International Journal of Psychophysiology 46 (2002) 243–255
Semantic analysis of auditory input during sleep: studies with
event related potentials
´ ` Bastujia,b,c,*, Fabien Perrina,b,c, Luis Garcia-Larreaa,b,d
Helene
a
´ ´
Institut Federatif
des Neurosciences de Lyon (IFNL), Lyon, France
b
EA-1880, University Claude Bernard, Lyon, France
c
Sleep Disorders Unit, Neurological Hospital, 59 bd Pinel, 69003 Lyon, France
d
Human Neurophysiology Laboratory at the CERMEP, 59 bd Pinel, 69003 Lyon, France
Received 7 July 2002; received in revised form 13 August 2002; accepted 3 September 2002
Abstract
This review summarises the results of event-related potentials studies exploring the extent to which the human
brain can extract semantic information from external stimuli during sleep. The persistence of a differential response
to the subject’s own name, relative to any other proper name, during stage 2 (S2) and paradoxical (REM) sleep (PS)
suggests that the brain remains able to discriminate an intrinsically relevant word during these sleep stages. The
similarities and the differences between these sleep cognitive responses and the waking P300 are stressed, and the
functional significance of this component discussed especially in relation with consciousness and memory of the
stimulus. Recent studies of the ‘N400’ potential evoked by semantically incongruous words, have shown that this
component may be also elicited during S2 and PS, indicating preserved detection of semantic discordance during
these sleep stages. However, linguistic incongruity appears to be processed in a different manner during PS than
during waking, since words devoid of meaning (pseudo-words), which are detected as anomalous and evoke N400
during waking, yielded responses similar to those of congruous words in PS. All these data support the view that
some semantic analysis of auditory stimuli remains possible in the human sleeping brain, and warrant further studies
to elucidate the extent and limits of these capabilities.
䊚 2002 Elsevier Science B.V. All rights reserved.
Keywords: P300; N400; Event-related potential; Sleep; REM; K complex; Semantic; Consciousness
‘The psyche´ isolates itself during sleep («) nevertheless
we are not always awakened by the mere sensory force of
the impression, but by the psychic relation of the same; an
indifferent word does not arouse the sleeper, but if called
by name he awakens«’ K.F. Burdach (1830).
ˆ
*Corresponding author. Unite´ d’Hypnologie, Hopital
Neurologique, 59, bd Pinel, F-69394 Lyon Cedex 03, France. Tel.:
q33-4-72357828; fax: q33-4-72357397.
E-mail address: [email protected] (H. Bastuji).
Lack of behavioural responsiveness and of
memory recollection of stimuli during sleep has
led to postulate a functional disconnection, in the
sleeping subject, between the cerebral cortex and
the external world (Horne, 1989; Jones, 1991;
Steriade, 1994). This hypothesis has been supported by electrophysiological results in animal studies
suggesting a strong decrease of sensory informa-
0167-8760/02/$ - see front matter 䊚 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 7 - 8 7 6 0 Ž 0 2 . 0 0 1 1 6 - 2
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H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
tion processing during sleep (Pompeiano, 1970;
Steriade et al., 1990). However, the well-known
fact that awakening may be induced by meaningful
stimuli of very low-intensity, as well as the incorporation of sensory information into the sleeper’s
dreams, clearly indicate that sensory integration is
not abolished by sleep (Aristotle trad 1955; Burdach, 1830; Maury, 1878; Formby, 1967; Burton
et al., 1988; Halasz, 1998; Hobson, 1990). In this
vein, the extent to which the brain processing of
external stimuli remains active during sleep has
been the subject of numerous studies since the last
century, notably using behavioural techniques.
