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One night of sleep is insufficient toachieve sleep-to-forget emotionaldecontextualisation processesGaétane Deliensab & Philippe Peigneuxab

a UR2NF – Neuropsychology and Functional Neuroimaging Research Groupat CRCN – Center for Research in Cognition and Neurosciences, UniversitéLibre de Bruxelles (ULB), Brussels, Belgiumb UNI – ULB Neurosciences Institute, Université Libre de Bruxelles (ULB),Brussels, BelgiumPublished online: 28 Oct 2013.

To cite this article: Gaétane Deliens & Philippe Peigneux , Cognition & Emotion (2013): One night of sleep isinsufficient to achieve sleep-to-forget emotional decontextualisation processes, Cognition & Emotion, DOI:10.1080/02699931.2013.844105

To link to this article: http://dx.doi.org/10.1080/02699931.2013.844105

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One night of sleep is insufficient to achieve sleep-to-forget emotional decontextualisation processes

Gaétane Deliens1,2 and Philippe Peigneux1,2

1UR2NF – Neuropsychology and Functional Neuroimaging Research Group at CRCN – Center forResearch in Cognition and Neurosciences, Université Libre de Bruxelles (ULB), Brussels, Belgium2UNI – ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium

Neutral memories unbind from their emotional acquisition context when sleep is allowed the nightafter learning and testing takes place after two additional nights of sleep. However, mood-dependentmemory (MDM) effects are not abolished after a restricted sleep episode mostly featuring non rapid-eye-movement (NREM) or rapid-eye-movement (REM) sleep. Here, we tested whether (1) onenight of sleep featuring several NREM-REM sleep cycles is sufficient to suppress MDM effects and(2) a neutral mood is a sufficiently contrasting state to induce MDM effects, i.e. interfere with therecall of information learned in happy or sad states. Results disclosed MDM effects both in the post-learning sleep and wake conditions, with better recall in congruent than incongruent emotionalcontexts. Our findings suggest that the emotional unbinding needs several consecutive nights of sleepto be complete, and that even subtle mood changes are sufficient to produce MDM effects.

Keywords: Mood-dependent memory; Sleep; Memory consolidation; Mood; Interference.

Although investigated in distinct fields of research

for a long time, cognition and emotion are closely

intermingled processes. Mood states impact various

cognitive processes including learning (Bertels,

Demoulin, Franco, &Destrebecqz, 2013), memory

(Deliens, Gilson, Schmitz, & Peigneux, 2013;

Deliens, Neu, & Peigneux, 2013; Kenealy, 1997),

attention (Tamir & Robinson, 2007) and executive

functions (Phillips, Bull, Adams, & Fraser, 2002).

Two distinct but not mutually exclusive phe-

nomena reflecting interactions between mood and

cognitive processes have been evidenced in the

memory domain, namely the mood-congruent

memory (MCM) and the mood-dependent

Correspondence should be addressed to: Philippe Peigneux and Gaétane Deliens, UR2NF – Neuropsychology and Functional

Neuroimaging Research Unit, Université Libre de Bruxelles, Avenue F.D. Roosevelt 50, B-1050 Brussels, Belgium. E-mail: Philippe.

Peigneux@ulb.ac.be; Gaetane.Deliens@ulb.ac.be

The authors thank Svenia Schreiner for help in data acquisition and Rachel Leproult for her careful proofreading of English

language. Gaétane Deliens is Research Fellows at the Belgian Fonds National de la Recherche Scientifique (FNRS).

This study was supported by FRS-FNRS (Belgian National Fund of Scientific Research—Fonds National Belge de la Recherche

Scientifique) [grant CC 1.5.184.10F].

