dream experience during rem and nrem sleep of

Brain Research Bulletin 63 (2004) 407–413

Dream experience during REM and NREM sleep ofpatients with complex partial seizures

Carlo Cipollia,∗, Enrica Bonannib, Michelangelo Maestrib, Michela Mazzettia, Luigi Murri b

a Department of Psychology, University of Bologna, Viale Berti-Pichat 5, Bologna 40127, Italyb Neurology Unit, Department of Neurosciences, University of Pisa, Italy

Available online 18 May 2004

Abstract

This study examined the effectiveness of the cognitive processes underlying dreaming in patients with complex partial seizures (CPS), byassessing the frequency of recall and the structural organization of dreams reported after awakenings provoked alternately during REM andstage 2 NREM sleep on 12 cognitively unimpaired CPS-patients (six with epileptic focus in the right hemisphere and six in the left one). Eachpatient was recorded for three consecutive nights, respectively, for adaptation to the sleep laboratory context, for polysomnography and fordream collection. The frequency of dream recall was lower after stage 2 NREM sleep than REM sleep, regardless of the side of epileptic focus,while the length and structural organization of dreams did not significantly differ in REM and NREM sleep. However, the length of story-likedreams was influenced by global cognitive functioning during REM sleep. These findings indicate that in CPSs-patients the elaboration ofdream experience is maintained in both REM and NREM sleep, while the access to information for conversion into dream contents and theconsolidation of dream contents is much less effective during NREM rather than during REM sleep. Further studies may distinguish betweenthese two possibilities and enlighten us as to whether the impaired memory functioning during NREM sleep is a side effect of anticonvulsanttreatment.© 2004 Elsevier Inc. All rights reserved.

Keywords: Partial epilepsy; REM and NREM sleep; Dream experience; Memory functioning

1. Introduction

Dream experience of patients with epilepsy seems of in-terest for a comprehensive account of dreaming as one of theoutputs of a complex system of information processing dur-ing sleep[16,17]. The functioning of this system for dreamproduction and recall has shown to be influenced not onlyby variations in the organization of sleep (i.e., stages andcycles: for review, see[24]), but also by sleep disturbances(for example, sleep apnea and narcolepsy).

Some alterations of sleep organization (such as the de-crease of REM sleep, stages 3 and 4 of NREM Sleep andsleep efficiency, and the increase of stages 1 and 2 of NREMsleep) have been more frequently observed in patients withpartial or generalized seizures than in healthy individuals.It seems thus legitimate to expect that the effectiveness of

∗ Corresponding author. Tel.:+39-051-2091816; fax:+39-051-243086.E-mail address: [email protected] (C. Cipolli).

cognitive processes underlying dream production and recallvaries with respect to the type and severity of epilepsy andpresumably according to the brain areas affected by the dis-ease.

The hypothesis of a varying effectiveness of cognitiveprocesses involved in the dream process of epileptic pa-tients, which was suggested by early clinical observations(for review, see[32]), has been recently strengthened by adream-diary study. In this study the frequency of sponta-neous morning recall of dream experience resulted muchhigher in patients with complex partial seizures (CPSs) thanin those with generalized seizures (respectively, in about55% versus 25% of days of the period considered[6]).

It is apparent that this hypothesis can be definitively cor-roborated only by laboratory data, namely by establishingthe frequency and characteristics of dream experience ofepileptic patients for all sleep stages. The data as yet avail-able, however, is largely incomplete, given that dream expe-riences elaborated in NREM sleep have not been assessed.Thus, before any attempt to sketch a comprehensive account

0361-9230/$ – see front matter © 2004 Elsevier Inc. All rights reserved.doi:10.1016/j.brainresbull.2003.12.014

408 C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407–413

of the relationships between sleep disturbances and the func-tioning of cognitive processes involved in dreaming, somepieces of evidence are needed regarding the basic character-istics (such as frequency of recall and structural organiza-tion) of dream experiences reported after awakenings duringNREM as well as REM sleep stages.

