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CHRONIC SLEEP DEFICIT AND PERFORMANCE OF A SUSTAINEDATTENTION TASK—AN ELECTROOCULOGRAPHY STUDY

Magdalena Fafrowicz,1 Halszka Oginska,2 Justyna Mojsa-Kaja,1

Tadeusz Marek,1 Krystyna Golonka,1 and Kinga Tucholska1

1 Department of Neuroergonomics, Institute of Applied Psychology, Jagiellonian University, Krakow, Poland 2 Department of Ergonomics and Exercise Physiology, Collegium Medicum, JagiellonianUniversity, Krakow, Poland

Electrooculography (EOG) was used to explore performance differences in a sus-tained attention task during rested wakefulness (RW) and after 7 days of partial sleepdeprivation (SD). The RW condition was based on obtaining regular sleep, and theSD condition involved sleep restriction of 3 h/night for a week resulting in a totalsleep debt of 21 h. The study used a counterbalanced design with a 2-wk gap

between the conditions. Participants performed a sustained attention task for 45 minon four occasions: 10:00–11:00, 14:00–15:00, 18:00–19:00, and 22:00–23:00 h. The

task required moving gaze and attention as fast as possible from a fixation point to atarget. In each session, 120 congruent and 34 incongruent stimuli were presented,totaling 1232 observations/participant. Correct responses plus errors of omission(lapses) and commission (false responses) were recorded, and the effect of time-of-dayon sustained attention following SD was investigated. The analysis of variance(ANOVA) model showed that SD affected performance on a sustained attention taskand manifested itself in a higher number of omission errors: congruent stimuli( F (1,64)= 13.3, p< .001) and incongruent stimuli ( F (1,64)= 14.0, p< .001). Reactiontimes for saccadic eye movements did not differ significantly between experimentalconditions or by time-of-day. Commission errors, however, exhibited a decreasingtrend during the day. The visible prevalence of omissions in SD versus RW was

observed during the mid-afternoon hours (the so-called post-lunch dip) for bothcongruent and incongruent stimuli ( F (1,16)= 5.3, p= .04 and F (1,16)= 5.6, p= .03,respectively), and at 18:00 h for incongruent stimuli ( F (1,13)= 5.7, p= .03). (Authorcorrespondence: [email protected])

Keywords Chronic sleep deficit; Omission and commission errors; Post-lunch dip;Saccadic eye movements; Sustained attention

This paper was presented at the 19th International Symposium on Shiftwork and WorkingTime, August 2–6, 2009, San Servolo Island, Venice, Italy

Address correspondence to Magdalena Fafrowicz, Department of Neuroergonomics, Institute of Applied Psychology, Jagiellonian University, 4 Lojasiewicza Street, 30-348 Krakow, Poland. E-mail:[email protected]

Chronobiology International, 27(5): 934–944, (2010)Copyright © Informa UK Ltd.ISSN 0742-0528 print/1525-6073 onlineDOI: 10.3109/07420528.2010.488981



INTRODUCTION

Attention, defined as the mental ability to select stimuli, responses,memories, or thoughts that are behaviorally relevant (Corbetta &Shulman, 2002), governs all human cognitive processes, from perceptionto decision and execution (e.g., Fafrowicz & Marek, 2007). According tocurrent theories, attention can be divided into two broad domains, repre-senting intensity and selection aspects (e.g., Sturm & Willmes, 2001).Whereas the intensity aspects are related to alertness and sustained-atten-tion processes, selection aspects are linked to orienting and executiveattention. Intensity aspects appear more fundamental and constituteprerequisite conditions for more complex and capacity-demanding atten-tion selectivity (e.g., Fan et al., 2003).

Over the last two decades, sleep-deprivation studies have recognizedalertness and sustained-attention as two components of cognition that aredrastically affected by periods without sleep (Lim & Dinges, 2008). Totalsleep-deprivation leads to an extreme form of sleep deficit (Casagrandeet al., 2006; Chee et al., 2006). However, chronic sleep-restriction (partialsleep-deprivation) is pervasive in modern society due to work demandsand social/lifestyle factors. Both acute sleep-deprivation (≥24 h) andshort-term, chronic sleep-restriction (<6 h sleep/night) may lead to areduction in vigilance, as well as a decrease in working memory andexecutive functions (Axelsson et al., 2008; Van Dongen et al., 2003).

