Resting spontaneous activity in the default mode network predicts performance decline during prolonged attention workload

Abstract

After continuous and prolonged cognitive workload, people typically show reduced behavioral performance and increased feelings of fatigue, which are known as "time-on-task (TOT) effects". Although TOT effects are pervasive in modern life, their underlying neural mechanisms remain elusive. In this study, we induced TOT effects by administering a 20-min continuous psychomotor vigilance test (PVT) to a group of 16 healthy adults and used resting-state blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to examine spontaneous brain activity changes associated with fatigue and performance. Behaviorally, subjects displayed robust TOT effects, as reflected by increasingly slower reaction times as the test progressed and higher self-reported mental fatigue ratings after the 20-min PVT. Compared to pre-test measurements, subjects exhibited reduced amplitudes of low-frequency fluctuation (ALFF) in the default mode network (DMN) and increased ALFF in the thalamus after the test. Subjects also exhibited reduced anti-correlations between the posterior cingulate cortex (PCC) and right middle prefrontal cortex after the test. Moreover, pre-test resting ALFF in the PCC and medial prefrontal cortex (MePFC) predicted subjects' subsequent performance decline; individuals with higher ALFF in these regions exhibited more stable reaction times throughout the 20-min PVT. These results support the important role of both task-positive and task-negative networks in mediating TOT effects and suggest that spontaneous activity measured by resting-state BOLD fMRI may be a marker of mental fatigue.

Keywords: Amplitudes of low-frequency fluctuation (ALFF); Default mode network (DMN); Fatigue; Functional connectivity; Time-on-task (TOT) effects.

Figure 1

Time-on-task effects during a 20-minute psychomotor vigilance test. (a) Median reaction time (RT, msec) increased as the task progressed and subjects exhibited significantly slower reaction times during the last quintile compared to the first. (b) Mental fatigue ratings (on a 9-point scale) increased significantly after the PVT. (c) Changes in median RT did not correlate with changes in self-reported mental fatigue. There were individual differences in the response to prolonged workload; the change in median RT (ratio = (Last Quintile − First Quintile) / First Quintile * 100%) ranged from −7.07% to 20.71%; four representative subjects are shown in (d), two who were vulnerable to the TOT effects of the PVT and two who were resistant to the TOT effects of the PVT. Error bar represents standard error. *p<0.05.

Figure 2

(a) Comparison between post- and pre-PVT resting states revealed significant ALFF changes in multiple brain regions. Blue-green colors indicate regions that exhibited resting-state ALFF decreases after the PVT and red-yellow colors indicate regions that exhibited resting-state ALFF increases after the PVT. The display threshold was set as uncorrected p<0.005. (b) Pre-PVT resting-state ALFF in the posterior cingulate cortex (PCC) and medial prefrontal cortex (MeFFC) were negatively correlated with the change in median RT on the PVT (ratio = (Last Quintile − First Quintile) / First Quintile * 100%). (c) There was a trend for a positive correlation between the change in ALFF in the PCC and the change in median RT on the PVT (ratio = (Last Quintile − First Quintile) / First Quintile * 100%).

Figure 3

Resting-state ALFF values in 12 resting-state networks before and after the 20-min PVT. ALFF was decreased in the DMN and increased in the visual network after the PVT. Error bar represents standard error. *p< 0.05.

Figure 4

(a) Comparison between post- and pre-PVT resting states revealed significant functional connectivity changes between the PCC and multiple brain regions. Blue-green colors indicate regions that exhibited resting connectivity decreases after the PVT and red-yellow colors indicate regions that exhibited resting connectivity increases after the PVT. The display threshold was set as uncorrected p<0.005. (b) Region-of-interest analysis showed reduced anti-correlations between the PCC and the right MFG during the post-PVT resting state compared to pre-PVT resting state.

Figure 5

(a) Comparison between the last and first quintile of the PVT revealed significant activation increases in multiple brain regions. Red-yellow colors indicate regions that exhibited activation increases during the last quintile. The display threshold was set as uncorrected p<0.001. (b) There was a trend for a negative correlation between the change in MFG activation and the change in median RT on the PVT (ratio = (Last Quintile − First Quintile) / First Quintile * 100%).