Generally, these studies focused on the behavioural
reactivity of sleeping subjects to auditory stimulation, and showed that a number of physical aspects
of auditory inputs influences reactivity during
sleep. High-intensity stimuli are known to awake
subjects from the different sleep stages, the awakening threshold depending on various other factors
(Bonnet, 1982). Low frequencies are more powerful than high frequencies to interrupt the sleeping
process (Levere et al., 1974). Weir (1976) reported
that the reactivity of sleeping new-borns is
increased to sounds around language frequencies,
suggesting that during sleep the auditory window
of reception might be restricted to stimulus with
biological significance. Furthermore, while responsiveness to repetitive stimuli are generally subject
to habituation during sleep, the reactivity to relevant or meaningful stimuli (for example the subject’s own name or the cry of a new-born for his
mother) seems to remain operative in spite of
repetition (Oswald et al., 1960; Langford et al.,
1974; McDonald et al., 1975). Overall, the results
of behavioural studies show that the discrimination
of important stimuli persists during sleep.
More recently, electrophysiological methods,
especially of evoked potentials, have been used to
demonstrate specific human brain responses to
sensory stimulation during sleep. Event related
potentials (ERP) studies have shown that the
discrimination of deviant from repetitive auditory
tones by the brain persists during all sleep stages
under certain circumstances (see review in Bastuji
and Garcia-Larrea, 1999). For instance, both in
sleep stage 2 (S2) and slow wave sleep (SWS),
deviant stimuli elicit K complexes (KCs) of higher
amplitude than those evoked by monotonous stimuli (e.g. Campbell et al., 1985; Ujszaszi and
Halasz, 1988; Nielsen-Bohlman et al., 1992; Bastuji et al., 1995; see Bastien and Colrain, in this
issue). Moreover, during paradoxical (PS) or REM
sleep, deviant stimuli give rise to a late positive
response that is reminiscent in latency and scalp
topography of the ‘P300’ wave (e.g. Bastuji et al.,
1990, 1995; Sallinen et al., 1996; Niiyama et al.,
1994; see review in Bastuji and Garcia-Larrea,
´ in this issue). Notwithstanding the
1999; Cote,
theoretical importance of this early work, it is of
note that the ‘significant’ stimuli delivered in these
studies differed from the background at least by
two features, namely their acoustic properties (i.e.
pitch or loudness) and their probability of occurrence. In this context, it is difficult to ascertain
whether the differential ERPs (including P300)
observed to ‘rare’ stimuli reflect the genuine discrimination of stimulus meaning (access to stimulus intrinsic significance) or rather the simple
detection of a change in the physical characteristics
of the input stream (change in acoustical properties
andyor probability of occurrence). This dichotomy
can only be addressed using more complex stimuli
whose intrinsic (i.e. semantic) information is partially independent from their physical attributes—
for instance words. ERP recording paradigms that
use verbal material as stimuli are therefore relevant
to assess whether, and to what extent, the detection
of a stimulus’ intrinsic meaning remains possible
during sleep.
1. Detection of the subject’s own name during
sleep
Three ERP studies were recently devoted to
detect whether sleeping subjects might or not
discriminate their first name—a very simple yet
highly significant word (Pratt et al., 1999; Perrin
et al., 1999, 2000). The reasons to choose this
type of stimulus were, firstly, that a person’s own
name, because of its emotional content and repetition along life, appears as one of the most
relevant stimulus for any human subject. Secondly,
there is evidence that hearing our own name during
wakefulness produces cognitive brain responses,
including a P300, even in the absence of explicit
H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
245
Fig. 1. Grand average ERPs to own (thick traces) and other (thin traces) names in passive (left) and active (right) conditions
during wakefulness before (top) and after the night sleep, (negativity up). In active condition, subjects were instructed to count the
number of own names; in passive conditions, the instruction was to remain quiet during the name presentation. P3 to own name
was present in the passive condition, with smaller amplitude than in the active one. Note that the P3 to other names, which was
present but small in pre-sleep session, disappeared after the night.
instructions, thus suggesting that a subject’s name
is automatically and implicitly processed as a
target stimulus (Berlad and Pratt, 1995). Indeed,
several studies have shown that the presentation
to waking subjects of their own name in ‘passive’
(i.e. ‘no task’) conditions is able to elicit a positive
wave peaking between 400 and 500 ms after the
beginning of the stimulus, with maximal amplitude
over parietal regions (Berlad and Pratt, 1995; Pratt
et al., 1999; Perrin et al., 1999). The characteristics
of this wave (latency, amplitude and scalp topography) are consistent with those of the cognitive
‘P300’ component recorded in target detection
tasks (Fig. 1), known to be determined by the task
relevance and the unpredictability of the stimulus
(reviews in Picton, 1992; Hansenne, 2000a,b).
