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. 2022 Feb 15;43(3):1011-1031.
doi: 10.1002/hbm.25703. Epub 2021 Nov 5.

Facing successfully high mental workload and stressors: An fMRI study

Mickaël Causse  1 , Evelyne Lepron  2 , Kevin Mandrick  1 , Vsevolod Peysakhovich  1 , Isabelle Berry  2 , Daniel Callan  3 , Florence Rémy  2
Affiliations

Facing successfully high mental workload and stressors: An fMRI study

Mickaël Causse et al. Hum Brain Mapp. .

Abstract

The present fMRI study aimed at highlighting patterns of brain activations and autonomic activity when confronted with high mental workload and the threat of auditory stressors. Twenty participants performed a complex cognitive task in either safe or aversive conditions. Our results showed that increased mental workload induced recruitment of the lateral frontoparietal executive control network (ECN), along with disengagement of medial prefrontal and posterior cingulate regions of the default mode network (DMN). Mental workload also elicited an increase in heart rate and pupil diameter. Task performance did not decrease under the threat of stressors, most likely due to efficient inhibition of auditory regions, as reflected by a large decrement of activity in the superior temporal gyri. The threat of stressors was also accompanied with deactivations of limbic regions of the salience network (SN), possibly reflecting emotional regulation mechanisms through control from dorsal medial prefrontal and parietal regions, as indicated by functional connectivity analyses. Meanwhile, the threat of stressors induced enhanced ECN activity, likely for improved attentional and cognitive processes toward the task, as suggested by increased lateral prefrontal and parietal activations. These fMRI results suggest that measuring the balance between ECN, SN, and DMN recruitment could be used for objective mental state assessment. In this sense, an extra recruitment of task-related regions and a high ratio of lateral versus medial prefrontal activity may represent a relevant marker of increased but efficient mental effort, while the opposite may indicate a disengagement from the task due to mental overload and/or stressors.

Keywords: acute stress; auditory stressors; fMRI; heart rate; mental effort; mental workload; pupil diameter.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Experimental design. (a) Toulouse n‐back task (TNT). The active blocks consisted of 12 trials and lasted 36 s. They were interleaved with 24‐s rest blocks (R). Participants responded to targets and nontargets by pressing one of two different buttons. The side of the buttons was counterbalanced across participants. (b) experimental timeline. The experiment included five functional runs (two safe runs without any sounds and three threat runs with the possible occurrence of aversive sounds), presented in a counterbalanced order. TNT difficulty levels (0‐back and 2‐back) were counterbalanced and alternated with rest periods. Unpredictable aversive loud sounds were presented randomly during threat runs and could occur during rest and active blocks
FIGURE 2
FIGURE 2
Subjective ratings, behavioral performance and autonomic nervous system activity measures for each level of TNT difficulty (0‐back and 2‐back) and threat conditions (safe and threat), n = 20. Top: anxiety (left panel) and task difficulty ratings (both safe and threat conditions averaged, right panel). Middle: percentage of correct responses (left panel) and mean reaction times (right panel). Bottom: Heart rate (left panel) and pupil size (right panel). Error bars are SEM. Light gray = 0‐back, medium gray = 2‐back, plain bar = safe, striped bar = threat
FIGURE 3
FIGURE 3
Brain activations and deactivations related to mental workload. (a) Statistical parametric maps illustrating the main effect of mental workload in the TNT. The colored bar indicates the t‐value (+10 to −10) of the activation height. Cortical areas evidencing increased (red color) and decreased (blue color) activations during the 2‐back versus 0‐back are presented. For illustrative purposes, maps are thresholded at p < .001 FWE corrected. Activations are superimposed on a subject anatomical T1 scan, normalized to the standard MNI space. ACC, anterior cingulate cortex; PCC, posterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; DMPFC, dorsomedial prefrontal cortex; PC, parietal cortex (superior parietal gyrus and inferior parietal lobule); SMA, supplementary motor area; VMPFC, ventromedial prefrontal cortex. (b) Barplots show the percentage of BOLD signal increase/decrease at peak voxel for 0‐back and 2‐back conditions relative to rest condition. MNI coordinates are indicated. The percentage is calculated over all blocks, that is, safe and threat, for each task difficulty level. Error bars are SEM. Light gray = 0‐back, medium gray = 2‐back
FIGURE 4
FIGURE 4
Brain activations and deactivations related to the threat of auditory stressors. (a) Statistical parametric maps illustrating the main effect of threat. The colored bar indicates the t‐value (+20 to −20) of the activation height. Cortical areas evidencing increased (orange‐red color) and decreased (green‐blue color) activations during the threat versus safe conditions are shown. For illustrative purposes, maps are thresholded at p < .005 FDR corrected. Activations are superimposed on a subject anatomical T1 scan, normalized to the standard MNI space. ACC, anterior cingulate cortex; DMPFC, dorsomedial prefrontal cortex; PC, parietal cortex (inferior parietal lobule); SMA, supplementary motor area; STG, superior temporal gyrus; VMPFC, ventromedial prefrontal cortex (orbitofrontal cortex). (b) Barplots show the percentage of BOLD signal increase/decrease at peak voxel for threat and safe conditions relative to rest condition. MNI coordinates are indicated. The percentage is calculated over all blocks, that is, 0‐back and 2‐back, for each threat level. Error bars are SEM. Plain bar = safe, striped bar = threat
FIGURE 5
FIGURE 5
ROI‐to‐ROI connectivity increases when comparing threat of auditory stressors and safe conditions (thresholded at p < .05 FDR‐corrected). (a) Higher connectivity between left amygdala and medial PFC ROIs during threat; (b) Higher connectivity between right amygdala and right supramarginal gyrus ROIs during threat. Barplots show average beta estimates of ROI‐to‐ROI connectivity in the group for safe and threat conditions. Error bars indicate SEM
FIGURE 6
FIGURE 6
Brain activations and deactivations evidenced in the Difficulty × Threat interaction. (a) Statistical parametric maps illustrating the interaction effects between mental workload and threat of stressors. The colored bar indicates the t‐value (+4 to −4) of the activation height. Cortical areas evidencing positive (red color) and negative (blue color) interactions are shown. Maps are thresholded at p < .05 FDR‐corrected. Activations are superimposed on a subject anatomical T1 scan, normalized to the standard MNI space. ACC, anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; PC, parietal cortex; SMA, supplementary motor area; VMPFC, ventromedial prefrontal cortex. (b) Barplots show the percentage of BOLD signal increase/decrease at peak voxel for each of the four experimental conditions relative to rest condition. MNI coordinates are indicated. Error bars are SEM. Light gray = 0‐back, medium gray = 2‐back, plain bar = safe, striped bar = threat
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