SHORT NOTE http://dx.doi.org/xxxxxxxxxxxxxxx
Sleep to Implement an Intention Susanne Diekelmann, PhD1,3; Ines Wilhelm, PhD1; Ullrich Wagner, PhD2; Jan Born, PhD1,3
1 Department of Neuroendocrinology, University of Lübeck, Lübeck, Germany; 2Division of Mind and Brain Research, Department of Psychiatry and Psychotherapy, Charité University Medicine Berlin, Berlin, Germany; 3Department of Medical Psychology and Behavioral Neurobiology, University of Tübingen and Center for Integrative Neuroscience, University of Tübingen, Tübingen, Germany
Study Objectives: Sleep supports the consolidation of new memories. However, this effect has mainly been shown for memories of past events. Here we investigated the role of sleep for the implementation of intentions for the future. Design: Subjects were instructed on a plan that had to be executed after a delay of 2 days. After plan instruction, subjects were either allowed to sleep or stayed awake for one night (Exp. 1) or had a 3-h sleep period either during the early night (SWS-rich sleep) or late night (REM-rich sleep; Exp. 2). In both experiments, retesting took place 2 days later after one recovery night. Setting: Sleep laboratory. Patients or Participants: A total of 56 healthy young adults participated in the study. Interventions: N/A. Measurements and Results: All of the subjects who were allowed to sleep after plan instruction executed the intention 2 days later, whereas only 61% of wake subjects did so (P = 0.004; Exp. 1). Also after early SWS-rich sleep all of the subjects remembered to execute the intention, but only 55% did so after late REM-rich sleep (P = 0.015; Exp. 2). Conclusions: Sleep, especially SWS, plays an important role for the successful implementation of delayed intentions. Keywords: Intentional memory, plans, consolidation, sleep, SWS, REM sleep Citation: Diekelmann S; Wilhelm I; Wagner U; Born J. Sleep to implement an intention. SLEEP 2013;36(1):XXX-XXX.
INTRODUCTION Planning for the future is a central feature of human cognition. The ability to form plans for future behavior and to implement the planned behavior at a specific point in the future represents an essential prerequisite for meaningful goal-directed behavior.1 Successful implementation of an intention requires a prospective memory for the intention that allows executing the planned action at the appropriate time.2 Sleep is well known to benefit the consolidation of memories.3 Subjects who are allowed to sleep after learning show better memory retention than subjects who spend an equivalent amount of time awake.4 Sleep thereby actively facilitates the consolidation and reorganization of memories for longterm storage rather than merely passively protecting memories against decay and interference.5 However, the beneficial effect of sleep on memory has been shown mainly for memories of past events, whereas the possible role of sleep for memories of plans and intentions for the future remained widely neglected.6 Here, we asked whether sleep supports the implementation of a plan after a delay of two days in a relatively naturalistic task and whether this effect depends on slow wave sleep (SWS) or REM sleep.
young adults participated in Experiment 1 and Experiment 2, respectively. All subjects reported regular sleep-wake cycles (≥ 6 h sleep per night); had no history of any neurological, psychiatric, or endocrine disorder; and did not take any medication at the time of the experiments. Prior to the experimental night, subjects in the sleep groups spent one adaptation night in the sleep laboratory. All subjects gave written informed consent and were paid for participation. Experimental Task Plans for future behavior were experimentally induced by means of a task introduced as a vigilance task (Figure 1A). During the initial “plan induction session,” subjects were required to rapidly respond to a dot appearing on the left or right side of a computer screen by pressing the corresponding button. The task included 40 trials with the dot appearing every 2-10 sec (task duration approximately 5 min). Importantly, the dot was in a specific color (e.g., red) throughout the session. Subjects were then instructed that at the retest session 2 days later they would be tested again on the task, but on a slightly different version with the dot in another color (e.g., green). The experimenter emphasized that the participant should pay attention that the correct version, with the dot in the new color, would indeed be presented at retesting, because sometimes, due to a software problem, the computer would display the wrong version. If such mistake occurred, the participant should immediately inform the experimenter because otherwise the whole experiment would have been performed in vain. To reduce possible effects of experimenter biases to a minimum but at the same time keep the instruction as naturalistic as possible, the experimenter literally read out a standardized instruction to the subjects. At retesting, without being reminded of the different versions and the instructed plan, all subjects were presented with the allegedly wrong version, i.e., with the dot in the same color as during the plan induction session, and it was recorded whether subjects
METHODS Participants A total of 35 (9 females, mean age [ ± SD] 23.83 ± 3.74 years) and 21 (6 females, mean age 23.90 ± 4.41 years) healthy
Submitted for publication February, 2012 Submitted in final revised form June, 2012 Accepted for publication July, 2012 Address correspondence to: Susanne Diekelmann, PhD, Department of Neuroendocrinology, University of Lübeck, Lübeck, Germany; Tel: +49451-5004602; Fax: +49-451-5003640; E-mail:
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Figure 1—Illustration of the experimental setup and results. (A) Experimental task. In the initial plan induction session, subjects performed on the vigilance task first, before the experimental plan was induced. At retesting after 2 days, it was recorded whether or not subjects executed the plan (i.e., to inform the experimenter about the wrong version). (B) Experimental design of Exp. 1 (sleep vs. wakefulness, upper panel) and Exp. 2 (SWS-rich early nocturnal sleep vs. REM-rich late nocturnal sleep, lower panel). PI (Plan induction), R (Retest). (C-D) Percentage of subjects executing the plan in Exp. 1 and Exp. 2. (E) Time spent in SWS and REM sleep in Exp. 2. Means ± SEM are shown. *P < 0.05, **P < 0.01, ***P < 0.001.
