Intern. J. Neuroscience, 116:11251138, 2006Copyright C 2006 Informa HealthcareISSN: 0020-7454 / 1543-5245 onlineDOI: 10.1080/00207450500513922

EFFECTS OF SLEEP DEPRIVATION ON LATERALVISUAL ATTENTION

ATHENA P. KENDALLMARY A. KAUTZWalter Reed Army Institute of ResearchSilver Spring, Maryland, USA

MICHAEL B. RUSSOUnited States Army Aeromedical Research LaboratoryFort Rucker, Alabama, USA

WILLIAM D. S. KILLGOREWalter Reed Army Institute of ResearchSilver Spring, Maryland, USA

Sleep loss temporarily impairs vigilance and sustained attention. Because thesecognitive abilities are believed to be mediated predominantly by the right cerebralhemisphere, this article hypothesized that continuous sleep deprivation resultsin a greater frequency of inattention errors within the left versus right visualfields. Twenty-one participants were assessed several times each day during a40-h period of sustained wakefulness and following a night of recovery sleep.At each assessment, participants engaged in a continuous serial addition task whilesimultaneously monitoring a 150 visual field for brief intermittent flashes of light.Overall, omission errors were most common in the leftmost peripheral field for

Received 9 June 2005.The views expressed in this article are those of the authors and do not reflect the official policy

or position of the Department of the Army, the Department of Defense, the U.S. Government, orany of the institutions with which the authors are affiliated.

Address correspondence and reprint requests to MAJ William D. S. Killgore, Ph.D.,Department of Behavioral Biology, Division of Psychiatry and Neuroscience, Walter ReedArmy Institute of Research, 503 Robert Grant Avenue, Silver Spring, MD 20910, USA. E-mail:william.killgore@na.amedd.army.mil

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all sessions, and did not show any evidence of a shift in laterality as a functionof sleep deprivation. Relative to rested baseline and postrecovery conditions, sleepdeprivation resulted in a global increase in omission errors across all visual locationsand a general decline in serial addition performance. These findings argue againstthe hypothesis that sleep deprivation produces lateralized deficits in attention andsuggest instead that deficits in visual attention produced by sleep deprivation areglobal and bilateral in nature.

Keywords attention, cognition, laterality, right-hemisphere, sleep deprivation,vigilance, visual field, visual perception

Normal, healthy individuals need adequate sleep for optimal cognitivefunctioning (Himashree et al., 2002). Without adequate sleep, humansshow reduced alertness (Penetar et al., 1993) and impairments in cognitiveperformance (Thomas et al., 2000, 2003). Prolonged sleep deprivation isassociated with decrements in elementary cognitive abilities such as vigilanceand sustained attention (Doran et al., 2001; Wesensten et al., 2004), as wellas impairments in complex, higher-order cognitive processes such as verbalfluency, logical thought, decision making, and creativity (Harrison & Horne,1997, 1999, 2000). In occupational settings such as aviation, air traffic control,and sustained military operations where constant vigilance is a necessity,extended periods of sleep loss have been associated with catastrophic accidents(Mitler et al., 1988) and may have been a factor in some friendly fire incidents(Belenky et al., 1994). Studies of sleep-deprived individuals show that errorsattention begin to emerge by 19 h of continuous wakefulness (Russo et al.,2004) and cognitive performance declines at a rate of approximately 25% foreach 24-h period of wakefulness (Belenky et al., 1994).

Sleep deprivation produces global decreases in cerebral metabolism andblood flow, with the greatest declines evident in those regions critical for higherorder cognitive processes (Thomas et al., 2000). These regions, the heteromodalassociation cortices, are associated with attention, vigilance, and complexcognitive processing, and reductions in activity within these regions areassociated with decrements in these higher-order cognitive process (Mesulam,1999). As a global blood flow and metabolic activity decline during prolongedperiods without sleep, the brain appears to compensate by recruiting cognitiveresources from nearby brain regions within the prefrontal and parietal corticesin order to maintain cognitive performance at acceptable levels (Drummondet al., 2001). Some evidence suggests that these compensatory activities maybe particularly prominent within the right cerebral hemisphere (Drummondet al., 2001). Consistent with these reports, other studies suggest that cognitive

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processes mediated by the right hemisphere are more adversely affected bysleep deprivation than those mediated by the left (Johnsen et al., 2004; Pallesenet al., 2004).