© 2013 Taylor & Francis 1

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memory (MDM) effects (Forgas & Eich, 2012).The MCM effect is a natural tendency to generatememories that are congruent with the current moodstate. At variance, the MDM effect is evidenced bya higher performance during recall for the learnedmaterial when the mood state during testing issimilar to the mood state during learning, thanwhen it is dissimilar. Whereas MCM is a robusteffect in the literature, MDM effect has been lessconsistently reported (Forgas & Eich, 2012).According to Eich and Macaulay (2000), threemain factors contribute to MDM effects. First,MDM effect would emerge when participantsengage in internal mental processes and generatethemselves the cues during the encoding phase (e.g.when instructed to memorise a list of words byassociating each word with a personal life event)(see Eich &Metcalfe, 1989). Indeed, MCM effectsimply that happy participants (respectively sad)tend to associate each item with a positive personalexperience (respectively negative). Consequently,the mood state is a potent cue for the delayed recallof the learned word, increasing the probability of aMDM effect during retrieval (Forgas & Eich,2012). For the same reasons, MDM effects mightalso emerge more frequently in a free recall condi-tion than in a cued recall or a recognition task(Eich, 1995a). Second, individual personality traitswould modulate sensitivity to emotional interfer-ence (Eich & Macaulay, 2000). And third, MDMeffects would occur when mood states (1) aresufficiently distinctive between the encoding andrecall session [e.g. sadness vs. happiness; Forgas andEich (2012), for a meta-analysis see Ucros (1989)]and (2) are not merely induced before the memorytask but are also continuously maintained duringthe task (e.g. by using an emotional backgroundmusic, see Eich, Macaulay, & Ryan, 1994). Fur-thermore, MDM effects would only be observedwhen changes in the emotional state are authenticrather than simulated (Eich & Macaulay, 2000).Accordingly, prior studies have found MDM afterinducing strongly contrasted moods during encod-ing and retrieval (e.g. sadness vs. happiness; forinstances see Deliens, Gilson et al., 2013; Deliens,Neu et al., 2013; Kenealy, 1997). It remains unclearwhether such mood-dependent effects are observed

when happy or sad moods are not opposed, but arecontrasted with a more intermediate, relativelyneutral mood state, an hypothesis tested in thepresent study.

Beside the relationships between memory andemotion, it is now widely recognised that post-learning sleep participates in the consolidation ofnovel information in long-term memory stores(Peigneux & Smith, 2010). How sleep modulatesMDM effects over time remains a barely investi-gated area, with seemingly paradoxical results.Although it was suggested that the mood-dependent effects are stronger with longer reten-tion intervals (Eich, 1995a), we showed that thepost-learning sleep but not wakefulness intervalsactually reduce MDM effects (Deliens, Gilsonet al., 2013). In this recent study, participantslearned a list of word pairs following a mood (sadvs. happy) induction procedure (MIP), then sleptor stayed awake during the post-learning night.After two recovery nights, all participants recalled50% of the word pairs after induction of the samemood than during learning, and 50% after induc-tion of a different mood state. Our results disclosedpreserved MDM effects in the post-learning sleepdeprived condition, but not anymore in the sleepcondition, in line with the predictions of theSleep to Forget and Sleep to Remember (SFSR)hypothesis (van der Helm & Walker, 2009). TheSFSR model proposes that sleep, and especiallyrapid-eye-movement (REM) sleep, promotes thedecoupling of the core information (here a verbalmemory) from its irrelevant emotional context,consequently reducing MDM effects as observedafter three nights of post-learning sleep in ourstudy (Deliens, Gilson et al., 2013). Therefore,we subsequently tested the van der Helm andWalker’s (2009) hypothesis of a specific role forREM sleep in the emotional unbinding processesusing a partial sleep deprivation paradigm aimed atcomparing “early” versus “late” periods of noc-turnal sleep, dominated by non rapid-eye-move-ment (NREM) and REM sleep respectively(Deliens, Neu et al., 2013). At variance with theSFSR prediction, however, MDM effects wereactually observed both in the early and late sleepconditions. Altogether, these results suggest that

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the demodulation process initiated during the firstpost-learning night, potentially during REM sleep,might need either several nights or at least severalsuccessive NREM-REM cycles across a wholenight to be complete.

