Kevin Wen-Kai Tsai1,2, Hsin-Ju Lee2, Ching-Po Lin2, Li-Wei Ko3, Wen-Jui Kuo2, Toni Auranen4, Simo Särkkä5, and Fa-Hsuan Lin6
1Aim for the Top University Project, National Taiwan Normal University, Taipei, Taiwan, 2Institute of Neuroscience, National Yang-Ming University, Taipei, Taiwan, 3Institute of Bioinformatics and Systems Biology, National Chiao Tung University, Hsinchu, Taiwan, 4Advanced Magnetic Imaging Centre, Low Temperature Laboratory, Aalto University, Espoo, Finland, 5Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland, 6Institute of Biomedical Engineering, National Taiwan University, Taipei, Taiwan
Synopsis
Simultaneous fMRI-EEG acquisition provides a good
spatial and temporal resolution from MRI and EEG respective to study the human
brain function. However, the EEG signal is impaired due to the strong magnetic
gradient switching of concurrent MR imaging. A simultaneous interleaved MR
InI-EEG recording strategy is proposed to minimize the distortion of the EEG.
Our results suggest that the proposed acquisition strategy can reveal similar BOLD
contract activation but preserve better auditory evoked potentials than
conventional EPI-EEG acquisition.PURPOSE
Functional MRI (fMRI) cannot detect primary neuronal activity directly
but only secondary hemodynamic responses
1. To probe the
neuronal basis of fMRI responses, it is possible to use simultaneous EEG and
fMRI measurements (for review, see 2). However, it has
been shown that measuring EEG and fMRI inside the magnet has many technical
challenges, including the contamination of signal when MRI gradient coil is
switching
2. This gradient
artifact (GA) has been commonly addressed by subtracting an artifact template,
created from averaging fMRI acquisitions, from the contaminated fMRI
measurements
3. However,
subject’s head motion, the jittering between EEG and fMRI measurements, and
insufficient EEG dynamic range can limit the performance of such average
artifact subtraction.
Here
we propose to minimize the fMRI acquisition duration and to maximize the EEG
acquisition duration in order to measure BOLD signals and high-quality EEG at
the same time. Specifically, inverse imaging (InI), a highly parallel fMRI method
capable of completing the whole-head measurement with 5 mm resolution at cortex
in 0.1 s
4,
intermittently measured the BOLD signal once every 2 s, in order to minimize GA
in concurrent EEG recordings. Experimental results show that our acquisition
strategy allows for fMRI similar to that of EPI and event-related potentials
measured outside MRI.
METHODS
InI (coronal
projection images) only sampled the first 100 ms in 2-s TR. This left a period
of 1.9 s (95% of the duty cycle) without artifacts related to MRI magnetization
and spatial encoding. Meanwhile, EEG (31 electrodes with impedance < 20 kΩ,
reference electrode = FCz) was recorded continuously by a MRI-compatible system
(BrainAmp MR Plus, Brain Products GmbH) with 5 kHz sampling rate. Importantly,
EEG was temporally synchronized to InI via a 10 MHz clock in the MR scanner. Auditory
stimulus (1000 Hz; 200 ms duration) was delivered randomly between 0.2 and 1.4 s
after the onset of each TR. There were 50 trials randomly distributed over a 5-minute
scan. For comparison, we also recorded the EEG outside MRI with the same
auditory stimuli. Conventional multi-slice EPI was also measured concurrently
with EEG inside MRI to evaluate how BOLD signal and auditory evoked potentials
(AEP) changed by the measurement environment (
Figure 1).
The InI analysis began by first reconstructing volumetric images the using
minimum-norm estimate
4.,
EPI were pre-processed by a customized stream (https://git.becs.aalto.fi/bml/bramila). Both InI and
EPI were further analyzed by General Linear Model using canonical models to
estimate hemodynamic response. The significance of BOLD signals (t-statistics) were
morphed to inflated hemispheres of a standard template (fsaverage in
FreeSurfer).
The
EEG analysis started by first removing gradient artifacts using a MRI artifact
template estimated directly from EEG-InI recording
3. Subsequently,
epochs of EEG were created by taking 0.2 s and 0.5 s before and after each
onset of auditory stimuli, respectively. AEP was calculated by taking average
over epochs and low-pass filtering (50 Hz) was also applied to AEP.
RESULTS
Figure 2
shows that significant hemodynamic activity was found at the superior temporal
gyrus of both hemispheres by EPI and InI. This suggests that both EPI and InI
has similar sensitivity and spatial specificity to detect the BOLD signal
elicited by auditory stimuli.
Figure 3 shows
AEPs at the T7 electrode (close to the left temporal lobe) measured outside MRI,
inside MRI with EEG, and inside MRI with InI. AEP’s before and after 50-Hz
low-pass filtering were shown. These results suggest that while low-pass
filtering on EEG-EPI measurements can generate acceptable AEP, we still found
significantly distorted AEP waveforms (before N1 and after P2). On the
contrary, EEG-InI can avoid such artifacts without losing information at high
frequency and much similar AEP to that measured outside MRI.
DISCUSSION
We proposed a simultaneous EEG-fMRI acquisition method by intermittently
measuring the BOLD signal (2 s TR) using ultra-fast fMRI acquisition (InI with
0.1 s sampling time) and concurrent EEG recording. High quality neuronal and
hemodynamic response were measured. While we used InI in this study, it is
possible to replace it with other fast imaging methods, such as simultaneous-multi-slice
CAIPI EPI
5 to further trade-off between fMRI spatiotemporal resolution and
EEG artifacts.
In
addition to GA, the other prominent noise in EEG acquired inside MRI is the
ballistocardiogram (BCG), which is induced EEG signal due to cardiac pulsation.
Luckily, BCG is typically below 15 Hz
6. In experiments
interested in cognitive functions, which are physiologically more related to
neuronal oscillation beta (~ 20 Hz) and gamma (> 40 Hz) bands, BCG can be
effectively suppressed by low-pass filtering.
Acknowledgements
We thank Dr. Jen-Ren Duann for helpful discussion.References
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