• Immediate associative score/80 65.41 (8.80) 63.69 (10.07)
  • Delayed associative score/80 58.13 (9.99) 51.50 (12.74)
  • Delayed relational score/40 20.39 (5.56) 17 (5.80)
    Note. AIT Associative Inference Tasks.
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    SLEEP IMPROVES ASSOCIATIVE AND RELATIONAL MEMORY 179
    referring to distinct types of consolidation that occurred during the learning
    process. The results of both groups (sleep or wake) are presented in Table 2.
    A delayed relational score was based on the number of correct recognition
    during the delayed relational recognition phase. To test our oriented hypothesis of
    a sleep benefit on relational memory performance, a one-tailed student’s t test was
    performed between the sleep (M 20.4, SD 5.56) and the wake group (M 17,
    SD 5.80) on this score. The test confirmed the hypothesis of an enhancement for
    the recognition of relational pairs (p .011, Cohen’s d .60). Concerning the
    relational recognition performance, we performed analysis of covariance controlling for the performance at the immediate associative recognition phase. There was
    a significant effect of the group (sleep and wake) on the relational performance
    after controlling for performance at the immediate associative recognition phase,
    F(2, 61) 5.82, p .019.
    Figure 3. Comparison of memory performance at immediate and delayed associative recognition
    phases.
    Table 2
    Independent Comparisons of the Four Recognition Profiles for Immediate and Delayed Associative
    Phases
    Immediate
    recognition
    Delayed
    recognition
    Sleep group
    M (SD)
    Wake group
    M (SD) p value Cohen’s d
    Incorrect Incorrect 8.00 (6.95) 10.09 (7.83) .282 0.49
    Incorrect Correct 6.58 (3.31) 6.22 (4.10) .702 0.09
    Correct Incorrect 13.87 (4.49) 18.41 (7.59) .015 0.73
    Correct Correct 51.55 (11.27) 45.28 (13.78) .059 0.50
    Note. Nonparametric tests were used in case of violation of the normality assumptions.
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    180 RIBEIRO, GOUNDEN, AND QUAGLINO
    Effect of Emotional Valence and Arousal
    Memory performance was different depending on the emotional valence, F(1,
    61) 75.71, p .001, and not significant for the interaction between valence and
    group, F(1, 61) .569, p .45. A pairwise t test post hoc analysis comparing each
    valence revealed that performance for the neutral valence (M 35.7, SD 6.61)
    was significantly less recognized than negative (M 42.1, SD 7.70) and positive
    (M 41.5, SD 6.99) valence (p .001), whereas positive valence was not
    significantly different from negative emotional valence.
    For relational recognition, a repeated measure ANOVA was performed
    with emotional valence as within-subject factor (negative, neutral, and positive),
    the group as between-subjects factor, and the associative performance of the
    immediate associations as covariance. The results were significantly different for
    emotional valence, F(1, 61) 4.26, p .016, but no interaction effects were
    demonstrated, F(1, 61) 0.79, p .51. Specifically, post hoc comparisons
    revealed that neutral valence (M 5.99, SD 2.54) was less recognized than
    negative (M 7.23, SD 2.22, p .013) and positive (M 7.23, SD 2.53,
    p .002) valence, whereas negative and positive valence were not significantly
    different.
    For the arousal reported by the participant during recognition, the period
    of recognition (immediate/delayed) and the correctness of recognition (association correctly recognized or not) served as an intrasubject factor and the group
    (sleep/wake) as a within-subject factor. Comparisons were significant for
    recognition period, F(1, 61) 8.89, p .004, and correctness, F(1, 61) 97.58,
    p .001. No significant interaction was observed between correctness and
    recognition period. These results suggest that correct recognition at immediate
    (M 3.86, SD 0.11) and delayed recall (M 3.81, SD 0.19) had a higher
    arousal score than incorrect recognition at immediate (M 3.59, SD 0.34)
    and delayed recall (M 3.55, SD 0.35).
    Dream and Memory
    Dream diary. As a reminder, the question in the diary evaluated the link with
    the whole experimental situation and memory performances. Answers were related to
    very different aspects of the study such as participating in a study “I dreamed that I was
    being forced to do an experiment against my will.” Or the associations seen during the
    learning such as “The girl who is tanning in the pictures seen in the experiment.”