In the present study, we tested the hypothesisthat the emotional unbinding process needs severalsuccessive NREM-REM cycles across a wholenight to achieve. To do so, we compared MDMeffects after a 12-hour post-learning interval, eitherfilled with daytime wakefulness or nocturnal sleep.Twenty-six participants learned a list of neutralword pairs after a happy or sad MIP (usingcombined imagery vignettes and music), either inthe morning (wake condition) or in the evening(sleep condition). They were then tested 12 hourslater after nocturnal sleep or daytime wakefulness.During the retrieval session, half of the list wasrecalled after a similar mood induction than duringthe encoding session [non-interference condition(NIC)]; the other half was recalled after a relativelyneutral mood induction [interference condi-tion (IC)].

METHOD

Subjects

Twenty-six young women (mean age ± SD 20.08 ±1.09 years) gave their written informed consent toparticipate in this study approved by the FacultyEthics Committee at the Université Libre deBruxelles. Since several studies have evidencedwomen as more reactive to MIPs (Gross &Levenson, 1995; Schaefer, Nils, Sanchez, & Philip-pot, 2010), only female participants were tested inthis study. Participants were recruited according tothe following criteria: native French speakers, nohistory of neurological disorders or sleep disorders(Pittsburgh Sleep Quality Index total score < 11;Buysse, Reynolds, Monk, Berman, & Kupfer,1989), Fatigue Severity Scale 3.36 ± .93; Krupp,LaRocca, Muir-Nash, & Steinberg, 1989), nomood disorders (Beck’s Depression scale < 9;Beck, Steer, & Garbin, 1988) and intermediate orneutral chronotype [Horne and Ostberg’s (1976)Morningness–Eveningness Questionnaire: range

36–64]. They were required to keep regular sleeppatterns and fill in sleep logs for the night precedingeach session. They were also asked to refrain fromdrinking alcohol or stimulant drinks (e.g. caffeine,energizers…) before each testing session. All sub-jects participated in both the wake (W) and sleep(S) conditions, spaced one week apart in a counter-balanced randomised order.

Material

A detailed presentation of the material and proce-dures can be found in Deliens, Gilson et al. (2013).Only essential information is reported here. For thelearning task, we used two parallel lists of 40French unrelated words pairs [e.g. cheval—salon(horse—lounge)], randomly assigned across indi-viduals to the sleep and wake conditions.

The MIP was a combined imagery vignettesand music procedure. Participants listened for oneminute to one of the following classic musicpieces: Delibes’s Coppélia, Bach’s BrandenburgConcerto No. 2 and Beethoven Symphony No. 3(happiness induction) and Chopin’s Préludes,Prokofiev’s Alexander Nevsky and Chopin’s Noc-turne No. 15 (sadness induction). Whilst listening,participants had to perform a guided imagery taskon eight vignettes presented on the computer’sscreen in a fixed order at 30-second intervals. Eachvignette was a descriptive sentence of a sad, joyfulor neutral situation (e.g. “A pet you were reallyfond of has died”). Participants were asked toimagine themselves emotionally engaged in eachsituation. For the neutral MIP, we created eightvignettes describing a neutral situation (e.g. “youtake the lift from the first to the fifth level”)combined with white noise. Background whitenoise was selected because it can be argued thatmusic is never emotionally neutral (Krumhansl,1997). Each MIP lasted 5 minutes.

The Affect Grid (Eich & Metcalfe, 1989), theBrief Mood Introspection Scale (BMIS; Mayer &Gaschke, 1988) and a visual analogue scale forvalence (VAS-mood), were administered beforeand after each MIP (neutral, happy or sad) to assesschanges in the emotional state attesting the effec-tiveness of the MIP. The Affect Grid is a nine lines

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by nine columns matrix in which the horizontal axisrepresents emotional valence and the vertical axisindicates arousal level, on a scale ranging from –4(very sad/non-aroused) to +4 (very happy/aroused).The square in the centre of the matrix representsneutral feelings. Subjects were asked to tick thesquare that fitted best their current feelings. TheBMIS is a self-evaluation questionnaire with 16adjectives (4 adjectives specific to each mood state:happiness, serenity, sadness and anger). Subjectswere asked to rank each adjective on a score rangingfrom one (no agree) to four (agree). Mean scoreswere calculated for the four groups of adjectives. Forthe valence VAS, subjects were asked to draw amark on a 100-mm line to indicate their moodperception between two extremes labelled from“very sad” to “very happy”.