Two teams (Perrin et al., 1999; Pratt et al.,
1999) have so far recorded ERPs to subjects’ own
names during sleep. Pratt et al. used the subject’s
own name against a single irrelevant word which
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H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
acted as ‘non target’. Probabilities of presentation
of both types of words were counterbalanced so
as the ‘target’ word could appear with either 30 or
70% probability. Results in wakefulness and in
sleep were compared using Principal Component
Analysis. These investigators observed a significant effect of stimulus type (own name vs. irrelevant word) during S2 and SWS for different
components between 300 and 700 ms, and especially a more prominent P450 during S2 in addition
to KC waveform. They also reported an effect of
stimulus probability during PS for the P3 component (rare targets eliciting higher P3’s than frequent targets), suggesting a resemblance to the
waking P300 wave. The authors concluded that
there was ‘continued evaluation of auditory input
salience during sleep, which diminishes during
deep sleep and is replaced by evaluation of stimulus context in a train of stimulus during REM
sleep’. Interpretation of their results in terms of
detection of stimulus meaning is, however, uneasy
because target and non-target words, although
counterbalanced, were not equiprobable (70 vs.
30%), thus making the responses sensitive to
habituation and ‘physical novelty’ effects, in addition to stimulus significance. In order to get rid of
possible ambiguities linked to these phenomena,
Perrin et al. (1999) used a paradigm where the
subject’s own name was presented in strict equiprobable fashion against 7 other first names (with
12.5% probability each). Auditory ERPs from ten
healthy volunteers were recorded under these conditions, both during wakefulness and all-night
sleep (SWS responses not analysed). During wakefulness and PS the general morphology of ERPs
was very similar (Fig. 2); notably, in both cases a
late positive wave at 400–600 ms was selectively
evoked by the subject’s own name, with maximal
amplitude over the posterior scalp areas (but more
posterior in PS than during waking). Since all
stimuli were equiprobable, such ERP effect could
not be due to differences in stimulus regularity,
and indicates that the brain mechanisms subserving
discrimination of a subject’s own name remain
operational during PS (REM), independently of
any ‘physical rarity’ effect.
Previous work on sleep P300 suggests that prior
familiarization (during waking) with the target
stimuli to be presented facilitates the elicitation of
a P300 during PS. Thus, deviant tones of same
intensity as background stimuli, appearing with
10% probability, were able to evoke P300-like
waves during PS in trained subjects (Bastuji et al.,
1990, 1995; Niiyama et al., 1994; Sallinen et al.,
1996), but could not evoke PS-P300 in subjects
that had not previously learned the task (Cote´ et
al., 2001). In these latter, however, P300-like
waves could be triggered during PS by very
deviant and intrusive stimuli (stimuli much louder
than background tones, and delivered at 5% probability) (Cote´ and Campbell, 1999; Cote´ et al.,
2001). This leads to the hypothesis that the probability that a given stimulus enters the cognitive
level of processing reflected by P300 depends on
two phenomena: first, the intrinsic relevance of
the stimulus itself, and second its physical intrusiveness. In the case of a previously learned
detection task, the significance of the target stimulus is accessible to the subject before going to
sleep, and this significance appears to be ‘transferred’ to the ensuing PS. We may postulate that
the subject’s own name constitutes an intrinsically
significant stimulus, the knowledge of which need
not be transferred since it is permanently operational; therefore, one’s own name can always enter
a higher level of processing—hence explaining the
emergence of a P300 in PS without the need of
previous training.
