The Effects of a Nighttime Nap on the Error-Monitoring Functions During Extended Wakefulness

Transcription

1 EFFECTS OF A NIGHTTIME NAP ON ERROR-MONITORING The Effects of a Nighttime Nap on the Error-Monitoring Functions During Extended Wakefulness Shoichi Asaoka, PhD 1,2 ; Kazuhiko Fukuda, PhD 3 ; Timothy I. Murphy, PhD 4 ; Takashi Abe, PhD 1,2 ; Yuichi Inoue, PhD, MD 1,2 1 Department of Somnology, Tokyo Medical University, Tokyo, Japan; 2 Japan Somnology Center, Neuropsychiatric Research Institute, Tokyo, Japan; 3 Faculty of Sociology, Edogawa University, Chiba, Japan; 4 Department of Psychology, Brock University, St Catharines, Ontario, Canada Study Objectives: To examine the effects of a 1-hr nighttime nap, and the associated sleep inertia, on the error-monitoring functions during extended wakefulness using the 2 event-related potential components thought to reflect error detection and emotional or motivational evaluation of the error, i.e., the error-related negativity/error-negativity (ERN/Ne) and error-positivity (Pe), respectively. Design: Participants awakened at 07:00 the morning of the experimental day, and performed a stimulus-response compatibility (arrow-orientation) task at 21:00, 02:00, and 03:00. Setting: A cognitive task with EEG data recording was performed in a laboratory setting. Participants: Twenty young adults (mean age 21.3 ± 1.0 yr, 14 males) participated. Interventions: Half of the participants took a 1-hr nap, and the others had a 1-hr awake-rest period from 01:00-02:00. Measurements and Results: Behavioral performance and amplitude of the Pe declined after midnight (i.e., 02:00 and 03:00) compared with the 21:00 task period in both groups. During the task period starting at 03:00, the participants in the awake-rest condition reported less alertness and showed fewer correct responses than those who napped. However, there were no effects of a nap on the amplitude of the ERN/Ne or Pe. Conclusions: Our results suggest that a 1-hr nap can alleviate the decline in subjective alertness and response accuracy during nighttime; however, error-monitoring functions, especially emotional or motivational evaluation of the error, might remain impaired by extended wakefulness even after the nap. This phenomenon could imply that night-shift workers experiencing extended wakefulness should not overestimate the positive effects of a nighttime 1-hr nap during extended wakefulness. Keywords: Nighttime nap, error monitoring, error-related negativity/error negativity, error positivity, night work Citation: Asaoka S; Fukuda K; Murphy TI; Abe T; Inoue Y. The effects of a nighttime nap on the error-monitoring functions during extended wakefulness. SLEEP 2012;35(6): INTRODUCTION If workers or drivers are aware of their own errors immediately after any incorrect behavior, they can correct their behavior before the occurrence of further errors that may result in a potentially deadly outcome. Therefore, this error-monitoring function is essential to prevent tragic accidents. Error-monitoring functions are primarily reflected in 2 event-related potential (ERP) components, i.e., error-related negativity 1,2 or errornegativity (ERN/Ne) and error-positivity (Pe). 3 The ERN/Ne is a negative deflection observed most prominently at FCz approximately 80 ms after an incorrect response, and is thought to primarily reflect performance monitoring, including errordetection. 4-6 The Pe is a positive component typically observed over parietal regions between ms after incorrect responses. This component is thought to be a P3-like component evoked by one s own error response. 7-9 The Pe is thought to reflect either possibly emotional or motivational evaluation of the error 10 or conscious recognition of the error. 8,11 Some researchers have shown that extended wakefulness attenuates this performance-monitoring function, reflected in these 2 ERP components. Scheffers and colleagues 12 reported Submitted for publication May, 2011 Submitted in final revised form January, 2012 Accepted for publication January, 2012 Address correspondence to: Shoichi Asaoka, PhD, Department of Somnology, Tokyo Medical University, 6-7-1, Nishishinjuku, Shinjuku-ku, Tokyo , Japan; Tel: (ext 5757); Fax: ; asaoka@gmail.com that ERN/Ne amplitude was reduced during 1 night of extended wakefulness; however, they did not report any effects on the Pe. Tsai and colleagues 13 showed that amplitudes of ERN/Ne and Pe declined after 1 night of sleep deprivation. However, in another experiment conducted in the same laboratory, they reported that the Pe was not reduced when study participants were instructed to correct any observed errors. 