Procedure

Participants learned a list of neutral word pairsafter a MIP (sad or happy) followed by a 12-houroff-line retention interval filled with sleep orwakefulness, in a within-subjects counterbalanceddesign. After the retention interval, half of the listwas recalled after a similar MIP than at theencoding session (NIC), and then the other halfafter a neutral MIP (IC). In the wake condition,participants learned the list of word pairs at 8:00(learning) and recalled at 20:00 (testing) after anactive daytime wakefulness period. In the Sleepgroup, subjects learned at 20:00 and were retestedat 8:00 after a night of sleep.

In the study phase, subjects had to fill in theKarolinska Sleepiness Scale (KSS, Åkerstedt &Gillberg, 1990) and to perform on a psychomotorvigilance task (PVT, 5-minutes duration; Dinges &Powell, 1985). Then, they were administered theMIP (either sadness or happiness, counterba-lanced) before learning the word pairs list with themusic played in the background. Immediately afterthe learning session, there was an immediate cuedrecall procedure: the first word of each pairappeared on the computer screen and subjects hadto write the corresponding word. After the subject’sresponse, the computer provided the correct answerto promote an error-free consolidation of items.

This cued recall procedure was repeated untilsubjects were able to recall at least 30 word pairs (i.e. a 75% learning criteria).When a pair was correctlycompleted, it was not presented in subsequent trialsanymore to avoid over-consolidation through repe-tition. The presentation order of the word pairschanged after each presentation of the list to preventserial learning. During the learning session andimmediate recall phases, the music piece used inthe induction procedure was played in a continuousloop to help participants keeping the induced mood.

In the recall session, subjects underwent thesame MIP than at the encoding phase except thatthe piece of music was different from the encodingsession, but aimed at inducing the same mood(NIC). This procedure aimed at precluding thehypothesis that any interference effect would beinherent to the musical piece per se. After havingcompleted the MIP, subjects continued listeningto the music piece, and provided the correspond-ing word upon presentation of the first word ofthe pair for 20 pairs from the learned list. In theIC, the MIP was aimed at inducing a relativelyneutral mood, and white noise replaced music.After that, the 20 other word pairs were recalled inthe same condition, and the white noise used inthe induction procedure was played in a continu-ous loop. The 20 words used in the IC wererandomly allocated to this condition at delayedrecall. The two delayed recall phases were spacedapart by a 20-minute break to minimise interfer-ence of the first mood induction on the secondone (Bertels et al., 2013).

During this break, subjects had to fill in theKSS (Åkerstedt & Gillberg, 1990). They were alsoadministered the PVT (Dinges & Powell, 1985)and several distracting questionnaires. The efficacyof the MIP was also assessed using the AffectGrid, BMIS and VAS-mood scales before andafter each MIP and after each recall session.

The following week, subjects repeated the sameprocedure using a parallel version of the list ofword pairs, while being engaged in the other post-training condition (i.e. Sleep or Wake). Moodinduction at learning was also opposite to themood induced the preceding week (i.e. sadness vs.

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happiness). Figure 1 shows an overview of theexperimental design.

Statistical analyses

Statistical analyses were performed using Statistica7.0 (Statsoft Inc., Tulsa, OK, USA). Repeatedmeasures analyses of variance (ANOVA) con-ducted on relevant parameters (see below) mainlyused only within-subject factors, followed byTukey’s post-hoc tests where appropriate. Signi-ficance was set at p ≤ .05, two-tailed.

RESULTS

Sleep and vigilance variables

Sleep variables

Average sleep duration during the pre-learningnight was higher in the S (8 hours 18 min ± 71min) than in the wake (6 hours 47 min ± 70 min,t(25) = 6.06; p < .001) condition. During the nightafter learning in the sleep condition, subjects slepton average 6 hours 55 min ± 1 hour 17min.

