NEUROREPORT
SLEEP
Detection of verbal discordances during sleep
Fabien Perrin,1,2,4,5,CA He¤le'ne Bastuji1,2,4 and Luis Garcia-Larrea1,3,4
1
EA-1880, University Claude Bernard, Lyon; 2Sleep Disorders Unit, Neurological Hospital; 3Human Neurophysiology Laboratory, CERMEP,
59 bd Pinel, 69003 Lyon, France; 4Institut Fe¤de¤ratif des Neurosciences de Lyon, 59 bd Pinel, 69003, Lyon, France; 5Present Address: Cyclotron
Research Centre, Lie'ge University, Ba“timent B30, Sart Tilman, Alle¤e du 6 aout, 8 B- 4000 Lie'ge, Belgium
CA
Corresponding Author
Received 21March 2002; accepted15 May 2002
We used an electrophysiological marker of linguistic discordance,
the N400 wave, to investigate how linguistic and pseudo-linguistic
stimuli are categorised during sleep as compared to waking.During
wakefulness, signs of discordance detection were, as expected,
greater for pseudo-words than for real but semantically incongruous words, relative to congruous words. In sleep stage 2 all signs of
hierarchic process of discordance disappeared. A new hierarchic
process reappeared in paradoxical sleep, which di¡ered from that
of waking, responses to pseudo-words being similar to those to
congruous words. Linguistic absurdity appears to be accepted in a
di¡erent manner during paradoxical sleep than during waking, and
this might explain why absurd contents are so naturally incorporated into otherwise plausible dream stories. NeuroReport
c 2002 Lippincott Williams & Wilkins.
13:1345^1349 Key words: Dream; Event-related potentials (ERPs); N400; Semantic; Sleep; Word and pseudo-word detection
INTRODUCTION
During the last 10 years, event-related potential (ERP)
methods have brought relevant data on the processing of
sensory information during human sleep. Contrary to the
view that sleeping subjects are isolated from their sensorial
environment [1,2], ERP data strongly suggest that the
sleeping brain remains able to discriminate between
different types of auditory stimuli. In both sleep stage 2
(S2) and slow wave sleep (SWS), deviant auditory stimuli
elicit electroencephalographic responses (K-complexes) of
higher amplitude and duration than those to monotonous
stimuli [3]. More importantly, during rapid eye movement
(REM) sleep, or paradoxical sleep (PS), the presentation of
deviant stimuli gives rise to a late positive response [4]
which is reminiscent in latency and scalp topography of the
P300 wave, a cerebral event that signals the detection of
changes in the sensory environment [5–7]. The notion that
some level of sensory discrimination may persist during
sleep has prompted in recent years experiments devised to
uncover the nature of the underlying processes. A number
of experiments have addressed the question whether the
signs of auditory discrimination during sleep were attributable to the recognition of the stimulus’ intrinsic meaning
(i.e. its semantic aspects) or simply to the detection of its
acoustic salience (i.e. the fact of being acoustically dissimilar
relative to a monotonous series). To this aim, Perrin and
collaborators removed the physical rarity of target stimuli
by using as sensory input a series of equiprobable first
names among which they included the sleeping subject’s
own name. It was shown that, both in S2 and in PS, the
subject’s own name produced responses that differed
significantly from those to any other first name, and which
concerned the P300 response [8,9]. Although these studies
c Lippincott Williams & Wilkins
0959- 4965 demonstrated that the sleeping brain remains able to
discriminate between words varying in their intrinsic
meaning, the use of the subject’s own name as a target
stimulus was a limitation, as proper names (and hence the
subject’s own name) have no strict semantic content
compared with common names [10–12].
To investigate the extent to which the sleeping brain can
perform a more elaborated semantic discrimination of
stimuli, we recorded ERPs to verbal stimuli composed
exclusively of common names, and excluding explicitly
emotional connotation and semantic ambiguity associated
to proper names. During wakefulness, verbal stimuli that
are semantically discordant (incongruous) with respect to a
preceding stimulus elicit a negative brain response at about
400 ms, the N400, which is larger than that evoked by
semantically concordant (congruous) words. The enhancement of the N400 response develops whether the incongruous word appears within a phrase [13] or as the second
word of a pair [14]. Brualla et al. [15] suggested that a N400like potential could be recorded during PS and in some
periods of S2 devoid of K-complexes (denoted as S2 (KC)),
albeit with much longer latency as compared to the waking
N400 wave. In the present study, we used different levels of
verbal incongruence which, in wakefulness, give rise to a
hierarchic amplitude enhancement of N400 [14]. Thus,
responses to semantically congruous and incongruous
words of various nature, as well as to pseudo-words, were
evaluated during wakefulness and all-night sleep.
