Simple motor memory has been shown to benefit from sleep; however, more complex motor skills have rarely been investigated so far. We investigated complex motor learning using a dance mat and choreographies in 36 healthy, young male subjects. Subjects performed one song and two new songs in three sessions distributed over 24 h to test sequence-specific learning and skill transfer. Each song had a unique choreography. One group learned the main song in the evening and was retested 12 and 24 h later on the main song and each one new song (PM-AM-PM). The second group underwent the same procedure; however, the first session was in the morning (AM-PM-AM). Thus, one group slept before the first retest (PM-AM-PM) while the other group slept between the first and the second retest (AM-PM-AM). Regarding sequence-specific learning, sleep induced a significant difference between the groups, which disappeared after both groups had slept. A significant transfer effect occurred independent of sleep. During both new songs, no difference between the groups was seen; however, the second and third songs were learned significantly faster than the first song. This study could show that complex motor sequence learning benefits from sleep while skill transfer seems to occur independently of sleep.

An overwhelming body of literature points to beneficial effects of sleep on memory consolidation [1,2,3]. This seems to be true for simple motor tasks (e.g. sequential finger tapping [1,2,3,4,5]) as well as for more complex motor skills (e.g. mirror tracing or trampolining [6,7]). However, simple motor sequence learning has been investigated far more thoroughly with regard to the effects of sleep than with regard to more complex motor sequence tasks, although research on online memory encoding showed that principles developed through the study of simple skills are not generalizable to more complex skills [8].

For simple motor sequence tasks an improvement can be induced by a whole night of sleep [4,5,9] as well as just a short nap [10,11,12,13,14]. The complexity of learning influences sleep-related improvements: subjects show similar overnight improvements in speed whether learning a five-element unimanual sequence, a nine-element unimanual sequence, or a five-element bimanual sequence in the finger tapping task, but they show increased overnight improvements with a nine-element bimanual sequence. Further, individual transition within the motor sequence that appears most difficult shows a stronger increase in speed overnight [15]. Interestingly, motor – tapping a finger in time with a rhythm – and perceptual – monitoring a rhythm for deviants – shares in temporal rhythm skill improve through sleep as well [16].

However, not only pure skill learning is important for memory processes: flexibility and the ability to transfer new skills to similar tasks are crucial as well. For example, the ability to transfer an original finger-tapping sequence to the other hand – known as bilateral transfer [17] – seems to be facilitated by sleep [18,19]. However, only the extrinsic or ‘goal’-oriented transfer rather than the intrinsic/movement-oriented transfer benefitted from sleep. Goal-oriented transfer was tested by using the other hand to tap the original sequence, while for the intrinsic transfer the mirror sequence was used [18,19]. Additionally, after learning a new motor task, healthy controls show a significant transfer to a similar task while patients with depression and schizophrenia do not seem to express this transfer [20]. It remains unclear what exactly this transfer process signifies. The effect of sleep on transfer has mainly been investigated in declarative memory tasks. It has been proposed that it may demonstrate a generalization and abstraction of newly acquired knowledge [21,22,23,24]. In motor skills, it may represent familiarization with the procedure (e.g. how to handle the testing unit) or the task itself. Transfer may also consist of more than just handling the testing unit. Trained musicians will learn a new piece of music and dancers a new dance move far more rapidly than beginners in the field. Furthermore, after learning a new skill (e.g. a full kayak roll) a similar task will be learned faster (e.g. a half roll) [8,17]. The ability to transfer new skills to similar tasks may signify the creation of a schema in which the similar task can be integrated and therefore learned faster [17,25]. The importance of schema building for systems consolidation of declarative knowledge has been shown previously [26,27,28,29]. Furthermore, it has been proposed that sleep may play a role in schema building [30]; however, this has not been proven so far.