We report here the results of a study on the effective-ness of the processes involved in dream experiences elabo-rated by patients with CPSs during REM and stage 2 NREMsleep. Patients with this type of epilepsy were chosen as sup-posed to be more likely to report dream experiences, accord-ing to the available data[1,2]. Moreover, the characteristicsof NREM-dreams were probed in stage 2, as it is presentin all cycles of sleep and with dream recall (DR) frequency(about 50%) close to that of other stages of NREM sleep inhealthy individuals[24,25]. Finally, given the preliminarynature of the expected evidence, the patients sampled werewithout cognitive deficits or brain lesions observable froma CT scan, in order to avoid possible biases (respectively,global or hemisphere-related) in the elaboration or recall ofdream experiences.

2. Materials and methods

2.1. Patients

Twelve patients with CPSs (four males, eight females)were selected among those entered in a dream-diary studycarried out at the Epilepsy Center of the University Hospitalof Pisa (Italy)[6].

To be enrolled patients had to be right-handed and capableto recall at least one dream per week over the 60-days periodof the dream-diary study, to have unilateral EEG focality (seebelow) and no neurological disorder (apart from CPSs), brainlesion (detectable at a CT scan), psychiatric disturbance orsubstantial cognitive deficit. The last constraint implied thatthey had to have scored above the cut-off point of cognitiveimpairment in all psychometric tests applied in the previousstudy, namely: (i) Raven Progressive Matrices[4] for theassessment of general intellectual and abstractive ability;(ii) Wechsler Memory Scale[35] for verbal memory span;(iii) Corsi Blocks Test[23] for spatial memory span; (iv)Immediate Visual Memory Test[19] for visual short-termmemory; (v) Benton Visual Retention Test[5] for visuallong-term memory.

Patients were classified as having a well-lateralizedtemporal region EEG focus in the right (R)- or left(L)-hemisphere (respectively, six and six) according to thetemporal region where scalp EEG abnormalities (sharpwaves and spikes as well as focal slow wave activities) wereobserved during wakefulness or during sleep following apartial sleep deprivation. Patients were receiving anticonvul-sant medication for<6 and >1 years with one or two con-ventional (carbamazepine, valproate) or newer antiepilepticdrugs (topiramate, lamotrigine), with daily doses stable for

at least 30 days before the study. The serum concentrationlevels for the former drugs were within therapeutic ranges,but were not available for the latter. Drugs type and doseswere comparable for patients with right and left EEG focus.

The study protocol was approved by the local EthicalCommittee. Informed written consent was obtained from allpatients.

2.2. Procedure

Each patient spent three consecutive nights (from 11 p.m.to 7 a.m.) in the Sleep Laboratory at the Neurology Unit ofthe University of Pisa.

Polygraphic sleep recording (Planet 200-Sistema Galileo,Esaote Biomedica, Firenze, Italy) included eight EEG(F1-C3, C3-P3, P3-O1, F2-C4, C4-P4, P4-O2, C3-A2,C4-A1) with electrodes positioned according to the 10-20International System, two electro-oculogram channels (rightand left outer canthi), one chin-EMG channel. Sleep stageswere assessed according to Rechtschaffen and Kales’[27]criteria.

The first night was intended for adaptation to laboratorycondition, the second (baseline) for evaluation of sleep orga-nization and the third night (experimental) for dream collec-tion. During the third night, awakenings in REM and NREMsleep were balanced over the two halves of the night, asthe length and complexity of dream experiences have beenshown to increase along with sleep cycles[25]. Provokedawakenings were scheduled after 5 min of the first four pe-riods of REM and stage 2 NREM sleep subsequent to eachREM period, amounting to, at the most, eight awakeningsper night. Stage 2 was chosen to probe NREM-dream char-acteristics as present in all sleep cycles and usually in ahigher proportion in the sleep of epileptic patients[3], to-gether with a DR frequency (about 50%) close to those ofother stages of NREM sleep in healthy individuals[24].