In all previous studies, using either tones or
words, the general morphology of ERPs was much
more complex during SWS than in waking or PS,
most probably because responses in SWS often
included KCs induced by auditory stimulation (for
reviews see Halasz, 1998; Bastuji and GarciaLarrea, 1999; and Bastien, in this issue). When S2
and SWS ERPs are averaged in the presence of
concomitant visible KCs on background EEG, the
responses include two biphasic consecutive waveforms, commonly labeled ‘N2yP3’ and ‘N3yP4’.
When stimuli were proper names, the latencies of
these waveforms were delayed as compared to
those obtained with tones (Fig. 3), probably
because of differences in stimulus duration; however, their morphology and scalp distribution were
equivalent to those of ‘N2yP3’ and ‘N3yP4’,
classically described during S2 and SWS (Halasz,
H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
247
Fig. 2. Grand average ERPs to own (thick traces) and other (thin traces) names during passive pre-sleep waking (top) and paradoxical sleep (PS), (negativity up). The topographic maps of P3 are represented for each condition. Note the posterior and left
maximal amplitude of P3 during PS and the absence of P3 to other names in this stage.
1998; Bastuji and Garcia-Larrea, 1999; and Bastien, in this issue). In the study of Perrin et al.
(1999), these two biphasic waveforms evolved
differentially in response to ‘subject’s own’ and
‘other’ names: while the amplitude of the late
complex (‘N3yP4’) was identical for both types
of stimuli, the early portion of the KC (‘N2yP3’),
and notably the positive wave P3, were of significantly higher amplitude to the presentation of
‘own’ names. Such differential behaviour strengthens the hypothesis of a ‘functional duality’ of KC
generating mechanisms, originally put forward by
Ujszaszi and Halasz (1988), who indeed suggested
that the early and late KC waveforms reflected the
activation of two distinct functional systems, of
which only the former would be connected to the
information processing of external stimuli.
When ERPs are averaged in the absence of
concomitant KCs in the EEG, only the early
portion of the response (‘N2–P3’), of low amplitude, is commonly observed (Perrin et al., 2000;
see Fig. 3). Both latency and scalp distribution
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H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
Fig. 3. (a) Grand average ERPs to own (thick traces) and other (thin traces) names during passive pre-sleep waking (top) and
stage 2 (S2) (negativity up). The topographic maps of P3 are represented for each condition and those of N3 and P4 for S2. (b)
Grand average ERPs in S2 of traces without KCs. (c) Grand average ERPs in S2 of traces with KCs. Note that a P3 to own names
was observed in S2 whether KCs were or not present and that a smaller P3 to other names was also recorded during this stage. The
amplitude of the N3yP4 was similar in response of both own and other names.
H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
strongly suggest that these N2–P3 waves, when
evoked alone, do correspond to the early portion
of the KC described previously. Perrin et al. (2000)
analysed these two early components with and
without the presence of a concomitant KC, and
showed that they were significantly enhanced in
response to the subjects’ own name relative to
other first names, to a similar degree whether they
were part of a KC or not. The P3 wave sensitivity
to the subject’s own name, both in presence and
in absence of a KC, suggests that the processing
of such stimulus significance during S2 is effective
even when the high amplitude N3–P4, which
corresponds to the typical form of KC, is not
elicited. This also means that the differential
response to the own name is not contingent of the
‘full’ KC. Therefore, even if the KC might be
elicited by an auditory stimulus, its evocation is
not necessary to the electrophysiological detection
of a relevant stimulus.
2. Are sleep and waking P3 functionally
equivalent?
The fact that a ‘P3’ component to the subject’s
own name may persist during S2 and PS clearly
indicates that some cognitive processing of relevant stimuli also persists during sleep. However,
the existence of sleep-P3s does not necessarily
imply that their underlying processes are equivalent to those of the waking counterparts, and the
question whether waking and sleep P3s can be
considered as functionally equivalent remains
open.
