Attention Bias for Sleep-Related Stimuli in Primary Insomnia and Delayed Sleep Phase Syndrome Using the Dot-Probe Task Kenneth M A MacMahon, PhD; Niall M Broomfield, PhD; Colin A Espie, PhD University of Glasgow Sleep Research Laboratory and Section of Psychological Medicine, Sackler Institute of Psychobiological Research, Southern General Hospital, Glasgow, Scotland, UK reported being good sleepers, and met no criteria for a current or previous sleep disorder. Interventions: N/A. Measurements and Results: As predicted, PI showed increased vigilance for sleep-related stimuli relative to GS and DSPS. No differences between GS and those with DSPS were found. The PI group showed shorter response latencies relative to the GS and DSPS groups. Conclusions: Results support an association between attention bias and PI. Further work must determine whether or not attention bias is a causal factor. Speeded responses in the PI group suggest heightened arousal, indicating that physiologic factors may play a related role. Keywords: Attention bias, insomnia, delayed sleep phase syndrome, cognitive arousal, circadian Citation: MacMahon KMA; Broomfield NM; Marchetti LM et al. Attention bias for sleep-related stimuli in primary insomnia and delayed sleep phase syndrome using the dot-probe task. SLEEP 2006;29(11):1420-1427. Study Objectives: Cognitive models of primary insomnia (PI) suggest attention bias as a maintaining process. This study used a hallmark measure of attention bias, the dot-probe task, to determine whether attention bias to sleep-related stimuli is present in individuals with PI. Control groups of good sleepers (GS) and individuals with delayed sleep phase syndrome (DSPS), a sleep disorder with no presumed cognitive pathway and, hence, no predicted association with attention bias, were included. Design: A between-groups (PI, DSPS, GS) design was employed. Participants completed a dot-probe task with stimuli comprising sleep-related and neutral words, balanced for length and frequency of usage. It was predicted a priori that PI would show greater attention bias to sleep stimuli compared with GS and DSPS groups. No difference between GS and DSPS was predicted. Participants: Sixty-three individuals completed the study (PI = 21; DSPS = 22; GS = 20), with those in PI and DSPS classified by International Classification of Sleep Disorders criteria according to self-report sleep diaries and actigraphy. GS scored < 5 on the Pittsburgh Sleep Quality Index, ing existing sleep difficulties. Recent cognitive models of PI8-10 have taken this notion further and suggest that the poor sleeper is selectively vigilant for internal stimuli indicative of wakefulness (when trying to sleep) and symptoms of fatigue (during daytime activities11). Any indication of difficulties in either of these areas serves to heighten anxiety about sleep difficulties and their consequences,12 thus leading to a redoubling of efforts to sleep and, paradoxically, reduced probability that sleep will occur.13,14 Selective vigilance, or “attention bias,” has been a focus of investigation in psychopathology for several years and is well established as a maintaining mechanism in several disorders, such as social phobia or panic disorder.15,16 However, at present, there are only 3 published studies that examine attention bias in PI, with equivocal findings that provide only limited evidence that sleep-related attention bias is present in those with PI. INTRODUCTION INSOMNIA IS A FREQUENT HEALTH COMPLAINT, WITH UP TO 33% OF THE GENERAL POPULATION REPORTING SLEEP DIFFICULTIES AT ONE TIME OR another and 9% reporting insomnia on a regular nightly basis.1 Insomnia can occur as a secondary consequence of physical or mental illness but also as a primary disorder in itself.2,3 Primary Insomnia (PI) is characterized as a disorder with the main complaint of disturbed or unrefreshing nocturnal sleep and associated daytime impairment, unrelated to a medical or mental disorder. An interplay of psychological and physiologic factors have been implicated in the development and maintenance of PI, for example, higher metabolic rates, increased nocturnal melatonin secretion,4,5 heightened cognitive arousal, and dysfunctional beliefs about sleep in those with PI.6,7 Given that sleep disturbance may be seen as a considerable anxiety generator to an individual with PI, behavioral formulations of PI suggest that repeated episodes of sleep difficulties may lead to the poor sleeper developing conditioned arousal to the bedroom environment, thus exacerbat- Attention Bias in PI Lundh et al,17 using the emotional Stroop task, found that participants with PI took relatively longer to name colors in trials containing sleep-related words, in comparison to neutral words, indicating an interference effect of sleep-related stimuli. However, they also found equivalent effects in “normal sleepers,” suggesting some degree of priming across the groups, or the presence of sleep difficulties in the “normal sleepers.” Taylor et al18 found a relatively heightened interference effect on the Stroop task for sleep-related words in a population with persistent insomnia (12 to 18 months), in comparison with a group with acute insomnia (up to 3 months). However, both of these groups were recovering