Brain Research Bulletin 63 (2004) 407413

Dream experience during REM and NREM sleep of

patients with complex partial seizures
Carlo Cipolli a, , Enrica Bonanni b , Michelangelo Maestri b , Michela Mazzetti a , Luigi Murri b
a

Department of Psychology, University of Bologna, Viale Berti-Pichat 5, Bologna 40127, Italy

b 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), by
assessing the frequency of recall and the structural organization of dreams reported after awakenings provoked alternately during REM and
stage 2 NREM sleep on 12 cognitively unimpaired CPS-patients (six with epileptic focus in the right hemisphere and six in the left one). Each
patient was recorded for three consecutive nights, respectively, for adaptation to the sleep laboratory context, for polysomnography and for
dream 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-like
dreams was influenced by global cognitive functioning during REM sleep. These findings indicate that in CPSs-patients the elaboration of
dream experience is maintained in both REM and NREM sleep, while the access to information for conversion into dream contents and the
consolidation of dream contents is much less effective during NREM rather than during REM sleep. Further studies may distinguish between
these two possibilities and enlighten us as to whether the impaired memory functioning during NREM sleep is a side effect of anticonvulsant
treatment.
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 interest for a comprehensive account of dreaming as one of the
outputs of a complex system of information processing during sleep [16,17]. The functioning of this system for dream
production and recall has shown to be influenced not only
by variations in the organization of sleep (i.e., stages and
cycles: for review, see [24]), but also by sleep disturbances
(for example, sleep apnea and narcolepsy).
Some alterations of sleep organization (such as the decrease of REM sleep, stages 3 and 4 of NREM Sleep and
sleep efficiency, and the increase of stages 1 and 2 of NREM
sleep) have been more frequently observed in patients with
partial 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: cipolli@psibo.unibo.it (C. Cipolli).

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

cognitive processes underlying dream production and recall

varies with respect to the type and severity of epilepsy and
presumably according to the brain areas affected by the disease.
The hypothesis of a varying effectiveness of cognitive
processes involved in the dream process of epileptic patients, which was suggested by early clinical observations
(for review, see [32]), has been recently strengthened by a
dream-diary study. In this study the frequency of spontaneous morning recall of dream experience resulted much
higher in patients with complex partial seizures (CPSs) than
in those with generalized seizures (respectively, in about
55% versus 25% of days of the period considered [6]).
It is apparent that this hypothesis can be definitively corroborated only by laboratory data, namely by establishing
the frequency and characteristics of dream experience of
epileptic patients for all sleep stages. The data as yet available, however, is largely incomplete, given that dream experiences elaborated in NREM sleep have not been assessed.
Thus, before any attempt to sketch a comprehensive account

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C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407413

of the relationships between sleep disturbances and the functioning of cognitive processes involved in dreaming, some
pieces of evidence are needed regarding the basic characteristics (such as frequency of recall and structural organization) of dream experiences reported after awakenings during
NREM as well as REM sleep stages.
We report here the results of a study on the effectiveness of the processes involved in dream experiences elaborated by patients with CPSs during REM and stage 2 NREM
sleep. Patients with this type of epilepsy were chosen as supposed to be more likely to report dream experiences, according to the available data [1,2]. Moreover, the characteristics
of NREM-dreams were probed in stage 2, as it is present
in all cycles of sleep and with dream recall (DR) frequency
(about 50%) close to that of other stages of NREM sleep in
healthy individuals [24,25]. Finally, given the preliminary
nature of the expected evidence, the patients sampled were
without cognitive deficits or brain lesions observable from
a CT scan, in order to avoid possible biases (respectively,
global or hemisphere-related) in the elaboration or recall of
dream 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 study
carried out at the Epilepsy Center of the University Hospital
of Pisa (Italy) [6].
To be enrolled patients had to be right-handed and capable
to recall at least one dream per week over the 60-days period
of the dream-diary study, to have unilateral EEG focality (see
below) and no neurological disorder (apart from CPSs), brain
lesion (detectable at a CT scan), psychiatric disturbance or
substantial cognitive deficit. The last constraint implied that
they had to have scored above the cut-off point of cognitive
impairment in all psychometric tests applied in the previous
study, namely: (i) Raven Progressive Matrices [4] for the
assessment 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-term
memory; (v) Benton Visual Retention Test [5] for visual
long-term memory.
Patients were classified as having a well-lateralized
temporal region EEG focus in the right (R)- or left
(L)-hemisphere (respectively, six and six) according to the
temporal region where scalp EEG abnormalities (sharp
waves and spikes as well as focal slow wave activities) were
observed during wakefulness or during sleep following a
partial sleep deprivation. Patients were receiving anticonvulsant medication for <6 and >1 years with one or two conventional (carbamazepine, valproate) or newer antiepileptic
drugs (topiramate, lamotrigine), with daily doses stable for