2.1. Paradoxical (REM) sleep
As regards PS, the general morphology, latency,
specificity to relevant stimuli and scalp distribution
of the ‘PS-P3’ recorded in this stage are close to
those observed during wakefulness. Waking P300
occurs when the subject is actively engaged in a
detection task; it is related to stimulus categorisation (Donchin and Coles, 1988; Picton, 1992) and
may represent a post-decisional ‘cognitive closure’
mechanism (Desmedt, 1980; Verleger, 1988,
1998). Considering the PS-P3 as a functional
equivalent of the waking P300 assumes therefore
249
that stimulus selection and categorisation remain
active during this sleep stage. This also implies
that some top–down processes remain operational
during PS, since comparison of incoming stimulus
against some pre-existing template is necessary for
stimulus selection. These assumptions are not
incompatible with current thoughts about the cognitive capabilities of PS (Hobson, 1990; Pare and
Llinas, 1995). However, although the PS-P3 and
the waking-P3 may have some common functional
significance, their respective cerebral generators
do not appear to be strictly the same. Indeed, the
scalp topography of PS-P3 consistently differs
from that of waking P3: frontal subcomponents
are lacking during PS, resulting in a significant
‘shift’ of PS-P3 towards the posterior regions of
the scalp that has been ascertained by several
investigators (Niiyama et al., 1994; Bastuji et al.,
1995; Cote´ and Campbell, 1999). It is tempting to
suggest that such topographical changes might
reflect a deficit in the activation of frontal P3
generators thought to subserve attentional control
and orienting during waking P3 (Baudena et al.,
´
1995; Bradzil
et al., 1999), such attenuation leading to a anterior–posterior disbalance during P3
generation, with predominance of posterior (visual) and parieto-temporal P3-related processes. This
suggestion fits with recent neuroimaging results
showing a deficit in frontal activation during this
stage, concomitant with an enhancement of the
temporo-posterior metabolism (review in Maquet,
2000).
From a neurochemical point of view, the balance
between noradrenergic and cholinergic brain systems also changes critically from wakefulness to
PS, with decrease in noradrenergic activity and
activation of cholinergic processes (Siegel and
Rogawski, 1988; Hobson, 1990; Steriade et al.,
1990). Taking into account that both systems are
important for P300 generation during waking
(Hammond et al., 1987; Harrison et al., 1988;
Pineda et al., 1989; Swick et al., 1994), and that
the noradrenergic projections, notably from the
locus coeruleus, are largely distributed over, and
influence the function of, the prefrontal cortex
(Oken and Salinsky, 1992; Arnsten et al., 1996),
it may be hypothesised that topographic changes
observed in electrophysiological and metabolic
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H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
Fig. 4. ERPs elicited at Cz by semantically related (thin traces) and unrelated (thick) target words in one subject during wakefulness,
stage 2, stages 3–4 and REM stage (PS). For each condition superimposed traces from two averaging (negativity down). A ‘N400’
was observed to unrelated words during waking, S2 and PS conditions. (Reproduced with permission from Brualla et al. (1998).)
studies during PS may also be related to the
decrease of noradrenergic tone during this stage.
Thus, while keeping close functional significance,
PS and waking P3 activities may be sustained by
generating mechanisms with only partial overlap.
Such differences might in turn help to explain the
disparities in the processing of sensory information
during the two stages, notably as regards stimulus
awareness and memory encoding, as recent animal
data suggest that memory storage is regulated by
an interaction of noradrenergic and cholinergic
influences (e.g. Introinicollison et al., 1996).