There is an extensive literature documenting the negative conse-quences of sleep loss, including a wide range of cognitive and perform-ance deficits (see Durmer & Dinges, 2005). In considering human error-proneness during the day, two temporal factors influencing the level of alertness should be taken into account: sleep-wake homeostasis and circa-dian rhythm (e.g., as modeled by the Three-Process Model; see, e.g., Åkerstedt et al., 2008). Sustained-attention tasks are recognized as beingsensitive to sleep loss, as well as to circadian misalignment (Dorrian et al.,2005).

The objective of this electrooculography (EOG) study was theassessment of sustained-attention task performance during the day underconditions of rested wakefulness and chronic sleep deprivation. Bothdiurnal rhythm factors, the homeostatic (total sleep debt), and circadian(time-of-day) are considered in this assessment.

METHODS

Subjects

Twelve healthy, right-handed women between 21 and 27 yrs of ageparticipated. Each was shown to have normal or corrected-to-normal

An Electrooculography Study 935



vision, reported good sleeping habits, was a nonsmoker, and was drug-free. Self-reported sleep duration was >6.5 h/each night the month before the study. Participants completed a survey that provided demo-

graphic data, chronotype, and sleepiness. Subjective phase and amplitudewere derived from the Chronotype Questionnaire (Oginska et. al, 2000),and the Epworth Sleepiness Scale (Johns, 1991) was used to assessdaytime sleepiness level. These measures were used to exclude partici-pants who were extreme circadian types and who experienced excessive/pathological sleepiness.

A laboratory experiment was conducted under two conditions: (1)rested wakefulness (RW) where participants had their usual sleep and (2)after undergoing sleep deprivation (SD) of 3 h/night for 7 nights(amounting to 21 h of sleep debt). Three participants were excluded

from the final analyses due to technical errors or an excessive number of lapses (>25% of total trials) during the RW session.Participants were briefed on the study requirements, and they signed

a written consent form. They were remunerated for their participation.The study protocol met the ethical standards established by the journalfor the conduct of human research (Portaluppi et al., 2008).

Procedure

The study was conducted in a laboratory environment that provideddim light, low noise level, and controlled room temperature.Participants visited the laboratory three times. The first session consistedof a briefing on the experimental procedure, and those that volunteeredundertook some practice on the attention task. The second and thirdvisits involved participating in the EOG experiment. The first exper-imental session took place 1 day after the initial visit. The order of thetwo experimental sessions (RW, SD) was counterbalanced across all par-ticipants. The sessions were separated by at least 2 wk to minimize theresidual effects of sleep deficit on performance of a sustained-attention

task. During experimental days, participants were allowed to engage innonstrenuous activities (e.g., reading, conversing, and watching videos).Research assistants observed the participants and were instructed toprevent them from napping by verbal reminders. Subjects were notallowed to drink or eat substances containing alcohol or caffeine (e.g.,tea, chocolate) either during the day of the experiment or during theprevious 48 h.

Before attempting each of the performance tasks, participants com-pleted the Activation-Deactivation Adjective Check List (Thayer, 1989) toreflect their energy, tiredness, tension, and calmness. Participants also

recorded their sleepiness using the Karolinska Sleepiness Scale (Åkerstedt& Gillberg, 1990).

M. Fafrowicz et al.936



Eye Tracking

The saccadometer system (Ober-Consulting, Poland) was used torecord saccadic responses to visual stimuli. Horizontal saccadic eyemovements were registered using a noninvasive, infrared reflectionrecording technique with a spatial resolution of 0.1° and time resolutionof 1 ms. This system allowed data to be recorded at a sample rate of 250 Hz. Stimuli generated by red and green laser diodes were pre-sented on a screen integrated with the EOG system. The system wasattached to the subject’s head with an adjustable headband (Figure 1),and the screen was located approximately 3 cm from the participant’seyes. Participants completed the sustained-attention task in an isolatedroom, with low levels of artificial light and assumed a recumbent

position.

