Handbook of Clinical Neurology, Vol.

161 (3rd series)

Clinical Neurophysiology: Diseases and Disorders
K.H. Levin and P. Chauvel, Editors
https://doi.org/10.1016/B978-0-444-64142-7.00062-X
Copyright © 2019 Elsevier B.V. All rights reserved

Chapter 25

Clinical neurophysiology of REM parasomnias

AMBRA STEFANI, EVI HOLZKNECHT, AND BIRGIT HOGL* €
Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria

Abstract
Rapid eye movement (REM) sleep behavior disorder (RBD), sleep paralysis, and nightmare disorder are
the three REM sleep parasomnias outlined by the International Classification of Sleep Disorders. In this
review we address the clinical neurophysiology of these disorders. The majority of neurophysiologic
studies have been conducted in RBD, and fewer studies have evaluated patients with nightmare disorder
or isolated sleep paralysis. Neurophysiologic studies of REM sleep parasomnias mostly used polysomno-
graphy (PSG), or were performed on animals to shed light on the pathophysiology of these disorders.
Fewer studies used electoencephalography or electromyography outside the context of PSG, evoked
potentials, or autonomic neurophysiologic studies. In this chapter, the main neurophysiologic findings
in REM sleep parasomnias are described and their implications and relevance are discussed.

INTRODUCTION REM SLEEP BEHAVIOR DISORDER

REM sleep behavior disorder (RBD), sleep paralysis,
and nightmare disorders are the parasomnias of REM
sleep, according to the International Classification of
Sleep Disorders, Third Edition (ICSD-3) (American
Academy of Sleep Medicine, 2014). We performed
a systematic literature search concerning the clinical
neurophysiology of these disorders, using the search
terms REM sleep behavior disorder (RBD), sleep
paralysis, nightmare disorders, and polysomnography
(PSG), electroencephalography (EEG), electrooculo-
graphy (EOG), rapid eye movements (REMs), evoked
potentials, electromyography (EMG), REM sleep
without atonia, nerve conduction velocity, event-
related potentials, evoked potentials, visual evoked
potentials, sensory evoked potentials, motor evoked
potentials, brainstem reflex, blink reflex, autonomic
dysfunction, transcranial magnetic stimulation, and
cortico-muscular coherence. The results are presented
in this chapter. Given that these disorders are sleep
disorders, the most used neurophysiologic method is
polysomnography. RBD is the best-studied disorder
neurophysiologically.
RBD is characterized by abnormal behaviors emerging
during REM sleep. These RBD behaviors manifest as
an enactment of dreams that are often unpleasant,
action-filled, and violent. RBD can cause sleep disruption
and can also cause injuries to the patient or to their bed
partner (American Academy of Sleep Medicine, 2014).
The current diagnostic criteria for RBD were
published in the International Classification of Sleep
Disorders, Third Edition, American Academy of Sleep
Medicine (2014) and require repeated episodes of
REM sleep–related vocalization and/or complex motor
behaviors as well as pathologically increased EMG
activity during REM sleep, as demonstrated by video-
PSG (American Academy of Sleep Medicine, 2014).
RBD can be idiopathic or associated with neurologic
disorders, mostly a-synucleinopathies (Parkinson’s
disease [PD], dementia with Lewy bodies [DLB], or,
rarely, multiple system atrophy [MSA]). RBD can also
be associated with autoimmune diseases (e.g., narco-
lepsy, Anti-IgLON5 disease) (Sabater et al., 2014;
H€ogl et al., 2015) or with other neurologic disorders
(H€ogl and Iranzo, 2017). The clinical relevance of

*Correspondence to: Birgit H€ogl, Department of Neurology, Medical University of Innsbruck, Anichstrasse 35, 6020 Innsbruck,
Austria. Tel: +43-512-504-81172, +43-512-504-23811, Fax: +43-512-504-23842, E-mail: birgit.ho@i-med.ac.at
382 A. STEFANI ET AL.
idiopathic RBD (iRBD) has been reconsidered during
recent years due to increasing evidence that the vast
majority of patients with iRBD develop a neurodegen-
erative disease over time, namely an a-synucleinopathy.
The risk of conversion is over 80% in longitudinal stud-
ies with follow-up over 10 years (Postuma et al., 2012;
Schenck et al., 2013; Iranzo et al., 2016). Moreover, a
recent study showed that even in iRBD patients who
did not convert after a follow-up of 10 years or more,
biomarkers of a-synuclein–related neurodegeneration
are present (Iranzo et al., 2017). In light of these data,
iRBD is now considered an early stage a-synucleinopa-
thy, manifesting in some cases many years before first
appearance of motor symptoms during wakefulness or
cognitive manifestations. Therefore, the term “isolated”
RBD has been suggested as more appropriate, reflecting
the continuum of progression (H€ ogl et al., 2018).
Neurophysiologic studies in animals to
investigate the pathophysiology of RBD
Several animal studies have reproduced, in different
ways, the cardinal features of RBD. At the neuroana-
tomic level, sublaterodorsal tegmental nucleus neurons
specifically activated during paradoxical sleep send des-
cending efferents to glycine/GABA neurons within the
ventral medulla, but not ascending projections to the
intralaminar thalamus. This suggests a crucial role of
sublaterodorsal tegmental nucleus neurons in muscle
atonia rather than in paradoxical sleep generation. In line
with this hypothesis, 30 days after adeno-associated
virus injections into the sublaterodorsal tegmental
nucleus, rats display a 30% decrease in daily paradoxical
sleep quantity and a significant increase of muscle tone
during paradoxical sleep concomitant with a large
increase in abnormal motor dream–enacting behaviors
(Valencia Garcia et al., 2017). Glutamate sublaterodorsal
tegmental nucleus neurons generate muscle atonia dur-
ing paradoxical sleep, most likely through descending
projections to glycine/GABA premotor neurons in the
ventral medulla (Valencia Garcia et al., 2017).