14 On the other hand, Murphy and colleagues 15 used a smaller amount of sleep deprivation (20 hr) and found no significant reduction in ERN/ Ne amplitude despite a significant reduction in Pe amplitude. Although the effect of sleepiness caused by extended wakefulness on the ERN/Ne and Pe has not been completely consistent among these experiments, taken as a whole these results strongly suggest deterioration of the error-monitoring function during extended wakefulness. In modern society, there are many people engaged in shift work. They must work at night against their internal biological clock regulating their sleep-wake pattern. In addition, this nighttime work tends to be preceded by an extended period of wakefulness. 16,17 Many studies suggest that during a night shift these workers often experience severe sleepiness, leading to the increased occurrence of accidents during this time frame Therefore, their sleepiness is thought to be affected by homeostatic processes as well as the circadian process of sleep regulation. For night- or rotation-shift workers, naps during the night shift are thought to be an effective countermeasure for sleepiness and possibly reduce the occurrence of job-related errors However, naps can also have a negative effect on workplace safety because of sleep inertia, an uncomfortable residual sleepiness experienced during the transient period SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

2 from sleep to full wakefulness. Previous studies have shown that cognitive performance as reflected in reaction time and/or response accuracy is lower during this transient period. 23,26-32 A previous study 33 also reported a diminished Pe amplitude during sleep inertia after a 1-hr afternoon nap. This result suggests that emotional or motivational evaluation of the error or conscious recognition of the error could be impaired immediately after the offset of nap. Severity of sleep inertia is influenced by several factors, such as existence of prior sleep deprivation and time of day of awakening as well as sleep duration and sleep stage prior to awakening. 30 Sleep inertia becomes more severe when participants have sleep debt, 34,35 when waking at the time near the nadir of core body temperature (i.e., early morning), 4,36 or when waking from deep sleep. 34,37 Shift workers who have a nap during night work often awaken during the period near the nadir of core body temperature and are liable to awaken from slowwave sleep; therefore, it is possible that they will experience more acute sleep inertia, leading to more severe deterioration of the error-monitoring function. Thus, naps taken after midnight could potentially have mixed effects on the error-monitoring function after extended wakefulness. However, there have been no studies exploring the effects of a nap on error monitoring in this situation. This study was designed to examine the effects of a nighttime 1-hr nap, and the associated sleep inertia, on error-monitoring function as reflected in the 2 previously described ERP components (i.e., ERN/Ne and Pe) after extended wakefulness (i.e. participants kept awake for 18 hr prior to nap or rest period). METHODS Participants Twenty healthy young adults (mean age 21.3 ± 1.0 yr, 14 males) without subjective sleep problems or habitual daytime napping consented to participate in this study. Before being accepted into the study, possible participants were screened using questionnaires regarding their daily sleep habits; those with extremely irregular sleep patterns and/or heavy consumers of alcohol, tobacco, or caffeine were excluded from the study. Written informed consent was obtained from all participants before the experiment. Participants completing the entire protocol were paid an honorarium. Half of the participants (mean age 21.5 ± 1.0 yr, 7 males) were randomly assigned to the nap condition, and the other participants were assigned to the rest condition (mean age 21.1 ± 1.1 yr, 7 males). There were no significant differences between these 2 groups in terms of age [t (18) = 0.86, P = 0.40] and morningness-eveningness preference 38 [t (18) = 0.28, P = 0.78], which is known to be related to the tolerance for nighttime work and/or rotation of shift work schedules. 39 Procedure Participants were instructed to ensure 7-hr sleep from 00:00 to 07:00 and to take no naps during the 3 days preceding the experiment. They were also prohibited from consuming caffeine and alcohol on the experimental day and the day prior to the experiment. Excessive physical exercise on the experimental day was also prohibited. Participants were asked to record sleep logs for 5 days prior to the experimental day and they also wore an actigraph (Actiwatch-L ; Mini-Mitter/Respironics, Bend, OR) for 3 days before the experiment to confirm their sleep-wake pattern. In both nap and rest conditions, participants awakened at 07:00 the morning of the experimental day and were prohibited from sleeping until the end of experiment except for the planned nap (01:00-02:00) in the nap group. The first cognitive task period started at 21:00 in an air-conditioned, soundproof chamber. In the nap condition, participants went to bed at 01:00, and they were awakened at 02:00. Ninety seconds after sleep offset, the second cognitive task period started, and the third task period started at 03:00. In the rest condition, participants had a 1-hr rest period in the experimental chamber instead of a nap, followed by performance of the cognitive task at 02:00 and 03:00. Thus, participants remained awake for 20 hr at 03:00 in rest condition. Twenty hr is the shortest period of extended wakefulness that has been reported to affect the error-monitoring function in previous studies. 