The effects of a single night of sleep deprivation on fluency and prefrontal cortex function during divergent thinking

Abstract

The dorsal and ventral aspects of the prefrontal cortex (PFC) are the two regions most consistently recruited in divergent thinking tasks. Given that frontal tasks have been shown to be vulnerable to sleep loss, we explored the impact of a single night of sleep deprivation on fluency (i.e., number of generated responses) and PFC function during divergent thinking. Participants underwent functional magnetic resonance imaging scanning twice while engaged in the Alternate Uses Task (AUT) - once following a single night of sleep deprivation and once following a night of normal sleep. They also wore wrist activity monitors, which enabled us to quantify daily sleep and model cognitive effectiveness. The intervention was effective, producing greater levels of fatigue and sleepiness. Modeled cognitive effectiveness and fluency were impaired following sleep deprivation, and sleep deprivation was associated with greater activation in the left inferior frontal gyrus (IFG) during AUT. The results suggest that an intervention known to temporarily compromise frontal function can impair fluency, and that this effect is instantiated in the form of an increased hemodynamic response in the left IFG.

Keywords: divergent thinking; executive function; fatigue; fluency; sleep.

FIGURE 1

Impairment in modeled cognitive effectiveness as a function of sleep deprivation. The vertical axis on the left side of the FAST^TM graphs represents fitted and transformed modeled cognitive effectiveness as a percentage of optimal performance (100%). The oscillating line in the diagram represents average modeled cognitive effectiveness as determined by time of day, biological rhythms, time spent awake, and amount of sleep. The vertical axis on the right side of FAST^TM graphs represents the Blood Alcohol Content (BAC) equivalency throughout the spectrum of modeled cognitive effectiveness. A value of 77% modeled cognitive effectiveness corresponds to a blood alcohol content of 0.05% (legally impaired in some jurisdictions). A value of 70% modeled cognitive effectiveness corresponds to a blood alcohol content of 0.08% (legally impaired in most jurisdictions). The dotted line represents the lower 10th percentile of modeled cognitive effectiveness. The green band (from 90 to 100%) represents acceptable modeled cognitive performance effectiveness for workers conducting safety sensitive jobs (e.g., flying, driving, weapons operation, command and control, etc.). The yellow band (from 65 to 90% modeled cognitive effectiveness) indicates caution. Personnel engaged in skilled performance activities such as aviation are recommended not to operate in this bandwidth. The area from the dotted line to the pink area represents the modeled cognitive effectiveness equivalent to the circadian nadir and a second day without sleep. The pink band (below 65%) represents performance effectiveness after two days and one night of sleep deprivation. The abscissa (x-axis) illustrates a single 15-min period (red bar) during the fMRI scans for each of the baseline and sleep deprivation conditions as well as sleep timing/duration (blue bars), darkness (gray bars), and time of day in hours. The red bar shows a thickening of the modeled cognitive effectiveness line (immediately above the red bar), reflecting cognitive effectiveness during the fMRI scans.

FIGURE 2

Patterns of brain activation for divergent thinking (fluency) and recalling characteristics following a night of normal sleep and sleep deprivation. Glass brains representing activations in relation to (A) uses–rest following a night of normal sleep (arrow points to the left inferior frontal gyrus), (B) recalling characteristics–rest following a night of normal sleep (arrow points to the left hippocampus), (C) uses–rest following sleep deprivation (arrow points to the left inferior frontal gyrus), (D) recalling characteristics–rest following sleep deprivation (arrow points to the left medial frontal gyrus). The complete list of activations appears in Table 1.

FIGURE 3

Following sleep deprivation the left inferior frontal gyrus was activated more when generating uses (fluency) in the divergent thinking task. Following sleep deprivation, there was greater activation in left inferior frontal gyrus when generating uses (compared to recalling characteristics) in the Alternate Uses Task. SPM rendered into standard stereotactic space and superimposed on to transverse MRI in standard space.