Cognitive benefit and cost of acute stress is differentially modulated by individual brain state

Abstract

Acute stress is associated with beneficial as well as detrimental effects on cognition in different individuals. However, it is not yet known how stress can have such opposing effects. Stroop-like tasks typically show this dissociation: stress diminishes speed, but improves accuracy. We investigated accuracy and speed during a stroop-like task of 120 healthy male subjects after an experimental stress induction or control condition in a randomized, counter-balanced cross-over design; we assessed brain-behavior associations and determined the influence of individual brain connectivity patterns on these associations, which may moderate the effect and help identify stress resilience factors. In the mean, stress was associated to increase in accuracy, but decrease in speed. Accuracy was associated to brain activation in a distributed set of brain regions overlapping with the executive control network (ECN) and speed to temporo-parietal activation. In line with a stress-related large-scale network reconfiguration, individuals showing an upregulation of the salience and down-regulation of the executive-control network under stress displayed increased speed, but decreased performance. In contrast, individuals who upregulate their ECN under stress show improved performance. Our results indicate that the individual large-scale brain network balance under acute stress moderates cognitive consequences of threat.

Keywords: brain state; executive control; functional connectivity; salience; stress.

Fig. 1.

The processing pipeline and rationale for the moderated moderation is depicted in this figure. We investigated if network connectivity changes under stress influence the correlation between brain activity and behavioral performance. Network connectivity changes were determined by applying dual regression and calculating stress related changes of the salience and executive control networks. The influence of these stress-related network changes on the correlation of brain activity and behavior is analyzed in the moderated moderation.

Fig. 2.

(a) Behavioral data for congruent and incongruent trials under stress (plain) and control (striped). Response accuracy given in percent correct responses (green). Mean reaction times (yellow) are displayed for correct response trials only. Error bars indicate 95% CI. (b) Association of increase in accuracy (green) and decrease in speed (yellow) in the task with increase in brain activation in stress compared to control (for incogruent trials only, controlled for main effect of stress). Results are cluster level corrected threshold (Z > 2.3, P < 0.05) and overlaid on an MNI template brain.

Fig. 3.

The moderation analysis can be illustrated at four prototypic ‘brain network connectivity profiles’. These profiles were characterized by a distinct pattern in change of connectivity in the two networks in stress. (a) profile which showed increase in connectivity in stress in SN and ECN (b) profile which showed increase in connectivity only in SN and decrease in ECN (c) profile which showed increase in ECN and decrease in SN and (d) profile which showed decrease in connectivity in both. For each brain state, the correlation between brain and behavior is displayed, the plots depict the correlation from the VOIs (frontal VOIs: DLPFC, IFG, pgACC, distributed VOIs: DMPFC, AG, MTG). Change in reaction time or percent correct is plotted on the y-axis and change in brain activation on the x-axis. Positive values represent an increase of activity in stress and negative a decrease in stress. Slopes and offset were generated by the moderated moderation based on + 1 and −1 SD in all scales, that is the different profiles represent the variance in network connectivity observed in our sample and how this variance influenced brain–behavior associations.