sleepiness and performance in narcolepsy

J. Sleep Res. (1996) 5, 128–134

Sleepiness and performance in narcolepsy

B E R N A D E T T E H O O D and D O R O T H Y B R U C KVictoria University of Technology, Victoria, Australia.

Accepted in revised form 10 April 1996; received 10 July 1995

SUMMARY Previous attempts to investigate the relationship between sleepiness and performancefor subjects with narcolepsy have been limited by both the ability of narcolepticsubjects to contain their sleepiness for brief testing periods and the potential lack ofsensitivity of routine performance tasks to sleepiness induced changes. The presentstudy developed a research protocol which allowed subjects with narcolepsy to expressstates of sleepiness and non sleepiness and to then compare the performance ofsubjects with narcolepsy to age, gender and IQ matched controls on tasks evaluatingautomatic, attentional and complex cognitive functioning. The results indicated thatat high arousal subjects with narcolepsy performed as well as controls on automatictasks suggesting that the capacity to perform for narcolepsy subjects is not restrictedby physiological factors but is secondary to the effects of sleepiness. Comparison ofboth the within subject effects for narcolepsy subjects of the transition between highand low arousal states, and the between subject effects of low arousal for narcolepsysubjects compared to controls indicate that complex cognitive tasks are the mostsensitive to arousal fluctuation. This study provides support for the subjectiveexperiences of subjects with narcolepsy of diminished cognitive function associatedwith the disorder.

induced sleepiness, narcolepsy, performance, sleep

INTRODUCTION restorative sleep. Horne (1988) further combines the attentionaland cognitive models proposing that performance decrements

In the one hundred years since Patrick and Gilbert (1896)associated with sleepiness can initially be compensated for by

reported on performance decrements associated withincreased attentional resources, but beyond some critical level

experimentally induced sleepiness in non clinical subjects, there of sleepiness, subsequent performance decrements are onlyhas been extensive interest in the physiological processes reversed by restorative sleep. The tasks most dependent onmediating the relationship between sleepiness and cognitive restorative sleep are those that assess more complex cognitivedysfunction. Two major theoretical models have evolved; function (Horne 1988).attentional and cognitive. Proponents of the attentional model Narcolepsy is a disorder characterized by excessive and(Kjellberg 1977a,b,c; Meddis 1982) argue that performance pervasive daytime sleepiness and therefore there is considerabledecline, associated with sleepiness, occurs as a function of the face validity to the suggestion that this sleepiness would leaddiminished attentional factors that sleepy subjects apply to to observable decrements in performance, in just the samea task. The implication of this model is that sleep-induced way as sleepiness leads to performance decrements in normalperformance decrements are reversible and contingent on populations. Subjective reports from narcoleptic subjectsbehavioural resources, such as attention or motivation. In support this prediction with over 40% of narcoleptics reportingcontrast, theorists supporting a cognitive model (Horne 1988) impaired memory function since the onset of the disordersuggest that sleepiness leads to fundamental changes in sensory (Broughton and Ghanem 1976).and cognitive processing capacity. These cognitive changes are Since the early 1980s there have been several studies thatnot reversed by compensatory effort but are contingent on have attempted to demonstrate the relationship between

sleepiness and performance for narcoleptic subjects (Broughtonet al. 1982; Aguirre et al. 1985; Levander and Sachs 1985;Correspondence: Bernadette Hood, Department of Psychology, VictoriaGodbout and Montplaisir 1986; Ollo et al. 1987; Henry et al.University (St Albans), PO Box 14428 MCMC, Melbourne, Victoria,

Australia 8001. Fax:+61/ 3 93652218; tel.:+61/ 3 93652334. 1988; Rogers and Rosenberg 1990; Pollack et al. 1992; Smith

1996 European Sleep Research Society128

Sleepiness and performance in narcolepsy 129

et al. 1992; Henry et al. 1993). The findings surrounding these be demonstrated experimentally, what is the impact of thatsleepiness on performance for narcolepsy subjects?studies, reflect the same theoretical dilemma that pervades2 If sleepiness for narcolepsy subjects is associated withthe general sleep deprivation literature – are performanceperformance decrements are attentional or complex processingdecrements in narcolepsy explained by attentional or cognitivetasks most sensitive to these sleepiness effects?; andmechanisms? Aguirre et al. (1985), Ollo et al. (1987), and3 Under conditions of high arousal or non sleepiness doRogers and Rosenberg (1990), would argue that performancesubjects with narcolepsy demonstrate diminished performancedecrements in narcolepsy have no organic base, but occur ason tasks measuring tonic arousal capacity compared to controls?a consequence of diminished attentional resources, that are

secondary to narcoleptic sleepiness. Performance decrementscan therefore be compensated for by increased attentional METHODeffort. This attentional model is supported by the finding that

