NeuroBOLT: Resting-state EEG-to-fMRI Synthesis with Multi-dimensional Feature Mapping

Functional magnetic resonance imaging (fMRI) is an indispensable tool in modern neuroscience, providing a non-invasive window into whole-brain dynamics at millimeter-scale spatial resolution. However, fMRI is constrained by issues such as high operation costs and immobility. With the rapid advancements in cross-modality synthesis and brain decoding, the use of deep neural networks has emerged as a promising solution for inferring whole-brain, high-resolution fMRI features directly from electroencephalography (EEG), a more widely accessible and portable neuroimaging modality. Nonetheless, the complex projection from neural activity to fMRI hemodynamic responses and the spatial ambiguity of EEG pose substantial challenges both in modeling and interpretability. Relatively few studies to date have developed approaches for EEG-fMRI translation, and although they have made significant strides, the inference of fMRI signals in a given study has been limited to a small set of brain areas and to a single condition (i.e., either resting-state or a specific task). The capability to predict fMRI signals in other brain areas, as well as to generalize across conditions, remain critical gaps in the field. To tackle these challenges, we introduce a novel and generalizable framework: NeuroBOLT, i.e., Neuro-to-BOLD Transformer, which leverages multi-dimensional representation learning from temporal, spatial, and spectral domains to translate raw EEG data to the corresponding fMRI activity signals across the brain. Our experiments demonstrate that NeuroBOLT effectively reconstructs unseen resting-state fMRI signals from primary sensory, high-level cognitive areas, and deep subcortical brain regions, achieving state-of-the-art accuracy with the potential to generalize across varying conditions and sites, which significantly advances the integration of these two modalities.

Paper

Similar papers

Peer review

Reviewer bwvZ4/10 · confidence 5/52024-07-11

Summary

This paper introduces NeuroBOLT, a transformer-based model. NeuroBOLT utilizes multi-dimensional representation learning across temporal, spatial, and spectral domains to translate raw EEG data into comprehensive fMRI activity signals across the entire brain. Experimental results showcase NeuroBOLT's ability to effectively reconstruct resting-state fMRI signals across primary sensory, high-level cognitive areas, and deep subcortical regions.

Strengths

1. The paper tackles one of the most challenging and competitive topics in neuroscience. 2. The motivation behind the paper is quite clear, and the experimental section is logically sound. 3. The figures and tables in the article are clear and well-organized, making it highly readable.

Weaknesses

1. The method abbreviation and the title are not closely related. It is unclear where 'BOLT' comes from in the title, and even after reading the abstract, it remains confusing. 2. In fact, there has been a lot of work on fMRI-EEG in recent years, especially in 2023 and 2024, but the author's related work lacks a significant amount of relevant literature. 3. In the abstract and introduction, the author's description of the method is inconsistent with the organization in the methodology section, resulting in a need for improved readability. 4. The writing of the article needs to be further standardized. For example, 'FMRI data' is sometimes written with a capital 'F' and other times as 'fMRI data'. 5. Although the layout and presentation of the tables are aesthetically pleasing, the font size is too small, making them difficult to read even when enlarged. 6. The paper does not provide code or data to support the reproducibility of results. 7. This paper lacks details on the parameter selection for the baseline methods. Although the authors state, 'The baseline models are from [44] and [16], where we choose the models with the best downstream classification task performance,' the datasets and tasks in references [16] and [44] are not entirely consistent with those in this paper. Therefore, the authors should specify the exact process of parameter selection. 8. The equations and symbols in the article are not very standardized. The authors should provide notation to help readers understand. 9. The authors should conduct statistical tests to validate the significance of their methods. 10. For readers in the NeurIPS community, the theoretical contribution of this paper appears to be weak. 11. I don't quite understand what the author means by the third point of contribution: 'Successful resting-state fMRI reconstruction To our knowledge, this is the first study to successfully reconstruct the resting-state fMRI signal from raw EEG data, with only 26 electrodes.' What is the significance of 26 electrodes? 12. Equation 2 does not appear to be a complete equation.

