The influence of pre-sleep cognitive arousal on sleep onset processes

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Abstract

Cognitive hyperarousal, resulting in enhanced cognitive activation, has been cited as an important contributor to the development and preservation of insomnia. To further understand this process, our study examined the effects of acutely-induced pre-sleep cognitive hyperarousal on sleep onset processes in healthy volunteers. Following an adaptation night, 15 subjects slept two nights in our sleep laboratory: one reference night and another one with cognitive arousal induction, in a counterbalanced order. In the cognitive arousal condition, subjects worked through half an hour of cognitive tasks without interference of an emotional component prior to retiring to bed. Objective sleep onset latency was significantly prolonged in the cognitive arousal condition compared to the reference condition. Significantly more high frequency activity was recorded during the first and second deep-sleep period. Moreover, differences in heart rate and proximal temperature during and after sleep onset were observed in the nights after the cognitive induction. Pre-sleep cognitive activation successfully induced a significant cognitive load and activation in our subjects to influence subsequent sleep (onset) processes.

Highlights

► Pre-sleep cognitive activation lengthens subsequent sleep onset latency. ► Pre-sleep cognitive activation accelerates EEG-activity in subsequent deep sleep. ► Cognitive arousal without emotional component negatively influences sleep (onset).

Introduction

Years of research have shown that sleep onset – the transition from the waking to the sleeping state – does not initiate sleep from 1 s upon the other, but rather is a process with several semi-independent, yet interactive changes (Ogilvie, 2001). It is a progressive process of decline in control over mental activity and gradual changes in perceived state of consciousness (Freedman and Sattler, 1982), accompanied by gradual decrease in arousal (De Gennaro et al., 2001, Espie, 2002). This decrease is evidenced by a depression in cortical activity (Davis et al., 1938), a slowing of the heart rate (Burgess et al., 1999, Jurysta et al., 2003, Okamoto-Mizuno et al., 2008), a decline in core body temperature (Kräuchi et al., 2000, Kräuchi and Wirz-Justice, 2001, Okamoto-Mizuno et al., 2008, van den Heuvel et al., 1998), an increase in distal and proximal skin temperature (Kräuchi et al., 1999, Kräuchi et al., 2000) and many more behavioural, cortical and physiological changes (Ogilvie, 2001). However, these are processes observed during sleep onset in healthy sleepers (Monroe, 1967). Subjects with sleep-onset problems, in particular those with sleep-onset insomnia, may not experience this specific series of events, or exhibit alterations of these processes (Espie, 2002, Monroe, 1967).

Hyperarousal is defined as either an enhanced basal level of arousal or the inability to down-regulate an excess of arousal (Pigeon and Perlis, 2006). It can express itself as somatic, cortical and cognitive arousal (Perlis, 2001, Pigeon and Perlis, 2006). In most models of insomnia, hyperarousal has been cited as an important contributor to the development and preservation of insomnia (Perlis et al., 2005). Depending on the model, emphasis is either put on cognitive (Espie, 2007, Hall et al., 1996, Harvey, 2002, Riemann et al., 2010, Wicklow and Espie, 2000), physiological/somatic (Bonnet, 2009, Bonnet and Arand, 2010) or cortical hyperarousal (Perlis et al., 1997).

Within the cognitive model of insomnia, a more important role is assigned to cognitive (hyper)arousal in the development of insomnia (Espie, 2007, Harvey, 2002, Wicklow and Espie, 2000). Being hyperaroused, insomniacs find it difficult to fall asleep and become highly attentive to sleep-promoting and sleep-disturbing factors (Tang et al., 2007). Other authors put insomnia in a more behavioural context, with cognitive hyperarousal as a factor in the maintenance of insomnia (Bonnet, 2009, Bonnet and Arand, 2010, Spielman et al., 1987). Several researchers incorporate both the behavioural and cognitive points of view into their models (Morin, 1993, Perlis et al., 1997, Riemann et al., 2010). In those models, a role for cognitive hyperarousal is formulated both in the development and maintenance of insomnia. It is hypothesized that by means of classic conditioning (of both cognitions and behaviours), the sleep environment becomes an arousing trigger (Morin, 1993, Perlis et al., 1997, Riemann et al., 2010). An over-activation of the sensory and information-processing systems results from increased arousal (Pribram and McGuinness, 1975), making it more difficult to fall asleep.