Subjectsnarcoleptics perform as effectively as controls in stimulatingtest environments (Aguirre et al. 1985; Rogers and Rosenberg Eight narcolepsy subjects participated in the experiment. All1990), but demonstrate performance decrements for repetitive subjects had specialist diagnosis of narcolepsy and met theand monotonous tasks, such as vigilance tasks, where there is International Classification of Sleep Disorders (1990) criteriaminimal motivation to apply compensatory effort (Valley and of excessive daytime sleepiness with the presence of recurrentBroughton 1983). However, the diminished performance of daytime naps and unequivocal cataplexy. The group comprisednarcoleptics on vigilance tasks could be explained within an seven females and one male subject. The age of the narcolepticalternative paradigm. On the basis of psychophysiological data subjects ranged from 28 y to 72 y with a mean age of 53 y (SD=Levander and Sachs (1985) suggest that narcoleptics may have 12.5). IQ scores of narcoleptics were determined using the K-a decreased tonic or habitual arousal state. Automatic tasks, Bit Brief Intelligence Scale (Kaufman and Kaufman 1990) andsuch as vigilance tasks, that tap into tonic arousal capacity, scores ranged from 93 to 123 with a mean score of 102 (SD=would then demonstrate performance decrements in 11.35). Of the eight narcolepsy subjects six were normally takingcomparison to controls. Additional support for this model stimulant medication: Dexamphetamine (N1, N3, N5),comes from the findings of Henry et al. (1988), and Henry et Methylphenidate (N2,N7)andMazidol (N8).Ascentralnervousal. (1993), who demonstrated that unmedicated narcoleptics system stimulant medication interferes with both arousal, andhad significantly increased response latencies on the Sternberg cognitive performance measures, subjects were requested toscanning task, suggesting a deficit in perceptual encoding withdraw from stimulants a minimum of 18 h prior to testing.capacity, consistent with diminished tonic arousal levels. This withdrawal period provided a compromise between

A methodological confound to many of the studies evaluating minimizing both the effects of stimulant confounds and the levelsubjective reports of performance decrements in narcolepsy is of disruption to subjects’ daily functioning. All otherthat narcoleptics are clearly able to contain their sleepiness medications, including tricyclic antidepressants, were continuedfor brief testing periods and often fail to demonstrate any throughout the test period. Any residual effects of medicationbehavioural signs of sleepiness during testing sessions (Aguirre were not considered to effect the validity of the study as theet al. 1985; Henry et al. 1993). Previous evaluations of the emphasis of the analysis relates to within subject changes inrelationship between performance and sleepiness in narcolepsy performance in a repeated measures, pre and post naphave operationalised sleepiness through either electro- experimental design. Measures of baseline arousal, free of anyphysiological definitions such as electroencephalography effects of medication, were therefore not critical to the study.(Valley and Broughton 1983; Rogers and Rosenberg 1990; Eight control subjects were selected from acquaintances ofPollack et al. 1992) and evoked potential measures (Broughton the experimenter and matched with narcoleptic subjects on theet al. 1982; Ollo et al. 1987), or behavioural (Aguirre et al. variables of gender, age (within an arbitrarily defined seven1985), or physiological parameters (Levander and Sachs 1985; year range), and IQ (within the 95% IQ confidence interval ofHenry et al. 1993). It is difficult to establish whether the often the narcoleptic subject). Although educational status has alsovery brief changes in narcolepsy arousal states identified by been demonstrated to effect performance measures, it was notthese measures reflect the day to day experience of sleepiness included as a matching variable in this study, as narcolepsyfor narcoleptics, and researchers have therefore questioned the has been demonstrated to substantially impair educationalexternal validity of laboratory based performance findings for attainment (Kales et al. 1982). Control subjects were screened tothis clinical population (Rogers and Rosenberg 1990; Rogers exclude subjects reporting nightime sleep disruptions, daytimeand Aldrich 1993). sleepiness or depression. One control subject (C6) was on

The present study aimed to establish a test protocol which medication for angina at the time of testing and this medicationallowed cognitive testing of narcolepsy subjects under stable was continued over the test period.states of sleepiness and non sleepiness, and to evaluate theeffect of sleepiness on performance for narcolepsy subjects

Apparatus and Procedureacross a range of cognitive tasks.