cancer patients, and no control group of good sleepers, without medical problems, was employed. Nonetheless, perhaps the most compelling evidence of atten- Disclosure Statement This was not an industry supported study. Drs. MacMahon, Broomfield, Espie have indicated no financial conflicts of interest. Submitted for publication June 15, 2005 Accepted for publication June 12, 2006 Address correspondence to: Colin Espie, PhD, University of Glasgow Sleep Research Laboratory and Section of Psychological Medicine, Sackler Institute of Psychobiological Research, Southern General Hospital, 1345 Govan Road, Glasgow G51 4TF, Scotland, UK; Tel: 00 44 141 211 3903; Fax: 00 44 141 357 4899; E-mail: [email protected] SLEEP, Vol. 29, No. 11, 2006 1420 Attention Bias in Insomnia and DSPS—MacMahon et al tion bias in PI was provided in a recent study by Jones et al.19 They used a novel “flicker” paradigm,20 involving repeated brief presentations of a visual scene with a single feature (either sleep or neutral) altered on each alternate presentation. Participants defined as “poor sleepers” (> 5 on the Pittsburgh Sleep Quality Index [PSQI]21) detected a change in a scene related to a “sleep” object (1 of a pair of slippers), significantly quicker than a nonsleep object (1 of a pair of gloves). Furthermore, a significant correlation between PSQI and detection latency for the sleep-related change was observed. There are some drawbacks with this study, most notably the use of a between-subjects design, with no assessment of whether individuals showed relatively greater bias toward the sleep-related change. Jones et al19 also used only a single object, rather than several exemplars of a class, and classification of poor sleepers as suffering from PI was inferred purely on the basis of PSQI scores, with no clinical interview to confirm diagnosis. Although studies in the addiction literature suggest that the flicker task is a valid measure of attention bias,22 there is little in the general psychopathology literature on its use at the present time. Aims and Predictions Aims This study examined whether individuals with PI show an attention bias toward sleep-related stimuli on the dot-probe task in comparison with control groups of GS and those with DSPS. Predictions (1) Participants with PI will show attention bias toward sleep-related stimuli in the form of reduced latency in dot-probe reaction time to sleep-related words, in comparison with neutral words. (2) Neither DSPS nor GS will show an attention bias toward sleep-related stimuli in the form of increased latency in dot-probe reaction time to sleep-related words, in comparison with neutral words. Ethics Ethical approval for the study was sought from, and granted by, Greater Glasgow Primary Care Trust NHS Ethics Committee. Overcoming Limitations of Previous Work METHODS The study reported in this article attempted to establish whether attention bias is associated with PI by overcoming some of the limitations of previous work in this area. Firstly, the dot-probe paradigm, a well-established “hallmark” measure of attention bias, was employed.23 In this task, pairs of words are simultaneously presented, 1 above the other, on a computer screen, and the ensuing distribution of visual attention is measured by recording detection latency for a visual probe that appears in the spatial location of either word, immediately after the display of that word has terminated. Thus, the task bypasses limitations of the Stroop by using a neutral response (key press) to a neutral stimulus (visual probe). The trials providing the data of interest are those in which 1 of the words has emotional salience. By examining the impact of such a word on the relative probe-detection latencies in the 2 spatial areas, it is possible to determine whether visual attention has shifted toward or away from such stimuli. In order to address the difficult question of whether attention bias is associated specifically with PI, and not simply with sleep disturbance, a control group of individuals with delayed sleep phase syndrome (DSPS) was employed. DSPS is, like PI, characterized by difficulties in initiating sleep.24 Although the cause of this difficulty, in PI, is presumed to involve psychological factors, DSPS is believed to be the result of a circadian timing disorder. Because there is no presumed cognitive pathway to explain the emergence or maintenance of DSPS, it was predicted that those individuals who suffer from DSPS would not show attention bias to sleep-related stimuli. A further limitation of previous studies in the sleep disorders literature has been a lack of clear differentiation between participants with PI and those who may have a mixed pattern of DSPS and PI.25,26 Thus, objective (actigraphic) assessment of circadian sleep parameters has been used in tandem with subjective (selfreport sleep log) assessment to differentiate between DSPS and PI in poor sleepers. Many sleep studies also define control participants as not “obvious” sufferers of insomnia,17 possibly leading to the inclusion of “noncomplaining” poor sleepers. Therefore, a further control group, who actively describe themselves as “good sleepers” (GS), rather than those who report “no sleep difficulties,” was used. SLEEP, Vol. 29, No. 11, 