Vigilance variables

Repeated measures ANOVAs were conducted onsubjective (KSS scores) and objective (PVT

median reaction time) vigilance parameters withwithin-subject factors Sleep (Sleep vs. Wake) andSession (Learning vs. Recall). The analysis on self-rated sleepiness scores (KSS) failed to reveal amain effect of sleep (F(1,25) = .15; p > .1) orsession (F(1,25) = .36; p > .1), but disclosed aSleep by Session interaction effect (F(1,25) = 5.33;p < .05). However, Tukey’s post-hoc tests failed todisclose any significant difference or even trendbetween conditions (all p’s > .16).

The analyses on objective vigilance parametersrevealed a main effect of session (F(1,25) = 8.11;p < .01) with slower mean reaction times beforethe recall than the learning sessions, but no maineffect of sleep (F(1,25) = 1.50; p = .23) norinteraction (F(1,25) = .58; p = .45).

Efficacy of the MIP

Separate repeated measure ANOVAs were com-puted on the Affect Grid, BMIS and VAS-moodscores respectively, with the within-subject factorsSessions (at encoding, at congruent mood recalland at incongruent mood recall) and inducedMood (happy vs. sad). Due to data loss, analyseswere conducted on 20 participants for the AffectGrid, 24 for the BMIS and 19 for the VAS-mood.Results disclosed a main effect of Mood with a

Figure 1. Randomised cross-over design with sleep and wake conditions. Groups 1 and 3 were in the sleep condition on the first week of

testing and in the wake condition on the second week (conversely for Groups 2 and 4). A MIP was administrated to participants before the

learning task. Induced mood type at learning and sleep conditions is counterbalanced across subjects in such a way that Groups 1 and 2

learned word pairs after a happy MIP (MIP+) on the first week of testing and after a sad MIP (MIP− ) on the second week (conversely for

Groups 3 and 4). At retrieval, half of the word pairs list is recalled in the same contextual mood state than at learning (NIC), then the other

half of the word pairs list is recalled in a neutral contextual mood state (IC), after a neutral MIP (MIPn).

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more positive valence after happy MIP than after

sad MIP and an interaction between Session and

Mood, but no main effect of Session (see Table 1

for statistics). Tukey’s post-hoc comparisons con-

ducted on the three mood scales confirmed a

similar mood state during encoding and retrieval

in the congruent mood condition for the sad and

happy moods (all p’s > .1). Post-hoc analyses

conducted on VAS and Affect Grid scores

disclosed a different mood state in the incongruent

mood condition for sad and happy moods (all p’s< .038). The effects were not significant using the

BMIS (p > .3).

Emotional interference on verbal memoryconsolidation

A repeated measure ANOVA was computed on

the number of correctly recalled pairs at delayed

recall with the within-subject factors Interval

(Sleep vs. Wake) and Interference [recall in the

same (NIC) vs. different (IC) emotional context].

This analysis disclosed a main effect of Interfer-

ence (F(1,25) = 8.60; p = .007), with a higher

recall score in the non-interference (15.61 ± 3.04

word pairs) than in the IC (14.58 ± 3.69 word

pairs) (Figure 2), and a trend for a better recall

after a retention interval filled with sleep than with

wakefulness (F(1,25) = 3.37; p = .08). The

interaction between Interval and Interference

factors was not significant (F(1,25) = 1.59; p =

.22). Also, the size of the interference effect (NIC

minus IC score) was not different after the post-

learning sleep than after the wake retention

interval (t(25) = 1.26; p = .22).

DISCUSSION

In the present study, we tested two complement-ary hypotheses. First, we tested the hypothesis thata night of post-learning sleep comprising severalNREM-REM sleep cycles is sufficient to unbindmemories from their emotional learning context,eventually reducing or suppressing MDM effects.Second, we tested the hypothesis that subtledifferences between mood states are still sufficientto observe MDM effects, without contrastingopposite mood states such as happiness andsadness. Consequently, participants learned a listof word pairs in a happy or a sad mood state. Afterpost-learning sleep or wakefulness, they had torecall 50% of the word pairs in the same moodstate than during learning (NIC), and the remain-ing 50% in a relatively neutral mood state (IC).Even in a condition in which the participants’mood was modified from an emotional to a

Table 1. Mood questionnaires

Affect grid scores BMIS scores VAS-mood

Induced mood effect F(1,44) = 11.98; p = .001 F(1,48) = 10.38; p = .002 F(1,43) = 17.07; p = .000Sessions effect F(2,88) = .8; p = .45 F(2,96) = 1.79; p = .17 F(2,86) = .64; p = .53Interaction F(2,88) = 11.07; p = .000 F(2,96) = 6.76; p = .002 F(2,86) = 12.83; p = .000

Note: Statistics of the repeated measure ANOVAs for the three mood questionnaires: affect grid scores, BMIS scores and VAS-mood.