Experimental Task

The sustained attention task consisted of two unpredictableconditions: one with a cue congruent to a target and the other in whichthe cue and target were incongruent. The spatial cuing paradigm,designed for the classic work of Posner (e.g., Posner, 1980; Vecera &Rizzo, 2003), was modified for the experiment with the central cue (enga-ging covert orienting attention) used to voluntarily shift the spatial atten-

tion and eye movement to the target location (employing overt orientingattention).

Each experimental trial began with the presentation of a fixationpoint (green laser diode) in the center of the screen. After 3000 or6000 ms, a cue (red diode) appeared at 1° to the right or left of the fix-ation point for 100, 250, or 500 ms. After a further 300–500 ms, a target

FIGURE 1 Eye-tracking system used in the study.




stimulus (red diode) was flashed for 100, 250, or 500 ms at 10° to the

right or left of the fixation point, with stimulus-onset asynchronies (SOAs)randomly distributed (Figures 2 and 3).

FIGURE 2 Schematic description of congruent task.

FIGURE 3 Schematic description of incongruent task.




Each participant was instructed to direct her gaze and attentionstraight ahead towards the fixation point. When the target appeared tothe left or right side, the participant was asked to execute a saccadic eye

movement, that is, to move gaze and attention from the fixation point tothe target and back to the fixation point as fast as possible. Execution of an eye movement for a given cue was not allowed to strengthen top-downmechanisms involved in voluntary shift of attention.

The participants performed the sustained-attention tasks four timesduring the day: at about 10:00–11.00, 14:00–15.00, 18:00–19:00, and22:00–23:00 h. In each 45-min session, 120 congruent (78%) and 34incongruent (22%) stimuli were presented.

RESULTS

The mean length of the self-reported sleep in the RW condition was7 h 52 min (SD± 45 min), and in the SD condition sleep duration was4 h 57 min (SD± 33 min).

The number of correct responses and two types of erroneous reac-tions (omissions and commissions) occurring in the four sessions for thetwo conditions (normal sleep versus sleep debt) were analyzed. Therewere three kinds of commission errors: error of direction, error of place,and error of both place and direction). Omissions were defined as no-reaction within 1 s from target appearance. Each participant provided amaximum of 1232 measurements. Statistical analyses were performed viaanalysis of variance (ANOVA) using Statistica (V. 8.0) software. Theresults show that chronic partial sleep-deprivation produces considerableperformance decrements on a sustained-attention task. As Table 1 shows,sleep deficit resulted in significantly more errors of omission. Significantdifferences in reaction time of saccadic eye movements were not found, but a tendency for slower reactions was observed.

TABLE 1 Parameters of performance of sustained attention task in state of rested wakefulness (RW)and chronic partial sleep deficit (SD; total sleep debt of 21 h)

ANOVA RW (n= 34) SD (n= 32) F (1, 64) p

Congruent cue% of correct responses 70.6± 29.7 64.0± 24.2 1.321 .255% of omissions 4.8± 6.4 16.2± 16.9 13.344 .001

% of commissions 24.5± 26.7 19.8± 19.1 0.685 .411Mean RT in correct response (ms) 194± 37 204± 44 0.987 .324

Incongruent cue% of correct responses 68.7± 29.9 58.1± 23.3 2.577 .113% of omissions 2.0± 4.0 13.6± 17.6 14.011 < .001

% of commissions 23.7± 28.9 20.4± 20.7 0.287 .594Mean RT in correct response (ms) 217± 47 235± 72 3.371 .071




For both congruent (Figure 4) and incongruent stimuli (not shown),chronic partial sleep-deprivation effect on performance was particularlyevident at 14:00 h ( F (1,16)= 5.31, p= .04; F (1,16)= 5.63, p= .03, respect-ively) and at 18:00 h for incongruent stimuli ( F (1,13)= 5.73, p= .03). In

contrast, the average percentage of commission errors actually decreasedduring the day, and this tendency appeared especially strong under SDconditions (Figure 5).