Caudal ventral mesopontine junction lesioned animals
show an increase in phasic motor activity in REM sleep,
resembling that seen in human RBD (Lai et al., 2008).
Transgenic mice with deficient glycine and GABA
transmission have a behavioral, motor, and sleep pheno-
type typical of RBD, including REM motor behaviors,
non-REM muscle twitches, sleep disruption, and EEG
slowing (Brooks and Peever, 2011).
Chemogenetic activation of glutamatergic neurons of
the red nucleus produces excessive muscle twitching
during REM sleep. The function of this brief muscle acti-
vation during REM sleep has been investigated, and a
study in neonatal rats established that muscle twitches
during REM sleep drive the activity and development
of the motor cortex (Fraigne et al., 2015). Twitches dur-
ing REM sleep are “self-generated events” that have been
proposed to function to promote motor learning and
development. An inhibitory drive onto skeletal motor
neurons produces a temporally coordinated pattern of
muscle twitches during REM sleep. Muscle twitches in
adult rats follow a well-defined temporal trajectory: they
are largely absent during REM initiation but increase
steadily thereafter, peaking toward REM termination.
A GABA and glycine drive onto motor neurons prevents
twitch activity during REM initiation, but progressive
weakening of this drive functions to promote twitch
activity during REM termination (Brooks and Peever,
2016). These findings in animal studies may explain
the observation that during a REM behavioral episode
the movement often starts with single muscle twitches,
similar to physiologic twitches in REM sleep, and
then extends to more muscles, and finally terminates
in a typical RBD movement, i.e., complex acting-out-
of-dreams movements. In line with the data reported
in animals by Brooks and Peever (Brooks and
Peever, 2016) in RBD patients, a progressive weaken-
ing of the GABA and glycine motor neuron inhibition
seems to occur, promoting twitch activity during
REM termination.
Neurophysiology of RBD
POLYSOMNOGRAPHY
During PSG, there are EEG, electrooculogram (EOG),
and EMG findings that have been investigated in RBD.
EEG
Studies of sleep architecture and power spectral
analyses by fast Fourier transforms in iRBD and healthy
controls have shown heterogeneous findings. Some
studies have reported a greater percentage of slow
wave sleep in iRBD compared with healthy controls
(Massicotte-Marquez et al., 2005; Ferri et al., 2017);
others showed no differences in sleep parameters
(Fantini et al., 2003; Latreille et al., 2011; O’Reilly
et al., 2015); some have shown EEG slowing (Fantini
et al., 2003; Sasai et al., 2013) when analyzing EEG
spectral power; and one study reported an increase in
delta and theta power in central regions only in RBD
patients with mild cognitive impairment (MCI)
(Iranzo et al., 2010). In line with this, a correlation
between increased delta power during REM sleep and
MCI has been reported (Sasai et al., 2013). One study
 CLINICAL NEUROPHYSIOLOGY OF REM
analyzed sleep spindles, showing smaller densities of
fast spindles but larger densities of slow spindles in
iRBD compared with controls (O’Reilly et al., 2015).
EOG
REM sleep can be subdivided into REM sleep with and
without rapid eye movements (REMs). It has been
reported that REM sleep with REMs acts as a function-
ally isolated and close intrinsic loop, whereas REM sleep
without REMs seems to be a state of reduced alertness,
suggesting that these two components of REM sleep
have different functions (Wehrle et al., 2007).
REMs have been analyzed in RBD, and density,
index, and complexity have not been shown to differ
between RBD patients and controls (Leclair-Visonneau
et al., 2010). However, RBD behaviors occur more fre-
quently during REM sleep with REMs than without
(Frauscher et al., 2009; Manni et al., 2009; Leclair-
Visonneau et al., 2010).
EMG
Persistence of tonic EMG activity in the chin during
REM sleep in patients with Parkinson’s disease was first
described in 1969 (Traczynska-Kubin et al., 1969) and
confirmed in 1975 (Mouret, 1975). In the 1970s different
names were used to describe REM sleep without atonia
(RWA). In the Japanese literature it was called “stage-1
REM with tonic EMG activity,” (Tachibana et al.,
1975) whereas Guilleminault et al. described it as
“sleep stage 7” (Guilleminault et al., 1976). Human
RBD was first described in Schenck et al. (1986) in five
patients showing variable loss of chin and limb EMG
atonia during REM sleep (Schenck et al., 1986).
The first scoring method to quantify RWA was
published in Lapierre and Montplaisir (1992). Since
then, different classification systems have been pub-
lished (Eisensehr et al., 2003; Bliwise et al., 2006;
Frauscher et al., 2012a). Scoring guidelines as suggested
for diagnosis of RBD in the ICSD-3 (American Academy
of Sleep Medicine, 2014) are defined in the AASM
Manual for the Scoring of Sleep and Associated Events
(American Academy of Sleep Medicine, 2016).
Classically, RWA has been evaluated in the chin
EMG, as this channel is routinely used in the PSG. While
several studies have shown that EMG activity of the
mentalis and submentalis muscles can distinguish RBD
from controls, it has also been shown that 65% of the
behavioral events would have been missed if an upper
extremity had not been recorded (Iranzo et al., 2011).
