Acute sleep deprivation and circadian misalignment associated with transition onto the first night of work impairs visual selective attention
Nayantara Santhi, Todd S Horowitz, Jeanne F Duffy, Charles A Czeisler, Nayantara Santhi, Todd S Horowitz, Jeanne F Duffy, Charles A Czeisler
Abstract
Background: Overnight operations pose a challenge because our circadian biology promotes sleepiness and dissipates wakefulness at night. Since the circadian effect on cognitive functions magnifies with increasing sleep pressure, cognitive deficits associated with night work are likely to be most acute with extended wakefulness, such as during the transition from a day shift to night shift.
Methodology/principal findings: To test this hypothesis we measured selective attention (with visual search), vigilance (with Psychomotor Vigilance Task [PVT]) and alertness (with a visual analog scale) in a shift work simulation protocol, which included four day shifts followed by three night shifts. There was a nocturnal decline in cognitive processes, some of which were most pronounced on the first night shift. The nighttime decrease in visual search sensitivity was most pronounced on the first night compared with subsequent nights (p = .04), and this was accompanied by a trend towards selective attention becoming 'fast and sloppy'. The nighttime increase in attentional lapses on the PVT was significantly greater on the first night compared to subsequent nights (p<.05) indicating an impaired ability to sustain focus. The nighttime decrease in subjective alertness was also greatest on the first night compared with subsequent nights (p<.05).
Conclusions/significance: These nocturnal deficits in attention and alertness offer some insight into why occupational errors, accidents, and injuries are pronounced during night work compared to day work. Examination of the nighttime vulnerabilities underlying the deployment of attention can be informative for the design of optimal work schedules and the implementation of effective countermeasures for performance deficits during night work.
Conflict of interest statement
Competing Interests: Potential competing interests for all authors are fully detailed in the Acknowledgments section.
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References
- Czeisler CA, Dijk DJ. Use of bright light to treat maladaption to night shift work and circadian rhythm sleep disorders. J Sleep Res. 1995;4:70–73.
- Horowitz TS, Cade BE, Wolfe JM, Czeisler CA. Efficacy of bright light and sleep/darkness scheduling in alleviating circadian maladaptation to night work. Am J Physiol Endocrinol Metab. 2001;281:E384–E391.
- Dijk DJ, Duffy JF, Czeisler CA. Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res. 1992;1:112–117.
- Jewett ME, Kronauer RE. Interactive mathematical models of subjective alertness and cognitive throughput in humans. J Biol Rhythms. 1999;14:588–597.
- Barger LK, Cade BE, Ayas NT, Cronin JW, Rosner B, et al. Extended work shifts and the risk of motor vehicle crashes among interns. N Engl J Med. 2005;352:125–134.
- Folkard S. Is there a ‘best compromise’ shift system? Ergonomics. 1992;35:1453–1463.
- Bureau of Labor Statistics. Workers on Flexible and Shift Schedules in May 2004. 2005
- Dinges DF, Orne MT, Whitehouse WG, Orne EC. Temporal placement of a nap for alertness: Contributions of circadian phase and prior wakefulness. Sleep. 1987;10:313–329.
- Lamond N, Dawson D. Quantifying the performance impairment associated with fatigue. J Sleep Res. 1999;8:255–262.
- Bartel P, Offermeier W, Smith F, Becker B. Attention and working memory in resident anaesthetists after night duty: group and individual effects. Occup Environ Med. 2003;61:167–170.
- Williamson AM, Feyer AM, Mattick RP, Friswell R, Finlay-Brown S. Developing measures of fatigue using an alcohol comparison to validate the effects of fatigue on performance. Accid Anal Prev. 2001;33:313–326.
- Falleti MG, Maruff P, Collie A, Darby DG, McStephen M. Qualitative similarities in cognitive impairment associated with 24 h of sustained wakefulness and a blood alcohol concentration of 0.05%. J Sleep Res. 2003;12:265–274.
- Graw P, Krauchi K, Knoblauch V, Wirz-Justice A, Cajochen C. Circadian and wake-dependent modulation of fastest and slowest reaction times during the psychomotor vigilance task. Physiol Behav. 2004;80:695–701.
- Van Dongen HP, Dinges DF. Sleep, circadian rhythms, and psychomotor vigilance. Clin Sports Med. 2005;24:237–viii.