2006 Participants An e-mail message sent round the student e-mail system requested those with “sleep problems,” “night owls,” or “good sleepers” to contact the first author. An initial, informal, screening process by e-mail or telephone was used to assess whether respondents were likely to meet necessary criteria. Seventy-nine individuals appeared to meet criteria and were invited to take part in the study. Participants met Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition2 and International Classification of Sleep Disorders-Revised3 criteria for either PI or DSPS, and those with PI were required to score > 6 on the PSQI. Exclusion criteria included active psychological or drug interventions for sleep problems or when a sleep disorder was suspected as being the result of substance misuse. GS scored < 5 on the PSQI, reported themselves as being “good” sleepers, and met no criteria for a sleep disorder at the present time or in the past. Actigraphy was used as an aid to differentiate between PI and DSPS in those reporting sleep difficulties. All participants had normal vision or corrected to normal vision. Final allocation of participants to groups for the purposes of analysis did not take place until all sleep-assessment data had been collated. No formally screened participants were excluded due to either psychological or drug interventions for sleep or because of substance misuse. However, 15 participants were excluded for the following reasons: failure to return all questionnaire measures (4); error score (making an upper key press for a lower target word and vice versa) on the dot-probe task above 5% threshold (1), “good sleepers” with PSQI scores > 4 (6), sleep difficulties were a combination of PI and DSPS (2), and “poor sleepers” who did not meet threshold of > 6 on the PSQI (2). One further participant (a “good sleeper”) was excluded as an “outlier” because her results fell more than 2 standard deviations from her group mean. This left a total of 63 participants who met all relevant criteria 1421 Attention Bias in Insomnia and DSPS—MacMahon et al and completed all measures and who were classified into PI (n = 21), DSPS (n = 22), or GS (n = 20) groups. A power calculation (using data from previous studies of attention bias17,18,27) carried out prior to the study suggested that 21 participants would be required in each of the 3 groups (PI, DSPS and GS) to detect statistically significant differences at a power of .8 with an α level set at .05. Table 1—List of Words for Dot-Probe Task With Frequency of Occurrence per Million in the British National Corpus Apparatus The dot-probe task was run on a Dell (Bracknell, UK) Optiplex GX270 computer, with software developed by the first author on the experiment-generating package, SuperLab Pro (Version 2.02; Cedrus Corporation; San Pedro, CA). The size of the screen was 28 cm (diagonally), with stimuli in 14-point Times New Roman font in white lettering on black background, positioned centrally, on a vertical plane; the viewing distance was 45 cm. Millisecond timing was made through SuperLab Pro and an external response box (Model RB-400; Cedrus Corporation; San Pedro, CA) to avoid timing errors associated with standard keyboard or mouse input. Actigraphy was facilitated by the Cambridge Neurotechnology (Cambridge, UK) Actiwatch system. This comprises wrist-worn actigraphs (Model AW-2), roughly the size of small wristwatches, and sleep-analysis software (Actiwatch Sleep Analysis v 1.06), capable of automatically calculating sleep parameters. There is general consensus that wrist actigraphy provides an accurate objective measure of circadian sleep and wake parameters.28 Materials A stimuli list comprising 88 words was developed for this study (see Table 1). Firstly, 8 neutral, non–sleep-related practice words were divided into 4 pairs (leisure/gallant; poetry/joyful; welcome/ capable; prizes/secure). Secondly, a list of 20 sleep-related words were matched to 20 neutral words. The 20 sleep-related words were originally used by Taylor et al18 in their study of insomnia in patients recovering from cancer. Taylor et al18 developed these words from Wicklow and Espie’s29 study of the content of presleep cognitions, and, thus, they have a high degree of salience to individuals with sleep difficulties. Finally, 60 further neutral, non–sleep-related words were selected and divided into matched pairs. Although each pair of words was used on 2 occasions in the study, repeated word pairs have been used before in this paradigm with no priming effects found.30 Matching of words into pairs was carefully done to ensure equivalence in length and frequency of usage in the English language. The latter was achieved by consulting frequency tables constructed from the British National Corpus, a representative sample of present-day spoken and written British English31(http://www. comp.lancs.ac.uk/ucrel/bncfreq). Analysis-of-variance (ANOVA) across the 4 sets of word pairs for frequency of occurrence in the British National Corpus showed no significant differences (F3,76 = 0.025, p = .995). Frequency 41 15 5 46 159 24 0 (20) 3 7 0 (14) 135 16 0 (25) 0 (22) 4 4 365 7 2 1 41.7 ± 87.95 Neutral Words Frequency Clubs 38 Impatient 7 Paddock 2 Grass 41 Red 149 Models 53 Shuffle 3 