To investigate the effect of sleep on complex motor sequence learning and transfer of motor skills, we utilized the video game DanceStage (Playstation 2, Sony), during which subjects are required to dance a set choreography on a dance mat. Dance choreographies are complex motor sequences with only minor repetitions compared with a simple motor sequence task such as the finger-tapping task. The subjects danced to one song in three sessions distributed over 24 h to test sequence-specific learning. Additionally, two new songs were danced at the retests to test for motor skill transfer. Each song was comprised of a unique choreography, which stayed the same for that song throughout the experiment. Half the subjects slept before the first retest (RT1), while the other half slept before the second retest (RT2).

Subjects

The experimental subjects were healthy, male volunteers (n = 36) aged 18–30 years. They were recruited mainly via the university and were paid for their participation in the study. We screened the subjects for psychiatric, physical or sleep disorders with a semi-structured interview, physical examination and the Pittsburgh Sleep Quality Index [31]. Further exclusion criteria were: shift work at night, a transmeridian flight or medical treatment during the last 3 months, substance abuse, having played the game DanceStage or other dancing games before, playing an instrument or taking dance classes regularly. The participants agreed to have regular sleep patterns throughout the experiment. The subjects were not aware of the aims and hypotheses of the study.

The Ethics Committee of the Ludwig Maximilian University Faculty of Medicine, Munich, Germany, approved this research project and the study is in accordance with the 1964 Declaration of Helsinki. All subjects gave their informed written consent prior to their inclusion in the study.

Procedures

The subjects were randomly divided into two groups of 18 subjects each. Group A subjects arrived in the morning, learned the DanceStage task and were retested 12 and 24 h later (8:00–20:00–8:00), while group B subjects arrived the first time in the evening and underwent the retest 12 and 24 h later (20:00–8:00–20:00). This resulted in half the subjects sleeping before RT1 while the other half slept before RT2. The participants were asked to refrain from rehearsal and sleep during the day. Subjective sleep lengths between the tests were noted as well.

Learning Task

To test complex motor sequence learning, we used the video game DanceStage (Playstation 2, Sony). For this task, the subjects are required to dance a set choreography, which is presented with four arrows (front, back, left and right) on a screen, on a dance mat with equivalent arrows printed on the corresponding positions. The game measures whether the subject stepped on the correct arrow and how accurately the movement corresponded to the rhythm of the music. The game gives constant visual feedback on how well the movement was executed. All these parameters are then summarized in one total score. The test apparatus provides a unique choreography for each song. Thus one song always corresponds to one set of sequential movements. The subjects were tested with one main song (for motor sequence learning) and with two other songs to test for transfer of the new motor skill to a similar task. We used three songs of similar difficulty, randomized as transfer or main songs and balanced across all subjects.

A fourth song was used during the initial visit. The subjects danced to this song once to accustom themselves to the task panel. Afterwards, they danced to the main song three times in a row. When they returned, 12 h later, they first danced three times to their main song and subsequently three times to a new song. This procedure was repeated after another 12 h with the main song and a different new song. For the study design, see figure 1. The three songs lasted 3 or 4 min.

Fig. 1

Study design. The subjects came three times (group A: 8:00–20:00–8:00 and group B: 20:00–8:00–20:00) to dance on the Playstation 2 game DanceStage. During the first visit, they danced three times to the main song (song 1) (LP), while on the second visit they first performed song 1 again three times (RT1), after which they performed a new song (song 2) three times to test for transfer (T1). All subjects returned again 12 h later to repeat song 1 again three times (RT2) and then danced another new song (song 3) three times (T2). Group A slept between the second and the third visit, while group B slept before the second visit.

Fig. 1

Study design. The subjects came three times (group A: 8:00–20:00–8:00 and group B: 20:00–8:00–20:00) to dance on the Playstation 2 game DanceStage. During the first visit, they danced three times to the main song (song 1) (LP), while on the second visit they first performed song 1 again three times (RT1), after which they performed a new song (song 2) three times to test for transfer (T1). All subjects returned again 12 h later to repeat song 1 again three times (RT2) and then danced another new song (song 3) three times (T2). Group A slept between the second and the third visit, while group B slept before the second visit.

