Habitual napping moderates motor performance improvements following a short daytime nap

Abstract

The effect of napping on motor performance was examined in habitual and non-habitual nappers who were randomly assigned to a nap or reading condition. Motor procedural learning and auditory discrimination tasks were administered pre- and post-condition. Both groups reported improved alertness post-nap, but not post-reading. Non-habitual nappers fell asleep faster and tended to have greater sleep efficiency, but did not differ from habitual nappers on other sleep architecture variables. Habitual nappers had greater alpha and theta EEG power in stage 1, and greater delta, alpha and sigma power in stage 2 sleep. Motor performance deteriorated for non-habitual nappers who napped, but improved for all others. The number of sleep spindles and sigma power (13.5–15 Hz) significantly predicted motor performance following the nap, for habitual nappers only. Results indicate that motor learning was consolidated in a brief nap and was associated with stage 2 spindles, but only for those who habitually take naps.

Introduction

Adults may choose to take daytime naps as compensation for lost sleep (replacement naps), in preparation for extended wake time (prophylactic naps), or simply for enjoyment (appetitive naps; Broughton and Dinges, 1989). Research has consistently shown that daytime napping improves mood, alertness, and performance (see Bonnet, 1991, Takahashi, 2003, for reviews). More specifically, a 20-min nap has been shown to be long enough to lead to benefits, but short enough to avoid post-nap grogginess (Hayashi and Hori, 1998, Hayashi et al., 1999a, Hayashi et al., 1999b). The frequency of napping may depend on general health, work demands, and cultural norms; it may also depend on individual differences in the opportunity to nap, as well as napping preference. In healthy adults, there are individuals who prefer to take daytime naps regularly, while others report that they rarely or never nap. Research on the benefits of napping has often restricted the sample to habitual nappers for practical reasons, to ensure that participants would be able to sleep in the laboratory during the daytime (e.g., Taub, 1977, Taub, 1979, Taub, 1982, Taub et al., 1976, Taub et al., 1977). Few studies to date have systematically investigated the benefits of napping in both habitual nappers and non-habitual nappers, and results of these studies have been limited to subjective improvements following naps. It may be that these groups differ in their ability to sleep during a daytime nap, the quality of their sleep, and/or the benefits derived from napping.

Habitual napping has been defined in a variety of ways. For example, Taub et al. (1976) considered individuals who napped in the afternoon one or more times per week, for a half an hour to 2 h, for at least 2 years, as habitual nappers. A similar definition has been used in related studies (Daiss et al., 1986, Lawrence and Shurley, 1972, Taub, 1977, Taub, 1979, Taub, 1982, Taub et al., 1977). Other studies have evaluated how often individuals nap in order to define a “napper.” Evans et al. (1977) defined “nappers” as those who indicated that they sometimes, usually, or always took naps during the day, and “non-nappers” as those who rarely or never napped. In addition, Evans et al. viewed “nappers” as those who found napping to have restorative effects, and “non-nappers” as those who found napping unpleasant. This view was validated by the fact that “nappers” reported feeling less sleepy, more satisfied, and greater subjective benefit than “non-nappers” following a 60-min afternoon nap. Similarly, Spiegel (1981) conducted a study comparing habitual and non-habitual nappers to determine how refreshing they found daytime naps. Results indicated that only habitual nappers awoke refreshed from a nap. One study examined the sleep architecture of a nap in habitual and non-habitual nappers in order to determine if they slept differently (Dinges, 1992). Results indicated that habitual nappers had more stage 1 and more stage shifts during a nap. Thus, daytime sleep for non-habitual nappers was more consolidated, which may in turn lead to greater sleep inertia upon awakening (i.e., grogginess). The extent of sleep inertia experienced by individuals may explain why some people choose not to nap despite opportunity to do so. Additionally, Johnston et al. (2001) reported that there were no polysomnographic differences between habitual and non-habitual nappers in their night time sleep, suggesting that the reason for habitual napping behaviour in young adults is not to compensate for poor sleep on the preceding night.

Few studies have examined the relationship between sleep during a daytime nap and benefits following the nap. In an early study using only habitual nappers, Taub et al. (1976) equated post-nap benefits with sleep itself and not with a particular stage of sleep or nap duration. Subsequently, Taub (1979) reported that stage 4 sleep was associated with increased sleepiness and REM with decreased sleepiness following the nap. More recent studies have applied modern neurophysiological techniques such as quantitative EEG and event-related potentials (ERPs) to investigate the role of sleep in post-nap performance improvements (Takahashi and Arito, 1998, Takahashi and Arito, 2000, Takahashi et al., 1998).