Because it is difficult to distinguish EMG activity
derived from increased respiratory efforts or snoring
383
artifacts from RBD-related tonic EMG activity in routine
recording settings, and because of the reduced sensitivity
of chin EMG alone (Fernandez-Arcos et al., 2017), the
SINBAR (Sleep Innsbruck Barcelona) group has recom-
mended the addition of upper limb muscle EMG chan-
nels in suspected RBD (Frauscher et al., 2012a,
2014a). Upper extremity muscles (biceps and flexor digi-
torum superificialis) combined with chin EMG have
been shown to better discriminate RBD and controls
according to phasic EMG activity in these muscles dur-
ing REM sleep, compared with leg or sternocleidomas-
toid muscles (Frauscher et al., 2012a). Phasic and
other EMG activity in the tibialis anterior muscle is
frequent in elderly subjects, such as from excessive
fragmentary myoclonus (Frauscher et al., 2014a;
Fraigne et al., 2015; Raccagni et al., 2016). The useful-
ness of recording upper-limb EMG was demonstrated in
a study showing that 18.4% of iRBD patients would
have been misdiagnosed using only the mentalis
EMG (Fernandez-Arcos et al., 2017). The SINBAR
montage also allows detection of EMG activity when
patients display abnormal behaviors only in the limbs,
a common situation in iRBD. The need for both
upper and lower extremity EMG monitoring to fully
evaluate RBD is noted in the ICSD-3 (American
Academy of Sleep Medicine, 2014). Evidence-based
cut-off data using any chin EMG activity combined
with bilateral phasic activity of the flexor digitorum
superificialis muscles (SINBAR EMG montage) enable
distinguishing RBD patients from controls (Frauscher
et al., 2012a).
It has also been shown that RWA as an EMG finding
during REM sleep in RBD has a remarkable stability
over several nights (Ferri et al., 2013), so that in most
RBD patients a single night of PSG is sufficient to
capture RWA. However, a percentage of patients may
not have enough REM sleep during the first night study
for adequate assessment. An alternative to EMG is
actigraphy using an accelerometer, which can be useful
in identifying subjects with iRBD (Stefani et al.,
2018). Periodic leg movements of sleep (PLMSs) have
been evaluated in RBD patients. In Caucasian RBD
patients, PLMSs have been reported to be common
(70% (Fantini et al., 2002) to 85%) (Manconi et al.,
2007). One study reported a higher PLMS index in
RBD compared to controls only during REM sleep
(Fantini et al., 2002). Another study found higher PLMS
indices in both NREM and REM sleep in RBD; how-
ever, in this study PLMSs also occurred more frequently
during REM sleep in patients with RBD (Manconi et al.,
2007). In another study of Japanese iRBD patients, only
33% had a PLMS index
15/h (Sasai et al., 2011).
In iRBD patients a reduction of cardiac and EEG
384 A. STEFANI ET AL.
activation associated with PLMS has been reported,
suggesting the presence of an impaired cortical
and autonomic reactivity to internal stimuli (Fantini
et al., 2002).
AUTOMATIC ANALYSIS OF NEUROPHYSIOLOGIC
PSG PARAMETERS
Several algorithms for automatic sleep stage classifica-
tion (Schaltenbrand et al., 1996; Koley and Dey, 2012;
Christensen et al., 2014; Wang et al., 2015; Hassan
and Bhuiyan, 2017) and automatic detection of REMs
have been developed (Tsuji et al., 2000; Suzuki et al.,
2001; Yetton et al., 2016). However, expert manual
scoring remains the gold standard.
To overcome cumbersome manual quantification of
muscle activity, computerized programs have been
developed (Ferri et al., 2008, 2010; Frauscher et al.,
2014a; Frandsen et al., 2015). This methodology requires
high-quality technical recordings and visual exclusion of
epochs with confounding EMG activity and artifacts.
Most computerized approaches are based on analysis
of chin EMG activity and are subject to the same limita-
tions as manual quantification of chin EMG; only a few
methods include automatic analysis of upper-extremity
EMG (Frauscher et al., 2014a).
WAKING EEG FINDINGS
Most studies have reported waking EEG slowing in
patients with iRBD. The first study performed by Fantini
et al. showed EEG slowing and impaired cortical activa-
tion during both wakefulness and REM sleep in iRBD
patients compared with controls (Fantini et al., 2003).
Another study reported more severe and more global
EEG slowing, indicating dysfunction of cortical activa-
tion similar to that found in neurodegenerative diseases
(Massicotte-Marquez et al., 2008). Another study of
patients with iRBD with a mean follow-up of 3.5 years
showed that waking EEG slowing predicted the onset
of a neurodegenerative disease (Rodrigues Brazete
et al., 2016). A study of iRBD patients measuring
functional connectivity from EEG recordings showed
decreased delta-band functional connectivity in the
frontal regions that correlated with verbal fluency perfor-
mance (Sunwoo et al., 2017). EEG slowing during wake
and REM sleep was confirmed in a study of iRBD
patients correlating RBD with mild cognitive impair-
ment (MCI) (Sasai et al., 2013). A study performed
EEG spectral analysis in patients with iRBD without
MCI, RBD and MCI, and healthy controls, finding
marked EEG slowing in those with RBD and MCI in
central and occipital regions during wakefulness and
REM sleep, compared with controls and to a lesser extent
with those with iRBD without MCI. This pattern was
similar to that of DLB and Parkinson’s disease–dementia
(Iranzo et al., 2010). Another study showed waking EEG
slowing in the posterior cortical regions only in RBD
patients with MCI, and suggested that this could be a
marker for increased risk of conversion to DLB or PD
(Rodrigues Brazete et al., 2013). In summary, EEG slow-
ing has been frequently reported in iRBD, and some
studies report the value of EEG as an early indicator of
conversion.