Texture 9 Scents 2 Pear 2 Hour 113 Linen 10 Consist 12 Quantifies 0 (11) Reforms 0 (30) Absurd 10 Money 374 Youthful 0 (5) Empower 1 Kinetics 2 Mean ± Sd 41.4 ± 87.96 Neutral Words Graft Featuring Cushion Meals Led Stairs Invoice Playful Margin Tops Book Habit Sandals Attendants Invents Graft Point Thankful Vaccine Wriggles Mean ± Sd Frequency 19 9 5 24 154 36 5 2 15 10 248 23 3 2 0 (20) 2 402 4 4 0 (1) 48.4 ± 103.45 Neutral Words Frequency Males 22 Scrubbing 2 Specify 13 Chord 6 Lot 246 Mirror 39 Prodigy 1 Tramped 1 Pencil 12 Laps 3 News 145 Steel 37 Potters 1 Speculates 0 (27) Drafted 7 Disarm 1 Water 350 Entrants 5 Embrace 10 Fixation 2 Mean ± Sd 45.2 ± 93.81 Note: When frequency of occurrence is less than 1 per million, as with several of the chosen sleep words, the range of sections in the British National Corpus (out of a maximum of 100) in which the word occurs is taken as a measure of frequency of usage; this range is given in parentheses in this table. to assess levels of state and trait anxiety. (3) National Adult Reading Test (NART34) to provide an estimate of reading vocabulary and ensure that participants’ reading level was sufficient for the stimuli used in the dot-probe task. (4) Caffeine Intake Questionnaire, an idiosyncratic questionnaire, to assess usual and actual recent intake of caffeine, comprising 3 questions examining caffeine intake in beverages in past 24 hours, the day so far, and usual caffeine intake. Intake was divided into units according to the caffeine content of these beverages. Self-Report Measures Demographic Measures (1) Beck Depression Inventory-Short-Form (BDI-SF32) to assess for symptoms of depression. (2) Spielberger State and Trait Anxiety Inventory (S-SAI/ S-TAI33) SLEEP, Vol. 29, No. 11, 2006 Sleep Words Tired Exhausted Fatigue Dream Bed Sheets Wakeful Silence Pillow Naps Dark Alert Snoring Overactive Arousal Sleepy Night Restless Tossing Lethargy Mean ± Sd 1422 Attention Bias in Insomnia and DSPS—MacMahon et al Sleep Measures RESULTS (1) PSQI21 to assess for presence and severity of sleep disturbance. (2) Anxiety and Preoccupation about Sleep Questionnaire (APSQ35) to assess for specific worry about sleep difficulties. (3) Morningness-Eveningness Questionnaire-Reduced Form (MEQ36) to assess preference for “morningness” or “eveningness” as an aid to classification of sleep disorder as PI or DSPS. (4) Stanford Sleepiness Scale (SSS37) to quantify level of alertness during testing. Participant Characteristics Mean age across all participants was 24.4 years (SD = 7.44 years), with a total of 35 females and 28 males. In terms of group differences, ANOVA and post-hoc testing with the Tukey Honestly Significant Differences (HSD) test demonstrated that the GS group was significantly older than the DSPS group (see Table 2 for data). Given this finding, further analysis between groups used analysis-of-covariance (ANCOVA), with age as a covariate, followed by Tukey HSD test. ANCOVA and Tukey HSD across the 3 groups revealed significantly lower mean levels of stateanxiety, trait-anxiety, and depression in the GS group (28.7, 31.5, and 0.5, respectively) in comparison with those with PI (37.9, 47.7, and 3.6, respectively) or DSPS (35.6, 46.1, and 4.0, respectively). No statistical difference was present between the PI and DSPS groups on these measures. No significant differences in vocabulary level emerged between any of the groups. No difference between groups in either regular or actual recent caffeine intake was reported either (all p values > .3). PROCEDURE Following recruitment and screening by e-mail or telephone, potential participants were met at the University. All testing was conducted in a quiet private room in the Department of Psychology. Subjects were given a brief written summary outlining the purpose of the study, stating that it was to “understand some of the reasons why people have difficulty sleeping.” No other details on the purpose or hypotheses lying behind the study were given at this stage and what would be required of them if they agreed to participate. Informed consent was then obtained. No financial remuneration nor course credits were offered for participation. Participants were then asked to complete the dot-probe task. Each participant viewed a set of instructions, on screen, and the task was explained verbally to ensure that it was fully understood. Following this, participants completed 4 practice trials, followed by the remaining 160 experimental trials. Pairs of words were presented in a random order, with rerandomization of the order for each participant, to ensure that order effects did not confound results. Each trial consisted of the following events: a fixation cross appeared in the center of the screen for 500 milliseconds, followed by the pair of words for 500 milliseconds; the words then disappeared, and a dot-probe, consisting of an asterisk, appeared in either the upper or lower position; this remained on screen until the correct response key (upper or lower) was pressed. Half of the trials contained a sleep-related word, and there was an equal probability that the probe would replace the sleep-related or the neutral word. The relative positions (upper or lower) of each pair of words were also counterbalanced within the experiment. An