Negative covariation between task-related responses in alpha/beta-band activity and BOLD in human sensorimotor cortex: an EEG and fMRI study of motor imagery and movements

Abstract

Similar to the occipital alpha rhythm, electroencephalographic (EEG) signals in the alpha- and beta-frequency bands can be suppressed by movement or motor imagery and have thus been thought to represent the "idling state" of the sensorimotor cortex. A negative correlation between spontaneous alpha EEG and blood-oxygen-level-dependent (BOLD) signals has been reported in combined EEG and fMRI (functional Magnetic Resonance Imaging) experiments when subjects stayed at the resting state or alternated between the resting state and a task. However, the precise nature of the task-induced alpha modulation remains elusive. It was not clear whether alpha/beta rhythm suppressions may co-vary with BOLD when conducting tasks involving varying activations of the cortex. Here, we quantified the task-evoked responses of BOLD and alpha/beta-band power of EEG directly in the cortical source domain, by using source imaging technology, and examined their covariation across task conditions in a mixed block and event-related design. In this study, 13 subjects performed tasks of right-hand, right-foot or left-hand movement and motor imagery when EEG and fMRI data were separately collected. Task-induced increase of BOLD signal and decrease of EEG amplitudes in alpha and beta bands were shown to be co-localized at the somatotopic sensorimotor cortex. At the corresponding regions, the reciprocal changes of the two signals co-varied in the magnitudes across imagination and movement conditions. The spatial correspondence and negative covariation between the two measurements were further shown to exist at somatotopic brain regions associated with different body parts. These results suggest an inverse functional coupling relationship between task-induced changes of BOLD and low-frequency EEG signals.

Figure 1

Schematic illustration of experimental paradigm and data analysis. An example of single-trial EEG activity from the imagination of right hand and its filtered traces (8 Hz – 12 Hz) were shown.

Figure 2

(A–C) Group Time-Frequency representation of EEG changes from C3, C4 and Cz electrodes. Power changes relative to baseline are depicted as t statistic thresholded by p < 0.05 (|t|>2.18, uncorrected for multiple comparison). Black squares in each plot indicate the alpha- and beta-frequency bands of interest. (D) Scalp topology of relative power changes in the beta band (p<0.05, uncorrected).

Figure 3

EEG and fMRI results during imagination and movement of right hand. (A–F) shows the group maps on an inflated cortical surface with white arrows indicating the peak changes at the primary sensorimotor cortex. (A–B) shows BOLD t statistic maps (p<0.001, uncorrected for multiple comparison). (C–F) shows average percent change (p<0.001, uncorrected) in beta and alpha bands. (G) shows the covariation between quantified responses in EEG beta and BOLD at the contralateral hand ROI from the pooled imagination (cyan) and movement (blue) tasks. (H) shows a similar linear relation between EEG alpha and BOLD responses. Different symbols in (G–H) indicate responses from different individual subjects.

Figure 4

EEG and fMRI results during imagination and movement of right foot. (A–D) shows the group maps on an inflated cortical surface with white arrows indicating the peak changes at the primary sensorimotor cortex. (A–B) shows BOLD t statistic maps (p<0.001, uncorrected for multiple comparison). (C–D) shows average percent change (p<0.001, uncorrected) in beta band. (E) shows the co-varied changes of EEG beta and BOLD at the foot ROI from pooled quantities of imagination (yellow) and movement (green). Different symbols in (E) indicate responses from different individual subjects.

Figure 5

Average changes of fMRI (A, C and E) and EEG (B, D, and F) in regions of interest for all task conditions under threshold p<0.001 (uncorrected for multiple comparison). Notice that no regions were found in BOLD maps for imagination of left hand, or EEG alpha maps for imagination of right foot.

Figure 6

Locations of maximum changes in EEG alpha (blue balls), beta (green balls) and BOLD (white arrows), superimposed on axial MRI images with BOLD t statistic maps. The thresholds for BOLD maps were adjusted for each task condition to show where the peaks were. t-value = 2.18 (p=0.05, uncorrected), 4.32 (p = 0.001, uncorrected).