at least 30 days before the study. The serum concentration

levels for the former drugs were within therapeutic ranges,
but were not available for the latter. Drugs type and doses
were comparable for patients with right and left EEG focus.
The study protocol was approved by the local Ethical
Committee. Informed written consent was obtained from all
patients.
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 of
the 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 10-20
International System, two electro-oculogram channels (right
and left outer canthi), one chin-EMG channel. Sleep stages
were assessed according to Rechtschaffen and Kales [27]
criteria.
The first night was intended for adaptation to laboratory
condition, the second (baseline) for evaluation of sleep organization and the third night (experimental) for dream collection. During the third night, awakenings in REM and NREM
sleep were balanced over the two halves of the night, as
the length and complexity of dream experiences have been
shown to increase along with sleep cycles [25]. Provoked
awakenings were scheduled after 5 min of the first four periods of REM and stage 2 NREM sleep subsequent to each
REM period, amounting to, at the most, eight awakenings
per night. Stage 2 was chosen to probe NREM-dream characteristics as present in all sleep cycles and usually in a
higher proportion in the sleep of epileptic patients [3], together with a DR frequency (about 50%) close to those of
other stages of NREM sleep in healthy individuals [24].
Dream reports of all patients were collected by the same
investigator (E.B.) using the non-directive instruction suggested by Foulkes [15], namely: What was going through
your mind before awakening? Having completed the verbal report of the spontaneously recalled dream contents, patients were asked to go back to sleep, and the procedure was
repeated until the morning awakening (about 7:00 a.m.).
2.3. Report analysis
All dream reports were tape-recorded and subsequently
transcribed. According to Cohens [12] criteria, reports were
classified as contentful (i.e., with at least one sentence describing contents of dream experience) or contentless (without such a sentence). Only contentful reports were taken into
account to evaluate the frequency of dream recall.
Investigators preliminarily pruned each contentful report
of all clauses not related to dream contents (e.g., Im not
sure, but I think . . . ) and of those clearly repetitive of
contents already encoded in that report. Reports were then

C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407413

SETTING

409

EVENT STRUCTURE

EPISODE 1

BEG

EPISODE 2

DEV

BEG

END

CR

DEV

CR

GP

SR

GL

END

AT OUT

SR

GP

GL

AT

ES

ES

EE

ES

IS

IE

EE

EE

EE

EE

ES

EE

IS

IS

IE

EE

10

11

12

14

15

13

16

OUT

Fig. 1. Example of a dream report parsed into statements and represented through a story-digraph. (1) Some burglars came into my home. (2) They
wanted 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) I
was 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) To
check 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, complex
reaction; SR, simple reaction; ACT, action; GL, goal; GP, goal path; AT, attempt; OUT, outcome; EE, external event; IE, internal event; ES, external
state; IS, internal state; , constituent not realised in report structure.