MATERIALS AND METHODS
Subjects: Nine volunteers (four women and five men, age
27.9 7 3. 1 years), right-handed, without audiological or
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NEUROREPORT
neurological disease and native French speakers participated to the study. All gave informed consent to the study,
which was conducted in agreement with the guidelines of
the Declaration of Helsinki. A tenth participant was
excluded due to his inability to remain asleep while
receiving auditory stimulation.
Stimulations: We elaborated 12 sequences of 72 stimuli,
containing 12 pairs of words (a prime word following in
50% of the case by a semantically congruous word, and in
the other 50% by a semantically incongruous word), one
different pseudo-word (syllable without sense) being
inserted between each pair. Previous to the study, the
degree of semantic association between each pair of words
was tested on 10 subjects different from those participating
to the ERP experiment, and words were selected from a
table of frequency for French words [16]. All stimuli (words
and pseudo-words) were monosyllabics, had a maximum
length of 500 ms and appeared with a regular SOA of
1700 ms. They were recorded by a same male voice and were
digitised and replayed binaurally at 60 dB SPL maximal
intensity. Finally, to minimise the physical effects between
the three types of words, each word was used as a
congruous stimulus in one sequence, as incongruous one
in another sequence, and as word following a pseudo-word
(prime words) in a last sequence.
Procedure: Electroencephalographic (EEG) signals from 31
tin electrodes (International 10–20 system) referenced to the
nose, electromyogram (EMG) from two electrodes on the
chin, and electrooculogram (EOG) from two electrodes
diagonally above and below the right eye were amplified
( 150 000) and sampled at 500 Hz, with an analogue
bandpass of 0.1–70 Hz. A ground electrode was placed
between Fz and Fpz and impedance at all electrodes was
o 5 kO.
After the installation of the head cap and of two miniearphones inserted into the external acoustic canals, the
subjects lay down on a comfortable bed. Before going to
sleep, the subjects heard, eyes closed, six sequences of
stimuli without any specific task (passive condition),
followed by other sequences with the aim that subjects
did not known what they will hear during the night. During
sleep, the subjects were stimulated every 20–30 min with a
sequence of 72 stimuli, in both the first and the second parts
of the night. If a stimulation awaked the sleeper, the
sequence was immediately discontinued. Fifteen minutes
after waking, six sequences of stimuli were also presented
without any specific task.
Data analyses: Sleep stages were visually scored off-line
by two investigators according to the criteria of Rechtschaffen and Kales [17]. Individual AEPs were analysed over a
1700 ms epoch, including a prestimulus baseline of 200 ms,
and were grouped according to the vigilance state (wakefulness (corresponding to the average of the waking state
preceding and that following the sleep session, since no
significant difference amplitude was shown between the
different types of stimulus) vs S2 without a concomitant KC
(KC) vs PS), blind to the type of stimulus. Data during S1,
S2 with a concomitant KC (KCþ) and SWS were not
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F. PERRIN, H. BASTUJI AND L.GARCIA-LARREA
analysed in this study. AEPs were then averaged according
to the type of stimulus (congruous word vs incongruous
word vs prime word vs pseudo-word) and the electrode
position. Prior to averaging, single epochs containing eye
movement or EMG artefact with amplitude exceeding
7 50 mV (thus excluding the epochs containing a high
amplitude K-complex during S2, i.e. KCþ). Single epochs
recorded during transition phases between two sleep stages
were also rejected from the analysis. Then, AEPs were
digitally filtered between 0.1 and 30 Hz (roll off 24 dB/
octave) and were averaged across subjects to create grandaveraged AEPs (used for illustrative purposes).
Statistical calculations were performed on averaged traces
from each individual: amplitudes (from baseline) of the
predominant components, labelled N1, P2 (N for negative
voltage, P for positive, number for the order of appearance),
and mean areas under the curve of the N400 were calculated
for each individual average. The mean area, instead of
single-point amplitude, was chosen for N400 so as to avoid
the problem related to a superimposed positive shift
induced by sleep [9,18]. Area calculation permitted to focus
the analysis on the differences between the different stimuli
during the three vigilance states. The window used for area
computation was chosen from inspection of grand-averaged
AEPs in each vigilance state: this comprised from 250 to
550 ms during wakefulness, and from 350 to 650 ms during
S2 and PS.