Figure 2. Recall scores for words pairs in mood IC and NIC

contexts in the sleep and wake conditions. Errors bars indicate

standard deviations. Significant differences between conditions and

stimulus types are indicated by asterisks, **p < .01.

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relatively neutral state, we found a significantmood-dependent effect with a higher recall inthe NIC than the IC condition. Consequently,this result contradicts Forgas and Eich (2012)statement that only a “substantial shift” in moodcould give rise to a mood-dependent effect.Although it is likely that substantial shifts wouldresult in bigger mood-dependent effects, our datasuggest that MDM can nonetheless be observedafter subtler mood changes. In this respect, Ucros(1989) reported a positive correlation between theamplitude of the difference between mood states(happiness vs. sadness, as opposed to happiness vs.neutral state) and the size of the mood-dependenteffect. Further studies are now needed to invest-igate this relationship. Considering that multiplefactors contribute to daily and/or hourly moodchanges, our findings are important for futureresearch in emphasising that even subtle changesin mood states can influence cognitive processes.Indeed, mood states can vary according to hor-mone levels, social activity and seasonal rhythms(see for e.g. Golder & Macy, 2011) as well ascircadian rhythms, especially for happiness (Mur-ray, Allen, & Trinder, 2002; Murray et al., 2009).Therefore, continuous fluctuations in mood statesincrease the probability to observe MDM effectsin learning and memory studies.

It is worth noticing that only female partici-pants were tested in this study, as women havebeen reported to be more reactive to MIPs (Gross& Levenson, 1995; Schaefer et al., 2010). How-ever, several studies also reported that fluctuationsin endogenous estrogens during the menstrualcycle influence memory formation and mainten-ance, and may also bias learning strategies (for areview see Korol, 2004). For instance, verbalmemory performance was enhanced during theluteal phase (i.e. when estradiol levels are high) inwomen using oestrogen-based oral contraceptives,but did not vary in naturally cycling women(Mordecai, Rubin, & Maki, 2008). Further stud-ies are needed to investigate the possible effects ofthe menstrual cycle on MDM.

Coming back to the effect of post-learning sleeponMDM, we initially found a marked reduction ofthe beneficial effect of a mood overlap between

encoding and retrieval sessions after three consecutivenights of sleep (Deliens, Gilson et al., 2013), in linewith the predictions from the “SFSR” model (vander Helm & Walker, 2009). However, in apparentcontradiction with the SFSR proposal that theunbinding of the emotional context takes placeduring REM sleep especially, we found in asubsequent partial sleep deprivation study a pre-served MDM effect after 3 hours of nocturnal sleepmostly filled either with predominant REM orNREM sleep (Deliens, Neu et al., 2013). Wetherefore reasoned that the emotional unbindingmight be the consequence of a sleep-dependentprocessing that takes place on the long term, viamultiple iterations of REM states throughout thenight, if not throughout multiple nights. Conse-quently, we surmise that the emotional unbindingprocess may complete only after a whole night ofsleep featuring several NREM-REM sleep cycles.If this hypothesis is true, a significant difference inthe size of theMDM effect should have been foundbetween participants sleeping a whole night versusstaying awake between the learning and recallsessions. This prediction was not fulfilled in thepresent study, as we found aMDM effect after boththe post-learning sleep and the post-learning wakeconditions. Considering that our choice to contrasthappy/sad to neutral mood states may have alreadyweakened the MDM effects (Forgas & Eich,2012), our results altogether suggest that a nightof sleep after learning is insufficient to achieve theunbinding of recently learned memories from theiremotional tagging context. Therefore, one remain-ing hypothesis is that several consecutive nights ofsleep including multiple NREM-REM sleep cyclesare needed to achieve the demodulation process. Inthis respect, we demonstrated an unbindingbetween verbal memories and their “affective blan-ket” tone after three nights of sleep as compared toone night of sleep deprivation followed by tworecovery nights of sleep (Deliens, Gilson et al.,2013). Combined with the findings of the presentstudy, these results indicate that the demodulationprocess initiates during the first post-learningnight, putatively during REM sleep if consideringthe SFSR model, but that this process needs several