realized the “mistake.” At retesting, a longer version of the vigilance task was used, including 80 trials (task duration approximately 10 min), to allow for more possibilities to detect the mistake. If subjects recognized the mistake, the experimenter immediately started the “correct” version of the vigilance task (including 40 trials again).
somnographic recordings. In the early sleep condition, initial performance on the task and plan instruction took place between 22:30 and 22:45, and subjects went to bed at 23:00 to allow a 3-h period of SWS-rich sleep. Subjects were awakened at ~02:00 and stayed awake in the laboratory until 07:00. After sleeping at home during the second night, they were retested the following morning at ~10:00. In the late sleep condition, subjects first slept for about 3 h between 23:00 and 02:00. To prevent effects of sleep inertia, subjects were always woken up from NREM sleep stages 1 or 2, and the initial session including performance on the task and plan induction started only 30 min after awakening. After this session, subjects went to bed again (~03:30) to spend a 3-h period of REM-rich retention sleep. After awakening in the morning, they left the laboratory and returned for the retest at ~14:00 the next day. The retest was shifted to 14:00 to match between conditions the length of retention intervals and the amount of wakefulness between plan instruction and retesting.
Procedures In Experiment 1, participants were instructed on the task in the evening before a night of sleep (n = 17) or wakefulness (n = 18; Figure 1B, upper panel). Subjects in both conditions reported to the laboratory at 21:00, filled in questionnaires, and in the sleep condition electrodes were attached for standard polysomnographic recordings. Initial performance on the vigilance task and instruction on the plan took place between 22:30 and 22:45 in both conditions. In the sleep condition, subjects were allowed to sleep between 23:00 and 07:00. Subjects in the wake condition stayed awake throughout the night under supervision of an experimenter, spending the time with standardized activities (reading, watching TV, or playing simple games). Subjects in both conditions left the laboratory in the next morning. After spending the day awake and another night of sleep at home, they returned to the laboratory for the retest session at ~10:00. This interval allowed subjects in the waking condition to recover from their initial sleep loss. In Experiment 2, subjects participated either in the early SWS-rich sleep (n = 10) or late REM-rich sleep condition (n = 11; Figure 1B, lower panel). As in Experiment 1, subjects in both conditions reported to the laboratory at 21:00, filled in questionnaires, and were attached to the electrodes for polySLEEP, Vol. 36, No. 1, 2013
Control Variables To control for general alertness and sleepiness, before the initial session and after the retest session subjects rated their subjective sleepiness on the Stanford Sleepiness Scale ranging from 1 (“feeling active, vital, alert, or wide awake”) to 7 (“no longer fighting sleep, sleep onset soon; having dream-like thoughts”). Also, reaction times and error rates in the vigilance task were analyzed. To this end, performance on the vigilance task in the initial session as well as performance on the “correct” version in the retest session was analyzed, i.e., the task that was started after subjects recognized the wrong version. 2
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retrieval of the plan was tested only after a second night, which allowed subjects in the wake condition to recover, excludes the possibility that sleep deprivation confounded retrieval by general changes in attention. When asking the subjects in the end of the experiment whether they actually remembered the instructed intention, all of the subjects reported to recall the instruction, excluding that those subjects who did not realize the mistake had simply forgotten the instruction per se. An explorative analysis of the questionnaire assessing rehearsal and strategies to remember the intention revealed that only 4 subjects used particular strategies (e.g., imagining the colors of traffic lights). Subjects in the sleep group reported that they had engaged in slightly more rehearsal of the instruction than the wake group, particularly during the day after the experimental night.
