Compensatory Neural Activity in Response to Cognitive Fatigue

Abstract

Prolonged continuous performance of a cognitively demanding task induces cognitive fatigue and is associated with a time-related deterioration of objective performance, the degree of which is referred to cognitive fatigability. Although the neural underpinnings of cognitive fatigue are poorly understood, prior studies report changes in neural activity consistent with deterioration of task-related networks over time. While compensatory brain activity is reported to maintain motor task performance in the face of motor fatigue and cognitive performance in the face of other stressors (e.g., aging) and structural changes, there are no studies to date demonstrating compensatory activity for cognitive fatigue. High-density electroencephalography was recorded from human subjects during a 160 min continuous performance of a cognitive control task. While most time-varying neural activity showed a linear decline over time, we identified an evoked potential over the anterior frontal region which demonstrated an inverted U-shaped time-on-task profile. This evoked brain activity peaked between 60 and 100 min into the task and was positively associated with better behavioral performance only during this interval. Following the peak and during subsequent decline of this anterior frontal activity, the rate of performance decline also accelerated. These findings demonstrate that this anterior frontal brain activity, which is not part of the primary task-related activity at baseline, is recruited to compensate for fatigue-induced impairments in the primary task-related network, and that this compensation terminates as cognitive fatigue further progresses. These findings may be relevant to understanding individual differences in cognitive fatigability and developing interventions for clinical conditions afflicted by fatigue.

Significance statement: Fatigue refers to changes in objective performance and subjective effort induced by continuous task performance. We examined the neural underpinnings of cognitive fatigue in humans using a prolonged continuous performance task and high-density electroencephalography with the goal of determining whether compensatory processes exist to maintain performance in the face of fatigue. We identified brain activity demonstrating an inverted U-shaped time-on-task profile. This brain activity showed features consistent with a compensatory role including: peaking between 60 and 100 min into the task, a positive association with behavioral performance only during this interval, and accelerated performance decline following its peak. These findings may be relevant to understanding individual differences in cognitive fatigue and developing interventions for clinical conditions afflicted by fatigue.

Keywords: Stroop; cognitive; event related potential; fatigue.

Figure 1.

Time-on-task effects on evoked activities and their spatial distributions. A, The color cue-related GFP waveforms for different time-on-task blocks. Time 0 on the x-axis denotes cue onset. B, Results of statistical tests on changes of GFP waveforms over time blocks. The dash line indicates p = 0.1. Evoked periods with p < 0.1 are shaded in Figure 2A and selected for further analyses. C, Statistical topographical maps of ERP changes over time blocks for the period of 336–420 ms and the period of 640–1272 ms. The color scales denote F values from ANOVA tests. Electrodes with significant ERP changes (p < 0.05, corrected) are marked by asterisks. D, ROIs selected for further analyses. The electrode layout is the standard 10–10 system. The anterior frontal ROI contains electrodes at AF9, AF7, Fp1, Fpz, Nz, Fp2, AF8, and AF10. The midline frontal ROI contains electrodes at F1, Fz, and F2. The midline parietal ROI contains electrodes at CP1, CPz, CP2, P1, Pz, and P2.

Figure 2.

ERP amplitude as a function of time on task. A, Linear decrease of ERP amplitude during the evoked period of 336–420 ms over the midline frontal and the midline parietal ROIs. B, Inverted-U function of ERP amplitude during the evoked period of 640–1272 ms over the anterior frontal ROI. Error bars indicate SE.

Figure 3.

Anterior frontal ERP and behavior. A–C, ERP waveforms from the anterior frontal ROI for fast, medium, and slow RT trials during the first time block (0–40 min; A), the middle time block (60–100 min; B), and the last time block (120–160 min; C). Time 0 on the x-axis denotes cue onset. Results of statistical tests on the ERP differences among different RT groups are plotted at the bottom of the figure. A significance threshold of p < 0.05 was applied. During the first time block, no significant ERP difference was observed for different RT groups. During the middle time block, significant ERP separations were found in the range of 468–1450 ms. During the last time block, significant ERP separations were found only in the range of 1360–1450 ms.

Figure 4.

Task performance during compensation and decompensation. A, ERP amplitude during 640–1272 ms from the anterior frontal ROI was used to define the compensation phase (0–80 min, shaded in blue) and the decompensation phase (80–160 min, shaded in red). B, Error rate in color incongruent condition as a function of time on task. Significant error rate increases compared to the beginning time block are marked by asterisks. C, Long RT trials (number of trials with RTs longer than 2 s) in the color incongruent condition as a function of time on task. Significant increases of long RT trials compared to the beginning time block are marked by asterisks. D, RT in the color incongruent condition as a function of time on task. Significant RT increases compared to the beginning time block are marked by asterisks. E, Slope of RT increase is higher in the decompensation phase than in the compensation phase (p < 0.05). Error bars indicate SE.