Questions

Please see the twelve weaknesses above.

Rating

4

Confidence

5

Soundness

2

Presentation

3

Contribution

2

Limitations

Limitations are discussed in the section of Discussion and Conclusion.

Authorsrebuttal2024-08-13

Thank you for the comments - Part 1

Thank you very much for your additional comments. Please note that this year, **authors are not permitted to upload the revised full manuscript or include links to external pages during this rebuttal period.** We were only allowed to upload a one-page PDF (please kindly refer to our [Global Response](https://openreview.net/forum?id=y6qhVtFG77&noteId=VLcizb9WHq)). Therefore, we are unable to provide the revised manuscript here (in response to your **Points 1 and 4.2**), but will upload it when permitted. Responses to your other new concerns are below: >**Point 2:** We appreciate the reviewers' thorough examination of related work. Our rationale for including particular baselines, and further discussion of your reference list ([1-6]), is provided below: **Ref. \[2\]** is an excellent review article on simultaneous EEG-fMRI, and we will add it to the other simultaneous EEG-fMRI articles that we have cited in our original manuscript (including Ritter et al., 2006; Laufs et al., 2003, 2006; Chang et al. 2013; de Munck et al., 2009). With regard to the DCM model in **Ref. \[4\]**, we had not selected it as a baseline since it requires specifying stimulus onsets along with the neuroimaging data. Since no stimuli are presented during resting state, this model can not operate on resting-state data without major modifications. In discussing their future directions, the authors of **Ref. \[4\]** state: “Finally, the expansion of the current task-based analysis to the corresponding resting-state methodology, where an equivalent canonical microcircuit formulation for cross spectral data features, will be needed.” **Ref. \[6\]**, aims to infer the effective (directed) connectivity of a brain network based on the complementary information provided by EEG and fMRI. This is interesting work too, but does not appear to provide a framework for inferring fMRI time courses from EEG. As we mentioned in our first rebuttal, we indeed plan to cite **Ref. \[3\]** (which is the preprint version of *\[3\]* in the previous response) and **Ref. \[5\]** (which uses the same model as *\[1,2\]* in the previous response). For **Ref. \[3\]**, we were unable to find the code, and some experimental settings are not specified in their paper, which would make a direct comparison potentially unfair and unreliable, so we did not include it as a baseline. For **Ref. \[5\]**, the model only accepts 64-channel EEG as input (according to the authors’ GitHub repo and PyPi sites). Since we are using EEG data from 32-channel caps, we did not include this model as a baseline here, but look forward to doing so in future studies with 64-channel data. **Ref \[1\]** explored three conventional architectures: FCNN, CNN, and Transformer. However, the paper did not provide code/model parameters and offered limited information about the training process. In our baselines, we have included models that are similar to or more advanced versions of these architectures (see Appendix B.2 in the original manuscript: CNNs *\[19, 23, 24, 32\]* and Transformers *\[16, 44, 36, 32\]*). | Baselines | If&nbsp;included | Rationale | | :---- | :---- | :---- | | [1] | ✗ | - Source code is not available; - Model parameters are not specified; - We already included baselines with similar or advanced versions of these architectures | | [3] | ✗ | - Source code is not available; - Model parameters are not specified | | [4] | ✗ | Not applicable without major modifications | | [5] | ✗ | Only supports 64-channel inputs | | [7] | ✓ | Provided in the manuscript. | | [8] | ✓ | Provided in the manuscript. | We hope that our response helps to clarify the rationale behind the baseline models selected for this submission. While the simultaneous EEG-fMRI field is indeed large, the area of EEG-to-fMRI synthesis is currently a niche but rapidly emerging subfield. We will also include the referenced papers in our revised manuscript, which will appear on this forum when we are permitted to submit. ### **Please see our responses to _<Point 3, Point 4 and references>_ in our [next comment block](https://openreview.net/forum?id=y6qhVtFG77&noteId=wkIJndrOr2)**