submitted to two psycholinguists (P.B. and E.R.) unaware of

the aims and design of the study. They applied an appropriate method in an independent way to identify the story-like
organization of dream experience. This method consisted
of a story-grammar adapted for Italian, whose rules allow
description of dream reports in terms of conceptual constituents (that is, content units) and their relationships (that
is, the structural organization).
As extensively described elsewhere [11], the outcome of
the story-grammar analysis can be represented as a tree
structure going from the top constituent (Story) to the basic
nodes (called Statements and corresponding to a description
of either a State or an Event), and are typically expressed as
sentences or parts of sentences. In its simplest form, a story
consists of a Setting (which identifies the protagonist and
part of the characters, time and place of the event to be narrated) and an Event structure, with one or more Episodes,
each potentially having several intermediate constituents.
The procedures of parsing report into Episodes, constituents
and statements are exemplified in the digraph of Fig. 1.
Inter-scorer agreement was higher than 98% in parsing
statements, 93% in classifying statements into constituents
(or basic nodes), 98% in classifying such constituents into
episodes, and complete in classifying episodes into stories.
The few cases of disagreement were resolved through discussion between the two psycholinguists.
The investigators calculated the number of stories per report and then for each story the length (in terms of numbers

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

(a) the number of statements per story realizing the Setting.
This indicates the Context organization, i.e., the time
and place where the narrated actions occur;
(b) the number of statements per story realizing the Event
structure, as indicative of the Sequential (i.e., temporal)
development of the actions of the story;
(c) the number of episodes per story, as indicative of the
Hierarchical organization of the actions of the story.
The frequency of dream recall and the story length were
considered as representative of the recall processes, and the
indicators of story-like organization as representative of the
processes of elaboration of dream experience [11].

3. Results
All patients completed the study and were included in the
data analysis, as no seizure occurred over three nights and
days of the study.
Preliminary univariate ANOVAs showed that patients with
R- and L-CPSs did not significantly differ with respect to
any demographic, psychometric and polysomnographic indicator (see Table 1).
The numbers of awakenings provoked during REM and
stage 2 NREM sleep were fully comparable in the two

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C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407413

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

Age
Education level
Raven PM 38
Wechsler verbal span
Corsi spatial span
Benton IVM
Benton VRT
Sleep latency (min)
Total sleep time (min)
Sleep efficiency (%)
Waking (min)
Stage 1-NREM (min)
Stage 2-NREM (min)
Stage 3-NREM (min)
Stage 4-NREM (min)
REM sleep (min)

R-CPS patients (n = 6)

L-CPS patients (n = 6)

Mean S.D.

Mean S.D.

46.67
7.33
49.83
5.33
4.50
20.67
29.33
30.17
394.33
89.86
34.50
27.00
196.33
46.00
59.33
56.00

13.26
4.41
3.25
0.52
0.84
1.21
1.03
37.98
70.62
11.05
29.82
9.67
30.45
15.18
31.84
24.96

34.83
8.83
50.67
5.67
5.00
21.17
29.67
16.83
431.00
96.70
13.83
21.67
230.33
55.67
57.67
75.33

P [F1,10 ]

8.70
4.36
2.80
0.52
0.89
0.75
0.81
17.74
46.98
3.83
17.07
9.35
40.64
20.64
22.76
7.97

0.108
0.567
0.645
0.290
0.341
0.411
0.549
0.409
0.314
0.182
0.171
0.354
0.132
0.377
0.918
0.101

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

groups of patients, being, respectively, 22 and 17 in R-CPSs

patients and 22 and 18 in L-CPSs patients (F1,10 = 0.009,
n.s.).
While all patients gave at least one contentful report after
awakening from REM sleep, only eight patients gave also
at least one contentful report after awakening from NREM
sleep. The frequency of dream recall (calculated on the individual proportions of contentful reports out of the number
of awakenings provoked during REM and NREM sleep) was
significantly 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 and
sleep type (F1,10 = 0.036, n.s.; see Table 2).
Only one story-like dream experience was found in each
report, regardless of sleep type. As only eight patients gave

both REM- and NREM-dream reports, statistical analyses

were carried out on the length and structural organization of
their dream experiences.
Story length did not significantly differ with respect to
patient 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 multiple
regression analysis (carried out using the stepwise method),
story length resulted significantly influenced by one of five
psychometric indicators taken as independent variables (see
Table 1), namely the global cognitive functioning (Raven
Matrices score), for REM reports ( = 0.785; R2 = 0.616;
F1,6 = 9.606, P < 0.05), but not for NREM reports. This
influence was confirmed by a supplementary analysis on the
values of story length in REM reports of all (12) patients (
= 0.790; R2 = 0.624; F1,10 = 16.626, P < 0.005).