    Analysis of the diary revealed that there were nine out of 32 participants in the wake
    group to report one dream or more about the study and 18 out of 31 participants in the
    sleep group to report one dream or more about the study. These 18 participants did not
    perform significantly better than the others in the study. The descriptive results are
    summarized in the Table 3.
    To identify and address the reports in which dreams were linked to specific
    items of the study, four independent evaluators, blind to the objectives and
    assumptions of our research, were recruited. They were requested to identify the
    specific items to which the dream reports were linked. For the sleep group, this
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    SLEEP IMPROVES ASSOCIATIVE AND RELATIONAL MEMORY 181
    revealed that the dreams of 10 out of 18 participants could be linked to one or more
    specific elements, with the remaining eight participants reporting dreams that were
    related only to participation in a study.
    For these 10 participants, 14 different items were identified. These items were
    logically involved in 28 associations (each item was involved in two associations
    according to the properties of the AIT). Among them, 26 were correctly recognized
    by the participants. All items identified by the independent readers were correctly
    recognized in the delayed recognition.
    As indicated in the paragraph on delayed recognition, participants were asked
    to indicate if they believed they dreamed of the association element. Ten out of the
    14 items were reported by participants as dreamed. All associations among these 26
    elements which were reported as dreamed were correctly identified.
    Delayed recognition. Participants in the wake group did not sleep between
    the learning phase and the recognition phase, whereas participants in the sleep
    group did sleep between learning and recognition. During the delayed recognition
    of associations, 15 out of 31 participants in the sleep group reported dreaming about
    one or more associations and eight out of 32 participants in the wake group
    reported dreaming about one or more associations in the past. A comparison of the
    number of associations pointed out by the participants as related to dreams
    between the Sleep group (M 2.81, SD 5.14) and the Wake group (M 0.91,
    SD 2.40) was performed using a Mann–Whitney test. It suggested a significant
    difference between these groups (U 362, p .033).
    As a reminder, participants indicated if they had dreamed about the association by choosing among these responses: “Yes, I don’t know, No.” A one-way
    ANOVA that compared all delayed associative scores depending on the response
    of the participants was performed, F(2, 283) 35.2, p .001. Tuckey’s post hoc
    analysis revealed that associations indicated as dreamed (a Yes response; M 0.91,
    SD 0.29) were better recognized compared with those that were supposedly not
    dreamed (No response; M 0.69, SD 0.47) or for which the participant did not
    know if he or she had dreamed about them (M 0.63, SD 0.48).
    Final questionnaire. In the final questionnaire, 16 out of 30 participants
    reported dreaming about the study in the sleep group. We performed a student’s t
    test comparing the task performance of those who reported dreams about the study
    and those who did not. Only the comparison of memory performance on delayed
    recognition of the associations was significant (p .016, Cohen’s d .91). To be
    descriptive, participants in the sleep group who reported dreaming about the study
    Table 3
    Scores for the Wake Group and Sleep Group Participants Who Reported Dreaming About the Study in
    the Final Questionnaire
    Phases
    Wake group Sleep group
    Dream
    (n 9)
    No dream
    (n 23)
    Dream
    (n 18)
    No dream
    (n 13)
    Immediate recognition 61.9 (10.65) 64.4 (9.99) 67.1 (5.07) 63.1 (12.11)
    Delayed recognition 47.6 (11.4) 53 (13.14) 60.3 (5.98) 55.2 (13.50)
    Relational performances 15 (5.74) 17.8 (5.75) 20.9 (4.09) 19.6 (7.24)
    Note. All scores are reported as such: M (SD).
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    182 RIBEIRO, GOUNDEN, AND QUAGLINO
    in the final questionnaire had an immediate associative score (M 70, SD 5.39)
    that did not differ from those who did not report any dream about the study (M
    66.50, SD 10.67). Participants in the sleep group who reported dreaming about
    the study in the final questionnaire had a better delayed associative score (M
    62.50, SD 5.62) than participants who did not report any dream about the study
    (M 54.10, SD 11.56). Participants in the sleep group who reported dreaming
    about the study in the final questionnaire did not obtain a significantly different
    delayed relational score (M 22.10, SD 1.33) than those who did not report any
    dream about the study (M 18.80, SD 1.40). In other words, participants of the
    sleep group who retrospectively indicated dreaming about the study had better
    performances in associative recognition that those who did not.