Neuropsychological evidence suggests that the right cerebral hemisphere isdominant for attentional processes (Heilman & Van Den Abell, 1980; Mapstoneet al., 2003). Much of the evidence supporting the dominance of the righthemisphere in attention comes from studies of patients with unilateral braindamage (Heilman & Van Den Abell, 1980; Weintraub & Mesulam, 1987).Lesions to the right cerebral hemisphere are more likely to produce contralateralhemispatial neglect than similar lesions to the left hemisphere (Behrmann et al.,2004; Mapstone et al., 2003, Mesulam, 1999). Further evidence supporting theprominent role of the right hemisphere in attentional processing comes fromseveral functional neuroimaging studies that reveal greater right hemisphereactivity in response to tasks requiring allocation of spatial attention (Fink et al.,2001; Macaluso et al., 2001). The accumulating evidence suggests that the leftcerebral hemisphere allocates its attentional processing predominantly towardthe contralateral (i.e., right) hemispace, whereas the right hemisphere appearsto distribute attentional processing more equally between both hemispaces, andis therefore considered dominant for attention (Mesulam, 1999). Consequently,the phenomenon of contralesional neglect occurs nearly exclusively followinglesions to the right hemisphere.

Given the apparently greater role of the right hemisphere in attentionalprocessing and the preliminary evidence that the cognitive processes mediatedby the right hemisphere may be more sensitive to the detrimental effects of sleepdeprivation, it was hypothesized that prolonged sleep loss results in greaterimpairment of right hemisphere visual attention mechanisms oriented towardthe contralateral (i.e., left) perceptual hemispace. Participants were assessedseveral times each day while remaining awake for 40 h. During each 15-mintesting session, participants monitored a 150 arc of lateral visual space forperiodic occurrences of brief flashes of light while simultaneously performinga continuous serial addition task.

METHODSubjectsTwenty-one active duty military personnel (9 females; 12 males; M age = 28.2,SD = 5.5) participated in the study. Volunteers were recruited through word ofmouth and flyers posted at the Walter Reed Army Institute of Research. Visual

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acuity was assessed prior to entry with a standard Snellen Chart. Screeningcriteria required distant acuity of 20/20 and near acuity of 20/25 withoutrefractive correction or from +1.00 D.S. to 3.00 D.S. with correction to20/20. All participants were in good physical health, had no evidence of acurrent sleep disorder, and were free of any history of neurologic, psychiatric, orserious medical condition, as determined by the study physician. All potentialvolunteers consented to a urine drug screen and were excluded if there wasany evidence of use of illegal substances or stimulants. Volunteers were alsoexcluded if they regularly consumed more than 300 mg of caffeine per day.Financial compensation was provided for participation in the study and allprocedures were conducted in accordance with the requirements of the HumanUse Committee at Walter Reed Army Institute of Research and the SurgeonGenerals Human Subjects Research Review Board.

ApparatusIn order to assess divided attention capacities, participants were required toengage in two demanding attentional tasks simultaneously. Attention to visualstimuli within the lateral visual field was assessed with the Choice VisualPerception Task (CVPT). The CVPT consists of a horizontal U-shaped barfitted with 11 light-emitting diodes (LEDs) located at 15 increments aroundthe arc (see Figure 1). The arc was placed at eye level and the center diode waslocated 18 inches from the bridge of the nose of the participant. RemainingLEDs were located in the left and right visual fields at 15 intervals (i.e.,L75, L60, L45, L30, L15, C, R15, R30, R45, R60, and R75). The task wasperformed against a black backdrop and ambient room light was maintained atapproximately 5 foot candles to ensure uniform visibility of the stimuli. A chinrest was used to stabilize head movement and volunteers were instructed tomaintain visual fixation on a focal point presented on a laptop computer. Eachstimulus appeared for 250 ms, with an interstimulus interval varying from 3.50to 15.25 s for each trial. Fifteen variations of visual stimuli were presentedrandomly 10 times for a total of 150 stimulus presentations for each trial.Each administration of the CVPT lasted 15 min. For single LED presentations,responses were made via a keypad with buttons for left, center, and right,corresponding to the location of the stimulus.