Table 2
Mean values and standard deviations of the indicators of dream recall and structural organization of dream reports
R-CPS patients

Dream recall (12 subjects)

Frequency

L-CPS patients

REM

2-NREM

REM

2-NREM

84.13 (20.40)

29.17 (40.05)

83.61 (18.57)

34.72 (22.52)

Structural organization of dream experience

12 subjects
Story length (number of statements)
Number of statements in Setting
Number of statements in Event structure
Number of episodes per story

7.08
1.40
5.68
1.62

(2.22)
(0.49)
(2.09)
(0.48)

8 subjects
Story length (number of statements)
Number of statements in Setting
Number of statements in Event structure
Number of episodes per story

7.53
1.47
6.07
1.65

(1.95)
(0.50)
(1.69)
(0.54)

7.83
1.50
6.33
2.00

(1.04)
(0.87)
(1.15)
(0.00)

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

7.35
2.01
5.34
1.50

(4.13)
(0.78)
(3.50)
(0.69)

8.02
2.21
5.81
1.60

(4.23)
(0.68)
(3.69)
(0.72)

6.10
2.10
4.00
1.40

(2.35)
(0.55)
(2.35)
(0.89)

C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407413

A MANOVA on individual averages of the three indicators of structural organization (see Table 2) did not show
significant differences with respect to patient group (F3,4
= 3.215, n.s.), sleep type (F3,4 = 1.735, n.s.) and their interaction (F3,4 = 0.792, n.s.). Thus, no further ANOVA was
computed on single indicators.

4. Discussion
In interpreting the present findings, it must be kept in
mind that they were obtained in the first study where the frequency of recall and the structural characteristics of dream
experiences elaborated during NREM sleep were observed
and compared with those elaborated during REM sleep in
epileptic patients. This fact implies that the indications provided by our findings are preliminary in nature and, thus,
have a prevalently heuristic value. Moreover, the methodological constraints of the study (namely, the collection of
NREM-dreams only in stage 2, the small size of the sample
and the restrictive criteria for inclusion of patients) suggest
caution in arguing from findings.
Keeping in mind these warnings, it seems legitimate to
draw two main inferences.
Firstly, the capacity of dreaming is maintained in
CPSs-patients, regardless of the side of the epileptic focus,
and with a substantial involvement of both the hemispheres
in the dream experiences developed during both REM
and NREM sleep, like that observed in healthy individuals [1,13]. This inference relies basically on two findings.
The level of global cognitive functioning influences the
length of REM-dream reports, as observed in dreams of
Parkinsons patients [7]. This finding confirms that also in
CPSs-patients the amount of cognitive resources involved
in dreaming is conspicuous and somehow proportional, albeit lower, to that available for each subject during waking
[29]. Moreover, the values of sequential and hierarchical
organization of REM- and NREM-dreams resulted fairly
comparable in the two groups of patients. This finding could
be an artifact of the study design, given that short periods
(such as the 5 min of this study) of a specific sleep stage
before awakening usually lead to short reports, in which the
differences between REM- and NREM-dreams are poorly
marked [18]. In fact, there was only one story-like structure
per dream report, while a certain variation in the amount of
stories per report (from one to four) has been observed in
dreams reported after longer periods of REM sleep [8,11].
Although the possibility of an experimental artifact cannot be ruled out on the basis of the present data, it seems
substantially weakened by the consistency of the comparable structural organization of REM- and NREM-dreams
in the two groups of patients with two neurophysiological and psychological pieces of evidence. These are the
inter-hemispheric propagation of the activation of temporal
areas in patients with focal epilepsy [14], and the similar
characteristics of contents of REM-dreams reported by pa-

411

tients after right-temporal lobectomy and by controls [22].