    In the wake group, they were four out of 31 participants to report dreaming
    about the study in the final questionnaire. We performed a student’s t test
    comparing the task performances of participants in the wake group who reported
    dreams about the study and those who did not. No comparison for the wake group
    was significant. Overall, participants in the wake group who reported dreaming
    about the study in the final questionnaire had an immediate associative score (M
    60.8, SD 4.76) that did not differ from those who did not report any dream about
    the study (M 64.2, SD 10.74). Participants in the wake group who reported
    dreaming about the study in the final questionnaire did not obtain any significantly
    different delayed associative score (M 51.6, SD 14.89) than those who did not
    report any dream in relation to the study (M 51.5, SD 12.63).
    Complementary Analysis
    For the sleep group, the average sleep duration was 7.21 hr (SD 1.55) in the
    diary and 7.47 (SD 0.99) in the initial questionnaire. For the wake group, the
    average sleep duration was 7.55 (SD 1.85) when reported in the diary and 7.31
    (SD 1.33) in the initial questionnaire. The student’s t test revealed no significant
    effect, t(61) 0.6, p .55.
    The average delay between the learning phase and the delayed recognition
    phase was 12.14 hr (SD 0.53) in the sleep group and 12.17 hr (SD 0.41) in the
    wake group. The t test revealed no significant effect, t(61) 0.25, p .80.
    To summarize, none of the comparisons we performed on these duration were
    significant, suggesting no difference between usual sleep schedules and sleep
    schedules in the present study. There was also no significant difference between the
    two groups on these variables.
    Discussion
    The present study was conducted to investigate how a full night’s sleep in a
    home setting could influence the recognition of visual associations and relational
    inferences based on these associations. Our expectations were to observe a
    quantitative benefit on memory consolidation for participants who slept after
    learning compared with those who remained awake. We also hypothesized that
    emotional salience would influence memory performances. Finally, the link beThis document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
    SLEEP IMPROVES ASSOCIATIVE AND RELATIONAL MEMORY 183
    tween dreaming and memory performances has been evaluated through retrospective evaluation questionnaires and a diary.
    Sleep Impact on Associative and Relational Processes in Memory
    Sleep has an important role in memory consolidation (Stickgold, 2005). In this
    study, we investigated this role and focalized our investigations on the associative
    dimension of memory and on the relations that emerged between these associations. We used the AIT, as it was specifically elaborated to allow these two
    dimensions (associative and relational) and to demonstrate memory enhancement
    for both (Bunsey & Elchenbaum, 1996). As expected in the present study,
    participants who slept had better performances for both associative and relational
    learning than participants who remained awake (Alger & Payne, 2016). Such
    enhancement was previously studied using laboratory investigations and different
    methodological designs. For instance, Ellenbogen and collaborators (2007) tested
    the effect of sleep on associative and relational memory. With a delay between
    learning and recognition similar to the present study, they showed a benefit of sleep
    and named this benefit an inferential boost. Such benefit was also demonstrated
    with nap design in the study of Lau et al. (2010) and of Alger and Payne (2016). Our
    study differed from previous research, as we investigated the sleep benefit for
    associative and relational memory performance using AIT, in the context of a usual
    sleep schedule in a home setting with a 12-hr delay. The fact that memory
    enhancement occurred in such varying situations is a robust confirmation of how
    sleep is critical for memory, notably on the maintenance of its associative and
    relational properties (Diekelmann, Wilhelm, Wagner, & Born, 2013; Klinzing,
    Rasch, Born, & Diekelmann, 2016).
    When a memory is activated during wake times, it tends to lead to changes in
    the memory trace. In contrast, it is interesting to note that this activation seems to
    lead to stabilization during sleep, making it more resistant to interference and
    therefore more likely to be recalled as in the present study (Diekelmann, Büchel,
    Born, & Rasch, 2011; Klinzing et al., 2016). The effect of sleep on associative
    recognition performances operated mainly on correctly learned associations in the
    present study. This corroborated previous results that assumed that sleep has a
    protective effect on previously well-integrated associations (Alger & Payne, 2016;
    Schreiner & Rasch, 2018).
