Neural Mechanisms of Inhibitory Response in a Battlefield Scenario: A Simultaneous fMRI-EEG Study

Abstract

The stop-signal paradigm has been widely adopted as a way to parametrically quantify the response inhibition process. To evaluate inhibitory function in realistic environmental settings, the current study compared stop-signal responses in two different scenarios: one uses simple visual symbols as go and stop signals, and the other translates the typical design into a battlefield scenario (BFS) where a sniper-scope view was the background, a terrorist image was the go signal, a hostage image was the stop signal, and the task instructions were to shoot at terrorists only when hostages were not present but to refrain from shooting if hostages appeared. The BFS created a threatening environment and allowed the evaluation of how participants' inhibitory control manifest in this realistic stop-signal task. In order to investigate the participants' brain activities with both high spatial and temporal resolution, simultaneous functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) recordings were acquired. The results demonstrated that both scenarios induced increased activity in the right inferior frontal gyrus (rIFG) and presupplementary motor area (preSMA), which have been linked to response inhibition. Notably, in right temporoparietal junction (rTPJ) we found both higher blood-oxygen-level dependent (BOLD) activation and synchronization of theta-alpha activities (4-12 Hz) in the BFS than in the traditional scenario after the stop signal. The higher activation of rTPJ in the BFS may be related to morality judgments or attentional reorienting. These results provided new insights into the complex brain networks involved in inhibitory control within naturalistic environments.

Keywords: electroencephalography (EEG); function magnetic resonance imaging (fMRI); inhibitory control; right temporoparietal junction (rTPJ); theta-alpha band.

Figure 1

Experimental design. (A) Stimuli in two scenarios; (B) order of events in the battlefield scenario (BFS). SSD indicates stop signal delay, and there are five different SSDs including SSD (cSSD), cSSD ± 40 ms, and cSSD ± 80 ms.

Figure 2

Clusters of dipole locations for the analysis of EEG dynamics. PreSMA and rMFG are for of inhibitory control and error detection, whereas lMOG and rMOG are used for processing visual stimul. Small spheres indicate individual participant’s dipole location, while large spheres indicate diploe locations of each cluster. lMOG, Left middle occipital gyrus; rMOG, Right middle occipital gyrus; preSMA, Pre-supplementary motor area; rMFG, Right middle frontal gyrus.

Figure 3

Inhibition function. Error rates (%) were calculated by dividing number unsuccessful stop trials with all stop trials under each SSD.

Figure 4

Inhibitory control related brain areas. All results were mapped onto a standard brain surface model in Caret (Van Essen et al., 2001). Left panel: horizontal sections under the BFS; middle panel: visualization of significant activations on the cortical surface for both scenarios (Red: BFS; Blue: symbol scenario [SBS]; Purple: overlap of both scenarios); right panel: horizontal slices under the SBS. The top-left number besides each slice indicate the z-axis. Right hemisphere is at the right side of the figure. Voxelwise statistical threshold was set at p < 0.0001, and cluster threshold alpha <0.01.

Figure 5

Error detection related brain areas. Left panel: horizontal sections under the BFS; Middle panel: visualization of significant activations on the cortical surface for both scenarios (Red: BFS; Blue: SBS; Purple: overlap of both scenarios); right panel: horizontal slices under the SBS. The top-left number besides each slice indicate the z-axis. Right hemisphere is at the right side of the figure. Voxelwise statistical threshold was set at p < 0.0001, and cluster threshold alpha <0.01.

Figure 6

The event-related spectral perturbation (ERSP) images of preSMA cluster under inhibitory control. Red solid line: onset of the go stimulus; yellow dash line: onset of the stop signal; purple dash line: onset of response; color bars indicate the magnitude of the ERSPs; statistical threshold at p < 0.01.

Figure 7

The ERSP images of rMFG cluster under inhibitory control. Red solid line: onset of the go stimulus; yellow dash line: onset of the stop signal; purple dash line: onset of response; color bars indicate the magnitude of the ERSPs; statistical threshold at p < 0.01.

Figure 8

The ERSP images of preSMA cluster under error detection. Red solid line: onset of the go stimulus; yellow dash line: onset of the stop signal; purple dash line: onset of response; color bars indicate the magnitude of the ERSPs; statistical threshold at p < 0.01.

Figure 9

The ERSP images of rMFG cluster under error detection. Red solid line: onset of the go stimulus; yellow dash line: onset of the stop signal; purple dash line: onset of response; color bars indicate the magnitude of the ERSPs; statistical threshold at p < 0.01.