Dream reports of all patients were collected by the sameinvestigator (E.B.) using the non-directive instruction sug-gested by Foulkes[15], namely: “What was going throughyour mind before awakening?” Having completed the ver-bal report of the spontaneously recalled dream contents, pa-tients were asked to go back to sleep, and the procedure wasrepeated until the morning awakening (about 7:00 a.m.).

2.3. Report analysis

All dream reports were tape-recorded and subsequentlytranscribed. According to Cohen’s[12] criteria, reports wereclassified as contentful (i.e., with at least one sentence de-scribing contents of dream experience) or contentless (with-out such a sentence). Only contentful reports were taken intoaccount to evaluate the frequency of dream recall.

Investigators preliminarily pruned each contentful reportof all clauses not related to dream contents (e.g., “I’m notsure, but I think. . . ”) and of those clearly repetitive ofcontents already encoded in that report. Reports were then

C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407–413 409

SETTING EVENT STRUCTURE

16 13151412

EEIE IS IS

ø ø

EE

SR GL AT OUT

CR GP

BEG DEV END

EPISODE 2

11

ES IS

GL AT OUT

CR GP

BEG DEV END

EPISODE 1

8 9 10 7 1 4 6 2 35

EE IE ES EE EE EE EE

SR

ESES

Fig. 1. Example of a dream report parsed into statements and represented through a story-digraph. (1) Some burglars came into my home. (2) Theywanted to take my jewels. (3) They insulted me, and gave me a punch on my chest. (4) They were hooded. (5) There was a grey and brown light. (6) Iwas terrified. (7) (Perhaps) I was alone at home. (8) The burglars were successful in finding my hidden jewels. (9) I saw their golden colour clearly. (10)(Then) The burglars, satisfied, left my house. (11) I watched them from the window, as they were leaving. (12) (Then) I went up to the attic. (13) Tocheck if all my childhood books were still there. (14) Even if I was sure that the burglars had not gone up there. (15) But I was very disorientated. (16)I started looking for these books in the middle of a lot of old things. Abbreviations: BEG, beginning; DEV, development; END, ending; CR, complexreaction; SR, simple reaction; ACT, action; GL, goal; GP, goal path; AT, attempt; OUT, outcome; EE, external event; IE, internal event; ES, externalstate; IS, internal state; Ø, constituent not realised in report structure.

submitted to two psycholinguists (P.B. and E.R.) unaware ofthe aims and design of the study. They applied an appropri-ate method in an independent way to identify the story-likeorganization of dream experience. This method consistedof a story-grammar adapted for Italian, whose rules allowdescription of dream reports in terms of conceptual con-stituents (that is, content units) and their relationships (thatis, the structural organization).

As extensively described elsewhere[11], the outcome ofthe story-grammar analysis can be represented as a treestructure going from the top constituent (Story) to the basicnodes (calledStatements and corresponding to a descriptionof either aState or anEvent), and are typically expressed assentences or parts of sentences. In its simplest form, a storyconsists of aSetting (which identifies the protagonist andpart of the characters, time and place of the event to be nar-rated) and anEvent structure, with one or moreEpisodes,each potentially having several intermediate constituents.The procedures of parsing report into Episodes, constituentsand statements are exemplified in the digraph ofFig. 1.

Inter-scorer agreement was higher than 98% in parsingstatements, 93% in classifying statements into constituents(or basic nodes), 98% in classifying such constituents intoepisodes, and complete in classifying episodes into stories.The few cases of disagreement were resolved through dis-cussion between the two psycholinguists.

The investigators calculated the number of stories per re-port and then for each story thelength (in terms of numbers

of statements) and three indicators of story-like (i.e., struc-tural) organization, namely:

(a) the number of statements per story realizing the Setting.This indicates theContext organization, i.e., the timeand place where the narrated actions occur;

(b) the number of statements per story realizing the Eventstructure, as indicative of theSequential (i.e., temporal)development of the actions of the story;

(c) the number of episodes per story, as indicative of theHierarchical organization of the actions of the story.