2.2. Sleep stage 2
The comparisons between sleep and waking P3s
are more difficult when it comes to sleep S2, the
significance of ‘P3’ during this stage remaining
still doubtful and subject to controversy. Indeed,
even if in S2 a ‘P3’ component (‘S2–P3’) is
enhanced in response to subjects’ own name, this
component may be also observed, with lower
amplitude, in response to other names (Perrin et
al., 1999, 2000) (Fig. 3), and even in response to
repetitive monotonous tones (Ujszaszi and Halasz,
1988; Nielsen-Bohlman et al., 1991; Bastuji et al.,
1995; Hull and Harsh, 2001). The ‘S2–P3’ thus
seems to be much less selective to relevant stimuli
than the PS-P3, and considering the family of S2–
P3s as pure reflects of the discrimination of a
relevant stimulus is hardly tenable. Weakening of
P300 selectivity to relevant stimuli has been reported in some pathological contexts such as schizophrenia (Wagner et al., 1997; Nieman et al., 1998;
Knott et al., 1999), and interpreted as a deficit in
non-target inhibition. Similar conclusions were
drawn on a patient with blindsight (Shefrin et al.,
1988), in whom a P300 was observed in response
to both rare and frequent stimuli delivered in the
blind hemifield, suggesting that both relevant and
irrelevant stimuli were processed as targets.
Although these results may be reminiscent of those
observed during sleep S2, they can hardly be
integrated in a same model, since their unique
convergence stands in the unselective behaviour
of P300. During SWS, the whole metabolic activity
of the cortex is decreased (Maquet, 2000) and
there is some experimental evidence to suppose a
specific inhibition of thalamo-cortical connectivity
(Steriade, 1994). The extent to which a reduced
capability for selective stimulus processing in S2
would be related to the functional changes in
thalamo-cortical network during this stage needs
further investigation. A further difference between
S2 and waking P3 is the presence, during S2
exclusively, of ‘N3’ and ‘P4’ potentials corre-
H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
251
Fig. 5. Grand average ERPs over Cz to congruous (thin traces), incongruous (thick traces) and pseudo-words (medium traces)
during wakefulness, PS and stage 2 (negativity up). Note that the amplitude of N400 is higher in response to incongruous words
during wakefulness, to pseudo-words during PS, and is similar for incongruous and pseudo-words during S2.
sponding to the late portions of the KC. The N2y
P3 and N3yP4 complexes may reflect the
occurrence of two parallel mechanisms in response
to stimulus presentation, of which only the first
would be sensitive to the stimulus’ intrinsic relevance, the second being related to its salience or
physical deviance (Perrin et al., 2000).
3. P300, consciousness and memory encoding
During wakefulness, P300 has been considered
as an electrophysiological event concomitant to
the access of information to consciousness and
memory (review in Picton, 1992). In favour of
this hypothesis stands the fact that, in waking, the
P300 is a response to events requiring controlled
processing, which is both effortful and conscious
¨
(Posner et al., 1973; Rosler,
1983). Several teams
have shown a relationship between P300 characteristics and subsequent memory of the stimulus
(Johnson et al., 1985; Howard and Polich, 1985),
and drugs with deleterious effects on memory,
such as anticholinergics, are also deleterious for
P300 (Potter et al., 1992). From results obtained
during sleep, it is obvious that the mere presence
of a P3 in average traces does not warrant the
access of stimulus to stable memory stores, since
this component can be recorded during PS (and
probably S2) even if subjects will not remember
the stimulus after awakening. A similar dissociation between P3 and conscious awareness has been
described in a few patients with very particular
cognitive disorders, such as the prosopagnosic
patient recorded by Renault et al. (1989) and the
patient with blindsight reported by Shefrin et al.
(1988). These results among others suggest different levels of stimulus encoding, and notably the
possibility of dissociation between instantaneous
and long-term awareness. Damasio’s model of
consciousness appears relevant in this context: in
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H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
this author’s view, (Damasio, 1998), a ‘low’ level
of consciousness, or ‘core consciousness’, would
correspond to the transient process that is incessantly generated relative to any object with which
an organism interacts, and during which a transient
‘core self’ or transient sense of knowing, are
automatically generated. A second, higher level,
or ‘extended consciousness’ would depend upon
the build-up of an autobiographical self and a set
of memories of past and anticipated experiences.