15 Participants were prohibited from exiting the experimental chamber from the start of the first cognitive task period to the end of the task period starting at 03:00, except for going to the lavatory. They were allowed to read magazines, books, comics, and newspapers during their 1-hr rest period and between the end of each cognitive task period and the start of the next period. The brightness in the experimental chamber was kept below 150 lx at the participants eye level during resting period, 30 lx during each cognitive task period, and 0 lx during the nap. After each cognitive task period, participants were asked to report their subjective estimation of alertness, sadness, tension, loss of motivation, happiness, weariness, calmness, and sleepiness, using a visual analog scale (VAS). 40 Task We tested a stimulus-response compatibility task referred to as the arrow-orientation (AO) task. 41 According to taxonomy described by Kornblum, 42 the AO task is in the type 8 ensemble (e.g., a spatial Stroop task). In this task, a white fixation cross on a black background was presented for 300 ms in the center of a computer monitor, placed 1 m in front of the participant. Then, a white arrow (pointing up or down) was presented above or below the fixation cross for 200 ms (Figure 1). Thus, stimuli consisted of 2 compatible and 2 incompatible stimuli in relation to the direction in which the arrow was pointing. The display then became blank for 500 ms until the next fixation point was presented. The task was to respond to the pointing direction of the arrow (up or down), but not to the location (above or below), by pressing a button with the corresponding hand. Both speed and accuracy were emphasized to the participants during task instructions. To familiarize participants with the task, a practice task (40 trials 4 blocks) was performed before the electroencephalogram (EEG) electrode attachment. Each experimental task period consisted of 4 blocks of 300 trials each. Participants had a 1-min rest period between each block. They also practiced the task (12 trials) before each task period. Each experimental period lasted approximately 25 min. Previous research from this laboratory has reported error rates of 5-6% for compatible stimuli and 15-16% for incompatible stimuli. 33 SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

3 Recording The EEG was recorded from FCz, C3, C4, Pz, Oz, A1 (left earlobe), and A2 (right earlobe) with Ag/AgCl electrodes using the averaged potential from A1 and A2 electrodes as the reference. Horizontal electrooculograms were recorded from the left and right outer canthi, and vertical electrooculograms from above and below the left eye. In the nap condition, the electromyograms (EMGs) were bipolarly recorded from the left and right side of the chin muscle. These were recorded with Hz high-pass and 140 Hz low-pass filters, using the biopotential amplifier (Leonardo Brainmap L48, Royal Medical Systems AG, Muehlheim am Main, Germany). All physiologic signals were digitized at a rate of 500 Hz. Behavioral Measures and ERP Analysis For each task period, reaction time (RT) for correct trials and number of correct responses were computed. These variables were calculated separately according to stimulus compatibility and condition. EEG artifacts due to eye blinks were corrected using the method outlined by Gratton et al. 43 It has been reported that the ERN/Ne and Pe may be accurately quantified with as few as 6 to 8 erroneous segments. 44 However, in comparison with incompatible stimuli, there were relatively fewer errors to compatible stimuli (e.g., 2 participants made only 2 errors for compatible stimuli in the task period starting at 21:00); therefore, we could not obtain stable ERP averaged waveforms for 5 participants in at least 1 task period. Thus, ERPs were calculated using only the segments with incompatible stimuli. We averaged responselocked waveforms with error and correct trials, respectively, and subtracted correct trial averages from error trial averages to clarify the ERN/Ne and Pe waveform for scoring. Finally, ERP waveforms were filtered off-line with a 10-Hz, high-cut filter. Mean voltage from ms prior to the response was used as a baseline, i.e., it was set to zero, to minimize any influence of the stimulus-related P3, 15 which is the large positive component observed approximately ms after the stimulus onset. The average RT for incompatible stimuli was approximately 400 ms in this study; thus, the period used for the baseline corresponded to the time that the fixation was presented on the display. ERN/ Ne amplitude was measured at FCz as the most negative peak voltage in the time window ranging from 50 ms before to 150 ms after the response relative to the baseline. The Pe amplitude was measured at Pz as the mean voltage from ms after the response relative to the baseline in accordance with previous studies examining these ERPs during extended wakefulness. 