The frequency of dream recall and the story length wereconsidered as representative of the recall processes, and theindicators of story-like organization as representative of theprocesses of elaboration of dream experience[11].

3. Results

All patients completed the study and were included in thedata analysis, as no seizure occurred over three nights anddays of the study.

Preliminary univariate ANOVAs showed that patients withR- and L-CPSs did not significantly differ with respect toany demographic, psychometric and polysomnographic in-dicator (seeTable 1).

The numbers of awakenings provoked during REM andstage 2 NREM sleep were fully comparable in the two


Table 1Demographic, psychometric and polysomnography data of patients with complex partial seizures (CPS)

Item R-CPS patients (n = 6) L-CPS patients (n = 6)

Mean± S.D. Mean± S.D. P [F1,10]∗

Age 46.67± 13.26 34.83± 8.70 0.108Education level 7.33± 4.41 8.83± 4.36 0.567Raven PM 38 49.83± 3.25 50.67± 2.80 0.645Wechsler verbal span 5.33± 0.52 5.67± 0.52 0.290Corsi spatial span 4.50± 0.84 5.00± 0.89 0.341Benton IVM 20.67± 1.21 21.17± 0.75 0.411Benton VRT 29.33± 1.03 29.67± 0.81 0.549Sleep latency (min) 30.17± 37.98 16.83± 17.74 0.409Total sleep time (min) 394.33± 70.62 431.00± 46.98 0.314Sleep efficiency (%) 89.86± 11.05 96.70± 3.83 0.182Waking (min) 34.50± 29.82 13.83± 17.07 0.171Stage 1-NREM (min) 27.00± 9.67 21.67± 9.35 0.354Stage 2-NREM (min) 196.33± 30.45 230.33± 40.64 0.132Stage 3-NREM (min) 46.00± 15.18 55.67± 20.64 0.377Stage 4-NREM (min) 59.33± 31.84 57.67± 22.76 0.918REM sleep (min) 56.00± 24.96 75.33± 7.97 0.101

Abbreviations: R-CPS, patients with CPS in the right hemisphere; L-CPS, patients with CPS in the left hemisphere; Benton IVM: Benton ImmediateVisual Memory; Benton VRT: Benton Visual Retention Test.

∗ Univariate ANOVA.

groups of patients, being, respectively, 22 and 17 in R-CPSspatients and 22 and 18 in L-CPSs patients (F1,10 = 0.009,n.s.).

While all patients gave at least one contentful report afterawakening from REM sleep, only eight patients gave alsoat least one contentful report after awakening from NREMsleep. The frequency of dream recall (calculated on the in-dividual proportions of contentful reports out of the numberof awakenings provoked during REM and NREM sleep) wassignificantly lower in NREM sleep (F1,10 = 44.113,P <

0.001), while it did not differ with respect to patient group(F1,10 = 0.151, n.s.) or to interaction between group andsleep type (F1,10 = 0.036, n.s.; seeTable 2).

Only one story-like dream experience was found in eachreport, regardless of sleep type. As only eight patients gave

Table 2Mean values and standard deviations of the indicators of dream recall and structural organization of dream reports

R-CPS patients L-CPS patients

REM 2-NREM REM 2-NREM

Dream recall (12 subjects)Frequency 84.13 (±20.40) 29.17 (±40.05) 83.61 (±18.57) 34.72 (±22.52)

Structural organization of dream experience12 subjects

Story length (number of statements) 7.08 (±2.22) 7.35 (±4.13)Number of statements in Setting 1.40 (±0.49) 2.01 (±0.78)Number of statements in Event structure 5.68 (±2.09) 5.34 (±3.50)Number of episodes per story 1.62 (±0.48) 1.50 (±0.69)