DISCUSSION

The effects of sleep loss and circadian rhythmicity have a detrimentalimpact on the cognitive functioning of individuals. Sleep deprivationinduces performance decline modulated by the interaction of two agents:

a homeostatic effect related to the increased effort of maintaining wake-fulness and an endogenous circadian effect (e.g., Durmer & Dinges,2005; Chee et al., 2006).

The findings from this study are not consistent with studies that haveemployed the Psychomotor Vigilance Test (PVT). The PVT has beenwidely used for the last two decades, and these findings confirm thatsleep deprivation results in more errors of omission and commission(Lim & Dinges, 2008). Omission errors, defined as lapsing or failing torespond in a timely fashion to a presented stimulus are related to micro-sleeps. Errors of commission or false alarms are considered to be com-

pensatory responses to drowsiness (Lim & Dinges, 2008; Miccoli et al.2008; Rogers et al., 2003). In the present study using EOG, chronic

FIGURE 4 Average percentage of omissions in a congruent sustained-attention task performed inrested wakefulness (RW) and sleep deficit (SD) conditions (n= 9, 120 trials/session).




sleep deficit was found to significantly stimulate only the appearance of errors of omission.

Dorrian et al. (2007) observed the effects of self-rated fatigue in train

drivers using a rail simulator. The results indicated a different pattern of errors depending on the level of fatigue. Under high-fatigue conditions,errors of omission increased, whereas errors of commission decreased, aphenomenon that Dorrian et al. explained as cognitive disengagement. Although the present study did not involve any workload causing fatigue,and followed very basic visual attention processes, an analogous effect (of increased omissions and decreased commissions) was observed, especiallyunder sleep deficit conditions, during the daytime. It may be hypoth-esised that sleep deficit affects the individual’s interaction with theenvironment in a similar way as fatigue.

The results described above are not congruent with the classicaleffects listed among various cognitive performance consequences of sleepdeprivation studied using the PVT. This observation is also inconsistentwith the current concept of state instability (Doran et al., 2001), whichassumes lapses of performance and compensatory increases in effort,especially in highly motivated individuals. Thus, people exhibiting poorperformance increase their effort and may produce both correctresponses and errors of commission. It may be that participants in thepresent study, although highly motivated, failed the challenge of sustained-attention in subsequent sessions and disengaged from the task.

The results also found a significant prevalence of omissions during themid-afternoon for both the congruent and incongruent stimuli in SD com-pared to RW subjects. This period—also referred to as the post-lunch dipin performance—has attracted much attention (e.g., Campbell, 1992;Carskadon & Dement, 1992; Wever, 1985). Based on a series of laboratorytests, Lavie (1986) confirmed the occurrence of a two-phase cycle of sleepi-ness in which the first strongly experienced phase of sleepiness occurred between 01:00 and 06:00 h, whereas the second, less intense phaseoccurred in the mid-afternoon. Strogatz et al. (1987) conducted laboratory

studies using a procedure of free-running methodology and likewise foundthat the sleepiness experience had a bi-phase character. In this study, par-ticipants experienced sleepiness most sharply when body temperaturedropped significantly: the very early morning hours. Other research(Owens et al., 2000) suggested that afternoon sleepiness was felt most inten-sely between the 8th and 9th h following the moment of waking.

Recent EOG and functional magnetic resonance imaging (fMRI)studies (Fafrowicz, 2006, 2008) investigating the effects of time-of-day onattention disengagement also support the ‘post-lunch dip’ hypothesis andsuggested that a period of decreased alertness occurs 8–9 h after usual

wakening time. Based on our finding that the dip in performance of asustained attention task during the mid-afternoon hours, we suggest this




may be attributed to the effect of circadian factor and exacerbated byhomeostatic mechanisms (sleep debt).

In the present study, 7 days of partial sleep deprivation was shown to

impair performance on a sustained-attention task, manifesting itself in agrowing number of omission errors. A significantly higher level of omis-sions, associated with deficits in top-down attention mechanisms, wasobserved at 14:00 h. This finding suggests there is a critical time-of-daywhen stronger attention performance decrease occurs than at other times.This performance decrement in sustained-attention task during the mid-afternoon hours has potentially serious implications for work safety.