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nights to be achieved. Further studies are needed toenlighten these issues.

CONCLUSION

To sum up, our results indicate that the succession

of NREM-REM cycles within a single night isinsufficient to achieve the demodulation process

that unbinds memories from their emotional

context, a process that may need several nights ofsleep. To the best of our knowledge, our study is

also the first to demonstrate a mood-dependentretrieval effect between emotional (sad/joy) and

neutral mood states, indicating that even moderatemood changes may affect memory retrieval

processes.

Manuscript received 15 May 2013

Revised manuscript received 9 September 2013

Manuscript accepted 9 September 2013

First published online 25 October 2013

References

Åkerstedt, T., & Gillberg, M. (1990). Subjective andobjective sleepiness in the active individual. Interna-tional Journal of Neuroscience, 52(1–2), 29–37.doi:10.3109/00207459008994241

Beck, A. T., Steer, R. A., & Garbin, M. G. (1988).Psychometric properties of Beck Depression Invent-ory: twenty-five years of evaluation. Clinical Psycho-logy Review, 8, 77–100. doi:10.1016/0272-7358(88)90050-5

Bertels, J., Demoulin, C., Franco, A., & Destrebecqz,A. (2013). Side effects of being blue: Influence of sadmood on visual statistical learning. PLoS ONE, 8,e59832. doi:10.1371/journal.pone.0059832.t003

Buysse, D. J., Reynolds, C. F. 3rd, Monk, T. H.,Berman, S. R., & Kupfer, D. J. (1989). ThePittsburgh sleep quality index: A new instrument forpsychiatric practice and research. Psychiatry Research,28, 193–213. doi:10.1016/0165-1781(89)90047-4

Deliens, G., Gilson, M., Schmitz, R., & Peigneux, P.(2013). Sleep unbinds memories from their emotionalcontext. Cortex, 49(8), 2221–2228. doi:10.1016/j.cortex.2012.11.014

Deliens, G., Neu, D., & Peigneux, P. (2013). Rapid-eye-movement sleep does not seem to unbind

memories from their emotional context. Journal ofSleep Research.

Dinges, D. F., & Powell, J. W. (1985). Microcomputeranalyses of performance on a portable, simple visualRT task during sustained operations. Behavior

Research Methods, Instruments, and Computers, 17,652–655. doi:10.3758/BF03200977

Eich, E. (1995a). Searching for mood dependent mem-ory. Psychological Science, 6(2), 67–75. doi:10.1111/j.1467-9280.1995.tb00309.x

Eich, E., & Macaulay, D. (2000). Fundamental factorsin mood-dependent memory. In J. P. Forgas (Ed.),Feeling and thinking: The role of affect in social

cognition (pp. 109–130). New York, NY: CambridgeUniversity Press.

Eich, E., Macaulay, D., & Ryan, L. (1994). Mooddependent memory for events of the personal past.Journal of Experimental Psychology: General, 123,201–215. doi:10.1037/0096-3445.123.2.201

Eich, E., & Metcalfe, J. (1989). Mood dependentmemory for internal versus external events. Journalof Experimental Psychology: Learning, Memory, and

Cognition, 15, 443. doi:10.1037/0278-7393.15.3.443Forgas, J. P., & Eich, E. (2012). Affective influences on

cognition: Mood congruence, mood dependence,and mood effects on processing strategies. Handbook

of Psychology, Experimental Psychology, 4, 61.Golder, S. A., & Macy, M. W. (2011). Diurnal and

seasonal mood vary with work, sleep, and daylengthacross diverse cultures. Science, 333, 1878–1881.doi:10.1126/science.1202775

Gross, J. J., & Levenson, R. W. (1995). Emotionelicitation using films. Cognition & Emotion, 9(1),87–108. doi:10.1080/02699939508408966

Horne, J. A., & Ostberg, O. (1976). A self-assessmentquestionnaire to determine morningness-eveningnessin human circadian rhythms. International Journal ofChronobiology, 4(2), 97–110.