For those subjects who did not realize the mistake, the first 40 trials of the wrong version were analyzed. The vigilance task duration of 5 min has been found to be sensitive to effects of sleep deprivation and fatigue.7 Standard polysomnographic recordings included electroencephalogram (at C3 and C4), electrooculogram, and electromyogram. Recordings were visually scored offline according to standard criteria.8 In the end of the retest session, subjects were debriefed about the purpose of the experiment. Those subjects who did not realize that they were presented with the wrong task version during retesting were asked by the experimenter whether they actually remembered the instruction. Further, all subjects had to fill out an explorative questionnaire assessing rehearsal of the instruction during the retention interval (i.e., in the evening after the instruction, during the day after the experimental night, and in the morning before the retest session) as well as the use of strategies to remember the instruction.
Experiment 2—SWS-rich vs. REM-rich Sleep To answer the question whether the beneficial effect of sleep on the implementation of intentions depends on SWS or REM sleep, in a second experiment subjects performed the same task as in Experiment 1, receiving exactly the same instructions, but slept thereafter for 3 h either during the early night (dominated by SWS) or during the late night (dominated by REM sleep). After SWS-rich early sleep, all subjects (100%) remembered the experimental plan to inform the experimenter about the allegedly wrong task version, whereas only half the subjects (55%) did so after late REM-rich sleep (χ2 = 5.97, P = 0.015, Figure 1D). As in Experiment 1, most subjects recognized the mistake in the first (n = 6), second (n = 6), third (n = 1), or fourth trial (n = 2). One subject of the REM-rich group recognized the wrong task version only after 57 trials. Again, there was no difference in the time point of recognizing the mistake between groups (P > 0.30). Polysomnographic recordings confirmed that the amount of SWS during the experimental night was 5-fold higher during SWS-rich early than during REM-rich late retention sleep, whereas the amount of REM sleep was about twice as high during late sleep as early retention sleep (P < 0.001, Figure 1E). Time spent in other sleep stages did not differ between the sleep periods (all P > 0.40; S1: 4.0 ± 0.9 vs. 5.0 ± 0.8 min, S2: 98.2 ± 11.2 vs. 108.2 ± 8.2 min, for the SWS-rich and REM-rich group, respectively). However, subjects in the late sleep condition displayed an overall shorter total sleep time than subjects in the early sleep condition (182.1 ± 8.4 vs. 213.6 ± 6.4 min in the REM-rich and SWS-rich group, respectively, P < 0.01). To exclude the possibility that the improved ability to implement the intention after the early period of sleep simply resulted from a longer total sleep time, we omitted the 3 subjects who displayed the longest sleep times in the SWS-rich group as well as the 3 subjects with the shortest sleep times in the REM-rich group from analysis, resulting in comparable total sleep time in both groups (194.9 ± 5.0 vs. 203.7 ± 1.9 min in the REM-rich and SWS-rich group, respectively, P > 0.10). In this subsample, again all of the subjects with high amounts of SWS during the retention interval remembered to execute the plan (100%), whereas only 50% of subjects with predominant REM sleep remembered to do so (χ2 = 4.77, P = 0.029). As in Experiment 1, both the SWS-rich and the REM-rich groups spent the second night at home and sleep time and sleep quality were assessed by self-report. Sleep time as and sleep quality did not significantly
Statistical Analysis The number of subjects who remembered to execute the plan and informed the experimenter about the wrong task version was analyzed using χ2-tests. Control variables were analyzed using analyses of variance (ANOVA) and post hoc t-tests. Level of significance was set to P = 0.05. Greenhouse-Geisser correction for degrees of freedom was applied where appropriate. RESULTS Experiment 1—Sleep vs. Wakefulness All subjects (100%) who slept after initially forming the plan remembered to inform the experimenter about the wrong task version when performing the vigilance task with the different color at delayed retesting, whereas only 61% of the wake subjects realized the mistake (χ2 = 8.26, P = 0.004, Figure 1C). Of those subjects who recognized the wrong task version, most did so in the first (n = 20), second (n = 5), or fourth trial (n = 2). Only one subject of the wake group realized the mistake after 32 trials. There was no difference in the time point of realizing the mistake between groups (P > 0.30). Subjects in the sleep group showed normal sleep patterns during the experimental night (total sleep time: 414.3 ± 14.2 min; stage 1 sleep [S1]: 19.7 ± 2.6 min; stage 2 sleep [S2]: 221.0 ± 10.4 min; SWS: 75.1 ± 4.9 min; and REM sleep: 75.6 ± 5.6 min). Both groups spent the second night at home and sleep time, and sleep quality (from 1 to 5 = “very