Close modal

The average score on the three trials was used as outcome score, measured in points, resulting in three values for the main song, i.e. learning phase (LP), RT1 and RT2, and two transfer values, i.e. first transfer test (T1) and second transfer test (T2).

Statistical Analysis

A repeated-measures ANOVA was used to test the main effects and the interaction effects of the outcome of the main song with the within-subjects factor test (LP, RT1 and RT2) and the between-subjects group (A and B). Further, a repeated-measures ANOVA was used to test the performance on the three different songs with the within-subjects factor test (LP, T1 and T2), the between-subjects group (A and B) and test × group interaction. The results were then further explored with unpaired t tests to compare the two groups with regard to the main song (LP, RT1 and RT2) and transfer testing (T1 and T2). The change in learning speed of the three new songs (LP, T1 and T2) was tested by paired, two-tailed t tests.

Subjective sleep length did not significantly differ between the two groups [group A: 6.8 ± 0.7 h; group B: 7.0 ± 0.97 h; T(34) = 0.798; p > 0.4]. The ANOVA for the main song revealed a significant test × group interaction [F(2, 33) = 3.397; p < 0.05] as well as a significant test effect [F(2, 33) = 62.688; p < 0.001], but no significant group effect [F(2, 33) = 2.089; p > 0.15]. The t test showed that the two groups did not significantly differ in their performance on the main song during LP [outcome score group A: 544,241 ± 125,590; group B: 591,549 ± 85,321; T(34) = 1.322; p > 0.19]. However, during RT1, when group A was in a postwake and group B in a postsleep session, there was a significant difference in the performance [group A: 633,552 ± 97,907; group B: 705,339 ± 73,500; T(34) = 2.488; p = 0.018]. After another 12 h, when group A was in a postwake-sleep and group B in a postsleep-wake session, the two groups did not show any difference in task performance [group A: 732,551 ± 84,661; group B: 732,493 ± 94,288; T(34) = 0.002; p > 0.99; fig. 2]. We additionally calculated the absolute change from one test to the next. From LP to RT1, group A (postwake session) improved by 89,310 while group B (postsleep session) improved by 113,790. From RT1 to RT2, group A (postsleep session) improved by 98,999 while group B (postwake session) improved by 27,154. While the change from RT1 to RT2 was significantly different [T(34) = 2.623; p = 0.007], the change from LP to RT1 did not reach significance (T = 1.052; p = 0.15).

Fig. 2

Shown are the average performances on the first song during the LP, RT1 12 h and RT2 24 h later. Group A slept (white arrow) between RT1 and RT2, while group B slept (black arrow) between LP and RT1. While the groups did not significantly differ at LP and RT2, group B performed significantly better during RT1 (* p = 0.02).

Fig. 2

Shown are the average performances on the first song during the LP, RT1 12 h and RT2 24 h later. Group A slept (white arrow) between RT1 and RT2, while group B slept (black arrow) between LP and RT1. While the groups did not significantly differ at LP and RT2, group B performed significantly better during RT1 (* p = 0.02).

Close modal

The ANOVA for the transfer song revealed a significant test effect [F(2, 33) = 59.373; p < 0.001], but no significant group effect or test × group interaction [group F(2, 33) = 1.074; p > 0.3; test × group F(2, 33) = 0.594; p > 0.5]. The t test showed that during the transfer tests there was no significant difference between the groups [T1: group A: 699,778 ± 93,761; group B: 718,772 ± 89,798; T(34) = 0.621; p > 0.5; T2: group A: 742,072 ± 83,983; group B: 753,440 ± 90,330; T(34) = 0.391; p > 0.6]. Both groups performed the second and the third songs significantly better than the first [group A: LP vs. T1 T(17) = 5.872; p < 0.001; LP vs. T2 T(17) = 7.179; p < 0.001; group B: LP vs. T1 T(17) = 6.252; p < 0.001; LP vs. T2 T(17) = 7.511; p < 0.001], but the performance on the third song was not better than that on the second [group A: T1 vs. T2 T(17) = 1.831; p = 0.085; group B: T1 vs. T2 T(17) = 1.312; p > 0.2; fig. 3].