Only this extended consciousness would require
conventional memory. A dissociation between
‘core’ and ‘extended’ consciousness during sleep
may be hypothesised, but not directly evaluated
since this would imply to have subjects awakened
immediately after the stimulus sessions, which was
not done in previous ERP studies. The question
whether some form of ‘core consciousness’ is
preserved in association to the evocation of P3
cannot, therefore, be answered at this stage. However, studies showing incorporation of external
stimulus to the oniric content (Burton et al., 1988;
Nielsen, 1993) give indirect arguments to the
possibility that core consciousness might be preserved at least during PS. Further evidence in this
line could be gathered in the future if the incorporation of external stimuli to dreams was shown
to be related to P3 generation.
4. Semantic discrimination during sleep
The studies reviewed in previous paragraphs
demonstrated that the sleeping brain remains able
to discriminate between words varying in their
intrinsic meaning (Perrin et al., 1999, 2000; Pratt
et al., 1999). However, the stimuli used in those
studies were proper names, which do not have a
strict semantic content as compared with common
names. From a linguistic point of view, the question whether the processing of proper names is or
not semantic remains controversial (Frege, 1949;
Searle, 1967; Muller and Kutas, 1996). Standing
on the observation of neuropsychological disorders
(Semenza and Zettin, 1988; Yasuda et al., 2000),
neuroimaging investigations (Damasio et al.,
1996) and ERP studies (Proverbio et al., 2001),
there is increasing evidence that common names
and proper names do not activate identical cerebral
networks. Therefore, even if the subject’s own
names were certainly ‘discriminated’ during sleep,
the actual level of discrimination (phonological vs.
semantical) performed by the sleeping brain cannot
be specified by these studies.
This question has been recently addressed by
two different teams that investigated the ‘N400’
wave of ERPs in response to common words
devoid of emotional context. During wakefulness,
the N400 wave is enhanced in response to words
that are semantically anomalous relative to a given
context, the amplitude of this effect being correlated to the degree of semantic incongruence
(Kutas and Hillyard, 1980; Bentin et al., 1985).
Brualla et al. (1998) were the first to report that a
negative deflection similar to the N400 persisted
during S2 and PS in response to semantically
unrelated words, suggesting that a simple semantic
association of common words remains operative
during these sleep stages (Fig. 4). We further
studied how linguistic and pseudo-linguistic stimuli were categorised during sleep as compared to
waking (Perrin et al., 2002), by presenting, during
waking, S2 and SP, different sequences of auditory
stimuli containing pairs of words which included
a ‘prime’ followed by either a semantically congruous word or by an incongruous word (50%
each). Between each pair, we inserted a disyllabic
sound without meaning (‘pseudo-word’), which
allowed to compare the N400 in response to (a)
congruous or (b) incongruous words following a
prime, (c) pseudo-words following a real word,
and (d) primes following a pseudo-word. During
wakefulness, the N400 wave developed higher
amplitude for pseudo-words than for real but
semantically incongruous words, as previously
described (Bentin et al., 1985). The N400 response
to incongruous words persisted during S2 and PS.
During S2, 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. However, no significant
difference existed between different levels of discordance, suggesting a loss in this sleep stage of
the hierarchic processes observed in wakefulness.
A hierarchic process of discordance reappeared
in PS, which however differed from that of the
H. Bastuji et al. / International Journal of Psychophysiology 46 (2002) 243–255
waking state. While incongruous and ‘prime’
words yielded, as in S2, higher N400 amplitudes
than congruous words, N400 amplitude to pseudowords was surprisingly similar to that elicited by
congruous words, suggesting that pseudo-words
were not detected as ‘incongruous’ stimuli during
PS (Fig. 5). These results are in accordance with
the fact that linguistic absurdity (such as onomatopoeia) is accepted in a different manner during
PS sleep than during waking, and this might
contribute to explain why absurd contents are so
naturally incorporated into otherwise plausible
dream stories.
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