Amplitudes and areas values were tested with a threeway ANOVA with repeated measures on the type of
stimulus (congruous word vs incongruous word vs prime
word vs pseudo-word), the vigilance state (wakefulness vs
S2 KC- vs PS) and the electrode position (Fz vs Cz vs Pz).
Only results reaching significance at p o 0.05 after Huynh–
Feldt correction are presented. Post-hoc bilateral paired
t-tests were performed when significant results emerged
on ANOVA.
RESULTS
ERPs showed the emergence of three major potentials in
response to all types of auditory stimuli, during wakefulness as well as during S2 (KC-) and PS: the N1, at about
130 ms after the beginning of the stimulus, with frontocentral maximum; the P2, culminating at 230 ms in central
sites; and the N400, for which maximum amplitude
difference between incongruous and congruous words
was obtained at central electrodes, at 390 ms during waking
state and at 480 ms during sleep (Fig. 1).
ANOVA did not show any effect of the type of stimulus
(congruous word vs incongruous word vs prime word vs
pseudo-word) during the first 300 ms of the response (N1
and P2 components). Conversely, there was a significant
effect of the vigilance state (wakefulness vs S2 vs PS) on P2
amplitude (F(2,16) ¼ 19.707, p ¼ 0.0004) and a near-significant effect on N1 amplitude (F(2,16) ¼ 4.436, p ¼ 0.0525 and
0.0293 before correction). This reflects that N1 amplitude
was more positive during S2 than during wakefulness
(t(8) ¼ 3.7, p ¼ 0.0059), and that P2 amplitude was more
positive during PS and S2 relative to the waking state
(respectively t(8) ¼ 4.8, p ¼ 0.0013 and t(8) ¼ 5.8, p ¼ 0.0004),
as has been reported previously [18].
DETECTION OF VERBAL DISCORDANCES DURING SLEEP
NEUROREPORT
Fig. 1. Event-related potentials to concordant and discordant stimuli. (a) Event-related potentials to congruous words (in green), incongruous words (in
red), prime words (in black) and pseudo-words (in blue) during waking, sleep stage 2 and paradoxical sleep represented at Fz, Cz and Pz sites. (b) Di¡erences waves between the congruous words and the three discordant stimuli: incongruous words minus congruous words (I-C), prime words minus congruous words (P-C) and pseudo-words minus congruous words (Pw-C).The di¡erences are illustrated by their scalp topography at their maximum.
Fig. 2. N400 area in the di¡erent vigilance states. Mean area (7 s.e.) of N400 component during waking state, sleep stage 2 and paradoxical sleep in
response to congruous words (open circle), incongruous words (solid circle), prime words (solid square) and pseudo-words (solid triangle). The asterisk
indicates that mean area was signi¢cantly di¡erent. In addition to interclass di¡erences, note that a progressive deviation of the EEG baseline shift all
transient potentials (i.e. ERPs) towards more positive values during sleep.
Concerning the N400, ANOVA showed a significant effect
of the type of stimulus (F(2,16) ¼ 10.109, p ¼ 0.0003), indicating that N400 was, as expected, enhanced after discordant
stimuli relative to congruous words. This latter effect was
modulated by the vigilance state, as reflected by the near
significant interaction observed between the factors type of
stimulus and vigilance state (F(6,48) ¼ 2.439, p ¼ 0.0387
when not corrected and p ¼ 0.0671 when corrected). On
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post-hoc t-tests, N400 was greater (i.e. more negative) after
incongruous words than after congruous words in all
vigilance states (t(8) ¼ 2.8, p ¼ 0.0233 during wakefulness;
t(8) ¼ 2.6, p ¼ 0.0096 during S2; t(8) ¼ 3.8, p ¼ 0.0055 during
PS). However, each vigilance state developed a characteristic hierarchy of amplitudes for the other discordant
stimuli, i.e. for prime words and pseudo-words (Fig. 1,
Fig. 2).
During wakefulness, N400 was higher for prime words
and pseudo-words than for congruous words (respectively
t(8) ¼ 3.9, p ¼ 0.0043 and t(8) ¼ 3.5, p ¼ 0.0078) and for
incongruous words (respectively t(8) ¼ 2.8, p ¼ 0.0229 and
t(8) ¼ 2.5, p ¼ 0.0396), which were in turn similar between
them. During S2, N400 was greater for prime words and
pseudo-words than for congruous words (respectively
t(8) ¼ 2.3, p ¼ 0.0485 and t(8) ¼ 2.7, p ¼ 0.0397), and was
similar for prime words, incongruous words and pseudowords. During PS, N400 was greater for prime words than
for congruous words (t(8) ¼ 4, p ¼ 0.0041) and similar for
prime words and incongruous words. Moreover, N400 was
not significant after pseudo-words, its amplitude being
intermediate to that of congruous and incongruous words.