8 subjectsStory length (number of statements) 7.53 (±1.95) 7.83 (±1.04) 8.02 (±4.23) 6.10 (±2.35)Number of statements in Setting 1.47 (±0.50) 1.50 (±0.87) 2.21 (±0.68) 2.10 (±0.55)Number of statements in Event structure 6.07 (±1.69) 6.33 (±1.15) 5.81 (±3.69) 4.00 (±2.35)Number of episodes per story 1.65 (±0.54) 2.00 (±0.00) 1.60 (±0.72) 1.40 (±0.89)

Abbreviations: R-CPS: right complex partial seizures; L-CPS: left complex partial seizures.

both REM- and NREM-dream reports, statistical analyseswere carried out on the length and structural organization oftheir dream experiences.

Story length did not significantly differ with respect topatient group (F1,6 = 0.124, n.s.), sleep type (F1,6 = 0.434,n.s.) and their interaction (F1,6 = 0.434, n.s.). At multipleregression analysis (carried out using the stepwise method),story length resulted significantly influenced by one of fivepsychometric indicators taken as independent variables (seeTable 1), namely the global cognitive functioning (RavenMatrices score), for REM reports (β = 0.785;R2 = 0.616;F1,6 = 9.606,P < 0.05), but not for NREM reports. Thisinfluence was confirmed by a supplementary analysis on thevalues of story length in REM reports of all (12) patients (β

= 0.790;R2 = 0.624;F1,10 = 16.626,P < 0.005).


A MANOVA on individual averages of the three indica-tors of structural organization (seeTable 2) did not showsignificant differences with respect to patient group (F3,4= 3.215, n.s.), sleep type (F3,4 = 1.735, n.s.) and their in-teraction (F3,4 = 0.792, n.s.). Thus, no further ANOVA wascomputed on single indicators.

4. Discussion

In interpreting the present findings, it must be kept inmind that they were obtained in the first study where the fre-quency of recall and the structural characteristics of dreamexperiences elaborated during NREM sleep were observedand compared with those elaborated during REM sleep inepileptic patients. This fact implies that the indications pro-vided by our findings are preliminary in nature and, thus,have a prevalently heuristic value. Moreover, the method-ological constraints of the study (namely, the collection ofNREM-dreams only in stage 2, the small size of the sampleand the restrictive criteria for inclusion of patients) suggestcaution in arguing from findings.

Keeping in mind these warnings, it seems legitimate todraw two main inferences.

Firstly, the capacity of dreaming is maintained inCPSs-patients, regardless of the side of the epileptic focus,and with a substantial involvement of both the hemispheresin the dream experiences developed during both REMand NREM sleep, like that observed in healthy individu-als [1,13]. This inference relies basically on two findings.The level of global cognitive functioning influences thelength of REM-dream reports, as observed in dreams ofParkinson’s patients[7]. This finding confirms that also inCPSs-patients the amount of cognitive resources involvedin dreaming is conspicuous and somehow proportional, al-beit lower, to that available for each subject during waking[29]. Moreover, the values of sequential and hierarchicalorganization of REM- and NREM-dreams resulted fairlycomparable in the two groups of patients. This finding couldbe an artifact of the study design, given that short periods(such as the 5 min of this study) of a specific sleep stagebefore awakening usually lead to short reports, in which thedifferences between REM- and NREM-dreams are poorlymarked[18]. In fact, there was only one story-like structureper dream report, while a certain variation in the amount ofstories per report (from one to four) has been observed indreams reported after longer periods of REM sleep[8,11].Although the possibility of an experimental artifact can-not be ruled out on the basis of the present data, it seemssubstantially weakened by the consistency of the compa-rable structural organization of REM- and NREM-dreamsin the two groups of patients with two neurophysiologi-cal and psychological pieces of evidence. These are theinter-hemispheric propagation of the activation of temporalareas in patients with focal epilepsy[14], and the similarcharacteristics of contents of REM-dreams reported by pa-

tients after right-temporal lobectomy and by controls[22].Both these pieces of evidence are fully compatible with thepersistence of a similar structural organization of dreamexperiences regardless of the side of the epileptic focus.