15,33 Polysomnographic Analysis Sleep stage scoring of the naps was performed off-line according to standard criteria using the electrooculogram, chin-emg, and EEG data from C3, C4, and Oz. 45 Total sleep time, time spent in each sleep stage, and movement time were determined. Statistical Analysis The sleep variables during the 3 nights (00:00-07:00) before the experimental day were calculated from the actigraph data using software algorithms (Actiware version 5.04 Mini-Mitter/ Respironics, Bend, OR). The sleep parameters were averaged across all 3 nights and compared across conditions using Welch s t tests. Using conditions and task periods as independent variables, each subjective measure from the VAS and 2 ERP amplitudes were compared with a 2 (condition: nap, rest) by 3 (time: 21:00, 02:00, 03:00) 2-way mixed analysis of variance. RT for correct responses and number of correct responses were compared with 3-way mixed analyses of variance using stimulus type (compatible versus incompatible) as an independent variable in addition to the 2 factors listed previously. If any interactions were significant, simple effects analyses were performed. Post hoc analyses were done using the Bonferroni correction. RESULTS Figure 1 The 4 types of arrow stimuli for the arrow orientation task. Participants were required to press the upper button for the 2 stimuli on the right (3 and 4) and the lower button for the other 2 stimuli (1 and 2). The stimuli presented in the outside positions (1 and 4) are compatible, and the other 2 (2 and 3) are incompatible. Nocturnal Sleep Before the Experiment Comparisons of sleep variables derived from the actigraphy data showed that there were no differences in sleep time (rest: ± 25.1 min, nap: ± 30.0 min, t < 1 ), snooze time (rest: 12.2 ± 6.8 min, nap: 14.8 ± 15.7 min, t < 1), sleep efficiency (rest: 82.6 ± 6.0%, nap: 85.0 ± 7.14%, t < 1), and wake after sleep onset (rest: 43.9 ± 17.2 min, nap: 42.2 ± 19.3 min, t < 1) between the 2 conditions. Nap Architecture Participants were kept awake continuously after 07:00 the morning of the experimental day. Those in the rest condition remained awake while those in the nap condition took a 1-hr nighttime nap from 01:00 to 02:00. The 1-hr nap period consisted, on average, of 5.5 ± 4.0 min of stage 1 sleep, 24.5 ± 10.7 min of stage 2 sleep, 20.4 ± 9.2 min of stage 3 sleep, 2.8 ± 4.4 min of stage 4 sleep, and 0.2 ± 0.3 min of movement time; every participant had at least 1 slow-wave sleep epoch, but no stage of rapid eye movement. Average total sleep time was 53.2 ± 9.0 min. Four participants were awakened from stage 3 sleep, and the other participants were awakened from stage 2 sleep. RT for Correct Responses In general, participants had shorter RTs [F (1, 18) = , P < 0.001, pη 2 = 0.93] for compatible stimuli (363 ± 8 ms) in comparison with those for incompatible stimuli (408 ± 9 ms) (Figure 2). The main effects of task period were significant in terms of RT [F (2, 36) = 15.10, P < 0.001, pη 2 = 0.46]. Post hoc analyses showed that participants responded slower at 02:00 and 03:00 than at 21:00 (P < 0.05, respectively), and RT at 02:00 was slower than that at 03:00 (P < 0.05). The interaction of task period stimulus type was also significant for RT [F (2, 36) = 9.30, P < 0.001, pη 2 = 0.34]. The simple effects analysis showed that the RT for compatible stimuli at 21:00 was SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

4 Reaction time (ms) Rest/Compatible Nap/Compatible Rest/Incompatible Nap/Incompatible Number of correct responses Rest/Compatible Nap/Compatible Rest/Incompatible Nap/Incompatible 0 0 Figure 2 Reaction time for correct responses at each task period. Error bars represent the standard errors. Figure 3 Number of correct responses at each task period. Error bars represent the standard errors. shorter than at 02:00 and 03:00 (P < 0.01). For incompatible stimuli, RT at 02:00 was slower than that in the other task periods (P < 0.05). The main effect of condition and other interactions were not significant for RT. Number of Correct Responses In general, participants had more correct responses for compatible stimuli than for incompatible stimuli [543 ± 9 vs. 441 ± 13, F (1, 18) = 68.13, P < 0.001, pη 2 = 0.79] (Figure 3). The main effect