AUTONOMIC DYSFUNCTION IN iRBD
Objective autonomic function tests (tilt table examination,
orthostatic standing test, Valsalva maneuver) show that
the degree of autonomic dysfunction in iRBD patients
is intermediate between controls and PD patients
(Frauscher et al., 2012b). Autonomic cardiac function
during sleep (Ferini-Strambi et al., 1996; Postuma et al.,
2010; Sorensen et al., 2012, 2013) showed reduced tonic
(vagal activity) and phasic (sympathetic activity) heart rate
variability, and reduced heart rate response to leg move-
ments. One study reported autonomic cardiovascular
dysfunction on the basis of peripheral cardiac/vascular
denervation rather than central autonomic dysregulation
(Dahms et al., 2016).
EVOKED POTENTIALS
Studies have assessed psychophysiologic parameters in
iRBD using auditory evoked potentials (active oddball
P300 paradigm and passive oddball paradigm) (Raggi
et al., 2007). The authors found no differences between
patients and matched controls, leading them to conclude
that cognitive evoked potentials are not sensitive to pre-
or subclinical cognitive abnormalities in iRBD, at least at
the early-middle stages of the disease. As cognitive def-
icits have been described in RBD, event related poten-
tials using a cognitive task have been evaluated in
patients with PD with and without RBD. An occipital
positive wave, the P2, appeared in patients with PD
and RBD, but it was nearly absent in controls. PD
patients without RBD were not significantly different
from PD patients with RBD, and the PD group without
RBD did not differ significantly from the control group,
suggesting that RBD accentuates cerebral dysfunctions
in PD (Gaudreault et al., 2013).
Motor evoked potentials, somatosensory evoked
potentials, and blink reflex have not been investigated
in RBD.
QUANTITATIVE SENSORY TESTING
Somatosensory function is altered in PD with iRBD.
Quantitative sensory testing revealed increased thermal
detection thresholds in iRBD compared to healthy
 CLINICAL NEUROPHYSIOLOGY OF REM
controls (Strobel et al., 2018). The authors hypothesized
that thermal sensory impairment might be due to func-
tional affection of the small nerve fibers.
TRANSCRANIAL MAGNETIC STIMULATION
A transcranial magnetic stimulation (TMS) protocol
relying on short latency afferent inhibition (SAI) of
the motor cortex (Tokimura et al., 2000) allows evalu-
ation of cholinergic circuits. SAI refers to the suppres-
sion of the amplitude of a motor evoked potential
produced by a conditioning afferent electrical stimulus,
usually applied to the median nerve at the wrist
approximately 20 ms prior to transcranial magnetic
stimulation of the hand area of the contralateral motor
cortex (Tokimura et al., 2000). Nardone et al. evaluated
SAI testing in iRBD, showing that mean SAI was
reduced in iRBD as compared to controls, and SAI
values correlated with disease duration and also with
episodic verbal memory and executive functions
(Nardone et al., 2012).
CORTICO-MUSCULAR COHERENCE
Cortico-muscular coherence (CMC) reflects functional
connectivity between the primary motor cortex, mea-
sured by EEG or magnetoencephalography, and a contra-
lateral effector muscle during isometric contraction. Jung
et al. compared CMC values measured by EEG of RBD
patients and healthy controls. In healthy subjects CMC
was significantly lower during REM sleep compared to
wakefulness, but this was not the case in the RBD
patients. CMC during REM sleep was significantly
higher in RBD patients than in controls, suggesting that
cortical locomotor drive during REM sleep is increased
in RBD (Jung et al., 2012).
BRAINSTEM REFLEXES
The startle response is an alerting reaction to sudden and
unexpected sensory stimuli probably originating in the
brainstem (Brown et al., 1991). A patient with RBD
was reported to have an excessive startle response to
visual stimuli, probably caused by a pontine lesion
(Peter et al., 2008).
NEUROPHYSIOLOGY IN THE DIFFERENTIAL
DIAGNOSIS OF RBD
Several large clinical case series show that self-
awareness of RBD is low (Frauscher et al., 2010;
Boeve et al., 2013; Fernandez-Arcos et al., 2016). Accu-
rate diagnosis is a challenge, as by history alone RBD is
easily confused with sleep apnea, non-REM parasomnia,
periodic limb movement disorder, epilepsy, and noctur-
nal wandering (Fernandez-Arcos et al., 2016). For a
385
definite diagnosis of RBD, video PSG (vPSG) is required
(American Academy of Sleep Medicine, 2014), and is
the only instrument enabling differential diagnosis of
RBD “mimics.”
Antidepressants and REM without atonia
RBD observed in patients on antidepressant treatment
was initially classified as “medication-induced second-
ary RBD” (Schenck et al., 1992). However, later studies
showed that cessation of antidepressant treatments did
not resolve the RBD. The International RBD Study
Group reported that patients with PSG-confirmed iRBD
(n ¼ 318) were more likely to report a history of depres-
sion and antidepressant use (due to selective serotoniner-
gic reuptake inhibitors, OR 3.6) than matched controls
(n ¼ 318) (Frauscher et al., 2014b). Lifetime antidepres-
sant use was more frequent than comorbid depression
(Frauscher et al., 2014b). Frequent antidepressant use
(60%) was also reported in another study of 115 RBD
patients (60% iRBD, 48% taking antidepressants at the
time of the diagnosis) (Ju et al., 2011). In another iRBD
cohort (n ¼ 100) 27% of patients who were taking
antidepressants had abnormalities on 12/14 tested neuro-
degenerative markers and were indistinguishable from
iRBD patients not taking antidepressants (Postuma
et al., 2013). In light of these findings, the development
of RBD with antidepressants is now seen as an early
sign of an underlying neurodegenerative disease
(Postuma et al., 2013; Postuma et al., 2015), suggesting
that these patients should also be followed up over the
long term as they are at risk of developing a neurode-
generative disorder (Wing et al., 2015). However, one
study showed a lower risk of conversion among those
with antidepressant-induced RBD, although patients
demonstrated biomarkers of neurodegeneration (motor
impairment, olfactory deficit, color vision impairment,
symptoms of autonomic dysfunction, cognitive defi-
cits) (Postuma et al., 2013). Further studies with
longer follow-up are needed to fully understand this
association.