Secondly, the effectiveness of some cognitive processesinvolved in dreaming appears lower in NREM than in REMsleep. The supposedly impaired processes concern memoryfunctioning rather than dream elaboration, given the fairlycomparable values of story length and structural organiza-tion in REM- and NREM-dream reports. Such processescould attain either the consolidation of dream contents forsubsequent recall or the access to items of information to beconverted into dream contents. Pertinent data to distinguishin favour of either hypothesis may be obtained using ade-quate strategies, aiming in particular to guide the retrievalof those contents which are not recalled spontaneously[10]and to establish both the frequency of access to given infor-mation (such as pre-sleep stimuli) during REM and NREMsleep and their retention rate at delayed recall[9].

What seems worth stressing here is that the two aboveinterpretative hypothesis have different implications. A pooreffectiveness of NREM sleep in consolidation of dreamcontents would determine a sort of all-or-nothing thresh-old for recall, over which the differences with respect toREM-dreams would be poorly marked, and under whichthe attempted recall would fail. This possibility is of weakerneuropsychological interest, although it seems fairly plau-sible. Indeed, the recall frequency of NREM-dreams ofCPS-patients resulted lower compared with the norma-tive one for healthy individuals (about 30% versus 50%),whereas that of REM-dreams was similar (about 80% inboth cases: for review, see[24]). Instead, a poor effective-ness of NREM sleep in the access to information to beconverted into dream contents would negatively influencethe whole functioning of memory, under the assumptionthat dreaming is one of the outcomes of a general system ofinformation (re-)processing during sleep[33]. Consistentlywith this view, several findings indicate that NREM sleepcan improve the consolidation level of recently acquireditems of declarative[26] and, in part, procedural knowledge[34]. This possibility is of greater neuropsychological inter-est, because the values of sleep parameters of our sample(as assessed in the baseline night) were in line with thoseof CPS-patients treated with anticonvulsant drugs[30] (seeTable 1) and, thus, can be in principle extended to this kindof patients. Indeed, anticonvulsant drugs have not only apositive effect on the control of seizures and the stabiliza-tion of sleep organization, but also a detrimental influenceon some cognitive functions[20,21]. The possibility thatthis influence impairs both dreaming and some of its un-derlying cognitive processes deserves attention, given thatother psychotropic medications (in particular, antidepres-sants) have shown both to impair cognitive functioning andlower the frequency of dream recall[2].

If the access to information and, thus, its reprocessingwere observed as impaired during NREM sleep on larger


samples of CPS-patients, it would become crucial to assesswhether this asymmetrical functioning of NREM and NREMsleep influences not only dream production, but also the ac-cess and further consolidation of recently acquired informa-tion, such as pre-sleep stimuli. Indeed, these are likely to bemost sensitive to re-processing in CPS-patients as well asin healthy individuals. A low effectiveness of NREM sleepfor the further consolidation of pre-sleep stimuli would cor-roborate the view that disturbed or insufficient sleep nega-tively influences memory functioning[28], while explainingat least partly the memory impairment often exhibited bypatients with focal epilepsy when performing waking tasks[31].

In conclusion, the present study on the one hand con-firms the existence of well-organized and frequent dreamexperiences during REM sleep in CPS-patients, probablyregardless of the side of the epileptic focus, consistentwith the dream-diary observation[6]. On the other hand,it raises the question of why some cognitive processes,involved in the access to information to be converted intodream contents or purely in the consolidation of dream con-tents, are much less effective in NREM than REM sleep,compared with the corresponding ones at work in healthyindividuals.

Acknowledgements

This study was supported by grants from the NationalProject Funds (MM06244347/2000) awarded to C. Cipolliand L. Murri. The authors are indebted to P. Baroncini andE. Rigotti who scored dream reports.

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