intertrial interval of 1000 milliseconds followed each trial. A brief screening interview was then conducted to assess sleep history and general psychological state. This was done after the experimental task to minimize priming for sleep difficulties on the dot-probe. The screening interview covered items in Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition and International Classification of Sleep Disorders criteria and the differential diagnosis of alternative sleep disorders, such as sleep apnoea and general mood state. Participants then completed the NART, the MEQ, and the SSS with the experimenter and the SSAI and CIQ by themselves. All participants then completed the PSQI, APSQ, BDI-FT, and S-TAI at home and filled-out a sleep diary each night over the next week. Those who reported sleep difficulties were also asked to wear an Actiwatch day and night for this week. On their return visit, approximately 1 week hence, participants were fully debriefed as to the purpose of the study, and their sleep data was reviewed. All participants were given a copy of the Good Sleep Guide,38 and those who complained of either PI or DSPS were given some general advice, based on the Good Sleep Guide, in managing their sleep difficulties. SLEEP, Vol. 29, No. 11, 2006 Sleep-Related Questionnaire Measures The GS group scored significantly lower on the PSQI and APSQ than either the PI or DSPS groups. Individuals in the DSPS group were rated, by the MEQ, as significantly more “evening” type than the other 2 groups (lower scores on the MEQ reflect a greater tendency to “eveningness”). On average, participants in the PI and DSPS groups report themselves to be significantly less alert (as measured by the SSS) than their GS counterparts. Table 2—Participant demographics within the PI, DSPS, and GS DemoPI DSPS GS F2,59a/ p Value graphic (n = 21) (n = 22) (n = 20) χ2 (2) Age 23.6 ± 6.9 21.8 ± 2.2 28.2 ± 10.1 4.50 ‡† .02 (years) Sex, male/ 7/14 12 /10 9/11 1.96 ‡† .38 female BDI-FT 3.6 ± 3.1 4.0 ± 3.6 0.5 ± 0.7 5.90 ‡† .005 S-SAI 37.9 ± 8.3 35.6 ± 7.3 28.7 ± 7.1 5.95 ‡† .004 S-TAI 47.7 ± 11.4 46.1 ± 9.7 31.5 ± 5.7 15.54 ‡† < .001 NART 13.5 ± 7.7 10.8 ± 3.7 11.4 ± 4.7 1.38 .26 PSQI 9.8 ± 2.4 7.4 ± 2.4 2.6 ± 1.9 46.60 ‡† < .001 APSQ 56.9 ± 17.7 53.9 ± 15.5 20.2 ± 11.1 30.78 ‡† < .001 MEQ 11.5 ± 3.5 8.6 ± 2.6 13.8 ± 4.4 7.55*† .001 SSS 2.9 ± 1.2 2.8 ± 0.9 2.1 ± 0.8 5.04 ‡† .01 Data are presented as mean ± SD unless otherwise indicated. a Age df2,60 PI refers to primary insomnia; DSPS, delayed sleep-phase syndrome; GS, good sleeper; BDI-FT; Beck Depression Inventory-Fast Track; S-SAI, Spielberg State Anxiety Inventory; S-TAI, Spielberg Trait Anxiety Inventory; NART, National Adult Reading Test; PSQI, Pittsburgh Sleep Quality Index; APSQ, Anxiety and Preoccupation about Sleep Questionnaire; R-HOMEQ, Horne and Ostberg MorningnessEveningness Questionnaire; SSS, Stanford Sleepiness Scale *Indicates significant (p < .05) difference between PI and DSPS with Tukey posthoc Test. ‡Indicates significant (p < .05) difference between PI and GS with Tukey posthoc Test. †Indicates significant (p < .05) difference between DSPS and GS with Tukey posthoc Test. 1423 Attention Bias in Insomnia and DSPS—MacMahon et al However, SSS scores did not correlate directly with the dot-probe performance measures. than 2 SD from her group mean. ANCOVA, with age as a covariate, confirmed that the groups did not differ significantly (F2,59 = 1.97, p = .15) on error rate (1.5% of total data) or in outliers (F2,59 = 1.62, p = .21), which comprised a further 3.1% of the remaining data (see Table 5 for data). However, significant differences between the groups (F2,9670) = 151.17, p < .001) were evident on mean RT, with posthoc testing confirming that the PI group responded more quickly to all stimuli than the GS group who, in turn, responded more quickly to all stimuli than the DSPS group (see Table 5 for data). Table 5 also details mean RT for each stimuli combination (position of sleep word and position of probe). In order to assess whether systematic differences were present between groups and stimuli combinations, an attention bias score was calculated, in accordance with general practice in this literature.40 The attention bias score was calculated using the following equation: attention bias score = [(SleepUProbeL+SleepLProbeU)-(SleepUProbeU + SleepLProbeL)]/2 where Sleep = sleep-related word; U = upper; and L = lower e.g., SleepUProbeL represents the mean RT when the sleep-related word is in the upper position and the probe is in the lower position). The attention bias score summarizes the interaction between sleep-word position and probe position on RT, providing a measure of the relative speeding of RT to probes that appear in the same location as sleep-related words. Positive values reflect vigilance for sleep words relative to neutral words, whereas negative values reflect avoidance. Mean and SD attention bias scores were +3.9 ± 9.4 for the PI group; +1.1 ± 8.3) for the DSPS group; and -2.5 ± 9.70 for the GS group. It was predicted, a priori, that a greater degree of attention bias to sleep-related stimuli would be shown by the PI group in comparison with the DSPS and GS groups. Orthogonal contrasts, with an assumption of equal variances, on