Residual, differential neurobehavioral deficits linger after multiple recovery nights following chronic sleep restriction or acute total sleep deprivation

Abstract

Study objectives: The amount of recovery sleep needed to fully restore well-established neurobehavioral deficits from sleep loss remains unknown, as does whether the recovery pattern differs across measures after total sleep deprivation (TSD) and chronic sleep restriction (SR).

Methods: In total, 83 adults received two baseline nights (10-12-hour time in bed [TIB]) followed by five 4-hour TIB SR nights or 36-hour TSD and four recovery nights (R1-R4; 12-hour TIB). Neurobehavioral tests were completed every 2 hours during wakefulness and a Maintenance of Wakefulness Test measured physiological sleepiness. Polysomnography was collected on B2, R1, and R4 nights.

Results: TSD and SR produced significant deficits in cognitive performance, increases in self-reported sleepiness and fatigue, decreases in vigor, and increases in physiological sleepiness. Neurobehavioral recovery from SR occurred after R1 and was maintained for all measures except Psychomotor Vigilance Test (PVT) lapses and response speed, which failed to completely recover. Neurobehavioral recovery from TSD occurred after R1 and was maintained for all cognitive and self-reported measures, except for vigor. After TSD and SR, R1 recovery sleep was longer and of higher efficiency and better quality than R4 recovery sleep.

Conclusions: PVT impairments from SR failed to reverse completely; by contrast, vigor did not recover after TSD; all other deficits were reversed after sleep loss. These results suggest that TSD and SR induce sustained, differential biological, physiological, and/or neural changes, which remarkably are not reversed with chronic, long-duration recovery sleep. Our findings have critical implications for the population at large and for military and health professionals.

Keywords: MWT; chronic sleep restriction; cognitive; fatigue; psychomotor vigilance test; recovery; sleepiness; total sleep deprivation; vigor.

Figure 1.

Experimental protocol. Participants were randomly assigned to one of two conditions: (A) SR: two nights of baseline sleep (B1 and B2, 10:00 pm to 08:00/10:00 am) followed by five nights of chronic SR (04:00 am to 08:00 am), followed by four nights of recovery sleep (R1–R4, 10:00 pm to 10:00 am) or (B) TSD: two nights of baseline sleep (B1 and B2, 10:00 pm to 08:00/10:00 am) followed by one night of 36-hour acute TSD followed by four nights of recovery sleep (R1–R4, 10:00 pm to 10:00 am).

Figure 2.

Neurobehavioral performance after sleep loss and recovery. (A) Both chronic SR and acute TSD produced performance deficits as measured by more lapses on the 10-min PVT. (B) PVT response speed (1/RT) was impaired after both SR and TSD. 1/RT returned to baseline after R1 and was maintained through R1–R4 in the TSD group but did not recover to baseline after four nights of recovery sleep following SR. 1/RT differed between the SR and TSD groups during R1 and R3. (C) DSST performance was impaired after TSD, but not SR, and subsequently exceeded baseline performance for all nights of recovery sleep for both conditions. Data are mean ± SEM. *p < 0.05; **p < 0.001; asterisks directly above data points are significant paired t-tests using Bonferroni corrections, which compared performance at each time point to baseline performance when the all-time point interaction was significant; asterisks above bars are significant one-way ANOVAs that compared differences between SR and TSD.

Figure 3.

Self-rated sleepiness, fatigue, and vigor after sleep loss and recovery. Both chronic SR and acute TSD produced impairments in all self-rated measures. (A) Self-reported sleepiness, as measured by the KSS, differed between the SR and TSD groups during sleep loss, with greater sleepiness in the TSD group. Sleepiness returned to baseline levels following one night of recovery sleep (R1) after both SR and TSD, and levels were maintained throughout 4 days of recovery (R1–R4). (B) POMS Fatigue scores significantly increased with both SR and TSD. (C) POMS Vigor scores significantly decreased in both the SR and TSD groups. Data are mean ± SEM. *p < 0.05; **p < 0.001; asterisks directly above data points are significant paired t-tests using Bonferroni corrections, which compared self-report scores at each time point to baseline scores when the all-time point interaction was significant; asterisks above bars are significant one-way ANOVAs that compared differences between SR and TSD.

Figure 4.

Physiologic alertness after sleep loss and recovery. Both chronic SR and acute TSD produced decreases in physiological alertness as measured by sleep latency onset during a modified MWT. Participants in both the TSD and SR conditions showed a return of sleep latency onset to baseline levels throughout 4 days of recovery. Sleep latency differed between the SR and TSD groups at R1, R3, and R4 (note: data were not collected for the second night of recovery [R2] after SR or TSD). Data are mean ± SEM. *p < 0.05; **p < 0.001; asterisks directly above data points are significant paired t-tests using Bonferroni corrections, which compared sleep latency at each time point to baseline latency when the all-time point interaction was significant; asterisks above bars are significant one-way ANOVAs that compared differences between SR and TSD.