Kenealy, P. M. (1997). Mood state-dependent retrieval:The effects of induced mood on memory reconsid-ered. The Quarterly Journal of Experimental Psycho-

logy, 50A, 290–317. doi:10.1080/713755711Korol, D. L. (2004). Role of estrogen in balancing

contributions from multiple memory systems. Neu-robiology of Learning and Memory, 82, 309–323.doi:10.1016/j.nlm.2004.07.006

Krumhansl, C. L. (1997). An exploratory study ofmusical emotions and psychophysiology. Canadian

Journal of Experimental Psychology/Revue canadienne de

psychologie expérimentale, 51, 336–353. doi:10.1037/1196-1961.51.4.336

DELIENS AND PEIGNEUX

8 COGNITION AND EMOTION, 2013

Dow

nloa

ded

by [

87.6

6.42

.94]

at 1

3:25

07

Dec

embe

r 20

13

Krupp, L. B., LaRocca, N. G., Muir-Nash, J., &Steinberg, A. D. (1989). The fatigue severity scale.Application to patients with multiple sclerosis andsystemic lupus erythematosus. Archives of Neurology,46, 1121–1123. doi:10.1001/archneur.1989.00520460115022

Mayer, J. D., & Gaschke, Y. N. (1988). The experienceand meta-experience of mood. Journal of Personalityand Social Psychology, 55(1), 102–111. doi:10.1037/0022-3514.55.1.102

Mordecai, K. L., Rubin, L. H., & Maki, P. M. (2008).Effects of menstrual cycle phase and oral contracept-ive use on verbal memory. Hormones and Behavior,54, 286–293. doi:10.1016/j.yhbeh.2008.03.006

Murray, G., Allen, N. B., & Trinder, J. (2002). Moodand the circadian system: Investigation of a circadiancomponent in positive affect. Chronobiology Interna-

tional, 19, 1151–1169. doi:10.1081/CBI-120015956Murray, G., Nicholas, C. L., Kleiman, J., Dwyer, R.,

Carrington, M. J., Allen, N. B., & Trinder, J.(2009). Nature’s clocks and human mood: Thecircadian system modulates reward motivation. Emo-tion, 9, 705–716. doi:10.1037/a0017080

Peigneux, P., & Smith, C. (2010). Memory processing inrelation to sleep. In M. Kryger, T. Roth, & W.

Dement (Eds.), Principles and practice of sleep medicine

(17th ed., pp. 335–347). Philadelphia, PA: Elsevier.Phillips, L. H., Bull, R., Adams, E., & Fraser, L.

(2002). Positive mood and executive function: Evid-ence from Stroop and fluency tasks. Emotion, 2(1),12–22. doi:10.1037/1528-3542.2.1.12

Schaefer, A., Nils, F., Sanchez, X., & Philippot, P.(2010). Assessing the effectiveness of a large databaseof emotion-eliciting films: A new tool for emotionresearchers. Cognition and Emotion, 24, 1153–1172.doi:10.1080/02699930903274322

Tamir, M., & Robinson, M. D. (2007). The happyspotlight: Positive mood and selective attention torewarding information. Personality and Social Psycho-

logy Bulletin, 33, 1124–1136. doi:10.1177/0146167207301030

Ucros, C. G. (1989). Mood state-dependent memory: Ameta-analysis. Cognition and Emotion, 3(2), 139–169. doi:10.1080/02699938908408077

van der Helm, E., & Walker, M. P. (2009). Overnighttherapy? The role of sleep in emotional brain proces-sing. Psychological Bulletin, 135, 731–748. doi:10.1037/a0016570

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