    Emotion Salience, Memory, Dream, and Sleep
    The fact that emotions have a beneficial effect on memory has been extensively
    demonstrated in the past (Reisberg & Hertel, 2003). In our study, emotional
    salience (valence and arousal) is, as expected, linked to better memory performances for the associative and relational dimensions. However, there was no
    significant interaction between sleep, emotion, and memory. With short periods of
    sleep occurring in the afternoon, Alger and Payne (2016) showed an advantage of
    sleep period (comparatively to wake period) over the most emotionally neutral
    associations. In addition, Sopp, Michael, and Mecklinger (2018) studied the
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    184 RIBEIRO, GOUNDEN, AND QUAGLINO
    enhancing effect of a morning nap on associative memory by considering the
    emotional salience of their objects. Like in the present study, their main analysis
    showed a group, time, and emotional salience effect, as well as an interaction effect
    between time and group. Interestingly, they also studied the nature of emotional
    salience effect on associative memory and showed that when the background
    scene of their associated pair (object and background) was negative and highly
    arousing, it had a detrimental effect on memory performances. It is noticeable
    that such detrimental effect did not appear in our present results based on a full
    night’s sleep.
    Among possible explanations, and as a prospect for future studies, it is possible
    that REM-rich sleep and NREM sleep have specific benefits on emotions and that
    their selective effect was combined in this study (Alger & Payne, 2016; Sopp et al.,
    2018). Another interesting point of discussion is that in this research, we encouraged participants to imagine a link between the two photographs without controlling the meaning of this link for them (Alger & Payne, 2016). It is thus difficult to
    establish how the current protocol induced authentic emotions or simply depicted
    emotions without any implication for oneself. As an argument for greater control
    in future studies, Conway argued that emotional content will affect episodic
    memory depending on how the self is at stake (Conway, 2005, 2009). Bennion,
    Payne, and Kensinger (2016) also discussed how information relevant to the future
    will influence the interaction between sleep, emotions, and memory. Therefore, we
    recommend that future studies should provide a situation that truly evokes relevant
    emotions for the participant rather than simply suggesting it with the material.
    A salient feature of sleep is the presence of dreams, which have also been
    posited to influence memory performance (Schredl, 2017). Consistent with recent
    research, the results of the present study demonstrated a link between dream
    content and memory performance (Schoch, Cordi, Schredl, & Rasch, 2019;
    Wamsley & Stickgold, 2019). In the present study, participants who indicated
    retrospectively to have dreamed about the associations had better performances
    than those who did not. This is in line with the research of Ribeiro, Gounden, and
    Quaglino (2016) illustrating how evaluation of sleep and dream contents by the
    means of a smartphone dream diary is informative. Diary evaluation is also
    complementary to a range of retrospective evaluations of sleep and dream activities
    (Ribeiro, Gounden, & Quaglino, 2018). Schredl and collaborators (2019) have
    shown that written report, as in the present study, is susceptible to gather more
    dream report and links with real life. However, reports with this methodology are
    generally shorter than other methods such as voice recorded reports. The number
    of dreams that one can report with only one wake per night can only underestimate
    the actual number of dreams he or she experiences during the whole night (Schoch
    et al., 2019). Consequently, our result, in which we were able to identify links
    between dream reports and memory performances, is encouraging. They indicate
    that the link between content of conscious experience during sleep and episodic
    experience during the day exists and is robust enough to be perceptible with a diary
    methodology.
    The fact that we explicitly encouraged our participants to voluntarily influence
    their dreams may have led to a possible compliance phenomenon that limits the
    scope of our observations. However, it is to be noted that the wake group did not
    elicit much inclusion in their dreams while they were encouraged to influence them.
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    SLEEP IMPROVES ASSOCIATIVE AND RELATIONAL MEMORY 185
    We nevertheless suggest that future studies should avoid such dream-induction
    solicitations to fully demonstrate that dream enhancement on associative and
    relational links occurs naturally.
    Conclusion and Perspective
    In conclusion, this study is a demonstration that a full night’s sleep at home
    improves memory, both at the associative and relational dimensions. Additionally,
    emotionally salient associations were better recognized without a significant
    influence of sleep. We proposed that future studies should evoke emotion rather
    than simply suggesting it with the material. Finally, our results also showed that
    dream experiences are beneficial for memory performance. As a future step, it
    could be interesting to influence the content of dreams to evaluate any subsequent
    improvements in associative and relational performances.
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