SLEEP PARALYSIS
Sleep paralysis is a transient, generalized, inability to
move and to speak occurring in the transitional period
between wakefulness and sleep (Nielsen and Zadra,
2000). It is characterized by the complete inability to
move in a subjectively awake person. It affects all
somatic (Chase and Francisco, 1994) muscles under
voluntary control (Nielsen and Zadra, 2000) except the
diaphragm, external eye muscles, and the stapedius,
similar to the physiologic muscle atonia experienced
in REM sleep (Kryger et al., 1994). Auxiliary respira-
tory muscles (e.g., the intercostal muscles) are also
386 A. STEFANI ET AL.
paralyzed, but the diaphragm is not affected, so that
sleep paralysis is often accompanied by feelings of suf-
focation. Sleep paralysis can last up to several minutes,
disappears spontaneously or upon external stimulation
(Hishikawa and Shimizu, 1995) and often occurs in
association with hypnopompic hallucinations (McCarty
and Chesson, 2009).
Sleep paralysis can occur in isolation, or as an
element of the clinical tetrad of narcolepsy, where it
has been reported in as many as 50% of patients
(Frauscher et al., 2013). It can be accompanied by hyp-
nagogic or hypnopompic hallucinations (H€ ogl and
Iranzo, 2017). The experience of a complete inability
to move despite subjective alertness is overwhelmingly
unpleasant and frightening, especially when it occurs
for the first time.
The diagnostic criteria for recurrent isolated sleep
paralysis, all of which must be met, include: recurrent
inability to move the trunk and all of the limbs at sleep
onset or upon awakening from sleep; each episode lasts
seconds to a few minutes; episodes cause clinically
significant distress including bedtime anxiety or fear
of sleep; and the disturbance is not better explained
by another sleep disorder (especially narcolepsy),
mental disorder, medical condition, medication, or
substance use.
Clinical features of sleep paralysis
The pathophysiology of sleep paralysis is reflected in
neurophysiologic manifestations, and includes atonia
of striated muscles under voluntary control, except the
diaphragm, external eye muscles, and stapedius, similar
to the atonia in REM sleep. Muscle twitches also occur.
Isolated sleep paralysis is often mistaken for other
neurologic disorders (H€ ogl and Iranzo, 2017) and neuro-
physiologic studies can help distinguish it from con-
founders. Sleep paralysis plays a role in the writing of
great novelists, including Dostoevsky (Stefani et al.,
2017) and Maupassant (“The Horla”) (Miranda and
Hogl, 2013; Miranda and Bustamante, 2015). In the fine
arts, Johann Heinrich F€ussli’s (1775) painting The Night-
mare may reflect sleep paralysis with a hypnagogic
hallucination (Baumann et al., 2007). The frequent
occurrence of isolated sleep paralysis in healthy persons
has led to popular designations for the phenomenon in
various parts of the world (e.g., in Mexico sleep paralysis
is called Se me subio un muerto [“A cadaver climbed on
me”] (Stefani et al., 2017). In Hong Kong, it is called “the
ghost oppression phenomenon” (Wing et al., 1994;
Stefani et al., 2017), reflecting the inability to move
and the presence of hallucinations. Sleep paralysis can
also be induced by sleep deprivation or chronically insuf-
ficient sleep (McCarty and Chesson, 2009).
Neurophysiology of sleep paralysis
The few neurophysiologic studies performed in patients
with isolated sleep paralysis have been based on PSG or
multiple sleep latency tests (MSLT). Some studies have
applied specific signal analysis, such as fast Fourier
transforms of EEG data. Only a few studies have focused
on other neurophysiologic techniques.
PSG and MSLT recordings obtained during sponta-
neously occurring or provoked sleep paralysis have
demonstrated characteristic changes in EEG, EOG,
and chin/extremity muscle activity. Different types of
manipulations of the slow wave sleep cycle have been
applied to induce sleep paralysis and are described in
following text.
POLYSOMNOGRAPHY
Early studies showed that auditory arousing stimuli pre-
sented repeatedly with increasing intensity during sleep
onset REM periods were correctly perceived in normal
individuals, but in patients with narcolepsy the subjective
response was not accompanied by a correct motor behav-
ioral response (pressing a button on an electrical switch).
This was attributed to false awakenings with REM-related
paralysis (Nan’no et al., 1970). Sleep paralysis has been
observed after acute reversal of the sleep–wake cycle
(Weitzman et al., 1970) and after massive manipulation
of the human sleep–wake cycle, such as a 90-min day
(Carskadon and Dement, 1975; Takeuchi et al., 1992).
According to these early studies, sleep paralysis was
linked to the occurrence of sleep onset REM period.
In a PSG study, Takeuchi et al. performed sleep inter-
ruptions during nocturnal PSG in healthy subjects, and
9.4% of these interruptions resulted in isolated sleep
paralysis. The reported subjective perception included
inability to move while recognizing the sleep laboratory
surroundings, often accompanied by auditory and visual
hallucinations. PSG recordings during this state were
characterized by dissociation between REM sleep and
wakefulness, demonstrating abundant alpha EEG or a
mixed pattern of alpha waves and low voltage slow
waves, and persistence of muscle atonia (Takeuchi
et al., 1992). Eye blinks were also noted. The authors
concluded that isolated sleep paralysis occurs in the tran-
sition between REM and wakefulness. Lucid dreaming
occurred during unequivocal REM sleep; whereas, iso-
lated sleep paralysis occurred during ambiguous REM
sleep or in the transition between REM and wakefulness.
