Clinical Neurophysiology 111, Suppl.

2 (2000) S60±S64
www.elsevier.com/locate/clinph

Sleep and EEG interictal epileptiform abnormalities in partial epilepsy

Gian Luigi Gigli a,*, Mariarosaria Valente b
a
Dipartimento di Neuroscienze, Azienda Ospedaliera Santa Maria della Misericordia, 33100 Udine, Italy
b
Clinica Neurologica, DPMSC, UniversitaÁ di Udine, Udine, Italy

Abstract
The relationship between sleep and EEG interictal epileptiform abnormalities (IEA) has been studied from different perspectives. One of
the most followed orientations regards the investigation of the effects of IEA on sleep organization, while another approach considers the
modulation of IEA caused by sleep. Only the latter approach, for its practical diagnostic implications, is covered by the present review. In
particular, on the basis of the literature and of personal studies, we review some relevant aspects of the relationship between the different
stages of the sleep and the EEG epileptic abnormalities in partial epilepsy. In addition, the modulation of IEA by ¯uctuations of the level of
arousal and by sleep microstructure is reviewed. Finally, the information obtained on localization of epileptic foci from recordings during
wakefulness and different sleep stages is discussed. q 2000 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Sleep; Interictal abnormalities; Partial epilepsy; Localization of spikes

1. Introduction ings have been reported by some authors, who found an

Many studies have indicated an increased spiking rate
during sleep in the majority of patients affected by focal
epilepsies (Gloor et al., 1958; White et al., 1962; Ross et
al., 1966; Rowan et al., 1982; Martins da Silva et al., 1984).
Spiking rates are reported to be increased mainly during
stages 1 and 2 of non-REM (NREM) sleep (Niedermeyer
and Rocca, 1972; Angeleri, 1975; Dalaskov, 1975; Kell-
away, 1985). Also focal epilepsies with secondary general-
ization are most likely to display their IEA during NREM
sleep (Ferroni et al., 1969; Billiard, 1982; Niedermeyer,
1982).
It is not surprising, therefore, that when comparing the
diagnostic gain of sleep EEG to that of the EEG during
wakefulness it was found that the sensitivity of the exam-
ination changed from 8±28% during wakefulness to 72±
98% during sleep (Gibbs and Gibbs, 1947; Ganshirt and
Vetter, 1961; Jovanovic, 1967; Ajmone-Marsan and Zivin,
1970; Declerck et al., 1982; Binnie, 1996).
Similar effects of NREM sleep have been shown in the
monkey with temporal lobe epilepsy after alumina cream
(Mayanagi, 1977). On the contrary, REM sleep caused a
block of IEA in experimental epilepsy obtained with injec-
tion of kainic acid in the amygdala (Cepeda et al., 1984,
1986; Cepeda and Tanaka, 1982). However, divergent ®nd-
* Corresponding author. Tel.: 139-0432-552720; fax: 139-0432-
552719.
E-mail address: prim.neuro@aoud.sanita.fvg.it (G.L. Gigli).
1388-2457/00/$ - see front matter q 2000 Elsevier Science Ireland Ltd. All rights reserved.
PII: S13 88-2457(00)0040 3-X
increase of focal discharge during REM sleep in patients
with temporal lobe epilepsy (TLE) (Passouant et al., 1965;
Mayersdorf and Wilder, 1974; Billiard, 1982). Increased
IEA during REM sleep has also been reported in models
of experimental epilepsy. Namely, increased discharges
during REM sleep have been found in limbic epilepsies
induced by intraseptal injection of ouabaine (Arias and
Passouant, 1971) and in monkeys with temporal foci
induced by application of alumina cream (Frank and
Pegram, 1974).
Some of the con¯icts previously reported could have been
due to the fact that some of these studies pooled together
patients with different epileptic syndromes, used classi®ca-
tion criteria different from current ones, and were limited by
the diagnostic instrumentation available at the time. A more
precise approach has been based on investigations
conducted on clinically homogeneous groups.
On the basis of the literature and our own investigations,
the relevant ®ndings of the relationships between IEA and
sleep in patients with partial epilepsy will be reviewed in the
following parts of this paper.