attention bias scores supported this prediction (t60 = -1.88, p = .03). It was also predicted, a priori, that the DSPS and GS groups would show an equivalent degree of attention bias, ie, no significant difference would be observed. This prediction was also upheld (t60 = -1.27, p = .10). Finally, the Pearson product-moment correlation coefficient was calculated between attention bias score and PSQI score to establish whether an underlying association existed across all participants. Although a positive correlation emerged, it did not reach statistical significance (r = +.19; p = .13). Sleep Data Sleep Diary ANCOVA, with age as a covariate, across groups for subjective bed time, arise time, sleep-onset latency, wake after sleep onset, and total sleep time all revealed significant (p < .05) differences across the groups (see Table 3 for data). Posthoc testing with the Tukey HSD test confirmed that the DSPS group reported going to bed and rising from bed significantly later than the other 2 groups. Both PI and DSPS groups reported longer sleep-onset latencies than did the GS group, although they did not differ between themselves. WASO and number of nighttime awakenings were significantly greater in the PI group in comparison with only the GS group. Total sleep time was equivalent across all 3 groups. Actigraphy Actigraphy aided in making the diagnosis between PI and DSPS in individual cases. Furthermore, nonparametric circadianrhythm analyses39 of L5 (time of onset of lowest 5 hours of activity) and M10 (time of onset of highest 10 hours of activity) confirmed that the phases of lowest and highest activity were, on average, significantly delayed (by around 2 hours) in the DSPS group, in comparison with the PI group (see Table 4 for data). Preparation of Response-Time Data Response times (RTs) from trials with errors were excluded, and those more than 2 SD above the mean were discarded as outliers.15 As detailed earlier, 1 participant had an error rate above 5% and was therefore excluded from all analyses, and 1 further participant was excluded as an “outlier,” with her results lying more Table 3—Sleep-Diary Parameters for the PI, DSPS and GS Groups Parameters Bed Time Arise Time SOL WASO TST Awakenings PI DSPS GS F2,60 p (n = 21) (n = 22) (n = 20) value 00:38 (46.1) 02:40 (83.0) 00:24 (55.5) 24.71*† < .001 09:18 (51.3) 11:10 (72.7) 08:32 (87.1) 21.48*† < .001 40.0 ± 20.8 31.1 ± 15.3 10.2 ± 8.8 15.37*† < .001 21.5 ± 29.0 18.7 ± 18.1 3.9 ± 5.3 5.58‡ .006 442.0 ± 80.2 468.0 ± 65.8 474.1 ± 57.6 1.73 .19 2.2 ± 2.1 1.33 ± 1.0 1.0 ± 1.2 5.28‡ .01 DISCUSSION Recent cognitive models of insomnia8,10 predict that individuals with PI, in comparison with GS, will demonstrate heightened vigilance for sleep-related stimuli. Results from this study provide support for this prediction. Those with PI, in comparison Data are presented as mean ± SD except for bed time and arise time, which are presented as mean 24-h clock times with SD of minutes in parentheses PI refers to primary insomnia; DSPS, delayed sleep-phase syndrome; GS, good sleeper; SOL, sleep-onset latency; WASO, wake time after sleep onset; TST, total sleep time; Awakenings, number of awakenings during the night *Indicates significant (p < .05) difference between PI and DSPS with Tukey posthoc Test. ‡Indicates significant (p < .05) difference between PI and GS with Tukey posthoc Test. †Indicates significant (p < .05) difference between DSPS and GS with Tukey posthoc Test. SLEEP, Vol. 29, No. 11, 2006 Table 4—Actigraphy L5 and M10 parameters for PI and DSPS Parameters L5 M10 PI (n = 21) 2:26 (61.7) 11:40 (131.9) DSPS (n = 22) 4:22 (70.6) 13:11 (136.9) t41 p value -5.73 -2.22 < .001 .03 Data are presented as mean 24-h clock times with SD of minutes in parentheses. PI refers to primary insomnia; DSPS, delayed sleepphase syndrome. 1424 Attention Bias in Insomnia and DSPS—MacMahon et al Table 5—Overall Response Times, Error Scores, and Response Times for Word-Pairs Errors Overall RTs SleepU ProbeU SleepU ProbeD SleepD ProbeU SleepD ProbeD PI (n = 21) 3.5 ± 4.1 384.2 ± 71.3 384.8 ± 73.7 388.5 ± 66.6 386.0 ± 68.7 380.5 ± 75.2 DSPS (n = 22) 2.0 ± 1.8 410.8 ± 75.4 410.1 ± 77.3 409.1 ± 73.5 410.9 ± 74.8 410.1 ± 74.8 GS (n = 20) 2.0 ± 2.1 397.1 ± 72.4 402.5 ± 75.9 394.0 ± 66.9 397.0 ± 72.7 394.2 ± 69.1 F2,59/ F2,9670 1.97 151.2*†‡ p value .15 < .001 Data are presented as mean ± SD unless otherwise indicated. All response times (RT) are shown with errors firstly removed. PI refers to primary insomnia; DSPS, delayed sleep-phase syndrome; GS, good sleeper. *Indicates significant (p < .05) difference between PI and DSPS with Tukey posthoc Test. ‡Indicates significant (p < .05) difference between PI and GS with Tukey posthoc Test. †Indicates significant (p < .05) difference between DSPS and GS with Tukey posthoc Test. with GS, showed relatively greater vigilance, as measured by the dot-probe task, for sleep-related stimuli. Although a positive correlation between attention bias score and PSQI score (a measure of sleep quality) was demonstrated, it did not approach statistical significance. Nonetheless, results provide support for the specific prediction, from cognitive models of PI, that suggest attention bias is a component of this disorder.8,10 Two other findings