The authors highlight the close relationship between
sleep onset REM periods and isolated sleep paralysis
(Takeuchi et al., 1992).
In patients with narcolepsy, sleep paralysis with or
without hypnagogic hallucinations is frequent but rarely
 CLINICAL NEUROPHYSIOLOGY OF REM
occurs during sleep attacks or short daytime naps, prob-
ably because the uncomfortable sleeping position, such
as standing or sitting, prevents the occurrence of sleep
onset REM episodes (Hishikawa and Shimizu, 1995).
PSG, MSLT and fast Fourier transform signal
analysis
In a study of provoked cataplexy in patients with narco-
lepsy, unprovoked sleep paralysis was observed (Dyken
et al., 1996). During the episode, PSG revealed a pattern
compatible with REM sleep, and the PSG REM sleep
pattern was electrophysiologically indistinguishable
from that recorded during cataplexy, sleep paralysis,
and hypnagogic hallucinations (Dyken et al., 1996).
This study was based on visual analysis of four EEG
channels and chin EMG and a single lower extremity
channel only.
In a vPSG and MSLT study, it was reported that
incomplete sleep paralysis can be the first symptom
of narcolepsy (Buskova et al., 2013). In this case sleep
paralysis occurred during an MSLT. EEG during the
episode showed recurrent alpha waves intermingled
with low-voltage fast activity; chin EMG showed inter-
mittent tonic and phasic muscle activity (Buskova
et al., 2013).
Another case report demonstrated sleep paralysis in a
patient with narcolepsy (Terzaghi et al., 2012). The sleep
paralysis episode occurred on awakening from sleep
onset REM (SOREM) during the MSLT, and miosis, dys-
arthric speech, and inability to protrude the tongue were
described. EEG showed recurrent alpha-like frequency
intermingled and irregularly alternating with low-voltage
fast frequency activity, persistence of REM bursts, and a
chin EMG pattern characterized by muscle atonia mixed
together with episodes of loss of atonia (Terzaghi et al.,
2012). The patient reported remembering details of the
conversation with the neurologist during sleep paralysis,
but wondered if it was a dream. EEG frequency domain
analysis and fast Fourier transform frequency spectra
calculations showed normal wake activity peaking at
9.5 Hz and REM activity in the 19-Hz range. In contrast,
the sleep paralysis episode presented two peaks in the
9.5-Hz and 17- to 18.5-Hz range. When the amplitudes
of wake with eyes closed and REM spectra were
summed, a new spectrum was constructed that matched
very closely the sleep paralysis episode. The authors
concluded that the patient was in an intermediate state
between wake and REM sleep during the paralysis
(Terzaghi et al., 2012).
EMG and nerve conduction velocity studies
In narcolepsy patients with sleep paralysis, suppression
of the H-reflex, in addition to suppression of tonic chin
387
EMG activity, has been noted during sleep onset REM
periods, supporting the concept that sleep paralysis is dis-
tinct from hypnagogic hallucinations and results from a
dissociation between the level of consciousness and the
somatic muscle and reflex activities (Hishikawa and
Shimizu, 1995).
Further studies on sleep paralysis involving PSG
In one PSG study of patients with obstructive sleep apnea
(OSA), 38.3% were reported to have experienced sleep
paralysis (Hsieh et al., 2010). The observation was based
only on a self-reported sleep questionnaire, so nonres-
torative sleep and early morning sleepiness causation
cannot be excluded. It was observed that OSA patients
with report of isolated sleep paralysis had higher
Epworth Sleepiness Scale (ESS) and Pittsburgh Sleep
Quality Index (PSQI) scores. This study highlights
how PSG is valuable in ruling out other causes of sleep
fragmentation, such as OSA, in patients with suspected
sleep paralysis (Hsieh et al., 2010).
Sleep paralysis is consistent with the concept of dis-
sociated states discussed by Mahowald and Schenck
(2005)). Terzahgi et al. have also discussed the possible
presence of simultaneously coexisting regional states of
wakefulness and sleep as local brain phenomena, previ-
ously documented in confusional arousal (Terzaghi
et al., 2009).
Another neurophysiologic study of narcoleptic
patients using 24-h sleep monitoring reported lower
coherences and delta power and higher muscle atonia
in lucid dreamers (those experiencing being aware of
dreaming while asleep and continuing to dream) (Dodet
et al., 2015). The occurrence of sleep paralysis did not
distinguish lucid and nonlucid dreamers.
NEUROPHYSIOLOGIC STUDIES IN ANIMALS TO
INVESTIGATE THE PATHOPHYSIOLOGY OF SP AND
RELATED CONDITIONS
Electrophysiologic studies in rats after specific lesions or
substance administration have been used to elucidate
mechanisms of physiologic REM sleep paralysis. They
have shown that trigeminal motor neurons and masseter
muscles are switched off during REM sleep in rats
(Brooks and Peever, 2012).
Carbachol injections in the nucleus pontis oralis pro-
duced carbachol-induced REM sleep or a waking state
with muscle atonia (representing cataplexy or sleep
paralysis induced by carbachol), depending on the state
in which the injection was performed (Torterolo et al.,
2016). The waking state showed high gamma coherence,
similar to what is seen during active wakefulness.