Fig. 3

The performance on the first song (LP) and two new songs during the second (T1) and third visits (T2) is shown for the two groups. Both groups performed significantly better on the second (T1) and third (T2) song (** p < 0.001) than on the first song (LP). There was no significant difference between T1 and T2. Group A slept (white arrow) between T1 and T2, while group B slept (black arrow) between LP and T1.

Fig. 3

The performance on the first song (LP) and two new songs during the second (T1) and third visits (T2) is shown for the two groups. Both groups performed significantly better on the second (T1) and third (T2) song (** p < 0.001) than on the first song (LP). There was no significant difference between T1 and T2. Group A slept (white arrow) between T1 and T2, while group B slept (black arrow) between LP and T1.

Close modal

This study tested complex motor sequence learning – performance of one long dance choreography – and transfer – dancing new choreographies on the same test aperture – over a period of 24 h with tests every 12 h. One group learned the main song in the evening and was retested 12 and 24 h later on the main song and each new song (PM-AM-PM). The second group underwent the same procedure; however, the first session was in the morning (AM-PM-AM). Thus half the subjects slept before RT1 while the other half slept between RT1 and RT2. Specific sequence learning benefited from sleep, while transfer occurred independently of sleep.

Complex Motor Sequence Learning

During RT1, the subjects who had already slept after task acquisition performed significantly better than their counterparts. After both groups had slept (RT2), similarly to LP, 24 h earlier, there was no significant difference between the groups. The fact that sleep, whether a nap or a whole night’s sleep [4,5,10,11,14], benefits motor sequence learning is well known. Classically, a finger motor sequence task is used [4,5], which can differ in length from five to nine elements and complexity (one or two hands). It seems that motor skill procedures that proved to be most difficult actually derive most benefit from sleep, with a nine-element bimanual sequence showing a higher increase than simpler sequences [5,15]. Our task is more complex and longer than the motor sequence tasks typically used in sleep and memory research, which should produce an even stronger sleep effect. However, whether the positive impact of sleep on performance in our study represents improvements in motor sequence recitation or in specific rhythm perception and execution cannot be determined. Sleep has been shown to improve motor and perceptual shares in temporal rhythm skill [16]. Further, it is possible that remembering the actual music better after sleep also influenced the performance outcome.

Other studies have investigated sleep and more complex and new motor learning tasks. However, these studies focused on induced changes in sleep features. Buchegger et al. [7] observed an increase in REM sleep after subjects had undergone a 13-week trampolining course. However, Erlacher and Schredl [32] did not see any change in REM sleep in subjects learning how to snakeboard. Perhaps, the difference in skill difficulty could explain the difference in results. We did not record any polysomnograms in this study. Perhaps future studies could combine the two approaches by investigating performance changes in complex motor tasks induced by sleep as well as changes in sleep architecture induced by the tasks.

Transfer of Skills

Additionally to sequence-specific learning, we tested transfer from a newly acquired skill to a similar task and could show that it is apparently not dependent on sleep. In general, when learning a new skill, two different components have to be considered. Learning the sequence or movement and in addition learning the task or procedure itself. After learning the procedure (e.g. how to handle the testing unit), it becomes easier to learn a similar task or movement. For example, after learning a new skill (e.g. a full kayak roll), a similar task will be learned faster (e.g. a half roll) [8,17]. In one study, Ethiopian patients with depression or schizophrenia and controls first learned one sequence of the sequential finger-tapping task and were retested on the first sequence after 24 h [20]. Directly after the retest of the first sequence, the subjects tapped a second, different sequence. The healthy controls displayed a significant practice-dependent increase from the first sequence to the second, while both patient groups only showed a small, nonsignificant increase. This indicates that the healthy subjects, in contrast to the patients, successfully transferred the newly acquired skill – they had never used a computer keyboard before – to a similar task and learned the second sequence significantly faster than the first sequence [20]. Western subjects have already used a computer keyboard before, so the sequential finger-tapping task does not show the properties of a new task and there is no transfer from one sequence to the next [4]. However, it has been shown that memory consolidation of the finger-tapping task is also disturbed in western psychiatric patients [33,34,35,36,37].