The experimental protocol used in the present study represents arelatively new approach to the investigation of sustained attention.Performance based on saccadic eye movements requires voluntary control

of elementary cognitive processes. Although it is widely known that nosingle task covers a single cognitive process, tasks are frequently con-sidered as if they were, in themselves, pure cognitive processes. Thechallenge in identifying all cognitive processes associated with a givenexperimental task is that all of them are ‘dirty’ (Firth et al., 2004), that is,they do not examine a single process. Our protocol addresses this issue by focussing on visual attention only and, thus, it provides a more precisemethodological approach. Another promising approach in studying vigi-lant attention is linked with the development of neuroimaging tech-niques. According to Chee and coworkers (2008), performance lapsesduring rested wakefulness and in sleep-deprivation conditions are similarfrom a behavioral perspective, but exhibit different neural activation

FIGURE 5 Average percentage of commission errors during performance of a congruent sustainedattention task in rested wakefulness (RW) and sleep deficit (SD) conditions (n= 9, 120 trials/session).




patterns. Therefore, further research should focus on applying neuroima-ging data while continuing to analyze changes in cognitive processes.

ACKNOWLEDGMENTS

The research work detailed in this study was supported by a grantfrom the Polish Ministry of Science and Higher Education N N106283935 (2008–2011).

Declaration of Interest: The authors report no conflicts of interest.The authors alone are responsible for the content and writing of thepaper.

REFERENCES

Åkerstedt T, Gillberg M. (1990). Subjective and objective sleepiness in the active individual. J. Neurosci. 52:29–37.

Åkerstedt T, Ingre M, Kecklund G, Folkard S, Axelsson J. (2008). Accounting for partial sleep depri-vation and cumulative sleepiness in the three-process model of alertness regulation. Chronobiol.

Int. 25:309–319. Axelsson J, Kecklund G, Åkerstedt T, Donofrio P, Lekander M, Ingre M. (2008). Sleepiness and

performance in response to repeated sleep restriction and subsequent recovery during semi-laboratory conditions. Chronobiol. Int. 25:297–308.

Campbell SS. (1992). The timing and structure of spontaneous naps. In Stampi C. (ed.). Why we nap:

evolution, chronobiology, and function of polyphasic and ultrashort sleep. Boston: Birkhauser, pp.71–81.

Carskadon MA, Dement WC. (1992). Multiple sleep latency tests during the constant routine. Sleep

15:396–399.Casagrande M, Martella D, Di Pace E, Pirri F, Guadalupi F. (2006). Orienting and alerting: effect of

24 h prolonged wakefulness. Exp. Brain Res. 171:184–193.Chee MWL, Chuach LYM, Venkatraman V, Zen Chan W, Philip P, Dinges DF. (2006). Functional

imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation:correlations of fronto-parietal activation with performance. NeuroImage 31:419–428.

Chee MWL, Chow Tan J, Zeng H, Parimal S, Weissman DH, Zagorodnov V, Dinges DF. (2008).Lapsing during sleep deprivation is associated with distributed changes in brain activation. J. Neurosci. 28:5519–5528.

Corbetta M, Shulman GL. (2002). Control of goal-directed and stimulus driven attention in the brain. Nat. Rev. 3:201–215.

Doran SM, Van Dongen HPA, Dinges DF. (2001). Sustained attention performance during sleepdeprivation: evidence of state instability. Arch. Ital. Biol. 139:253–267.

Dorrian J, Rogers NL, Dinges DF. (2005). Psychomotor vigilance performance: neurocognitive assaysensitive to sleep loss. In Kushida CA. (ed.). Sleep Deprivation. Clinical issues, pharmacology, and sleep loss effects. New York: Marcel Dekker, pp. 39–70.

Dorrian J, Roach GD, Fletcher A, Dawson D. (2007). Simulated train driving: fatigue, self-awarenessand cognitive disengagement. Appl. Ergon. 38:155–166.

