Differential electrophysiological coupling for positive and negative BOLD responses during unilateral hand movements

Abstract

The coupling between neural cellular activity and blood oxygen level-dependent (BOLD) signal is of critical importance to the interpretation of fMRI. Largely unknown, however, is the degree to which different neuronal events (i.e., excitation and inhibition) maintain or disrupt the neural-hemodynamic relationship, especially in humans. In the present study, we compared local electroencephalographic (EEG) oscillations and the positive/negative BOLD responses of simultaneously recorded data from healthy human volunteers performing unilateral finger tapping at graded rates. By quantifying the single-trial modulations of EEG using source imaging, we tested for their correlation with positive BOLD response (PBR) and negative BOLD response (NBR) after coregistering their spatial locations. PBR was found to be overlapped with and correlated to the decrease of alpha (8-13 Hz) and beta (13-30 Hz) band EEG in the contralateral sensorimotor cortex. Regional EEG modulations at the sensorimotor cortex further predicted a spatially distributed and interconnected network of motor-related cortical areas. Alternatively, no significant correlation was found at the ipsilateral sensorimotor cortex between the NBR and EEG despite their spatial overlapping. This differential electrophysiological coupling of the positive and negative BOLD responses suggests that the underlying neuronal events may not only influence the direction of the signal change but also the neural-hemodynamic relationship.

Figure 1.

Illustration of the experimental design. A mixed block and event-related design was used to accommodate the simultaneous EEG and fMRI analysis. Task and rest blocks lasted for 30 s each. Within a task block, task events of 2 s (trials 1, 2, 3, etc) were interleaved with intertrial intervals of varying duration from 1 to 2 s. Tapping frequency was held constant within a run but varied across runs from 0.5 to 3.5 Hz. Light gray rectangles indicate left-hand movement tasks and dark gray rectangles indicate right-hand movement tasks.

Figure 2.

Task-induced responses of BOLD and alpha band EEG in individuals and the group of right-handed subjects. A, Fixed-effect group analysis results for left- and right-hand movements. Rows 1 and 2 are from two typical subjects; the third row is the group average. White curves on the images indicate the central sulcus. Note that the contralateral PBR and ipsilateral NBR are located in close vicinity to the central sulcus. All displayed images were statistically thresholded by p < 0.05 [after Bonferroni correction (Bonf) for whole-brain]. B, C, Fixed-effect group images of EEG power changes in the alpha band for right- and left-hand movements, respectively (p < 0.05, Bonferroni corrected for whole-brain). White arrows indicate where the central sulcus is located on the inflated cortical surface. D, Areas of conjunct PBR for contralateral movement and NBR for ipsilateral movement (p < 0.001, uncorrected). Only the primary sensorimotor areas were identified in the conjunction analysis of PBR and NBR. The pink region in the right hemisphere is associated with PBR during left-hand movements and NBR during right-hand movements. The light blue region in the left hemisphere is associated with PBR during right-hand movements and NBR during left-hand movements.

Figure 3.

EEG response, BOLD response, and EEG–BOLD correlation. A, C, E, G, Time courses (mean ± SEM) of the change of EEG power in the alpha band (A, C) and the percentage change of BOLD (E, G) at the contralateral (A, E) and ipsilateral region (C, G) in response to the dominant (black) and nondominant (gray) hand movements. Note the different time scales for the BOLD and EEG responses. The BOLD lasted for >30 s while the EEG returned to baseline after ∼2 s. B, D, F, H, Amplitudes (mean ± SEM) of EEG power change (B, D) and BOLD signal change (F, H) as a function of the tapping rate for the dominant (black) and nondominant (gray) hand at the contralateral (B, F) and ipsilateral (D, H) region. I, J, Scatter plots of the amplitude of the single-trial EEG responses as a function of the PBR at the contralateral (I) and the NBR at the ipsilateral (J) region. The plot depicts the variations in the BOLD response and EEG power decrease in single trials relative to their mean responses across all rate conditions (the mean responses were removed and variance was normalized across subjects; see Materials and Methods). Each dot depicts one trial corresponding to the movement of the dominant hand. The line represents the result of linear fitting, which considered measurement errors in both coordinates. K, Temporal correlation between EEG and PBR at the contralateral region compared with the EEG–NBR correlation at the ipsilateral side in both the right- (black) and left- (gray) handed groups.

Figure 4.

Correlation map between the BOLD signal and the contralateral regional EEG response during right-hand movements. The EEG regressor was derived from responses constrained within the contralateral sensorimotor ROI as indicated by the white arrow and circle (A). The correlation map (B) was computed by comparing the EEG regressor with the BOLD signal on a voxel-by-voxel basis and is compared with the task-effect fMRI map (C). Results were computed in the group of right-handed subjects. A, C, Same as in Figure 2 but displayed on an inflated cortical surface. The correlation map was thresholded at p < 0.001 (uncorrected). The maps of EEG and BOLD responses were thresholded at p < 0.05 (Bonferroni corrected for whole-brain). The white arrow in B and black arrow in C indicate the ROI where the EEG response was derived.

Figure 5.

Correlation maps between the BOLD signal and the ipsilateral regional EEG changes during movement of the dominant hand. B, E, EEG–BOLD correlation maps associated with right-hand movements in the group of right-handed subjects (B) and left-hand movements in the left-handed subjects (E). A, D, EEG power changes during movement of the dominant hand in the right- (A) and left- (D) handed groups. The EEG regressor was derived from responses constrained within the ipsilateral sensorimotor ROI, as indicated by the white arrow and circle. The correlation maps B and E are compared with the task-effect fMRI maps C and F, respectively. The white arrows in B and E and black arrows in C and F indicate the ROI where the EEG response was derived.

Figure 6.

A–C, Correlation between BOLD and EEG in beta (A), theta (B), and delta (C) bands. The EEG–PBR correlation at the contralateral region was compared with the EEG–NBR relationship at the ipsilateral side in both the right- (black) and left- (gray) handed groups. The black and gray dashed lines indicate the threshold of p = 0.001 and p = 0.05, respectively.