This study also used a new task. The subjects first learned one choreography but had to learn a second and a third choreography 12 and 24 h later. Both groups acquired the second choreography significantly faster than the first, showing transfer of the new skill. There was no difference in performance between the second and third song. Since group A slept between the second and third test while group B slept between the first and the second test, transfer seems to be independent of sleep and to solely depend on time.

Transfer may represent the integration of new memories into existing neocortical knowledge or schemata [25]. In general, it has been shown that if new information can be incorporated into an existing schema, memory consolidation from the hippocampus to the neocortex can occur much more rapidly [26,27,28,29]. Further, it has been proposed that sleep may play a role in schema building [30]. Schmidt’s [25] schema theory proposes that a generalized motor program serves as a central, memory-based mechanism for the control of motor skill performance. The generalized motor program is an abstract representation of a class of movements that is stored in memory and retrieved when a skill involving that class of movements is performed [17,25]. Transfer of a motor sequence from the left hand to the right hand, known as bilateral transfer [17], has also been shown. Specifically, transfer for the extrinsic/goal-oriented sequence (original sequence) was saved by nocturnal sleep, while intrinsic/movement-oriented transfer (mirror sequence) was not affected by sleep or wake [18,19]. Cohen et al. [19] proposed that the movement sequence is enhanced over the day whereas only goal-oriented representation is enhanced over a night’s sleep. That no significant sleep-specific transfer effects were seen in our study may perhaps be due to the fact that it did not represent goal-based transfer. However, extrinsic/intrinsic transfer of the same sequence may also represent a different process than transfer of a new skill to a similar task with a different sequence even though both could be viewed as a generalization of skill.

In general, transfer of new skills to similar tasks has been investigated in online memory encoding of motor tasks while the aspect of offline periods and sleep in motor skill transfer has not been investigated as thoroughly [8]. The effect of sleep on transfer has been investigated more thoroughly in declarative memory and has been associated with generalization and abstraction of newly learned content [21,22,23,24].

Time-of-Day Confounder

An important caveat in studies using the AM-PM-AM design is a circadian effect on performance. One previous study attributed apparent sleep effects to a time-of-day confounder [38]. However, this would not explain why a significant difference in memory consolidation is seen in nap studies [10,11,12,13,14]. A more recent study investigated the time-of-day effect by utilizing different time periods of learning/retest (morning/evening) as well as different time periods of sleep (day nap/night sleep) [39]. Kvint et al. [39] could show that during training, the acquisition rate of the sequence order was significantly higher in the AM-trained than in the PM-trained group; however, there were no differences in the kinematic optimization processes. Independent of the timing of sleep, subjects tested higher after sleep compared to wake in both the declarative and implicit learning component of the motor task [39]. In the current study, we found no significant difference in baseline performance between the AM and PM group and when creating an average over all AM and PM testing – main song as well as transfer tests – no significant difference was seen (data not shown). In contrast to the observations of Kvint et al. [39], our AM group performed actually slightly, but not significantly, worse than the PM group during baseline, which argues against an effect induced by the timing of testing. Furthermore, while we did find group differences in the main song during RT2, we did not find any group effect in the new song they performed during RT2. If the difference had been solely induced by the timing of testing, it should have been visible for both songs.

Caveats

The results of this study should be viewed in light of some caveats. Firstly, we only assessed subjective sleep length and quality, which may have been over- or underestimated by the subjects. A further caveat is that while the absolute performance was significantly different in the main song during RT2 between the groups, only the performance change from RT1 to RT2 but not the change from LP to RT1 reached significance. This is most likely due to the small number of participants and thus the study should be replicated with a larger number of subjects.

This study could show that specific sequence learning of a complex motor task seems to benefit from sleep while transfer of a new skill to a similar task seems to occur independently of sleep.

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