Authorsrebuttal2024-08-13

Thank you for the comments - Part 2

### **Here are the responses to <Point 3, Point 4 and references>** (For responses to **Point 1 and Point 2**, please see the **[comment block above](https://openreview.net/forum?id=y6qhVtFG77&noteId=ssbQ088SCz)**) >**Point 3:** If we understand correctly, the reviewer suggests running a grid search for each baseline model to find the parameters that perform optimally on the current dataset and with the current evaluation metrics. In our study, we had adopted the parameter settings recommended by the authors. When evaluating baselines, it is common practice to use the parameters suggested by the original authors, due to the computational burden associated with a comprehensive parameter search across the search space for each application. Moreover, we would like to clarify that we **used the same evaluation metrics as in \[7,8\], i.e., correlation coefficient (i.e., R values).** For the other EEG encoding models, the tasks in the original papers are different (mostly classification tasks like detection of seizures, event type classification, etc.), so metrics like accuracy, AUC, Cohen’s Kappa, and weighted F1 were used in these papers. To further address your concern regarding differences in dataset, we conducted additional experiments on the ***same dataset*** as in refs. \[7,8\] (eyes open/close task fMRI), predicting the ***same brain regions***, using the ***same settings and objective*** (i.e., intra-subject prediction). The results (R ± S.D) are shown below, with the best values in bold. **We find that our model still outperforms \[7,8\].** | Model | Pallidum | Caudate | Putamen | Accumbens | Average | | :---- | :---- | :---- | :---- | :---- | :---- | | Ours | **0.57 ± 0.18** | **0.58 ± 0.11** | **0.57 ± 0.16** | **0.60 ± 0.11** | **0.58 ± 0.02** | | \[7\] | 0.43 ± 0.15 | 0.49 ± 0.12 | 0.51 ± 0.14 | 0.43 ± 0.13 | 0.47 ± 0.04 | | \[8\] | 0.37 ± 0.04 | 0.47 ± 0.14 | 0.48 ± 0.16 | 0.42 ± 0.05 | 0.44 ± 0.05 | >**Point 4:** * **4.1)**: We apologize for the confusion, but our intention here for saying *"validate the robustness and applicability of our learned representations across neural data from different sites and scanners"* was to convey that our model shows promising applicability to another dataset, even if it is collected in a different condition (task) and on a different scanner (see **[Global response](https://openreview.net/forum?id=y6qhVtFG77&noteId=VLcizb9WHq)** and **Part 1** in the one-page PDF). We now notice that the word ”robustness” could cause confusion so we will omit this word in our revised manuscript. Evaluating the influence of noise requires simulating different noise levels, which is a bit out of the current scope of this paper, but it is a very interesting future direction. * **4.2)**: We had planned to provide further details on the building blocks of our model, including specific details of the multi-scale spectral representation learning module. Multiscale temporal representations and Short-Time-Fourier-Transform (STFT) are proving to be highly effective in representing neural data \[9,10\]. While the components of this module have well-established theoretical foundations in signal processing, our key contribution lies in integrating these components to work effectively together, resulting in a novel method and application (shown through ablation studies in *Section 4.4 Table 2*). Our planned additions include the following: 1. Formally describe (i.e. provide mathematical notations) how we utilized STFT to convert EEG time sequences into time-frequency features. 2. Discuss how the dimensions of frequency features depend on the time-window length with equations illustrating this relationship, and emphasize the rationale for selecting specific window lengths. 3. Introduce the trade-off between temporal and frequency resolution, further clarifying the reasoning behind using an approach that considers multiple window lengths. Thank you once again for your valuable comments. We hope our responses fully address your concerns. **References:** [1-6]: see refs. [1-6] in the Reviewer’s previous comment [7] Li et al. “Leveraging sinusoidal representation networks to predict fMRI signals from EEG” [8] Kovalev et al. “fMRI from EEG is only Deep Learning away: the use of interpretable DL to unravel EEG-fMRI relationships.” arXiv preprint. [9] Van De Ville et al. “When makes you unique: Temporality of the human brain fingerprint." [10] Samiee et al. “Epileptic seizure classification of EEG time-series using rational discrete short-time Fourier transform”