poor” to “very good”) was assessed by self-report. As expected, subjects in the wake group slept longer during this night, thus compensating for the sleep loss (520 ± 27 vs. 427 ± 19 min, P = 0.009); rated sleep quality was comparable between groups (sleep: 4.41 ± 0.12, wake: 4.44 ± 0.12, P > 0.80). Sleep and wake subjects were closely comparable in reaction times ([in ms] sleep: initial session 318.1 ± 4.8, retest 327.8 ± 8.3; wake: initial session 330.8 ± 6.9, retest 332.6 ± 6.9) and error rates (in %; sleep: initial session 5.1 ± 1.0, retest 2.9 ± 0.8; wake: initial session 7.4 ± 1.2, retest 4.5 ± 0.8), in actual vigilance performance, and in self-reported general sleepiness (sleep: initial session 2.4 ± 0.3, retest 2.2 ± 0.2; wake: initial session 2.2 ± 0.2, retest 2.5 ± 0.2) during the plan induction session and at retesting (all P > 0.14). This, together with the fact that SLEEP, Vol. 36, No. 1, 2013
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differ between groups (SWS-rich vs. REM-rich, sleep time: 519 ± 22 vs. 475 ± 22 min, P > 0.17; sleep quality: 3.70 ± 0.37 vs. 4.27 ± 0.27, P > 0.20). There was no difference between the groups in reaction times ([in ms] sleep: initial session 346.4 ± 11.7, retest 336.8 ± 10.6; wake: initial session 353.4 ± 10.8, retest 339.8 ± 10.4) and error rate (in %; sleep: initial session 4.3 ± 0.7, retest 5.0 ± 0.9; wake: initial session 4.5 ± 0.7, retest 3.2 ± 0.6), in the vigilance task, or in subjective sleepiness (sleep: initial session 2.3 ± 0.2, retest 2.1 ± 0.2; wake: initial session 2.0 ± 0.2, retest 2.1 ± 0.2) during the initial session and at retesting (all P > 0.18). As in Experiment 1, asking the subjects for their memory of the instruction in the end of the experiment confirmed that all of the subjects recalled the instruction. Explorative analyses of the rehearsal/ strategy questionnaire revealed that none of the subjects used particular strategies to remember the instruction, but subjects in the SWS-rich group reported to have engaged in slightly more rehearsal of the instruction, particularly before the retest session in the morning.
slow wave activity, and specific neurotransmitter constellations (e.g., low levels of acetylcholine and cortisol).3 On the other hand, these findings show that sleep does not simply passively protect intentional memory traces against interfering inputs but rather actively facilitates the maintenance of intentions. Particularly, to the sleep/wake comparison of Experiment 1, it could be objected that subjects in the wake group were exposed to a longer period of wakefulness during the retention interval, thus experiencing a higher amount of interference that could have disrupted the intentional memory. In Experiment 2, however, subjects of the SWS-rich and REM-rich sleep groups were exposed to exactly the same amount of wakefulness and sleep during the retention interval, and thus external stimulus inputs were completely comparable for both groups. The finding that, despite similar amounts of interfering inputs and protective sleep periods, only subjects who obtained high amounts of SWS benefited from sleep, indicates that the benefit of sleep for intentions is not a passive protection against wake interference but rather depends on active processes, particularly during SWS.5 The finding that the SWS-rich group outperformed the REMrich group in intention execution is even more striking when considering that the SWS-rich group suffered from partial sleep deprivation during the experimental night. The SWS-rich group was allowed to sleep from 23:00 to 02:00 only and had to stay awake thereafter, whereas the REM-rich group had an almost normal night of sleep with only one forced wake period for the plan induction session. The fact that a short sleep period containing high amounts of SWS can compensate even for the effects of partial sleep deprivation underlines the potential importance of SWS for the successful execution of delayed intentions. Apart from a beneficial effect of sleep, rehearsal of the instructed intention might also have affected the likelihood of executing the intention. One of the main characteristics of prospective memory is that there are no prompts to execute the intention, but rather the individual has to self-generate the intention at the appropriate time. To manage this self-generation successfully, it might be important to keep the intention active in mind over a longer time period. This can be effectively achieved, for example, by occasional self-reminding or rehearsal of the intention. Although we have no conclusive data on the use of rehearsal in the present study, our explorative questionnaire on rehearsal of the instructed intention suggests that subjects in the sleep group and subjects in the SWS-rich sleep group might have rehearsed the instruction slightly more than wake subjects and subjects of the REM-rich group. However, it remains unclear how these differences in rehearsal can be interpreted. It could be speculated that active consolidation processes in the sleep group and the SWS-rich group enhanced the activation and availability of the intentional memory trace thereby increasing the likelihood of spontaneous rehearsal. Alternatively, sleep deprivation in the wake group and circadian differences in the time-point of encoding in the REM-rich group might have impaired the ability or motivation for rehearsal of the instruction. To clarify this issue, the possibility of rehearsal as a factor influencing intention execution should be looked at more closely in future studies using more elaborate measures to assess rehearsal and self-reminding strategies. Together, our results suggest that sleep, and particularly SWS, can foster the implementation of intentions after a delay