Three specific research questions were addressed: Testing was carried out at the Victoria University SleepLaboratory. The laboratory is a two-bedroom temperature-1 If changes in levels of sleepiness for narcolepsy subjects can

1996 European Sleep Research Society, J. Sleep Res., 5, 128–134

130 B. Hood and D. Bruck

Figure 1. Schematic representation of testingschedule for subjects with narcolepsy. LA, lowarousal, HA, high arousal.

controlled facility shielded from the external environment. Control subjects demonstrated no behavioural signs ofsleepiness across testing sessions though this observation wasFigure 1 provides an overview of the testing schedule.not quantified in the present study.Subjects attended the laboratory the night prior to testing and

their overnight sleep was recorded, using standard recordingmeasures (Rechtschaffen and Kales 1968). The testing day Performance tasksincorporated four testing sessions with each session being

Tasks were selected on theoretical grounds to test automaticdivided into a low arousal (LA) and high arousal (HA)(reaction time, Stroop dots and physical match); attentionalcondition. The period prior to low arousal testing was(digit symbol substitution, Rey Auditory Verbal Learning Task,structured in line with the protocol demonstrated by Volk etD2 concentration endurance task), and complex cognitiveal. (1984) to provide an environment facilitating low arousalfunctioning (word fluency, paced auditory serial addition task,conditions. The initial 25 min of the low arousal inductioncomplex semantic reasoning, Stroop colours and semanticinvolved subjects having free quiet time. Subjects used thismatching). Where possible brief tasks were selected to minimizetime to read or listen to music. For the 15 min immediatelyfatigue effects. Administration and scoring of the Stroop, digitprior to LA testing subjects completed the WAVT task whichsymbol, Rey Auditory Verbal Learning task (RAVLT), wordhas been demonstrated to be a sleep inducing task forfluency, D2 concentration endurance task (D2), and the pacednarcoleptic subjects (Valley and Broughton 1983). Subjectsauditory serial addition task (PASAT) followed standardwere observed during this period and were wakened if anyprotocols recommended by Spreen and Strauss (1991). Repeatbehavioural signs of sleepiness occurred. Following thisadministrations of the Stroop, RAVLT and the word fluency

manipulation subjects completed a 20 min LA test block.task utilized published alternate versions. Additional tasks

Testing sessions were limited to this period to minimize theincluded a two choice reaction time measure and two

effect of fatigue on performance scores. Directly following thecomputerized cognitive tasks that assessed the speed of visual

testing period narcolepsy subjects were given the opportunityand semantic processing and response latencies for simple

to nap for 30 min. The literature demonstrates that naps haveand complex semantic reasoning tasks. Full details of these

an alerting effect on narcolepsy subjects (Roehrs et al. 1984)computerised cognitive tasks are given in Levy et al. (1979).

and that naps as short as 15 min may be as refreshing as moreextended nap durations (Roehrs 1985). In line with the findings

Test presentationof Mullington and Broughton (1994) a refractory period wasincluded, following the nap, and before HA testing, to allow Since narcolepsy is associated with high intersubject variabilitynarcolepsy subjects to achieve full alertness. The tasks in arousal a repeated-measures experimental design was usedpreviously presented in the LA test period were then repeated and all narcolepsy subjects completed the performance tasksunder HA conditions. This sequence of LA and HA under both low and high arousal conditions. To control formanipulation for testing was repeated for four test blocks both order and differential carry over effects test presentationacross the day, with tasks evenly distributed between testing was counterbalanced using a digram balanced Latin squaresessions. To assess the effectiveness of the arousal manipulation, design (Wagenaar 1969). However, the sequence of arousalnarcolepsy subjects completed a visual analogue scale (VAS) fluctuation was not counterbalanced, and all tasks weremeasure of subjective sleepiness prior to each test session. The completed at low and then high arousal. This low arousal/highscale line was 100 mm in length with anchor points of 0 mm= arousal order of testing was maintained to allow for direct,lost struggle to remain awake, and 100 mm=alert wide awake. practice-free comparison of performance scores between lowControl subjects completed a similar testing protocol, but no arousal narcoleptics and controls. For the comparison of highattempts were made to manipulate their arousal condition so arousal scores of narcolepsy subjects compared to controls,the WAVT was not utilized with the control group. No structure performance for both subject groups, represented the secondwas imposed on control subjects’ use of time between testing testing session, and practice effects were considered equated

between groups.sessions, except that no naps were permitted across the day.



