Effects of sleep deprivation on dissociated components of executive functioning

Abstract

Study objectives: We studied the effects of sleep deprivation on executive functions using a task battery which included a modified Sternberg task, a probed recall task, and a phonemic verbal fluency task. These tasks were selected because they allow dissociation of some important executive processes from non-executive components of cognition.

Design: Subjects were randomized to a total sleep deprivation condition or a control condition. Performance on the executive functions task battery was assessed at baseline, after 51 h of total sleep deprivation (or no sleep deprivation in the control group), and following 2 nights of recovery sleep, at fixed time of day (11:00). Performance was also measured repeatedly throughout the experiment on a control task battery, for which the effects of total sleep deprivation had been documented in previously published studies.

Setting: Six consecutive days and nights in a controlled laboratory environment with continuous behavioral monitoring.

Participants: Twenty-three healthy adults (age range 22-38 y; 11 women). Twelve subjects were randomized to the sleep deprivation condition; the others were controls.

Results: Performance on the control task battery was considerably degraded during sleep deprivation. Overall performance on the modified Sternberg task also showed impairment during sleep deprivation, as compared to baseline and recovery and compared to controls. However, two dissociated components of executive functioning on this task--working memory scanning efficiency and resistance to proactive interference--were maintained at levels equivalent to baseline. On the probed recall task, resistance to proactive interference was also preserved. Executive aspects of performance on the phonemic verbal fluency task showed improvement during sleep deprivation, as did overall performance on this task.

Conclusion: Sleep deprivation affected distinct components of cognitive processing differentially. Dissociated non-executive components of cognition in executive functions tasks were degraded by sleep deprivation, as was control task performance. However, the executive functions of working memory scanning efficiency and resistance to proactive interference were not significantly affected by sleep deprivation, nor were dissociated executive processes of phonemic verbal fluency performance. These results challenge the prevailing view that executive functions are especially vulnerable to sleep loss. Our findings also question the idea that impairment due to sleep deprivation is generic to cognitive processes subserved by attention.

Figure 1

Laboratory study design. Subjects stayed inside the laboratory from 15:00 on day 1 until 22:00 on day 7. Black areas represent 10 h nocturnal periods of time in bed for sleep (22:00–08:00). Gray areas represent 10 h nocturnal periods (22:00–08:00) when subjects in the TSD group were kept awake while subjects in the control group were in bed to sleep. The subjects in the TSD group stayed awake continuously for a total of 62 h during the study. Diamonds indicate the 3 administrations of the executive functions task battery (11:00) at 48-h intervals: after 3 h of scheduled wakefulness at baseline; after 51 h of continuous wakefulness in the TSD group, or 3 h of scheduled wakefulness in the control group; and after 3 h of scheduled wakefulness following 2 nights of recovery sleep. Dots indicate the repeated administrations of the control task battery (bullets overlapping gray background denote test bouts performed in the TSD condition only). The first 2 administrations of the control task battery served as practice bouts. Tick marks denote time of day.

Figure 2

Performance on the control task battery. The top panel displays number of lapses on the PVT (upwards is worse performance). The middle panel shows number of correct responses on the DSST (downwards is worse performance). The bottom panel shows subjective sleepiness as rated on the KSS (upwards is greater sleepiness). Means ± standard errors are shown for the TSD group (black circles) and the control group (gray boxes), across all test bouts that the 2 groups had in common (i.e., test bouts administered at night for the sleep-deprived subjects are not shown). The abscissa shows cumulative clock time (e.g., 24 is midnight of the second day, 48 is midnight of the third day). The 62-h period of TSD took place between hours 32 and 94 (vertical dashed lines).

Figure 3

Performance on the modified Sternberg task. The top panels show the intercept of the linear relationship between memory set size and RT, which measures the non-executive component processes involved in performing the task (e.g., encoding the probe, deciding on a response, and executing the motor response). The middle panels display the slope of the linear relationship between memory set size and RT, which measures the executive functions component of working memory scanning efficiency. The bottom panels display the difference in RT between recent and non-recent negative probes, which measures the executive function of resistance to proactive interference. Means ± standard errors are shown for baseline (BL), total sleep deprivation or control (TSD/CTRL), and recovery (REC), in the TSD group (left panels) and the control group (right panels).

Figure 4

Performance on the probed recall task. The top panels show overall number of items recalled accurately. Higher on the ordinate indicates greater accuracy. The bottom panels show the difference in the number of items recalled between interference-release trials and interference-maximum trials. Lower on the ordinate represents greater resistance to proactive interference. Negative difference scores indicate that, paradoxically, more items were recalled in the trials set up to induce interference. Means ± standard errors are shown for baseline (BL), total sleep deprivation or control (TSD/CTRL), and recovery (REC), in the TSD group (left panel) and the control group (right panel).

Figure 5

Performance on the phonemic verbal fluency task. The top panels display the number of words generated per test bout, representing global performance on the task. The middle panels display the average phonemic cluster size (where cluster size is defined as the number of phonemically related words minus 1), representing automatic (non-executive) processing. The bottom panels display the number of switches between phonemic clusters, which measures executive processing related to cognitive flexibility and mental set shifting. Means ± standard error are shown for baseline (BL), total sleep deprivation or control (TSD/CTRL), and recovery (REC), in the TSD group (left panels) and the control group (right panels).