Falling asleep should be a rather automatic and unconscious process. Conscious attempts to fall asleep might even disturb the sleep onset process (Espie, 2007, Harvey, 2000). Sleep itself, and worries, are the focus of pre-sleep cognitive activity in insomnia patients. More than good sleepers, they complain of non-intentional pre-sleep cognitive activity (Harvey, 2000). Intrusive pre-sleep thoughts cause stress and are highly correlated with sleep onset problems (Hall et al., 1996, Wicklow and Espie, 2000). These thoughts are an important target for such therapeutic interventions as thought-stopping and articulatory suppression (Bootzin and Rider, 1997, Levey et al., 1991, Morin, 1993). They all focus on short-term memory and working memory. Although insomnia patients tend to blame their sleep problems more on intrusive cognitive-arousing thoughts than on physical arousal (Lichstein and Rosenthal, 1980), the disturbing role of changes in processes controlled by the autonomous nervous system – such as heart rate (Hall et al., 2004) and body temperature (Morris et al., 1990, van den Heuvel et al., 1998) – must be taken into account.

It should also be noted that, in the context of sleep, cognitive activation is relevant not only with regard to patient populations. For instance, research has shown that such pre-sleep activities as computer gaming, television watching (Dworak et al., 2007) and using the internet (Reynolds et al., 2010, Van den Bulck, 2004) significantly disturb the weekly sleep patterns of young adolescents with negative effects on their learning and memory performance (Dworak et al., 2007). Higuchi et al. (2005) studied young adults and obtained the same results, but also eliminated the possibility that these effects of pre-sleep activity might be due to the exposure to bright light emitted by monitors.

Earlier research has shown that sleep is sensitive to the level of arousal induced by specific pre-sleep activities. However, this depends on the characteristics of the pre-sleep activity (physical and/or cognitive activities) (Bonnet and Arand, 2001, De Bruin et al., 2002, Hauri, 1969, Tang and Harvey, 2004) and the time elapsed between the activity and bed-time (Baekeland and Lasky, 1966, Hauri, 1968). De Bruin et al., 2002, Hauri, 1968 observed that neither a six- nor an eight-hour sustained mental workload immediately before going to sleep, had any effect on subsequent sleep macrostructure. However in both studies participants went to sleep immediately after finishing the cognitive tasks. Hauri (1968) analysed only the first 3, 5 h of sleep. He discussed this as an important shortcoming, because by referring to Baekeland and Lasky, 1966, Hauri, 1968 pointed out that pre-sleep activities have rather a delayed than an immediate effect on sleep-parameters. In another report (Hauri, 1969), however, Hauri observed a significant delay of 6 min in sleep onset after studying, compared to after physical activity and relaxation.