- Horowitz TS, Cade BE, Wolfe JM, Czeisler CA. Searching night and day: a dissociation of effects of circadian phase and time awake on visual selective attention and vigilance. Psychol Sci. 2003;14:549–557.
- Van Dongen HPA, Dinges DF. Investigating the interaction between the homeostatic and circadian processes of sleep-wake regulation for the prediction of waking neurobehavioural performance. J Sleep Res. 2003;12:181–187.
- Caputo G, Guerra S. Attentional selection by distractor suppression. Vision Res. 1998;38:669–689.
- Wolfe JM. Visual search. In: Pashler H, editor. Attention. Hove, England: Psychology Press/Erlbaum (UK) Taylor & Francis; 1998. pp. 13–73.
- Weiner E. Vigilance and inspection. In: Warm J, editor. Sustained attention in human performance. New York: J Wiley & Sons; 1984. pp. 207–246.
- Parasuraman R. Cambridge, MA: The MIT Press; 1998. The Attentive Brain.
- Belenky G, Wesensten NJ, Thorne DR, Thomas ML, Sing HC, et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose-response study. J Sleep Res. 2003;12:1–12.
- DeCostre P, Buhler U, DeGroot LJ, Refetoff S. Diurnal rhythm in total serum thyroxine levels. Metabolism. 1971;20:782–791.
- Lamond N, Dorrian J, Roach GD, McCulloch K, Holmes AL, et al. The impact of a week of simulated night work on sleep, circadian phase, and performance. Occup Environ Med. 2003;60:e13.
- Purnell MT, Feyer AM, Herbison GP. The impact of a nap opportunity during the night shift on the performance and alertness of 12-h shift workers. J Sleep Res. 2002;11:219–227.
- Treisman A, Sato S. Conjunction search revisited. J Exp Psychol Hum Percept Perform. 1990;16:459–478.
- Dinges DF, Gillen KA, Powell JW, Carlin M, Ott GE, et al. Discriminating sleepiness by fatiguability on a psychomotor vigilance task. Sleep Res. 1994;23:129.
- Wolfe JM. Guided search 2.0: A revised model of visual search. Psychonomic Bulletin & Review. 1994;1:202–238.
- De Gennaro L, Ferrara M, Curcio G, Bertini M. Visual search performance across 40 h of continuous wakefulness: Measures of speed and accuracy and relation with oculomotor performance. Physiol Behav. 2001;74:197–204.
- Monk TH, Buysse DJ, Reynolds CF, III, Berga SL, Jarrett DB, et al. Circadian rhythms in human performance and mood under constant conditions. J Sleep Res. 1997;6:9–18.
- Scheffers MK, Humphrey DG, Stanny RR, Kramer AF, Coles MG. Error-related processing during a period of extended wakefulness. Psychophysiol. 1999;36:149–157.
- Mikulincer M, Babkoff H, Caspy T, Sing H. The effects of 72 hours of sleep loss on psychological variables. Br J Psychol. 1989;80 (Pt 2):145–162.
- Jewett ME, Dijk DJ, Kronauer RE, Dinges DF. Dose-response relationship between sleep duration and human psychomotor vigilance and subjective alertness. Sleep. 1999;22:171–179.
- Williams HL, Lubin A, Goodnow JJ. Impaired performance with acute sleep loss. Psychol Monogr. 1959;73:1–26.
- Santhi N, Duffy JF, Horowitz TS, Czeisler CA. Scheduling of sleep/darkness affects the circadian phase of night shift workers. Neurosci Lett. 2005;384:316–320.
- Sternberg S. High-speed scanning in human memory. Science. 1966;153:652–654.
- Macmillan NA, Creelman CD. Cambridge, MA: Lawrence Erlbaum; 2004. Detection theory:A user's guide.
- Rouder JN, Speckman PL. An evaluation of the Vincentizing method of forming group-level response time distributions. Psychon Bull Rev. 2004;11:419–427.
- Ratcliff R, Smith PL. A comparison of sequential sampling models for two-choice reaction time. Psychol Rev. 2004;111:333–367.
- Smith PL, Ratcliff R, Wolfgang BJ. Attention orienting and the time course of perceptual decisions: response time distributions with masked and unmasked displays. Vision Res. 2004;44:1297–1320.