Reviewer rcEv8/10 · confidence 4/52024-07-12

Summary

The manuscript proposes an EGG-to-fMRI synthesis model. The framework implements a transformer architecture and uses a multi-channel feature combination expanded across the temporal axis. To evaluate the proposed model, EGG and fMRI data from 22 participants were recorded while they were in the resting state with eyes closed.

Strengths

The manuscript addresses an interesting problem and can open opportunities for multimodal neuroimaging analysis. Overall, this line of investigation is little explored, therefore, the present manuscript is novel and of interest to the community. The present manuscript is quite complete, (1) the model and rationale behind are sound; (2) a dataset is collected which allows a faithful evaluation of the proposed translation (from EEG to fMRI); (3) it's rather easy to read and follow the manuscript, (4) the reported results are promising.

Weaknesses

The biggest weakness is that the framework and the dataset are only addressing the resting state. While this is an important baseline to investigate, it would have been great to explore the fidelity of the proposed framework when participants are presented with some stimuli. It is unclear whether the source code and dataset will be released publicly. The stability of the results is fully guaranteed given no statistical analyses are performed.

Questions

What is "In-scan" in Table 1? This is not explained in the manuscript. It is unclear to me why all methods are not evaluated for both inter-subject and in-scan. For example, isn't it possible to evaluate BIOT [44] for inter-subject data?

Rating

8

Confidence

4

Soundness

3

Presentation

3

Contribution

4

Limitations

The manuscript sufficiently discusses its current limitations. I think the limitations section should tap into the particular scenario that the model has been evaluated on (resting state) and whether the results will be generalisable to other scenarios remains to be shown.

Reviewer EkS25/10 · confidence 5/52024-07-19

Summary

In this work, the authors present a deep learning architecture for inferring functional magnetic resonance imaging (fMRI) signal from electroencephalography (EEG) data. The proposed model, named NeuroBOLT, utilizes transformer backbones to provide spatial, temporal, and frequency-based features from the EEG are utilized for reconstruction. The authors demonstrate the performance of their architecture on a small (N=22) data set using a propriatary data set of simultaneously measured EEG-fMRI.

Strengths

fMRI reconstruction from simultaneous EEG is a fascinating topic, and a difficult problem to tackle. The approach taken by the authors in this work is novel for the task at hand, i.e. using a multi-scale spectral feature embedding. Although the decision to use multi-scale spectral embeddings is not new in MRI analysis, as far as I could find the approach has not been utilized for this particular problem and the authors address novel problems for their application to simultaneous EEG-fMRI data in a deep learning architecture. At best this paper is a novel methodological tweak applied with state of the art architectures to see improvements over other deep learning baselines. The breadth of the experiments attempted by the authors is promising; however, see my discussion below for more of a discussion of the limitations of the experiments performed. The authors also perform an ablation study to explore how the inclusion of Multi-Scale Spectral features improves model performance, thus demonstrating the benefit of combining the multi-scale spectral features with the spatiotemporal. This is well appreciated.