of task period was significant for the number of correct responses [F (2, 36) = 3.59, P < 0.05, pη 2 = 0.17]. Post hoc analyses showed that participants had fewer correct responses at 03:00 than at 21:00 (P < 0.05). The interaction of condition task period was also significant [F (2, 36) = 4.38, P < 0.05, pη 2 = 0.20]. The results of the following simple effects analysis revealed that the significant difference in the number of correct responses between 21:00 and 03:00 was observed only in the rest group, and the number of correct responses was larger in the nap group compared with the rest group at 03:00 (P < 0.05). In addition, the interaction of task period stimulus type was significant [F (2, 36) = 7.86, P < 0.01, pη 2 = 0.30]. Simple effects analysis showed that the number of correct responses for compatible stimuli at 21:00 was larger than that at 03:00 (P < 0.01), and the number tended to be larger than that at 02:00 (P = 0.09), although there were no differences between the task periods in terms of incompatible stimuli. The other interaction and main effects of nap were not significant in terms of the number of correct responses. Subjective Measures Subjective alertness showed significant main effects of condition [F (1, 18) = 8.02, P < 0.05, pη 2 = 0.31] and task period [F (2, 36) = 14.88, P < 0.001, pη 2 = 0.45], and a significant interaction of condition task period [F (2, 36) = 8.08, P < 0.01, pη 2 = 0.31]. Simple effects analysis showed that subjective alertness of the nap group was higher than that of the rest group at 02:00 and 03:00 (P < 0.01, respectively), whereas there was no difference between the groups at 21:00. The analysis also showed that the deterioration of subjective alertness at 02:00 and 03:00 compared with that at 21:00 was confirmed only in the rest group (P < 0.001). Subjective sleepiness was higher at 02:00 and 03:00 than at 21:00 [main effect of task periods, F (2, 36) = 9.32, P < 0.001, pη 2 = 0.34; post hoc, P < 0.01, respectively], but there were no significant interactions or main effects of condition. Subjective tension was higher at 21:00 than that at 03:00 [main effect of task period, F (2, 36) = 4.95, P < 0.05, pη 2 = 0.21; post hoc, P < 0.05]. In terms of motivation, the main effect of task period was significant [F (2, 36) = 8.71, P < 0.01, pη 2 = 0.33], and the interaction was in the expected direction although it failed to reach significance [F (2, 36) = 2.55, P = 0.09, pη 2 = 0.12]. Simple effects analysis showed that the rest group had higher motivation scores at 21:00 than at 03:00 (P < 0.01), and the participants of the nap group reported significantly lower motivation at 02:00 than at 21:00 (P < 0.05). Subjective happiness significantly declined at 02:00 and tended to decline at 03:00 than at 21:00 [main effect of task period, F (2, 36) = 5.22, P < 0.05, pη 2 = 0.23, post hoc, P < 0.01, P = 0.09, respectively]. The score of weariness was higher at 03:00 than that at 21:00 [main effect of task period, F (2, 36) = 4.38, P < 0.05, pη 2 = 0.20, post hoc P < 0.01]. (See Table 1.) ERP Measures Response-locked ERPs are shown in Figure 4A. The difference waves (erroneous correct response) shown in Figure 4B showed a large negativity (ERN/Ne) peaking at approximately 50 ms after the response, and a later positivity (Pe) peaking SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

5 Table 1 The results of subjective measures at the end of each task period Rest Nap Rest Nap Rest Nap Alertness (23.28) (14.99) (9.58) (18.73) (21.09) (29.19) Sadness (26.76) (36.13) (20.16) (33.89) (18.55) (33.16) Tension (23.93) (31.68) (20.63) (25.67) (23.98) (19.40) Motivation (14.69) (10.90) (17.22) (25.41) (20.57) (14.97) Happiness (15.70) (19.01) (14.40) (24.21) (15.59) (24.81) Weariness (15.14) (18.10) (26.46) (16.57) (19.12) (19.12) Calmness (22.02) (18.16) (22.44) (22.08) (29.74) (20.91) Sleepiness (17.99) (20.03) (14.26) (27.41) (29.08) (19.83) Values are expressed as mean (standard deviation). A FCz Rest/Error Nap/Error Rest/Correct Nap/Correct Pz B ERN/Ne Rest condition Nap condition FCz Pz Pe Figure 4 Waveforms of response-locked ERPs for erroneous responses and correct responses (A), and difference waves (B) (erroneous correct response). ERN/Ne, error-related negativity/error negativity; Pe, error positivity. at approximately 290 ms. ERN/Ne and Pe showed maximum amplitudes at FCz and at Pz, respectively. The number of segments with erroneous responses for incompatible stimuli used for the averaging was per task period in the nap condi- SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