emerged. Firstly, participants with DSPS, in comparison with GS, did not show significant evidence of attention bias, as predicted. A second, notable, finding was the significantly shorter RTs from the PI group, in comparison with GS and, in turn, with DSPS (see Table 5). There were no significant differences in overall error rates that might explain this as a speedaccuracy trade off (indeed, overall error rates were low; see Table 5). It is possible to speculate that those with DSPS are less alert (as shown by their higher SSS scores) than their GS peers, but this is unlikely to explain slowing because SSS scores per se did not predict dot-probe data. However, the speeded responses (in spite of their equally high SSS scores) of the PI group may be a reflection of increased arousal levels in this population, something that has been demonstrated in studies of physiologic aspects of PI.4,5 Self-report ratings in the DSPS group are also of some interest, with unexpectedly high levels of state-anxiety, trait-anxiety, and worry about sleep (see Table 2). Although differentiated, in this study, on a case-by-case basis from those with PI, there is clearly some overlap between the disorders. This raises the question of whether those with DSPS can form a “pure” enough control group against which to compare those with PI on psychological factors.41 Indeed, some authors have suggested that circadian dysfunction may act as a precipitating mechanism in PI.42 Interestingly, in this study, there does appear to be some degree of phase delay in the PI group, with a relatively late L5 onset of 2:26 AM (see Table 4), although it should be borne in mind that the use of a relatively young University sample suggests that social factors may be a causal factor in this late L5. Perhaps future studies would be best served by screening more carefully for DSPS but still exercising caution in the interpretation of results from this group, with the assumption that some overspill of PI may be inevitable. There are several limitations in the current study that should be considered. Firstly, the sample was drawn from a university population, thus narrowing the age and education range of the participants (see Table 2). Furthermore, students have greater flexibility to adjust work schedules than do those in regular (9:00 AM to 5:00 PM) employment.43 Thus, failure to sleep at night, or perform at a set time of day, may pose less of a threat to (and hence less of a SLEEP, Vol. 29, No. 11, 2006 focus of attention for) both the PI and DSPS groups, than would occur in a comparative sample with regular employment. Thus, potentially, this study may underestimate the degree of attention bias in both of these groups. However, participants met both Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition and International Classification of Sleep Disorders-Revised criteria for PI, and the mean PSQI scores for PI and DSPS groups were well above the mean for the GS group (9.8 and 7.4, respectively, versus 2.6). Furthermore, mean APSQ scores are comparable to those of a recent study on PI44 and indicate a significantly greater degree of worry about sleep in the PI group and DSPS groups in comparison with the GS group (56.9 and 53.9, respectively, versus 20.1). In this case, the comparative levels of concern about sleep in the DSPS and PI groups are not reflected in the degree of attention bias, further supporting the argument that cognitive factors may play a role in PI, whereas physiologic factors may underpin DSPS. Secondly, although this is a positive finding, discrepant findings are not uncommon in the attention-bias literature, with the role of mood state often implicated in this.45 For example, in a study using the dot-probe task, Mogg et al46 failed to find evidence of attention bias to exam-related stimuli in a high trait-anxious population when testing was conducted out with the exam period. However, when exams were imminent, the processing bias appeared. Again, it is feasible that a larger effect would have been seen in our study if participants were tested at a time when sleep loss was a salient threat; for example, in the evening prior to an examination or other important event the following day. A testing laboratory in the middle of the day, with no cost attached to “poor” performance on the experimental task, may fail to activate dormant schema. However, when loss of sleep is imminently threatening, such as in the early hours of the morning, or when performance on a task is particularly valued, increased vigilance for indicators of sleep readiness (at night) or negative consequences of sleep loss (in the daytime) may be observed. This leads to a further limitation of the present study. It was not possible, for both practical and theoretical reasons, to adjust time of testing for participants’ circadian rhythms. Testing on the dot-probe task was conducted at the first available opportunity; hence, actigraphic assessment (which could potentially have provided information to set testing times according to individual circadian rhythms) followed the testing session. To wait until actigraphic assessment had been completed and then set specific testing times would have significantly increased the demands on participant time and would also have raised the