Distinct Non-Additive Effects of Acute and Chronic Sleep Loss and Circadian Phase on Inadvertent Attentional Failures

Abstract

Introduction : In modern societies, many humans are exposed to a combination of acute and chronic sleep loss and circadian misalignment. We previously reported non-additive effects of these three factors on performance measures derived from the psychomotor vigilance task [Cohen et al., Sci Transl Med, 2010]. Here we tested whether this result were specific to this task or whether it reflects a more fundamental principle of sleep-wake regulation by quantifying the impact of these three factors on the occurrence of spontaneous attentional failures (AF) derived from continuous electro-oculographic (EOG) recordings in that same study. Methods : Nine volunteers (age 21-34 years, 4F) completed a three-week forced desynchrony protocol consisting of 12 consecutive 42.85-h sleep-wake cycles with 32.85 h of scheduled wakefulness and 10 h of scheduled sleep (sleep:wake ratio of 1:3.3). Over three weeks, the protocol therefore induced an increasing chronic sleep loss while allowing extended wake and sleep episodes to occur at all circadian phases. Continuous EOG recordings were obtained. AF were quantified as number of 30-s epochs with visually scored slow eye movements per hour of wakefulness. Data were analyzed by time since scheduled wake onset in 4.1-h bins (acute sleep loss), study week (chronic sleep loss), and circadian phase derived from plasma melatonin. Results : During the first 8.2 h of a wake episode, the number of AF (nAF) was low (< 1/h), irrespective of study week. Across the subsequent wake bins, nAF increased steadily, with the rate of increase being higher in weeks 2 and 3 compared to week 1 (mixed ANOVA, Week x Wake bin, p=0.001). At the end of the wake episode, nAF was 2.0±0.4/h (±SEM), 3.8±0.5/h, and 3.0±0.8/h in weeks 1, 2, and 3, respectively (effect of Week in final wake bin, p<0.0001). Moreover, the effects of acute and chronic sleep loss on nAF were magnified during the biological night (Phase x Wake bin, Phase x Week, both p<0.0002). Conclusion: A single episode of extended recovery sleep can temporarily–i.e., for the first few hours of subsequent wakefulness–restore to baseline levels attentional impairment associated with chronic sleep loss. Chronic sleep loss speeds up the accumulation of inadvertent AF during a wake episode. Thus, acute and chronic sleep loss in combination with circadian phase should be considered as distinct factors that interact in a non-additive way to affect waking function