1.1. IEA in idiopathic partial epilepsies (IPE)
Idiopathic partial epilepsies show an important activation
during sleep, particularly during slow wave sleep (SWS),
but also during REM sleep (Dalla Bernardina and Beghini,
1976; Ambrosetto et al., 1977; Dalla Bernardina et al.,
1984). During SWS, the maximum spiking rate occurs
CLINPH 1033
 G.L. Gigli, M. Valente / Clinical Neurophysiology 111, Suppl. 2 (2000) S60±S64
during stages 3 and 4 of the ®rst cycle of sleep, i.e. during
the maximum of SWS pressure (Clemens and Majoros,
1987). Even if, in a minority of patients, it is possible that
during SWS there are only a few spikes, or that spiking rates
in wakefulness are not increased by SWS, in no case is
wakefulness able to increase spiking rates observed during
SWS (Billiard et al., 1990). IEA during SWS spread to
adjacent regions of the same hemisphere and to the homo-
logous regions of the contralateral one (Dalla Bernardina et
al., 1992). These observations are based mainly on studies
on idiopathic partial epilepsy with rolandic spikes, but are
con®rmed by reports on idiopathic partial epilepsy with
occipital paroxysms (Dalla Bernardina et al., 1982; Gastaut,
1982), on epilepsies with discharges evoked by somato-
sensory stimulation (De Marco and Negrin, 1973) and on
a particular form of partial epilepsy associated with fragile-
X (Musumeci et al., 1988). Some cases of IPE, which are
very activated during sleep, raise the question of a possible
continuum between IPE, Landau±Kleffner syndrome and
electrical status epilepticus during sleep (ESES) (Autret,
1995).
1.2. IEA in cryptogenetic and symptomatic partial
epilepsies
1.2.1. Spiking rates
Spiking rates of lesional partial epilepsies usually show
an important increase during stages 3 and 4 of SWS and a
suppression or diminution during REM sleep. However, an
increased discharge rate during REM sleep has been docu-
mented in some TLE patients (Passouant et al., 1965;
Mayersdorf and Wilder, 1974; Billiard, 1982; Sammaritano
et al., 1991). These results have been con®rmed in experi-
mental models of partial epilepsy (Wyler, 1974; Shouse et
al., 1989a; Gigli and Gotman, 1991). In patients with foci
located in the amygdala and/or the hippocampus, Montplai-
sir et al. (1980) observed also that the activation of spiking
during NREM sleep was inversely related to the spike
frequency during wakefulness: the lower the spiking rate
during wakefulness, the larger the level of activation during
NREM sleep.
Severely lesioned brains are less subject to modulation by
modi®cations of the state of vigilance, and epileptic
syndromes with important cerebral damage are most likely
to present IEA randomly distributed during the sleep±wake
cycle. The lack of modulation of IEA during sleep in
patients with effective pharmacological treatment can be
considered along the same lines, with the observation of
dispersion of the residual, most resistant IEA across the
sleep±wake cycle (Lockard et al., 1987).
1.2.2. Spike topography
Concerning the topography of IEA of lesional partial
epilepsies, during NREM sleep spikes tend to spread from
the primary focus to ipsi- and contralateral brain regions. In
addition, during NREM sleep it is possible to observe the
S61
activation of independent foci, especially contralateral to
the main focus. The observations made with scalp EEGs
have been con®rmed by depth EEG recordings, showing
that the maximal focalization of IEA is present during
REM sleep (Perria et al., 1966; Rossi et al., 1974, 1984;
Lieb et al., 1980; Montplaisir et al., 1980, 1982; Wieser,
1983). The stability of IEA during wakefulness and different
sleep stages has been considered as a sign of autonomy of
IEA across behavioral states speci®c to the epileptogenic
zone (Perria et al., 1966; Cavazza et al., 1973; Rossi et
al., 1974, 1984; Montplaisir et al., 1980; Wieser, 1984).
Similar ®ndings of stable EEG discharges during different
conditions of vigilance had already been observed by Lugar-
esi et al. (1966) in patients with epilepsia partialis continua.
1.2.3. Spike morphology
NREM sleep increases amplitude and duration and
decreases sharpness of interictal spikes compared to wake-
fulness and REM sleep. During REM sleep spikes become
smaller, shorter and sharper compared to NREM sleep.
Changes of spike morphology associated with REM sleep
are similar to those observed after pharmacological control
of seizures (Frost et al., 1991).
1.3. IEA and localization of foci in TLE
Personal observations in a series of 40 patients with TLE
selected from candidates for epilepsy surgery (Sammaritano
et al., 1991) revealed an activation of spiking activity during
sleep in 39 out of 40 cases. Among patients activated by
sleep, maximal spiking rates were observed during SWS in
34 cases and during REM sleep in 5 cases.