In narcoleptic mice, orexin gene transfer into the
zona incerta neurons suppressed muscle paralysis, and
388 A. STEFANI ET AL.
analysis of nuchal muscle tone and EEG activity
suggested that zona incerta neurons can serve as a target
of drugs to control muscle paralysis in narcolepsy (Liu
et al., 2011). It was suggested that this technique could
be used to identify target brain areas for drug develop-
ment (Liu et al., 2011).
NEUROPHYSIOLOGY IN THE DIFFERENTIAL
DIAGNOSIS OF SLEEP PARALYSIS
Video-EEG and PSG should be used to assess for focal
epileptic seizures that may mimic sleep paralysis
(Galimberti et al., 2009). One patient who met criteria
for sleep paralysis demonstrated focal epileptic seizures
during sleep paralysis attacks captured on video-EEG
and PSG. EEG showed onset over the right posterior
temporal regions with fast sharp recruiting activity
spreading to both parietal and occipital regions and fol-
lowed by a sudden suspension of deltoid and anterior
tibialis EMG activity bilaterally, whereas EMG activity
of chin and sternocleidomastoid muscles was preserved.
Later, the EEG activity stopped abruptly. The video
showed abrupt cessation of body movement coincident
with discharge onset. Later, the patient reported a typical
sleep paralysis attack. After levetiracetam was prescribed,
the attacks ceased (Galimberti et al., 2009). Sleep paralysis
needs to be differentiated from epilepsy and this can be
achieved by performing vPSG or video-EEG during the
attack.
NIGHTMARE DISORDER
The diagnosis of nightmare disorder consists of three
criteria, all of which must be met:
1. Repeated occurrence of extended, extremely dys-
phoric, and well-remembered dreams that usually
involve threats to survival, security, or physical
integrity.
2. On awakening from the dysphoric dreams, the
person rapidly becomes oriented and alert.
3. The dream experience, or the sleep disturbance
produced by awakening from it, causes clinically
significant distress or impairment in social, occupa-
tional, or other important areas of functioning
(American Academy of Sleep Medicine, 2014).
Nightmares are frequent, occurring in an estimated
6.6% of the general population (Ohayon and Schenck,
2010) and in 16% of a 700-patient cohort with sleep
disorders (Krakow, 2006).
There has been some controversy about whether
a diagnosis of nightmare disorder requires awakening
from the nightmare, or fear of returning to sleep. This
distinction is no longer explicitly stated in the current
versions of the ICSD3 and DSM 5 criteria (American
Psychiatric Association, 2013; American Academy of
Sleep Medicine, 2014).
Nightmares can occur as a primary complaint without
other comorbidity (H€ogl and Iranzo, 2017) or in the
context of other sleep disorders, psychiatric disorders,
or systemic diseases. Nightmares are frequent in RBD
(Schenck et al., 1987; Valli et al., 2012, 2015), narco-
lepsy, and sleep apnea, according to some reports. They
can occur in the context of neurologic diseases, including
certain forms of epilepsy, and can be medication/
substance-induced. Nightmares and nightmare disorder
need to be distinguished from sleep terrors, hypnagogic
hallucinations with or without sleep paralysis, and
nocturnal panic attacks.
Historic neurophysiologic research
in nightmares
In the first decades of polysomnographic sleep research,
nightmares associated with REM sleep, sleep terrors, and
nightmares associated with non-REM sleep were not
well differentiated. Broughton reasoned that nightmares
occur in “confusional states of arousal,” not in “dreaming
sleep” (Broughton, 1968). Typical nightmare attacks
during abrupt arousal from slow-wave sleep and one
following arousal from slow-wave sleep were recorded
in normal subjects and sleepwalkers, and none of these
attacks were associated with REM sleep or detailed
dreams (Broughton, 1968).
Fisher et al. conducted a PSG study identifying three
types of nightmares: “major stage four nightmares,”
“REM anxiety dreams,” and “nightmares associated with
spontaneous awakening out of sleep stage 2 sleep during
the initial nonREM sleep cycle” (Fisher et al., 1970).
The authors also recorded REM dreams in subjects in
whom anxiety was present, finding dream content that
was “not as panicky as in the nonREM nightmare”
(Fisher et al., 1970). However, this study was later
criticized (Nielsen and Zadra, 2000) for the presence
of posttraumatic stress disorder (PTSD) in some patients.
In these historic studies, nightmares always occurred
during REM sleep, usually during particularly long REM
periods late during the night and sometimes during REM
sleep periods with increased eye movements (Hartmann,
1984). It was reported that in nightmares arising from
REM sleep there was an increase in the cardiorespiratory
rate and a marked increase in the number of eye move-
ments (Fisher et al., 1970).
In a subsequent psychophysiologic study of night-
mares and night terrors, transcriptions of interviews from
spontaneous non-REM awakenings were analyzed
(mainly out of Rechtschaffen and Kales Stage 3 and 4
sleep) (Fisher et al., 1973). The interviews were taken
 CLINICAL NEUROPHYSIOLOGY OF REM
during several years from a series of subjects with night
terrors. The authors reported that there was a 58% rate of
dream recall, mainly out of stage 3–4 sleep. However, the
clinical differentiation of nightmares and terrors was not
well established. Only later was the terminology differ-
entiated to separate nightmares and night terrors, the
first occurring during REM sleep and the latter during
non-REM sleep (Newell et al., 1992).
Nightmare disorder is currently classified among the
REM-related parasomnias associated with REM sleep.
However, in adults dream-like imagery can be associated
with some non-REM sleep parasomnias. This is also true
for night terrors (Uguccioni et al., 2013).
