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Are BOLD signal amplitude and synchronous low frequency fluctuations of EEG power related?
Wanyong Shin1, Balu Krishnan2, Ajay Nemani1, Anna Crawford1, and Mark J Lowe1
1Radiology, Cleveland Clinic, Cleveland, OH, United States, 2Epilepsy, Cleveland Clinic, Cleveland, OH, United States

Synopsis

Resting state motor network is investigated using EEG theta to beta ratio (TBR) and compared with calibrated fMRI.

Introduction

Resting-state functional MRI (rs-fMRI) has become perhaps the most popularly method to investigate neuronal functional connectivity (FC) [1,2]. Integration of fMRI with direct neuronal measurement such as EEG enhances the utility of fMRI studies. [3,4]. Analysis of whole-brain temporal fluctuations of EEG signals and quantification of their spatial coherence within the resting-state network (RSN) is challenging since scalp-recorded EEG measurements are attenuated by the resistivity of skull and dura.
In this study, we investigated low frequency fluctuation of EEG power within the resting-state motor network and compare it with simultaneously acquired fMRI, blood flow and cerebral metabolic rate of oxygen data, calibrated using a hypercapnia challenge.

Methods

Simultaneous EEG-fMRI data were collected from 7 MS patients. EEG was acquired using 64 channel gold-cup electrodes placed on the scalp. Seven minutes of eyes-closed resting-state EEG data were acquired before and during an MRI scan.
MRI Data Acquisition: rsfMRI data were acquired at 3T using 2d GRE EPI PACE sequence (TR/TE=2800/27 ms, voxel size = 2x2x4 mm3, 31 slices). In addition, an in-house simultaneous multi-slice excited double echo pseudo-continuous tagging arterial spin labeling sequence was used for the following fMRI and hypercapnia scans [5]. Four blocks (48s On/Off periods) of 2 Hz paced unilateral finger tapping task was performed during the fMRI scan. The study was repeated two times inside the scanner. Five percent of CO2 mixed gas was delivered two times with 2 mins of periods during 12 mins of scanning.
EEG analysis: For EEG acquired inside the scanner, template subtraction was used to remove the MR gradient artifact [6]. Cardioballistic artifacts, eyeblink artifacts were also identified and removed. EEG data were downsampled to 250 Hz and band-pass filtered using a Chebyshev filter at the following frequencies: 1-4 Hz (delta), 4-8Hz (theta), 8-13 Hz (alpha), 13-20 Hz (low beta), 20-30 (high beta), 30-40 Hz (low gamma), and 40–70 Hz (high gamma) [6]. The bandpassed EEG signals were Hilbert transformed and the absolute Hilbert envelope are calculated. The absolute Hilbert envelope values were averaged for every 2.8 seconds, equivalent to TR of fMRI [3]. We selected theta to low beta power ratio (TBR) to monitor the resting-state brain network [7]. Low-frequency bandpass filter (0.005Hz< < 0.1Hz) was applied to the TBR signal. Pearson correlation coefficient (CC) of the TBR signal between C3 (targeting left motor cortex ) and C4 (right motor cortex) was calculated, as shown in Fig1.
MRI analysis: Activation maps are produced by performing a standard GLM analysis convolving the ASL and BOLD timeseries data with the reference function corresponding to the task. Region-of-interest (ROI) of activated M1 is defined using voxels activated with p <0.01 in time series of perfusion-weighted signal (subtractin tagged and untagged ASL images). The percent change in CBF and BOLD contrast during the activation and hypercapnia condition is calculated within the activated ROI, and the change of the cerebral metabolic rate of oxygen (CMRO2) during the activation is calculated using the calibrated fMRI model [8,9].

Result

Figure 1 compares CC of TBR at EEG contact C3 (left central) and C4 (right central) for inside/outside MR scanner. The result indicates that EEG data during MR scanning, with all scanner-related artifact corrections, is comparable to resting-state EEG data recorded outside the scanner.
Figure 2 shows CC of TBR at C3 and C4, and BOLD contrast change in the activated ROI. Although not significant (p<0.13), there is clearly a trend toward a relationship. Figure 3 compares CC of TBR at C3 and C4 with the calculated CMRO2 values in the activated ROI. A similar trend is noted. Figure 4 compares CC of TBR at C3 and C4 with the resting-state fluctuation amplitude (RSFA) values in the activated ROI [10]. It should be noted that the data in Figure 3 is calculated using data from Figure 2, so those results are not independent. However, Figures 2 and 4 are independent measurements and both clearly show a trend toward a relationship to correlated synchronous left/right motor cortex TBR low frequency fluctuations.

Discussion & Conclusion

As stated, the MRI data used to produce Figures 2 and 3 are related because CMRO2 is calculated using the BOLD signal change and the observed CBF change in the same scan. However, Figure 2 and Figure 4 are only related through a physiologic mechanism possibly related to cerebrovascular reactivity[13]. If these are truly correlated, and more data is needed to verify this, the result is highly suggestive that right/left primary motor cortex TBR synchrony is somehow related to cerebrovascular reactivity (CVR), i.e. higher network TBR synchrony implies higher BOLD signal amplitudes for a given underlying neuronal response.
We presented the feasibility of low-frequency fluctuation of TBR signals to investigate the resting state network. Even though no statistical significance was observed in this preliminary data set (n=7), we demonstrated that there exists a relationship between low-frequency TBR signal estimated using EEG signal and fMRI functional connectivity analysis of resting-state networks.
TBR is known to be negatively related to cognitive control, showing the possible link to ADHD [11] and schizophrenia [14]. Quantification of temporal fluctuation of TBR could be a potential technique to investigate resting-state brain networks in simultaneous EEG and fMRI studies.

Acknowledgements

Authors appreciate the technical support from Siemens.

References

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Figures

Fig 1. 10-20 EEG electronode location map. Note C3 and C4 for central motor cortex

Fig 2. Pearson correlation coefficient of theta to beta ratio (TBR) between C3 and C4 in the resting state. X and Y axes represent Out of scanner and Inside of scanner[mjl1] data. [mjl1]Label the x and y axes

Fig 3. X and Y axes represent Pearson correlation coefficient of theta to beta (TBR) fluctuation between C3 and C4 in the resting state, and percentage BOLD contrast change during finger tapping in activated left M1 ROI.

Fig 4. X and Y axes represent Pearson correlation coefficient of theta to beta fluctuation between C3 and C4 in the resting state, and estimated CMRO2 values in activated left M1 ROI.

Fig 5. X and Y axes represent Pearson correlation coefficient of theta to beta fluctuation between C3 and C4 in the resting state, and percentage resting state fluctuation amplitude (RSFA) in activated left M1 ROI.

Proc. Intl. Soc. Mag. Reson. Med. 29 (2021)
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