In 15 patients with unilateral focus showing spiking
during wakefulness, NREM and REM sleep, the electrical
®eld was restricted in 9/15 cases during REM sleep
compared to wakefulness, and in 12/15 cases during wake-
fulness compared to SWS. In addition, during NREM sleep,
new contralateral independent foci were observed in 53% of
patients. More importantly, considering the information
given by recordings in terms of lateralization of EEG
abnormalities for surgical decisions during NREM sleep,
EEG led to misleading lateralization or no side predomi-
nance of spikes in 5/18 patients with bitemporal indepen-
dent foci. On the contrary, in only one of the 8 patients with
bitemporal independent foci during wakefulness was there
no side predominance. There was instead no problem of
lateralization during REM sleep, all foci being only unilat-
eral and concordant with the ®nal localizing diagnosis, as
determined by the side of surgical intervention, based on
history, neurological examination, neuroimaging, neuropsy-
chological evaluation, electrocorticography and seizure
onset. Except for the lack of bitemporal independent foci
during REM sleep, wakefulness and REM sleep showed
similar ®eld distribution and spiking rates of epileptic foci.
In summary, our results suggest that localization of the
primary epileptogenic area is more reliable in REM sleep
S62 G.L. Gigli, M. Valente / Clinical Neurophysiology 111, Suppl. 2 (2000) S60±S64
compared to wakefulness and that it is more reliable in
wakefulness than in SWS.
Somewhat different results were obtained by Adachi et al.
(1998), who retrospectively studied the reliability of waking
and sleep EEG in patients after successful surgery for TLE.
They found that the reliability of discharge lateralization
improved from wakefulness to NREM sleep, especially in
those patients showing no IEA or no side predominance
(,75%) of spikes during wakefulness. However, in patients
with incorrect lateralization during wakefulness, no
improvement in reliability was obtained in sleep recordings.
This result was obtained mainly thanks to the activating
effect of NREM sleep. Unilateral discharges or discharges
showing a clear side predominance (.75%) in the awake
state were generally unchanged during sleep, whether ipsi-
lateral or contralateral to the epileptogenic zone.
The results obtained by Adachi et al. (1998) are not very
different from ours (Sammaritano et al., 1991). First, they
did not consider REM sleep, but only compared wakeful-
ness to NREM sleep. In addition, with respect to discharge
lateralization, considering unilateral spiking or clear side
predominance, in our study the predictive value of EEG
changed from 62.2% of all patients in wakefulness to
91.9% in sleep. The main difference is that Adachi et al.
(1998) pooled the patients with no spiking and with no side
predominance with those giving incorrect information
(spiking contralateral to the side of operation). This
increased the yield of the sleep recordings, a result that
was present also in the series of Sammaritano et al.
(1991). However, incorrect lateralizations were observed
in 10.8% of the cases during wakefulness and in 10.9%
during NREM sleep, which is not negligible in a series of
patients who were all successfully operated. This ®nding is
not distant from that of Sammaritano et al. (1991), who
found incorrect lateralizations in 2.5% of recordings during
wakefulness and in 7.5% during NREM sleep, but none
during REM sleep.
1.4. IEA modulation by ¯uctuations of the level of arousal
Transitional phases between wakefulness and sleep and
the states of unstable vigilance are reported to promote a
powerful activation of spiking in focal lesional epilepsy
(Montplaisir et al., 1982; Rossi et al., 1984; Wieser, 1984;
Declerk and Wauquier, 1989; Touchon et al., 1987, 1991).
These observations are particularly important considering
that sleep in TLE has been characterized by instability, with
a signi®cant increase in the number and duration of awaken-
ings and stage shift (Touchon et al., 1987; Gigli et al., 1997).
Similar sleep instability has been found in the experimental
epilepsy model of kindling in amygdala (Gigli and Gotman,
1992). The role of arousal ¯uctuations in modulating epilep-
tiform abnormalities has been con®rmed in experimental
models of epilepsy, like kindling (Shouse, 1987; Shouse et
al., 1989b; Gigli and Gotman, 1991). Similar results have
been reported in stereo EEG studies, relating IEA during
sleep to arousal phasic events of NREM sleep (Hess et al.,
1982).