DISCUSSION Our findings show that sleep, and especially SWS, is important to keep future intentions active in memory. These findings add to the literature on the role of sleep in memory consolidation by providing evidence that sleep does not only foster consolidation of memories for the past3 and memories for the future in a standard prospective memory task,6 but sleep can also benefit the implementation of intentions in a relatively naturalistic task. We assume that this consolidation during sleep originates from reactivation of the representation during SWS that, aside from hippocampal networks,9 extend to prefrontal cortex regions,10 specifically accommodating intentional aspects of the representation. Intentions are typically thought of consisting of two aspects, a prospective component (intent, to remember that something has to be done) and a retrospective component (content, to remember what has to be done), both of which are necessary for the successful implementation of an intention.2 We assume that sleep benefits both the prospective and retrospective component. However, in the task reported here, we used an intention with a rather “easy” retrospective component, i.e., to remember performing on the vigilance task with a different dot color. Asking subjects after the experiment confirmed that all of the subjects recalled the content of the instructed intention but had simply failed to execute the intention at the appropriate time. Thus, although we cannot fully exclude the possibility that sleep had a subtle effect on the retrospective component as well, the superior ability to implement the intention in sleep subjects and subjects who obtained high amounts of SWS observed in the present study was probably the result of sleepdependent improvements in the prospective component. Future studies will have to apply more complex prospective memory tasks to disentangle the effect of sleep on the prospective and retrospective aspects of intentions. The finding that it is specifically SWS that benefits the execution of an intention is particularly important in two regards. On the one hand, it suggests that the consolidation of intentional memories might depend on physiological processes occurring during SWS, such as hippocampal-neocortical reactivations, SLEEP, Vol. 36, No. 1, 2013
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of two days. Such a mechanism might be highly adaptive in everyday life where we are busily engaged in all kinds of activities while bearing in mind our lasting intentions. Considering the importance of intentions and plans in coordinating everyday life, our findings also give a clear idea of how devastating sleep deprivation can be to efficient human daytime functioning.
2. Kliegel M, McDaniel MA, Einstein GO. Prospective memory: cognitive, neuroscience, developmental, and applied perspectives. Mahwah, NJ: Lawrence Erlbaum Assoc Inc, 2007. 3. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci 2010;11:114-26. 4. Stickgold R. Sleep-dependent memory consolidation. Nature 2005;437:1272-8. 5. Ellenbogen JM, Payne JD, Stickgold R. The role of sleep in declarative memory consolidation: passive, permissive, active or none? Curr Opin Neurobiol 2006;16:716-22. 6. Scullin MK, McDaniel MA. Remembering to execute a goal: sleep on it! Psychol Sci 2010;21:1028-35. 7. Roach GD, Dawson D, Lamond N. Can a shorter psychomotor vigilance task be used as a reasonable substitute for the ten-minute psychomotor vigilance task? Chronobiol Int 2006;23:1379-87. 8. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques, and scoring system for sleep stages of human subjects. Bethesda, MD: US Department of Health, Education, and Welfare - NIH, 1968). 9. Rasch B, Buchel C, Gais S, Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007;315:1426-9. 10. Euston DR, Tatsuno M, McNaughton BL. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 2007;318:1147-50.
ACKNOWLEDGMENTS The authors thank Steffen Sauer and Roland Thele for help with data collection. DISCLOSURE STATEMENT This work was supported by a grant from the Deutsche Forschungsgemeinschaft (SFB 654 “Plasticity and sleep”). The authors have indicated no financial conflicts of interest. REFERENCES
1. Atance CM, O’Neill DK. Episodic future thinking. Trends Cogn Sci 2001;5:533-9.
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