Secondarily, ANOVA showed a significant effect of the
vigilance state on N400 area (F(2,16) ¼ 14.378, p ¼ 0.0003),
which corresponds, as for N1 and P2 components, to a
positive shift during PS compared to the waking state
(t(8) ¼ 4.6, p ¼ 0.0018).
DISCUSSION
The general morphology of ERPs during paradoxical sleep
(PS) and sleep stage 2 (S2 KC), was very similar to that of
the waking state. This similarity of responses is a robust
result that has been replicated many times during PS [19–21]
and more recently during S2 without concomitant Kcomplexes (KC) [9].
During both PS and S2 (KC), a higher N400-like wave
was observed for semantically incongruous words than for
semantically congruous words, the latency and scalp
topography of which were very similar to those of waking
N400. These similarities suggest functionally equivalencies
between waking N400 and sleep N400-like components,
thus that the sleeping brain might be able to detect the
appearance of a semantic incongruence in its sensory
environment. This was also the conclusion of Brualla et al.
[15], who reported a N400-like during sleep, with, however,
a more delayed latency than ours. The differences between
our results and those of Brualla et al. could be explained by
the differences in stimulus paradigms, notably stimulus
duration which was much shorter in the present study
(maximum length of 500 ms vs 480–790 ms). In spite of the
differences, our study confirms Brualla et al.‘s data, who
observed sleep N400-like potentials after semantically
correct but incongruous words. Furthermore, our results
show that, as compared to wakefulness, a different
hierarchic process of linguist and pseudo-linguistic stimuli
appears to take place during sleep, and may be specific to
each sleep stage.
During S2 (KC), all discordant stimuli, regardless of
their category (incongruous words, prime words following
pseudo-words and pseudo-words following words) yielded
enhanced N400 responses relative to congruous words.
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F. PERRIN, H. BASTUJI AND L.GARCIA-LARREA
However, no significant difference existed between different
levels of discordance, suggesting a loss of hierarchic process
of verbal discordances in this sleep stage.
A hierarchic process of discordance reappeared in PS,
which however differed from that of the waking state. While
incongruous and prime words yielded, as in S2, higher
N400 amplitudes than those of congruous words, N400
amplitude to pseudo-words was surprisingly similar to that
elicited by congruous words, suggesting that pseudo-words
were not detected as incongruous stimuli during PS.
Stickgold et al. [22] have observed that subjects awakened
from REM sleep showed an abnormal pattern of semantic
behavioural priming, characterised by greater effects to
weak primes (e.g. thief-wrong) than to strong primes
(e.g. hot-cold), this effect being not observed during neither
waking nor S2. The authors concluded that cognition during
PS was qualitatively different from that of waking and S2
and may reflect a shift in associative memory systems,
underlying the bizarre and hyperassociative character of
dreaming. Our study provides a neurophysiological support
to this notion, by suggesting that linguistic absurdity
(auditory stimuli close to onomatopoeia) is accepted during
PS in a different manner than during waking. It may explain
why absurd contents are so naturally incorporated into
otherwise plausible dream stories.
Sensory responses preceding N400 (notably P2) appeared
to be affected by changes in vigilance (but not by
incongruence), as has commonly been reported in previous
studies [4]. While this effect does not invalidate the general
conclusion that a degree of semantic discrimination remains
effective during sleep, changes in early sensory processing
might have altered the overall auditory input received by
semantic comparison cortical networks, and thus may have
influenced the modulation of sleep-N400 by different types
of incongruence, notably the absence of hierarchic processing during sleep stage 2.
CONCLUSION
Different hierarchic processes of word semantic discordances were detected in wakefulness and sleep. In waking
state, brain signals reflecting the detection of discordance
were, as expected, maximal for pseudo-words (i.e. inexistent
words). Conversely, in sleep stage 2 all signs of hierarchical
process of linguistic discordance disappeared, while a
qualitatively different hierarchy reappeared in paradoxical
sleep, whereby responses to pseudo-words did not differ
from those to congruous words. Failure to detect linguistic
absurdity during paradoxical sleep might contribute to the
explanation of why illogical contents are so naturally
incorporated into otherwise plausible dream stories.
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NEUROREPORT
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Acknowledgements: We are indebted to Professor Michel Jouvet for his precious comments on an earlier version of this manuscript.
We also deeply thank Professor FrancGois Mauguie're for his soutien sans faille all along this work. F.P. was supported by
Sano¢-Synthe¤labo.
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