Weaknesses

The major weaknesses of this work come down to weaknesses in the empirical evaluation. I am afraid that in its current state, the evaluation does not lead to a convincing demonstration of this method for fMRI reconstruciton, and the claims in the introduction about novelty coming from the application to multiple brain regions and resting-state fMRI seem somewhat overemphasized. Currently this brings it to a full reject as the paper is otherwise sound but the limitations in the evaluation are significant enough to bring it well below the threshold, and cannot be easily addressed in the rebuttle I believe. First, I will highlight the lack of reported standard deviations or error bars in any of the results. No standard deviations are provided in tables 1 or 2, or in any of the figures providing results. In the checklist, the authors state "Error bars are not reported at the current stage because it would be too computationally expensive to compute over all the brain regions and for all participants,also there is limited space in the paper to put all the statistics. But we could always add this information if reviewers think it’s important to know." While I appreciate the authors' acknowledgement of this exclusion, I do think error bars are absolutely necessary to demonstrate the efficacy of the proposed method. The demonstrated improvements are often quite small (e.g. improvement from 0.540 to 0.588 in table 1), and it is not clear if the purported improvements can be explained away from model noise. I could not find any information about controlling model initialization or seeds as well to ensure that random initializations played a less significant role between experiments even with the same architecture on different regions. I absolutely think error bars are necessary for this work, and the reasoning provided by the authors is not mitigated elsewhere or behind a more significant barriers other than training and evaluation time. Additionally, the authors could have mentioned this omission in the limitation section of their main paper since I had to go to the checklist to be sure the authors were aware of the issue. Second, in the abstract the authors highlight the ability to "generalize to other brain areas" and "other conditions (such as resting state)". Unless I am missing something, I cannot find any experiments by the authors that address these particular gaps. The authors do provide inter- and intra-subject predictions which is interesting; however, their model is still only trained on individual ROIs, and they don't include any experiments demonstrating transfer learning between models trained on other regions, and they do not include any experiments studying other tasks BEYOND resting-state fMRI. Thus, the paper falls into the same limitation as past works which were only focused on task, just in the other direction. This work would have been much more compelling if they could demonstrate a model which trained well both on task and rest related data, or even better, which could reconstruct task-related data despite only being trained on resting-state fMRI. The acknowledgement of the limitations in the literature is thus misleading as the proposed method still suffers from these same limitations. The choice to only demonstrate the results for several ROIs highlights this limitation - it would be okay if the authors did not seem to imply elsewhere that their model gets around the single-ROI training approach from past methods. Clearly, the N in this study is quite small. This is to be expected as simultaneous EEG-fMRI is still quite rare as a sequence to collect; however, the authors seem to gloss over all of the myriad issues which will come with training their data over such a small data set. I am not penalizing this work for the small N in and of itself, but as I cannot find any mention of common obstacles such as overfitting, bias towards particular kinds of reconstruction errors, and other limitations that would inevitably arise. I am extremely surprised I could find no mention of pretraining anywhere in this work, which I almost imagine would be hugely necessary for these kinds of studies with very small data sets. Again, it's not necessarily a limitation in and of itself to not do these things, with how the paper currently reads these seem to be touted as benefits of the new approach which are not backed up by evidence.

Questions

How well does the model trained on other ROIs transfer to reconstruction of completely different ROIs? How might scanner model and particular parameters of the resting state sequence affect reconstruction? Why do you not compare anywhere with Source Localization? Source Localization is only mentioned once offhand, and its limitations and efficacy as a reconstruction technique are not gone into in detail. I am surprised it was not included as a baseline method in fact.

Rating

5

Confidence

5

Soundness

3

Presentation

3

Contribution

3

Limitations

The authors do provide some discussion of the limitations of their work; however, as I have noted above, there are some limitations which are ommitted from the main body of text which at least should have been acknowledged in this section. The authors state they have IRB approval in section 4.1 of their paper. I see no reason for additional review.

Reviewer EkS22024-08-09

Score Adjustment

The rebuttal provided by the authors addresses much of the concerns raised here. The requested error bars somewhat lower the impact of the model compared to baselines, as there is high variance and many baselines perform fairly comparably; however, there is demonstrative improvement. I have raised my score to a borderline accept.