Gross and Borkovec (1982) found a significant effect of cognitive intrusions on the sleep onset latency of good sleepers (differences between experimental and control groups ranging between 5 and 12 min). In line with the previous experiment, two studies have identified the effects of induced intrusive thoughts — one on subsequent sleep onset and continuity (Hall et al., 1996) and another one on daytime sleep onset, using the Multiple Sleep Latency Test procedure (De Valck et al., 2004). Ansfield et al. (1996) found that under high mental load (March music) the urgency to fall asleep increased sleep onset latency in normal subjects whilst under a low mental load (new age music) the urgency to fall asleep caused subjects to fall asleep sooner than without the urgency under the same mental load. Kobayashi et al. (1998) found that mental activity affected the timing of REM-periods later at night and Koulack et al. (1985) found that both easy and difficult versions of intelligence tests increased subsequent sleep onset latency and negatively influenced REM density. Moreover, pre-sleep engagement in exciting computer games increased sleep onset latency (Dworak et al., 2007, Higuchi et al., 2005). Yet, these studies did not differentiate between the pure cognitive effects of inducing cognitive arousal and the possible consequences of arousing emotional factors (Vandekerckhove and Cluydts, 2010) in their induction — e.g. a financial reward (Hauri, 1968), the stress of a 15-minute evaluated speech in the morning (Hall et al., 1996), musical preference (Ansfield et al., 1996), a television interview (De Valck et al., 2004) or speech (Gross and Borkovec, 1982), driving a car for 600 km on the highway (Kobayashi et al., 1998), fear of failure (Koulack et al., 1985) and playing shooting (Higuchi et al., 2005) or race games (Dworak et al., 2007). Research has shown that cognitive tasks with no emotional load (i.e. where performance is independent of reward or punishment) performed once or repeatedly prior to sleep onset have a significant detrimental effect on cortical and physiological processes. The effect on cortical processes was indicated by decreased EEG delta power density during the first non-REM-sleep cycle (Takahashi and Arito, 1994), whilst the lack of effect on physiological processes was indicated by changes in arterial blood pressure and R–R intervals (Takahashi and Arito, 1996a, Takahashi and Arito, 1996b). However, these last two studies also involved sleep restriction procedures (subjects slept from 02:00–07:00) that could have influenced the results.

Since most of the afore-mentioned studies did not differentiate well between cognitive and emotional arousal, the aim of this study was to use a subset of cognitive tasks: a Digit Span task, a Stroop task, a Recognition task and the Symbol Substitution task (Wechsler, 1997), (see Materials and methods). These are maximally exclusive of emotional components. Earlier studies have demonstrated the effects of these tasks on cognitive loading and cortical and physiological arousal (Baddeley, 2003, Fairclough and Houston, 2004, Kamarck et al., 1994, Larson et al., 1995, Manuck et al., 1992, Matthews et al., 2004, Pattyn et al., 2010).

Within the framework of the cognitive behavioural model, this study investigates the way in which a set of cognitive tasks known to load on working memory, and known to induce a physiological response, influences the sleep onset process in healthy sleepers. Sleep onset is hypothesised to be prolonged, and during sleep onset, heart rate is expected to be elevated and the increase in proximal temperature to be reduced. An increased presence of high frequency EEG-activity is expected during deep sleep.

Section snippets

Participants

15 volunteers (7 men and 8 women), between the ages of 18 and 28 (mean = 22.07 years; SE = 0.81) participated in our study. Subjects were recruited among a student population unknown to the experimenter and unaware of the purpose of the study. All were healthy sleepers, non-regular smokers and non-abusers of alcohol or other substances that influence the central nervous system. Adherence to these standards was ensured using the Pittsburgh Sleep Quality Index (Buysse et al., 1989), the Insomnia

Results

For the sake of clarity, all questionnaire data were rescaled (if necessary) to make sure that each scale's minimum score would be zero. Sample size may differ due to technical problems in the PSG recordings of either the REF- or COG-night or due to missing questionnaire data. PSG- and FFT- variables that take the whole night into account are executed on 13 subjects. Recordings from 2 subjects contained insufficient data to be included in all the analyses. Heart rate analyses include 11 instead

Discussion

In accordance with the aim of our study we succeeded in inducing a cognitive load, void of an emotional component. That is, no statistically significant effects on emotional experience were observed. In line with our hypotheses and consistent with earlier research (Gross and Borkovec, 1982, Haynes et al., 1981), 80% of our subjects experienced longer sleep onset after pre-sleep induced cognitive arousal — a sleep onset latency with a mean increase of 8 min, compared to the reference condition.

No

Acknowledgements

This study was financially supported by the agency for Innovation by Science and Technology (IWT).

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