6 tion and in the rest condition. As hypothesized, there was a decline in the ERN/Ne amplitude at FCz across the task period and the main effect was significant [F (2, 36) = 4.54, P = 0.02, pη 2 = 0.20]. The results of post hoc analyses showed that the amplitude at 21:00 tend to be larger than that at 03:00; however, it failed to reach significance (P = 0.06). In terms of the amplitude of the Pe at Pz, the main effect of task period was significant [F (2, 36) = 6.95, P < 0.01, pη 2 = 0.28]. Post hoc analyses showed declines in the Pe amplitude at both 02:00 and 03:00 compared with that at 21:00 (P < 0.05, respectively). However, main effect of condition [ERN/Ne: F < 1, pη 2 = 0.00; Pe: F < 1, pη 2 = 0.00] and interaction of condition task period [ERN/Ne: F < 1, pη 2 = 0.05; Pe: F < 1, pη 2 = 0.01] for the amplitudes of ERN/Ne and Pe were not significant. DISCUSSION We explored the effects of a 1-hr nap on cognitive performance, especially focusing on ERP components associated with error-monitoring functions during extended wakefulness. The deterioration of various cognitive functions during extended wakefulness has been previously reported in numerous studies. 46 In the current experiment, delayed response and deterioration of response accuracy during the late-night task periods were also observed. Furthermore, the amplitude of the Pe significantly decreased at 02:00 and 03:00 compared with that at 21:00, whereas the ERN/Ne amplitude did not clearly show a significant decline among the task periods. These results are compatible with the findings of a previous study, 15 which showed that 20 hr of wakefulness caused significant declines in Pe amplitude, but not in ERN amplitude. Previous studies have advocated the effectiveness of a nap to maintain cognitive performance and alertness levels during nighttime work The results of the current study confirmed the effectiveness of a nap on subjective alertness and accuracy of the responses during extended wakefulness. However, of particular note, our study revealed that there were no significant recovery effects of nap on error-monitoring functions as reflected in the amplitudes of ERN/Ne and Pe. This result implies that the workers experiencing extended wakefulness might not be able to adequately evaluate their own errors even after a 1-hr nighttime nap, and therefore it is possible they may underestimate the significance of an error. This result does not appear to be to the result of low power only. The behavioral and subjective effects accounted for large amounts of variance (pη 2 ranging from = 0.17 to 0.93 with many above 0.30), whereas the ERP results related to condition failed to account for significant variance (pη 2 ranging from ). This limited effect of nap on cognitive function might be partly attributed the vulnerability of the Pe to sleepiness. Some previous studies also reported that the effects of sleepiness on behavioral measures (i.e., reaction time and/or response accuracy) and psychophysiologic measures reflecting error-monitoring function, especially Pe amplitude, were incongruent, and psychophysiologic measures were sensitive to sleepiness. 15,33 In this study, there were no significant differences in terms of subjective sleepiness between groups, and this could suggest that a 1-hr nap could not completely diminish the sleepiness resulting from 18 hr of extended wakefulness. Accordingly, the decline of subjective evaluation processes relevant to one s own error reflected in ERP components could not be sufficiently restored by the nap. If executive function is defined as the ability to plan and coordinate a willful action in the face of alternatives, to monitor and update action as necessary on the task at hand, 47 the amplitudes of the ERN/Ne and Pe can be considered to reflect some aspects of executive functions. Previous studies have shown that executive functions are vulnerable to sleepiness 46,47 ; therefore, the results of this study are consistent with this suggestion. However, the mechanism that causes vulnerability of the error monitoring function to sleepiness is unclear. Previous research has revealed that Pe amplitude is reduced by increasing attentional demand while performing a cognitive task 48 and the decline of Pe amplitude with sleepiness might be prevented by the redirection of attention to the error responses with the explicit instruction of immediately correcting errors. 14 Therefore, it might be speculated that attentional resources reduced by sleepiness and its control regarding participants response strategy might be associated with these incongruent results between the correct response rate and Pe amplitude. In this study, partially recovered attentional resources after taking a nap might be directed toward performing the cognitive task accurately, but not the error evaluation processes. Further research will be required to examine the possibility in more detail. On the other hand, the subjective evaluation process for one s own error was reported to be disturbed due to sleep inertia after a 1-hr daytime nap. 33 As mentioned previously, sleep inertia is known to become more severe after arising during the period near the nadir of body temperature and when individuals have a sleep deficit. 