Authorsrebuttal2024-08-13

Thank you for increasing your score

Thank you so much for your prompt response and raising the score. We are happy that our additional experiments have improved this work, and sincerely appreciate your feedback, which helps to improve the quality of our paper. We acknowledge that the error bars are relatively large across all methods. While variability in the performance across individuals presents a challenge, we find it promising that our method achieves consistently higher mean performance than the baselines for all (or all but one) of the ROIs in the intra/inter-scan comparisons (Figs. R1.2, R2.1, R2.2 in the one-page PDF), though indeed not all of these differences are statistically significant. By contrast, considering only the baseline methods, these appear to vary across ROIs in terms of which model achieves the highest mean performance. Additionally, we believe this is the first study to incorporate and adapt these state-of-the-art EEG Encoding baselines in this specific application of EEG-to-fMRI translation. We believe that your comment is highly valuable, and will include a discussion of this limitation in our revised manuscript. In addition, we are planning further in-depth exploration of the factors that may drive performance variability across individuals in our future work, as this is indeed an important issue. Thank you once again for your valuable comments!

Reviewer bwvZ2024-08-12

Thank you for the author's response. 1. Some specific modifications by the author were not observed, such as W3, W5, W6. 2. Regarding W2, [1-6].... Aside from the paper titled "EEG-to-fMRI Synthesis," many papers titled "simultaneous EEG/FMRI" also align with the direction of this work. Among the articles cited and compared by the author, only 19 and 24 are related to EEG-fMRI translation, while most focus on EEG Encoding. The insufficient comparative experiments also stem from a lack of thorough research in the related work. 3. Regarding W7, the author stated, "We strictly adhered to the model settings provided in their original papers when training." However, the datasets and evaluation metrics used by the author may differ from those in the original paper, which may not be entirely fair. 4. Regarding question 10, the author mentioned "validate the robustness and applicability," but based on the appendix results, it appears that the author did not conduct an in-depth study of robustness, such as the method's robustness under different fMRI and EEG noise levels. Additionally, "We will include more detailed theoretical derivations and explanations of spectral representations in the appendix to strengthen the theoretical foundation of our work." These specific details should also be clarified. [1] Bricman P, Borst J. EEG2fMRI: Cross-Modal Synthesis for Functional Neuroimaging[J]. 2021. [2] Trujillo-Barreto N J, Daunizeau J, Laufs H, et al. EEG–fMRI Information Fusion: Biophysics and Data Analysis[M]//EEG-fMRI: Physiological Basis, Technique, and Applications. Cham: Springer International Publishing, 2023: 695-726. [3] Liu X, Tu T, Sajda P. Inferring latent neural sources via deep transcoding of simultaneously acquired EEG and fMRI[J]. arXiv preprint arXiv:2212.02226, 2022. [4] Wei H, Jafarian A, Zeidman P, et al. Bayesian fusion and multimodal DCM for EEG and fMRI[J]. Neuroimage, 2020, 211: 116595. [5] Calhas D. EEG-to-fMRI Neuroimaging Cross Modal Synthesis in Python[J]. 2023. [6] Tu T, Paisley J, Haufe S, et al. A state-space model for inferring effective connectivity of latent neural dynamics from simultaneous EEG/fMRI[J]. Advances in Neural Information Processing Systems, 2019, 32. .........

Reviewer rcEv2024-08-13

I thank the authors for responding to my questions. I do not have any further questions.

Authorsrebuttal2024-08-14

Thank you!

Thank you once again for your valuable and encouraging feedback! We sincerely appreciate the time and effort you put into the review process.

Authorsrebuttal2024-08-14

Thank you very much for the review! We will provide detailed information on data sources and IRB in the updated manuscript.

Authorsrebuttal2024-08-14

Thank you very much for the review! Our volunteers are all healthy controls, consisting of 12 females and 10 males, with an average age of 35.22 ± 16.86 years. Additional detailed demographic information, along with data sources and IRB details, will be provided in the updated manuscript.

Program Chairsdecision2024-09-25

Decision

Accept (poster)

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