Durmer JS, Dinges DF. (2005). Neurocognitive consequences of sleep deprivation. Semin. Neurol.

25:117–129.Fafrowicz M. (2006). Operation of attention disengagement and its diurnal variability. Ergonomia

IJEH. 28:13–32.Fafrowicz M, Marek T. (2007). Neuronal attention networks, task demands, and human error. Occup.

Ergon. 7:73–81.




Fafrowicz M, Golonka K, Marek T, Mojsa-Kaja J, Tucholska K, Oginska H, Urbanik A, Orzechowski T.(2008). Diurnal variability of attention disengagement process—EOG and fMRI studies. InKarwowski W, Salvendy G. (eds.). Conference Proceedings. 2008 Applied Human Factors and Ergonomics

Conference (AHFE). USA Publishing, pp. 1–9.

Fan J, Raz A, Posner MI. (2003). Attentional Mechanisms. In Aminoff MJ, Daroff RB. (eds.). Encyclopedia of neurological sciences. New York: Elsevier Science, pp. 292–299.Firth C, Gallagher H, Maguire E. (2004). Mechanism of control. In Frackowiak SJ, Friston KJ, Frith

CD, Dolan RJ, Price CJ, Zeki S, Ashburner J, Penny W. (eds.). Human brain function. New York:Elsevier Science, pp. 329–362.

Johns MW. (1991). A new method for measuring daytime sleepiness: the Epworth Sleepiness Scale.Sleep 14:540–545.

Lavie P. (1986). Ultrashort sleep—waking schedule. “Gates” and “forbidden zones” for sleep. Electroenceph. Clin. Neurophysiol. 63:934–944.

Lim J, Dinges DF. (2008). Sleep deprivation and vigilant attention. Ann. N. Y. Acad. Sci. 1129:305–322.Miccoli L, Versace F, Koterle S, Cavallero C. (2008). Comparing sleep-loss and sleep inertia: lapses

make the difference. Chronobiol. Int. 25:725–744.Oginska H, Pokorski J, Oginski A, Pietsch E. (2000). Predicting individual shiftwork tolerance –

practical aspects. In Marek T, Oginska H, Pokorski J, Costa G, Folkard S. (eds.). Shiftwork 2000 — implications for science, practice, and business. Krakow: Jagiellonian University, pp. 267–292.

Owens DS, Macdonald I, Tucker P, Sytnik N, Totterdell P, Minors D, Waterhouse J, Folkard S.(2000). Diurnal variations in the mood and performance of highly practiced young womenliving under strictly controlled conditions. Br. J. Psychol. 91:41–60.

Portaluppi F, Touitou Y, Smolensky MH. (2008). Ethical and methodological standards for laboratoryand medical biological rhythm research. Chronobiol. Int. 25:999–1016.

Posner MI. (1980). Orienting of attention. Q. J. Exp. Psychol. 41A:19–45.Rogers NL, Dorrian J, Dinges DF. (2003). Sleep, waking and neurobehavioural performance.

Frontiers Biosci. 8:1056–1067.Strogatz SH, Kronauer RE, Czeisler CA. (1987). Circadian pacemaker interferes with sleep onset at

specific times of day: role of insomnia. Am. J. Physiol. 253:R172–R178.Sturm W, Willmes K. (2001). On the functional neuroanatomy of intrinsic and phasic alertness.

NeuroImage 14:S76–S84.Thayer RE. (1989). The biopsychology of mood and arousal. New York: Oxford University Press,

Appendix I.Van Dongen HPA, Maislin G, Mullington JM, Dinges DF. (2003). The cumulative cost of additional

wakefulness: dose-response effect on neurobehavioral functions and sleep physiology fromchronic sleep restriction and total sleep deprivation. Sleep 26:117–126.

Vecera SP, Rizzo M. (2003). Spatial attention: normal processes and their breakdown. Neurol.

Clin. N. Am. 21:575–607.Wever RA. (1985). Men in temporal isolation: basic principles of the circadian system. In Folkard S,

Monk TH. (eds). Hours of work: temporal factors in work scheduling. Chichester: J. Wiley & Sons,pp. 15–28.




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