EEG measures index neural and cognitive recovery from sleep deprivation

Abstract

Sleep deprivation impairs many cognitive abilities, but these impairments can be reversed after a certain quantity and quality of sleep. The ability to inhibit responding is particularly susceptible to disruption after prolonged wakefulness. How recovery sleep (RS) alters brain activity, leading to improved performance on a variety of cognitive tasks, remains unclear. This issue was examined in the current study using spectral analysis of electroencephalogram (EEG) data during sleep. These measures of sleep physiology were acquired after both normal sleep (NS) and RS, and were related to measures of inhibitory control and concurrent brain activity. Subjects were nine young adults who underwent functional magnetic resonance imaging twice, after 9 h of NS and after 10 h of RS that followed 38 h of being awake. A multiple regression model was used to examine differences between conditions in (1) EEG spectral power during sleep, (2) probability of successful inhibition in a go/no-go task, and (3) activation within a region of right prefrontal cortex during the task. Performance recovery, as indexed by reduced performance differences between conditions, was predicted by increased delta power and decreased sigma power in RS compared with NS. These EEG variables predicted most of the variance in inhibitory performance difference between conditions. Regressions also suggested that RS improved performance because of changes in brain function including prefrontal regions that resulted from delta rebound. We thus propose that slow waves, reflected in delta power during RS, act to restore brain function, thereby improving cognitive performance that entails response inhibition.

Figure 1.

A–C, Study protocol (A) and schematic representation of the go/no-go task, showing a single trial (B) and multiple trials (C). In the study protocol (A), subjects were studied on two separate occasions for a baseline visit and a sleep deprivation visit. Solid gray bars represent periods of polysomnographic (PSG) recordings of sleep, and the unfilled bar represents a period where participants remained awake when they would normally sleep. Solid black bars represent fMRI scans. On the go/no-go task (B), each trial consisted of fixation display followed by a nonspatial cue presented for 200, 400, or 800 ms. After the cue, a stimulus was presented for 100 ms followed by an intertrial interval. An example of a series of five trials is presented (C). The correct response pattern is go/no-go/no-go/go, inhibiting responses to nontarget and lure events, respectively. The fifth trial represents the intermittent inclusion of null events, which last between 2.1 and 6.3 s.

Figure 2.

The cluster marked by the blue cross was extracted to examine right prefrontal activity after NS and RS (no-go/go contrast). The blue cross represents the coordinate of the cluster maxima (x = 36; y = 21; z = 6; 349 voxels).

Figure 3.

Delta and σ power differences between NS and RS predict differences in inhibitory performance and prefrontal brain activity (cluster maxima: x = 36; y = 21; z = 6; 349 voxels; no-go/go contrast). A, C, Percentage difference in absolute delta power is associated with inhibitory performance difference (A) and right prefrontal activity (C). B, D, Percentage difference in absolute sigma power is associated with inhibitory performance difference (B) and right prefrontal activity (D). E, Prefrontal activity difference is associated with inhibitory performance difference.

Figure 4.

Inhibitory activation change (no-go/go contrast; NS–RS) associated with percentage increase in σ power from NS to RS. Increased sigma power from NS to RS is associated with decreased activation in the right superior frontal sulcus (A) from NS to RS conditions and increased activation in left superior frontal sulcus (B) and superior parietal lobule (C) from NS to RS conditions. All peaks are significant at p < 0.05 corrected across the entire brain volume at the cluster level.