Both these pieces of evidence are fully compatible with the
persistence of a similar structural organization of dream
experiences regardless of the side of the epileptic focus.
Secondly, the effectiveness of some cognitive processes
involved in dreaming appears lower in NREM than in REM
sleep. The supposedly impaired processes concern memory
functioning rather than dream elaboration, given the fairly
comparable values of story length and structural organization in REM- and NREM-dream reports. Such processes
could attain either the consolidation of dream contents for
subsequent recall or the access to items of information to be
converted into dream contents. Pertinent data to distinguish
in favour of either hypothesis may be obtained using adequate strategies, aiming in particular to guide the retrieval
of those contents which are not recalled spontaneously [10]
and to establish both the frequency of access to given information (such as pre-sleep stimuli) during REM and NREM
sleep and their retention rate at delayed recall [9].
What seems worth stressing here is that the two above
interpretative hypothesis have different implications. A poor
effectiveness of NREM sleep in consolidation of dream
contents would determine a sort of all-or-nothing threshold for recall, over which the differences with respect to
REM-dreams would be poorly marked, and under which
the attempted recall would fail. This possibility is of weaker
neuropsychological interest, although it seems fairly plausible. Indeed, the recall frequency of NREM-dreams of
CPS-patients resulted lower compared with the normative one for healthy individuals (about 30% versus 50%),
whereas that of REM-dreams was similar (about 80% in
both cases: for review, see [24]). Instead, a poor effectiveness of NREM sleep in the access to information to be
converted into dream contents would negatively influence
the whole functioning of memory, under the assumption
that dreaming is one of the outcomes of a general system of
information (re-)processing during sleep [33]. Consistently
with this view, several findings indicate that NREM sleep
can improve the consolidation level of recently acquired
items of declarative [26] and, in part, procedural knowledge
[34]. This possibility is of greater neuropsychological interest, because the values of sleep parameters of our sample
(as assessed in the baseline night) were in line with those
of CPS-patients treated with anticonvulsant drugs [30] (see
Table 1) and, thus, can be in principle extended to this kind
of patients. Indeed, anticonvulsant drugs have not only a
positive effect on the control of seizures and the stabilization of sleep organization, but also a detrimental influence
on some cognitive functions [20,21]. The possibility that
this influence impairs both dreaming and some of its underlying cognitive processes deserves attention, given that
other psychotropic medications (in particular, antidepressants) have shown both to impair cognitive functioning and
lower the frequency of dream recall [2].
If the access to information and, thus, its reprocessing
were observed as impaired during NREM sleep on larger

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C. Cipolli et al. / Brain Research Bulletin 63 (2004) 407413

samples of CPS-patients, it would become crucial to assess

whether this asymmetrical functioning of NREM and NREM
sleep influences not only dream production, but also the access and further consolidation of recently acquired information, such as pre-sleep stimuli. Indeed, these are likely to be
most sensitive to re-processing in CPS-patients as well as
in healthy individuals. A low effectiveness of NREM sleep
for the further consolidation of pre-sleep stimuli would corroborate the view that disturbed or insufficient sleep negatively influences memory functioning [28], while explaining
at least partly the memory impairment often exhibited by
patients with focal epilepsy when performing waking tasks
[31].
In conclusion, the present study on the one hand confirms the existence of well-organized and frequent dream
experiences during REM sleep in CPS-patients, probably
regardless of the side of the epileptic focus, consistent
with 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 into
dream contents or purely in the consolidation of dream contents, are much less effective in NREM than REM sleep,
compared with the corresponding ones at work in healthy
individuals.

Acknowledgements
This study was supported by grants from the National
Project Funds (MM06244347/2000) awarded to C. Cipolli
and L. Murri. The authors are indebted to P. Baroncini and
E. Rigotti who scored dream reports.

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