Data analysis attentional task also demonstrated a 14% increment under thehigh arousal condition and the automatic tasks of physical

All data were analysed using SPSSx. Discriminant functionmatch and Stroop dots demonstrated residual arousal effects

analyses were used to identify the tasks which were the mostof five and eight percentage, respectively.

powerful discriminators between experimental groups.

(ii) Comparative performance on attentional and complex tasks,RESULTS

between narcolepsy subjects at low arousal and controlsManipulation of arousal

To evaluate the tasks most sensitive to sleepiness for subjectswith narcolepsy a stepwise discriminant function analysis wasEach narcolepsy subject was asked to complete the VASperformed using the attentional and complex performancesleepiness rating on eight occasions. Four of these ratingstasks as predictors of the grouping variables of narcolepsyrepresented manipulated low arousal conditions and foursubjects at low arousal, and control subjects. For both groupsmanipulated high arousal conditions. Of the possible 64 ratingsperformance scores represented the first testing session and52 were completed by subjects, with the missing data equallywere therefore free of practice effects. To meet the criterion ofdistributed between arousal conditions. For the low arousaldiscriminant analysis that the number of predictor variablesmanipulation the mean arousal rating was 27.35, SD=19.62,be less than the group sample size (Tabachnick and Fidelland for the manipulated high arousal condition the mean1989), the variables of STM and LTM were excluded from thearousal rating was 74.73, SD=17.55. Dependent t-test analysesdiscriminant analysis, as they demonstrated no clear residualof these findings demonstrated a significant difference betweenarousal effect (Table 1). The predictor variables included inarousal conditions, t25=12.13, P=0.000.the analysis were digit symbol, word fluency, PASAT, Stroopcolours, complex reasoning and semantic match.

Performance measuresThe calculated discriminant function was highly significant

with a v23=18.36, P=0.0004. The function accurately classified(i) The impact of sleepiness on performance for narcolepsy

subjects group membership for 100% of cases. The structure matrix ofMean performance scores for narcolepsy and control subjects, correlations between predictors and the discriminant functionacross all performance tasks, are presented in Table 1. suggests that the best predictors for distinguishing between low

Descriptive statistical analyses of the data in Table 1 indicate arousal narcolepsy subjects and controls are the complex tasksthat with repeated testing of control subjects mean scores for of PASAT (−0.47635) and semantic matching (0.46395).10 of the 12 performance measures demonstrated an increment Narcolepsy subjects at low arousal have decreased performanceon the second testing session. The percentage change in on the PASAT (mean=19.12, SD=10.33) compared to controlsperformance scores between the two testing sessions, ranged (mean=30.12, SD=6.42) and took significantly longer tofrom five to 24 percent (column C), and provides an estimate complete the semantic matching task (mean=105.62, SD=of the level of practice associated with repeated testing. For 27.21) than controls (mean=78.37, SD=17.23).two tasks, long-term memory and complex reasoning, thesecond control testing session was associated with performance

(iii) Comparative performance on automatic tasks betweendecrements, possibly representing fatigue or interference effects.

narcolepsy subjects at high arousal and controlsRepeated testing of subjects with narcolepsy under LA andHA conditions led to increments in performance at the second A discriminant function analysis was performed using threetesting session for all tasks except both memory tasks, which tasks as predictors of membership between the two groups.demonstrated a performance decline under high arousal Predictors were the automatic tasks of reaction time, stroopconditions. The percentage increment in performance scores dots, and visual match. Groups were narcolepsy subjects, underfor narcolepsy subjects between low and high arousal conditions the high arousal condition, and controls. For both groups,(column F) provides an estimate of the cumulative effects of scores represented performance measures at the second testingboth practice and arousal change. Column G represents the session, and practice effects were therefore considered equatedresidual increment in performance for narcolepsy subjects, between groups.between low and high arousal conditions following the removal The calculated discriminant function was not statisticallyof practice effects. Of the 12 initial tasks completed by the significant with a v2

3=0.25, P>0.05. The tasks tappingsubjects with narcolepsy, seven demonstrate some performance automatic processing do not discriminate between controlincrement, free of practice, between low and high arousal subjects and narcoleptics at high arousal.testing conditions. Specifically the percentage change due toarousal fluctuation ranges from five to 75 percentage with

DISCUSSIONthe complex tasks of word fluency, semantic match, complexreasoning, and the PASAT demonstrating the greatest The present study aimed to explore the impact of sleepiness

on performance for subjects with narcolepsy in an experimentalsensitivity to arousal fluctuation with percentage increments athigh arousal of 14, 18, 28 and 75%, respectively. The D2 setting that allowed for the expression of behavioural states of



Table 1 Mean performance scores and percentage change for practice and sleepiness effects across all performance tasks.