30 In general, body temperature becomes higher in the afternoon and lower during the night. Therefore, it is plausible that severity of sleep inertia and disturbance of error-monitoring functions immediately after the nap in this study was higher than in our previous study, which explored the effects of daytime nap. 33 However, there were only minimal effects of sleep inertia on cognitive performance in this study. This phenomenon might be related to the fact that more than half of participants were awakened from stage 2 sleep. Additionally, in this study the cognitive functions under the condition with sleep inertia were compared with those during extended wakefulness at 02:00, when the participants were expected to have a certain decline in cognitive performance, but not with those during the fully awake condition. This protocol might reduce the difference of cognitive performance between the groups after the 1-hr active rest or nap, possibly leading to a masking of the effects of sleep inertia on these functions. However, because sleep inertia has been reported to primarily affect speed but not accuracy, 30 it is possible that the effects of sleep inertia on RT diminished the nap effects on this parameter after the nap. It might cause the difference between the effects of nap on RT compared with the number of correct responses. Concerning the time course of sleep inertia, the results of previous studies were inconsistent, ranging from 3 min to 2 hr. 30 It has previously been reported that there is approximately min of sleep inertia after a short (< 1 hr) nighttime nap in a daytime sleep condition. 22 However, because participants in this study were exposed to moderate sleep deprivation, it is possible that a longer duration of sleep inertia occurred in comparison with that of this previous study. SLEEP, Vol. 35, No. 6, Effects of a Nap on Error-Monitoring Asaoka et al

7 There were some limitations in the current study. First, the relatively small number of participants in this study and the between-subjects design was not completely ideal. However, every measure used in this study showed no statistically significant difference between the groups at baseline before the 1-hr nap/rest period i.e., at 21:00, and the effect sizes of the interactions of condition by task period for the measures that failed to reach significance were small. Therefore, the results concerning the differences of RTs and ERPs between the conditions would likely not change, even if additional participants were enrolled and/or a within-subjects design was adopted. Second, our results might not be representative of error-monitoring function during nighttime work in the general population. In a more natural workplace, workers might have naps of longer than 1 hr that might begin at various times other than at 01:00. Follow-up studies might examine the effects of nap length and its timing. In conclusion, a 1-hr nap could be helpful for maintaining or reestablishing response accuracy and subjective sleepiness, but not for reaction speed and error-monitoring functions. Therefore, night-shift workers with extended wakefulness should not overestimate the effects of a 1-hr nap during the night. Error monitoring is a critical function in reducing the likelihood of tragic accidents, and our data show that a 1-hr nap during extended wakefulness may be inadequate compensation for people such as healthcare workers who require high levels of attentiveness to perform their job safely. In addition, considering the fact that the disturbed error evaluation might lead to an overestimation of performance, 33 workers and employers should be aware of any possible uncertainty in terms of workers self-estimation for their performance not only during overnight extended wakefulness without a nap but also after a nap. However, the results of some research have shown that a shorter duration (e.g., 20 min) nap is desirable for maintaining workers alertness during the night. 23,25 Further research with various sleep schedule settings and nap durations before and during nighttime experimental periods will be required to determine optimal schedules to minimize sleepiness and maximize safety. ACKNOWLEDGMENTS Work for this study was performed at Department of Somnology, Tokyo Medical University, Tokyo, Japan. This research was supported by KAKENHI (Grant-in-Aid for Young Scientists (B), No and No ) from the Japan Society for the Promotion of Science to Dr. Asaoka. DISCLOSURE STATEMENT This was not an industry supported study. The authors have indicated no financial conflicts of interest. REFERENCES 1. Gehring WJ, Coles MGH, Meyer DE, Donchin E. The error-related negativity: an event-related brain potential accompanying errors. Psychophysiology 1990;27:S Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E. 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