ERPs are brain potentials recorded following the presentation of stimuli that represent various stages of information processing (Picton et al., 1995). The late components of the auditory ERP (N1-P2-P300) vary predictably according to changes in arousal and attention (see Muller-Gass and Campbell, 2002 and Campbell and Colrain, 2002, for reviews). Specifically, during drowsiness and at sleep onset, N1 amplitude decreases while P2 amplitude increases. This change is thought to be due to removal of a long-lasting negative wave called ‘processing negativity’ (PN, Näätänen, 1982, Näätänen, 1990). When attention wanes, the increasing negativity due to PN overlaps and summates with N1 and P2 components. P300 remains apparent only when the subject detects the rare target stimulus (Duncan-Johnson and Donchin, 1977, Cote, 2002). It has thus been interpreted to reflect high-level processing such as stimulus categorization (target versus non-target) or conscious processing of the stimulus (Picton, 1992). Moreover, Donchin and Coles (1988) have proposed that the P300 represents the updating of working memory that is necessary when the infrequently occurring target stimulus is presented. In general, the latency of the P300 reflects the time to stimulus classification, whereas, P300 amplitude reflects the amount of attention allocated (Picton, 1992). P300 latency is delayed and its amplitude diminished following total sleep deprivation (Harsh and Badia, 1989, Lee et al., 2003). Thus, ERPs are an ideal tool for assessing changes in waking cognitive processing that may accompany changes in alertness following a nap.

Takahashi and Arito (2000) and Takahashi et al. (1998) investigated changes to the P300 component of the ERP following a nap. They found that in sleep-deprived participants, P300 latency was shorter following a nap, but its amplitude was not affected. These studies indicate that napping in sleep-deprived individuals improves information processing capabilities, particularly stimulus evaluation time. In another study, Takahashi and Arito (1998) reported that greater delta power during a nap was associated with a longer P300 latency following the nap, indicating that deeper sleep was associated with slowed information processing, likely due to sleep inertia. In these studies, there was no differentiation made between habitual and non-habitual nappers, which would allow for investigation of whether changes in waking performance following a nap might be related to experience with napping.

In order to explore individual differences in napping behaviour, the present study first investigated whether habitual and non-habitual nappers differed in their sleep architecture (i.e., time in various sleep stages) and/or EEG characteristics during a nap. EEG power values that reflect depth or quality of sleep, such as delta and theta power, may differ between habitual nappers and non-habitual nappers. In addition, differences in sleep phasic events, such as K-complexes and sleep spindles, may represent individual differences in sleep-related information processing such as consolidation of newly learned skills. Such EEG characteristics may predict performance improvements following a nap.

Recent research in the field of sleep has focused on the hypothesis that sleep is required for the efficient consolidation of newly learned skills and information (see Smith et al., 2003, for review). Specifically, following stage 2 sleep disruption, memory for motor procedural skills is compromised (Smith and McNeil, 1994). Additionally, an intense period of motor skills learning has been found to increase the duration of stage 2 sleep, stage 2 sleep spindles, and sigma power during a subsequent nocturnal sleep period (Fogel et al., 2001). Nader and Smith (2003) reported that the association between spindles/sigma power and motor learning was most robust at midline sites. Together, these findings indicate that stage 2 sleep may be particularly important for the efficient consolidation of motor skills memory. Whereas, it was once thought a full night of sleep was necessary for consolidation of learning to take place, recent studies demonstrate that the association between sleep and learning can be shown in a brief daytime nap (Mednick et al., 2002, Mednick et al., 2003). Specifically, it was shown that consolidation of a visual texture discrimination task occurred following 60- and 90-min naps that contained both slow-wave sleep (SWS) and rapid-eye movement (REM) sleep (Mednick et al., 2003).

The aim of the present study was to investigate whether experience with napping moderates performance benefits following a brief 20 min nap, particularly memory of newly learned skills. The present study was designed to (i) investigate the difference between habitual nappers and non-habitual nappers in terms of EEG characteristics in a nap; (ii) investigate how waking function, as measured by event-related potentials (ERPs), performance, and subjective measures, differs between habitual nappers and non-habitual nappers following a nap; (iii) examine whether EEG characteristics of the nap might predict unique post-nap performance for habitual nappers and non-habitual nappers; (iv) examine how other personality characteristics may underlie individual differences in napping behaviour. Habitual nappers and non-habitual nappers were hypothesized to have different EEG characteristics within an afternoon nap; it was expected that these differences would influence the benefits of napping. Specifically, it was thought that sleep spindles and sigma power might predict performance improvements on a procedural motor task following a nap, since they have previously been shown to be related to consolidation of motor learning following a full night of sleep. An ERP task was used to provide behavioural data on reaction time (a measure known to be sensitive to sleepiness), and neurophysiological data on information processing. It was predicted that group differences in the benefits of napping (i.e., improved physiological alertness and attention) would be reflected in increased N1 and decreased P2 amplitudes following the nap. In addition, P300 latency and RT data were investigated to determine if napping leads to changes in motor ability (e.g., if RT delayed but not P300), or in stimulus evaluation processes (e.g., if P300 latency delayed but not RT). In general, benefits of napping were expected for participants in the nap condition, and especially for those who habitually nap. To investigate these hypotheses, a 20-min nap in young adults was employed because a brief nap is most often recommended to restore alertness, will result in minimal sleep inertia, and will normally contain mostly stage 2 non-REM sleep, a period with high spindle density. This would allow for the role of stage 2 sleep in the consolidation of procedural motor learning to be investigated in isolation given that 20-min naps would generally be too short for slow-wave sleep or REM sleep to take place.