously? -->?>

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available??>

The PLOS Data policy

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English??>

Reviewer #1: Yes

Reviewer #2: Yes

**********

Reviewer #1: I have reviewed the manuscript "No evidence of reduced capacity during highly demanding cognitive tasks in healthy

older adults at electroencephalographic risk of cognitive impairment" for the previous submission and recommended revisions. The authors have responded to my queries and incorporated it into the manuscript, along with feedback from other reviewers, which I believe improved the quality of the MS acceptable to be published.

Reviewer #2: Reviewer’s Reassessment of Manuscript PONE-D-24-42123R1

The revised manuscript titled “No evidence of reduced capacity during highly demanding cognitive tasks in healthy older adults at electroencephalographic risk of cognitive impairment” has been carefully evaluated following the incorporation of the recommended revisions. The authors have demonstrated a rigorous and methodical approach in addressing the concerns raised during the initial review, resulting in a significantly refined and robust manuscript.

Strengths of the Revised Manuscript

Comprehensiveness of Methodological Enhancements

The study's methodological framework has been strengthened through clearer articulation of the rationale for group selection, particularly in distinguishing between the risk and control groups based on theta absolute power (AP) z-scores. The authors have also elaborated on the statistical approaches employed, ensuring transparency in the permutation testing, principal component analysis (PCA), and multiple comparison corrections, which add robustness to the analytical rigor of the study.

Clarification of the Study’s Scope and Predictive Framework

The clarification regarding the cross-sectional nature of the study and the explicit reference to prior longitudinal studies (Prichep et al., 2006; Gouw et al., 2017) effectively contextualizes the findings. By acknowledging the limitations of a single-time-point design while reinforcing the predictive validity of theta AP excess through prior evidence, the authors have provided a balanced discussion that situates the present findings within the broader literature.

Refinement of Statistical Limitations and Sample Considerations

The acknowledgment of the study’s relatively small sample size and its implications for detecting subtle cognitive differences has been appropriately incorporated. Additionally, the discussion regarding potential biases introduced by the high level of education within the sample has been expanded, reinforcing the need for future studies to examine diverse educational backgrounds.

Enhanced Discussion on Cognitive Reserve and Compensatory Mechanisms

The manuscript has been notably strengthened by the expanded discussion on cognitive reserve and compensatory neural mechanisms. The references to the HAROLD model and potential bilateral recruitment in older adults exhibiting high theta AP provide a compelling theoretical framework that adds depth to the interpretation of null findings. Furthermore, the inclusion of prior research linking physical activity, inflammation markers, and genetic risk factors to EEG-based cognitive predictions adds a valuable multi-dimensional perspective.

Integration of Broader Neurophysiological and Biomarker Considerations

The discussion of additional EEG frequency bands (e.g., alpha, delta, beta) and their potential role in cognitive decline strengthens the manuscript's neurophysiological breadth. While theta power remains the primary focus, the authors have effectively contextualized its relevance within a broader spectrum of electrophysiological biomarkers.

Commitment to Open Science and Data Transparency

The inclusion of a publicly accessible dataset via the GitHub repository is commendable and aligns with best practices in scientific transparency. The explanation regarding the delayed release of LASSI-II scores until the completion of the normative database provides a reasonable and ethical justification.

Areas for Further Consideration

Potential for Nonlinear Analytical Approaches

While the manuscript primarily explores linear relationships between theta power and cognitive function, cognitive decline is increasingly understood to exhibit nonlinear patterns, particularly in individuals with high cognitive reserve. The suggestion to explore non-parametric or machine learning approaches (e.g., random forests, support vector machines) is well-founded and could be incorporated into future research directions.

Utility of Task-Based EEG Measures

The resting-state EEG approach remains a widely used and valid neurophysiological tool; however, the potential benefits of event-related potentials (ERPs) in elucidating task-specific neural dynamics have been acknowledged. Future studies incorporating cognitive task-based EEG paradigms could yield more granular insights into compensatory mechanisms.

Generalizability and Population-Level Implications

Although the study provides valuable insights into EEG-based risk assessment, the high level of education within the sample poses limitations for generalizability. Additional discussion regarding how these findings translate to populations with lower cognitive reserve or different cultural contexts could enhance the study’s applicability.

Final Assessment

The revisions implemented in response to the initial peer review have substantially strengthened the manuscript. The authors have demonstrated a commendable commitment to refining the clarity, depth, and methodological precision of their work. The study stands as a meaningful contribution to the field of cognitive aging and EEG-based biomarkers, offering insights into the potential resilience of older adults with high theta AP in cognitively demanding contexts. The expanded discussion on cognitive reserve, compensatory mechanisms, and broader biomarker integration enhances the interpretability and impact of the findings.

With these improvements, the manuscript is now well-positioned for publication, with only minor considerations for future research directions. The careful attention to prior critiques and the methodical approach in addressing them reflect the authors' commitment to high scientific standards.

Recommendation: Acceptance with minor considerations for future research directions.

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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:  Bochao Danae Lin

Reviewer #2: Yes:  Jacob A. Eder, PhD

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