- Luce RD. Decomposition into decision and residual latencies. In: Thomas VS, editor. New York: 1986.
- Lockley SW, Cronin JW, Evans EE, Cade BE, Lee CJ, et al. Effect of reducing interns' weekly work hours on sleep and attentional failures. N Engl J Med. 2004;351:1829–1837.
- Folkard S. The nature of diurnal variations in performance and their implications for shift work studies. In: Colquhoun P, Folkard S, Knauth P, Rutenfranz J, editors. Proceedings of the Third International Symposium on Night and Shift Work. Opladen, Germany: Westdeutscher Verlag; 1975. pp. 113–122.
- Budnick LD, Lerman SE, Baker TL, Jones H, Czeisler CA. Sleep and alertness in a 12-hour rotating shift work environment. J Occup Med. 1994;36:1295–1300.
- Folkard S, Lombardi DA. Modeling the impact of the components of long work hours on injuries and “accidents”. Am J Ind Med 2006
- Pternitis C. Shift work: work load, fatigue and states of vigilance. In: Reinberg A, Vieux N, Andlauer P, editors. Night and Shift Work: Biological and Social Aspects. Oxford: Pergamon Press; 1981. pp. 171–177.
- Neri DF, Czeisler CA. Effect of bright light on vigilance and subjective sleepiness during a simulated shiftwork rotation. Sleep Res. 1996;25:144.
- Dinges DF, Powell JW. Sleepiness is more than lapsing. Sleep Res. 1988;17:84.
- Dorrian J, Rogers NL, Dinges DF. Psychomotor Vigilance Performance: Neurocognitive Assay Sensitive to Sleep Loss. In: Kushida CA, editor. Sleep Deprivation. Clinical Issues, Pharmacology, and Sleep Loss Effects. New York: Marcel Dekker; 2005. pp. 39–70.
- Suzuki K, Ohida T, Kaneita Y, Yokoyama E, Miyake T, et al. Mental health status, shift work, and occupational accidents among hospital nurses in Japan. J Occup Health. 2004;46:448–454.
- Dula DJ, Dula NL, Hamrick C, Wood GC. The effect of working serial night shifts on the cognitive functioning of emergency physicians. Ann Emerg Med. 2001;38:152–155.
- Drake CL, Roehrs T, Richardson G, Walsh JK, Roth T. Shift work sleep disorder: prevalence and consequences beyond that of symptomatic day workers. Sleep. 2004;27:1453–1462.
- Folkard S, Tucker P. Shift work, safety and productivity. Occup Med (Lond) 2003;53:95–101.
- Rajaratnam SM, Arendt J. Health in a 24-h society. The Lancet. 2001;1358:999–1005.
- Åkerstedt T, Czeisler CA, Dinges DF, Horne JA. Accidents and Sleepiness: A consensus statement from the International Conference on Work Hours, Sleep and Accidents, Stockholm, 8–10 September 1994. J Sleep Res. 1994;3:195.
- Horrocks N, Pounder R. Working the night shift: Preparation, survival and recovery. A guide for Jr. Doctors. 2006
- Crowley SJ, Lee C, Tseng CY, Fogg LF, Eastman CI. Combinations of bright light, scheduled dark, sunglasses, and melatonin to facilitate circadian entrainment to night shift work. J Biol Rhythms. 2003;18:513–523.
- Eastman CI, Hoese EK, Youngstedt SD, Liu L. Phase-shifting human circadian rhythms with exercise during the night shift. Physiol Behav. 1995;58:1287–1291.
- Schweitzer PK, Randazzo AC, Stone K, Erman M, Walsh JK. Laboratory and field studies of naps and caffeine as practical countermeasures for sleep-wake problems associated with night work. Sleep. 2006;29:39–50.
- Dinges DF, Whitehouse WG, Orne EC, Orne MT. The benefits of a nap during prolonged work and wakefulness. Work and Stress. 1988;2:139–153.
- Wyatt JK, Cajochen C, Ritz-De Cecco A, Czeisler CA, Dijk DJ. Low-dose, repeated caffeine administration for circadian-phase-dependent performance degradation during extended wakefulness. Sleep. 2004;27:374–381.
- Landolt HP, Retey JV, Tonz K, Gottselig JM, Khatami R, et al. Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology. 2004;29:1933–1939.
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