A B C D E F G (F−C)

(Mean) (Mean) Practice (Mean) (Mean) Arousal+ ArousalCont 1 Cont 2 Effect % LA Narc HA Narc Prac Effect Effect

% %

AutomaticReaction time (s) 0.74 0.56 24 0.71 0.57 20 –Stroop dots (s) 13.71 13.04 5 15 13.07 13 8Physical match (msec) 89.75 71.25 21 90.5 67.13 26 5

AttentionalDigit symbol (total) 41.25 47.37 15 49.5 54.25 10 –D2 444.62 495.75 9 400.87 492 23 14Short termmemory (total) 5.87 6.37 9 6.12 6 −2 –

Lomg termmemory (total) 8.75 8 −9 8.62 8 −7 –

ComplexWord fluency(total) 42.37 47.87 13 33.12 42.12 27 14

PASAT (total) 30.12 32.37 7 19.12 34.87 82 75Stroop colours (s) 33.20 25.67 23 34.14 27.4 20 –Complex reasoning(msec) 562.25 588 −5 850.5 651.12 23 28

Semantic match(msec) 78.37 73.62 6 105.62 80.5 24 18

For tasks with time (msec s−1) as the outcome measure the percentage change score for practice (C) is derived from the percentage differenceof A–B, and the percentage change score associated with practice+sleepiness (F) is derived as a percentage difference of D–E. Where totalnumber of items correct (total) is the outcome variable the procedure is reversed, and the effect of practice (C) is derived from the percentagechange B–A, and the percentage change associated with practice+sleepiness (F) is derived from the percentage difference E–D. Residualpercentage sleepiness effect (G) always represents F–C.

sleepiness and non sleepiness. Visual analogue scale ratings of Rogers and Rosenberg (1990) that the consistent failureof research to demonstrate sleepiness associated performanceof sleepiness under the manipulated high and low arousal

conditions demonstrated a highly significant change in decrements for narcolepsy subjects may be partly explained bythe use of standardized tests which are insensitive to highersubjective sleepiness between conditions indicating the

effectiveness of the experimental manipulation. One criticism order cognitive functioning. The most sensitive measure ofsleepiness for narcolepsy subjects in the present study was theof the use of subjective sleepiness ratings is that they have

diminished validity for subjects with excessive daytime PASAT. This task measures central information processingcapacity and requires subjects to respond verbally to ansleepiness. Dement et al. (1978), suggest that this diminished

validity may occur as a consequence of chronically sleepy externally paced auditory addition task and simultaneouslyinhibit the automatic encoding of their response and direct theirsubjects losing an appropriate frame of reference by which to

measure their sleepiness state. This potential limitation of attentional resources to the next incoming stimulus (Spreen andStrauss 1991). As the task is externally paced subjects cannotsubjective rating scales is not, however, seen to invalidate the

findings of the present study where the effectiveness of the compensate for sleepiness by increasing the processing andresponse time. The divided attention and central processingarousal manipulation was evaluated as a consequence of

subjects’ estimations of change in their sleepiness state rather demands of the task may reflect everyday experiences ofcompeting cognitive demands, and sleepiness in narcolepsythan an absolute estimate of sleepiness.

For the narcolepsy subjects in the current study this may interfere with the capacity to respond to this cognitiveload. This finding may provide some objective support forexperimentally induced sleepiness was associated with

performance change across a range of tasks. Comparison of the subjective impressions of some people with narcolepsy ofdiminished cognitive capacity. Performance on the PASAT hasboth the within-subject effects for narcolepsy subjects, of the

transition between high and low arousal states, and the been shown to correlate with subjective ratings of cognitiveimpairment amongst other clinical groups (Gronwall 1976).between-subject effects of low arousal for narcolepsy subjects

compared to controls, indicate that complex cognitive tasks To determine whether narcolepsy is associated withdiminished habitual or tonic arousal levels, non sleepyare the most sensitive to arousal change for this clinical

population. This finding provides support for the conclusions narcoleptic subjects were compared to controls on automatic



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