possibility of priming to sleep-related 1425 Attention Bias in Insomnia and DSPS—MacMahon et al the development or maintenance of PI, and not merely as an associative factor, further work to demonstrate a direct link between attention bias and PI is necessary. For example, the repeat administration of the dot-probe task at intervals when sleep difficulties are waxing and waning might demonstrate a concurrent increase and decrease in attention bias. Perhaps of even more interest would be to determine whether increasing attention to sleep-related material would lead to an increase in sleep difficulties, as has been suggested in parallel studies in the anxiety literature.52 Furthermore, measurement of attention bias following successful and unsuccessful treatment for PI would be helpful, particularly with regard to the impact of sleep medication (effective in the short term) in comparison with the relatively enduring effects of cognitive behavioral treatment. Further work, utilizing pictorial stimuli, additional psychophysiologic measures, and carefully screened participants, is still necessary before definitive conclusions can be drawn on any potential role of attention bias in PI. However, if further evidence emerges to support the findings of this study, it would be an important step in finding an “objective” measure of PI. At present, the cognitive arousal reported by those with PI is only measured by self-report; attention-bias tasks may offer the possibility of objective measures, sensitive to the experience of PI. stimuli. Nonetheless, this is something that would be of value to consider in future studies. One potential limitation of this study was the inclusion of sleep-related words that might not be considered “sleep-threatening,” such as “pillows” or “nap.” However, the words used in this study were taken directly from previous work that elicited presleep cognitions of individuals with PI.29 Thus, it was predicted that they would be selectively processed by individuals with attention bias to sleep-related stimuli. Indeed, even if the word sets used in this study were not considered to be sufficiently “threatening,” this suggests that a magnified effect could be detected if alternate word sets were used. At the time of study development, this word set, taken directly from presleep cognitions, was felt to provide the most ecologically valid option. Furthermore, the DSPS group reported sleep difficulties equal to those of the PI group (as evidenced by PSQI scores, see Table 2), yet did not show equivalent attention bias scores, suggesting that the word set used in this case appropriately discriminated by sleep disorder, rather than simply reflecting the degree of “interest” expressed by individuals in sleep problems. Alternate grouped categories of neutral words (eg, household items or animals) have been used in some studies of attention bias to limit the possibility that bias is shown as a result of target words falling into categories, rather than actual category itself being differentially processed. The lack of categorized neutral words is a noted limitation of the present study. However, no effect of either neutral or sleep-related word lists was seen in the GS group, suggesting that the systematic bias seen in the PI group is unlikely to have been purely the result of using a category in itself. Nonetheless, future studies utilizing this paradigm should consider developing matched categories for neutral word lists. Furthermore, although considered a relatively pure measure of attention,16 the dot-probe task has also been described as a “relatively fragile index of anxiety related attentional biases in non-clinical studies, particularly when using word stimuli that have relatively mild threat value.”47 A possible lack of emotional salience in the word-based stimuli may minimize the vigilance effect in the present study. Future studies might consider the use of a pictorial dot-probe paradigm to maintain the degree of experimental control available from the dot probe but maximize the possibility of uncovering processing biases by increasing the saliency of stimuli.48 Furthermore, because RT is an indirect measure of vigilance, a future study might also consider the use of psychophysiologic measures of attention, such as heart rate49 or eye tracking,50 in order to add credence to results. Notwithstanding these limitations, using a “hallmark” measure of attention bias and a carefully screened sample, our results offer evidence of attention bias in young people with PI; this is consistent with cognitive models of PI.8,10 In particular, the results are in keeping with the attentional component of a proposed “attentionintention-effort pathway” in the development of psychophysiologic insomnia.9 Our findings also provide some support for the neurocognitive model of PI.51 This model suggests that those with PI have greater cortical arousal, something that may be reflected in the speeded RTs recorded in the present study. Notably, Perlis et al51 did not make recourse to attention bias as a maintaining factor in their model. However, our results would suggest that both aspects may operate, possibly in a complementary fashion, during the development of PI. 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