On the other hand, a role of synchronization processes
during NREM sleep on facilitation of IEA and epileptic
seizures has also been suggested (Steriade et al., 1994). It
is the ascending limb of maximal delta power (during which
patients move to the deeper stages of NREM sleep), the part
of the sleep cycle during which spikes cluster (Malow et al.,
1998). In the same study, in fact, only a minority of spikes
was preceded or followed by an arousal from sleep.
Similar results have been observed in children by Nobili
et al. (1999b). The apparent contradiction between the acti-
vating effects of arousals and those of synchronization has
been interpreted by the fundamental works of the school of
Parma.
1.5. IEA and the sleep microstructure
Terzano et al. (1985) described a method for analysis and
measurement of arousal ¯uctuations in EEG during NREM
sleep, distinguishing periods of instability, characterized by
repetitive sequences of cyclic alternating pattern (CAP),
from periods of stability or non-CAP (NCAP). Within
CAP it was possible to identify a phase of activation
(phase A) and a phase of quiescence (phase B). The ratio
between the time spent during CAP and the total duration of
NREM sleep (CAP rate) has been considered as a measure
of sleep instability. This method of analysis of sleep micro-
structure has been applied to different clinical situations,
proving to be an effective descriptor not only of insomnia,
but also of motor phenomena like periodic limb movements
during sleep (PLMS), bruxism, or sleep walking.
The same method has also been applied to epilepsy,
showing that in primary generalized epilepsies phase A of
CAP exerts a strong activating in¯uence on epileptic
discharges, with phase B acting as a condition of inhibition
and NCAP as an intermediate situation (Terzano et al.,
1989; Gigli et al., 1992).
Idiopatic partial epilepsies with rolandic spikes have a
completely different behavior, showing mainly a strong
association of IEA with sleep stages (phases of synchroni-
zation) (Terzano et al., 1991b), even if, more recently, an
association between sigma activity (sleep spindles) and IEA
has been shown (Nobili et al., 1999a). Symptomatic and
cryptogenetic focal epilepsies showed a kind of behavior
somewhat in between, being related to CAP but also to
the mechanisms of synchronization (Loh et al., 1997;
Terzano et al., 1991b). CAP (especially phase A) exerts
an even more powerful in¯uence on the secondary bisyn-
chronous bursts (Terzano et al., 1991a). It is mainly the
phase A1 subtype, linked to the descending phase of the
sleep cycle (increasing delta power), which produces a
stronger activating in¯uence on IEA, at least in idiopathic
generalized epilepsies.
Terzano interprets his ®ndings as if, compared to general-
ized EEG abnormalities, there was a weaker modulation of
 G.L. Gigli, M. Valente / Clinical Neurophysiology 111, Suppl. 2 (2000) S60±S64
arousal control on focal manifestations. It is for this reason
that there is no regulation of IEA by CAP/NCAP modality
in idiopathic partial epilepsies with rolandic spikes, a kind
of epilepsy with foci very peripheral to the thalamo-cortical
circuits, for which a greater dependence of functional corti-
cal EEG abnormalities on the degree of synchronization
during sleep is suggested. On the contrary, generalized
interictal bursts seem to be entrained by the regulatory
mechanisms of CAP (arousal modulation in a state of
lower vigilance). Focal lesional spikes are likely submitted
to a dual regulation (arousal control and EEG synchroniza-
tion during sleep).
2. Conclusions
It is clear from this review that the IEA are activated
during NREM sleep in the majority of cases of partial
epilepsy. However, the reason why maximum spiking
rates occur in a few patients during REM sleep remains
unexplained. In addition, the question of whether REM
sleep really causes a lateralization and a focalization of
spikes in the proximity of the epileptogenic zone remains
open. A positive answer to this question would be relevant
for surgical treatment of medically intractable epilepsies. In
fact, if REM sleep is the condition of maximal focalization
of interictal spikes, recordings containing spikes during
REM sleep should be considered a low-cost and precise
method for localizing epileptic foci. A further contribution
to the solution of this problem could be given by recordings
obtained from subjects: (i) with known lateralization of the
epileptic focus (e.g. post-ischemic epilepsy); (ii) with suf®-
cient amount of spikes coming from bilateral independent
foci; and (iii) producing spikes also during REM sleep.
Finally, the modulating role of CAP needs to be clari®ed,
with reference to the different cryptogenetic and sympto-
matic partial epileptic syndromes. Possible differences
between partial and generalized epilepsies for the speci®c
contribution of A1 phases to the activation of spikes should
be veri®ed.
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