Double simultaneous stimuli were also presented on 40 trials. Thesepresentations always included the center stimulus (C) and an additional stimuluslocated within the left or right peripheral field (i.e., C+L75, C+L60, C+R60,and C+R75). During presentations of double simultaneous stimuli, responses

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Figure 1. An example of a participant engaged in the Choice Visual Perception Task (CVPT) andSerial Addition Test (SAT). The SAT was presented on a laptop computer placed in front of theparticipant. The CVPT apparatus includes a laterally placed U-shaped bar with light emitting diodesplaced at 15-degree intervals around a 150 degree arc of the visual field. Participants completedthe SAT continuously while monitoring the CVPT for intermittent light flashes.

were made by pressing the two corresponding buttons simultaneously (e.g.,center and right keys). All volunteers were instructed to use their right-handfor the keypad response, regardless of reported handedness. Hits, misses, andresponse omissions were recorded for each stimulus presentation.

In conjunction with continuous monitoring of the light locations of theCVPT, participants were required to sustain continuous performance on a SerialAddition Task (SAT). During the SAT, participants were required mentallyto add sequences of single digit numbers that were presented on the screenand then vocally report the answers for each trial. During each sequence, anumber from 0 to 9 would appear on the screen for 750 ms, which would beimmediately replaced by a plus-sign (+) for 750 ms, then a second number,followed by an equal sign ( = ). At the presentation of the equal sign, theparticipant would vocally report the sum of the preceding two digits. The

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SAT stimuli were presented three inches below the center LED on a 15-inch(diagonal) computer screen placed immediately below the CVPT. The targetstimuli were presented in 72-point bolded Tahoma font at a screen resolutionof 1024 768 pixels. Participants were required to continuously engage inthe SAT while simultaneously monitoring the CVPT for periodic stimulusoccurrences.

Design and ProcedureEach study run was conducted over two consecutive weeks. On the first day(Monday) of the baseline phase, volunteers reported to the sleep laboratoryat approximately 0945. Each volunteer was fitted with an actigraph watch,given a sleep log to record their daily sleep habits, and reminded to abstainfrom caffeine, alcohol, and tobacco products. On that same day, the volunteerswere trained on a battery of neuropsychological tests and the CVPT-SAT.Baseline testing concluded at approximately 1130. The residential phase beganthe following week.

Volunteers arrived at the sleep laboratory at 0800 to begin the residentialphase. The residential phase involved a second baseline testing session, 40 hof sleep deprivation, 9 h of recovery sleep, and a postrecovery sleep testingsession. On day 1 (Monday), subjects completed CVPT-SAT at 2-h intervalsto provide a second rested baseline measure. Starting at 24:00 (midnight)volunteers received 8 h time in bed. The 40 h sleep deprivation period beganwhen participants awakened at 0800 on day 2 (Tuesday). Volunteers remainedawake until 2400 (midnight) on Day 3 (Wednesday). Throughout the course ofthe sleep deprivation period, the CVPT-SAT was administered at 2-h intervals.After the 40 h sleep deprivation period was concluded, each volunteer received9 h of time in bed to obtain recovery sleep. On Thurs (day 4) volunteerswere awakened at 0900, were retested twice on the CVPT-SAT, debriefed, andreleased from the study at 18:00. Each CVPT-SAT administration lasted for 15min.

Data AnalysisTo control for the effects of circadian influences, data were averaged andcompared across blocks of time encompassing the same time periods eachday (i.e., 1500, 1700, and 1900). For each trial, the number of single anddouble stimulus response omissions was calculated and averaged across trialsfor each session. Similarly, the percentage correct for each trial of the serial

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addition task was calculated and averaged across trials for each session. Datawere analyzed using repeated measures analysis of variance, with Greenhouse-Geisser corrections for lack of sphericity. Stimulus location within the visualfield (11 locations) and testing session (4 sessions) were entered as repeatedmeasures variables. The criterion for significance was set at = .05. Becausea greater number of errors were hypothesized within the leftmost peripheralfield as a consequence of sleep deprivation, the authors conducted plannedcomparisons between the number of errors at the leftmost peripheral location(L75) versus the central (C) and rightmost peripheral (R75) sites, with =.05, uncorrected. Post hoc comparisons were conducted using a Bonferronicorrection to = .05 for experiment-wise error rate.

RESULTS AND DISCUSSIONAccumulating evidence suggests that sleep deprivation affects lateralizedprocessing of stimuli (Iskra-Golec, 2001), and may be particularly disruptive tocognitive and perceptual processes that involve the right hemisphere (Johnsenet al., 2002; Pallesen et al., 2004). It was predicted, therefore, that sleep depri-vation is associated with a general decline in alertness and attention to visualstimuli and that these deficits would be most evident within the left peripheralvisual field. There was a significant main effect of session, (F3,60 = 45.18, p