More recent PSG studies in nightmares
A PSG study compared patients suffering from posttrau-
matic nightmares and those suffering from idiopathic
nightmares with a healthy control group and reported that
patients who suffered from posttraumatic nightmares
exhibited significantly more nocturnal awakenings than
patients with idiopathic nightmares or control subjects
(Germain and Nielsen, 2003).
Other neurophysiologic studies of
nightmares: EEG, evoked potentials
Only a few studies have been performed to assess other
neurophysiologic aspects of patients with nightmare dis-
order. In one study, 60-min EEG studies and auditory
evoked potentials (AEP or BAEPs) were performed on
subjects afflicted with recurrent nightmares (Newell
et al., 1992). They reported that all had normal EEGs.
BAEPs and AEPs were also within clinical norms, with
amplitudes of N100, P160, and N200 not significantly
different from controls (Newell et al., 1992). Nightmare
sufferers were reported to have significantly less sleep,
more awakenings, and reduced slow-wave sleep during
overnight sleep recording, compared to published sleep
norms (Newell et al., 1992).
Using EEG power spectra, during nightmares higher
absolute and relative alpha-power and higher fast beta
power over frontotemporal regions, as well as a distinct
amplification of classic posterior alpha were seen, com-
pared with frontal brain sites (Nielsen and Zadra, 2000).
In a later study of subjects with frequent nightmares and
healthy controls, REM sleep propensity and increased
REM sleep pressure were studied after partial REM sleep
deprivation. The partial REM deprivation mildly reduced
REM percentage from 17.8% to 13.1% N2 (P ¼ 0.002)
in nightmare sufferers, and from 19.0% to 13.2%
in controls (P ¼ 0.001). Subjects with nightmares
showed less evidence of REM rebound. Nightmare suf-
ferers had signs of lower-than-normal REM propensity
for deprivation sleep as well as during recovery sleep.
389
These findings suggested that increased REM propensity
did not contribute to the occurrence of nightmares,
but the study only mildly increased REM propensity.
AUTONOMIC CHANGES IN NIGHTMARES
Increases in respiratory and heart rate were observed
with severe nightmares in an early study, although a con-
founding with sleep terrors cannot be excluded (Fisher
et al., 1970).
In nine patients with nightmare disorder without
psychiatric comorbidity, heart and respiratory rate
recordings during nightmare and nonnightmare REM
sleep episodes confirmed earlier reports of sympathetic
arousal during some nightmares (Nielsen and Zadra,
2000). Mean heart rate for REM sleep with nightmare
was elevated during 3 min before awakening, but respi-
ratory rate was not affected. Most subjects (78%) showed
heart-rate acceleration during nightmare sleep, whereas
the same number showed heart-rate deceleration during
nonnightmare REM (Nielsen and Zadra, 2000).
Abnormal reduced heart-rate variability has also
been reported in a wide spectrum of anxiety disorders,
including PTSD and panic disorder, conditions frequently
associated with intense nightmares (Nielsen and Zadra,
2000; Nielsen et al., 2010).
OTHER PSG AND EEG SIGNAL ANALYSIS STUDIES
An EEG study of 17 young individuals with frequent
nightmares without neurologic, psychiatric, or sleep
disorders showed reduced sleep efficiency, increased
wakefulness, less slow-wave sleep, and increased noc-
turnal awakenings from N2 sleep compared with controls
(Simor et al., 2012). A longer duration of REM sleep was
reported to be mediated by heightened negative effect.
The sleep architecture was clearly disturbed in the night-
mare group in spite of adequate subjective sleep quality
reported by the subjects. The authors discuss that frag-
mented sleep could trigger the appearance of dysphoric
dreams, especially in comorbid trait-like effects of affec-
tive dysregulation or state-like effects of current stress, or
that the high number of awakenings and more superficial
sleep could promote the recall of dreams including the
dysphoric ones, concluding that impaired sleep continu-
ity is an integral part of nightmare disorder (Simor et al.,
2012). The same group investigated relative spectral
power values for non-REM and REM sleep in individ-
uals with nightmare disorder and found increased high
alpha (10–14.5 Hz) and frontocentral increases in high
delta (3–4 Hz) power during REM sleep and a trend
toward increased frontocentral low alpha (7.75–9 Hz)
power in non-REM sleep, independent of waking
emotional distress (Simor et al., 2013b). They concluded
that high REM alpha and low non-REM alpha power
390 A. STEFANI ET AL.
are strongly related in nightmare, suggesting the
possible presence of wake-like features during REM and
signs of increased alertness during non-REM (Simor
et al., 2013b).
In a further study the same group reported increased
alpha power and no increased heart-rate variability
during pre-REM periods in subjects with nightmares,
indicating compromised non-REM/REM transition in
these subjects (Simor et al., 2014).
A subsequent study concluded that non-REM sleep
microstructure is altered even during nonsymptomatic
nights in patients with frequent nightmares and that
disrupted sleep seems to be related to abnormal arousal
processes (Simor et al., 2013a). Another group found
that patients with idiopathic nightmares had significantly
less microarousals from N3 sleep and significantly
more microarousals from REM sleep compared to
patients with sleepwalking. The total REM percentage
did not differ between the two groups (Perogamvros
et al., 2015).
Nightmares in posttraumatic stress disorder
EVOKED POTENTIALS
A study of combat veterans with PTSD investigated
the P1 midlatency auditory evoked potential and its
habituation with a paired stimulus (Gillette et al.,
1997). Compared to various control groups, PTSD
subjects exhibited significantly diminished habituation
of the P1 potential, which is correlated with the intensity
of PTSD symptoms, such as trauma-related nightmares
and flashbacks. Based on these findings, the authors
suggested the presence of a sensory gating defect at
the brainstem level in PTSD (Gillette et al., 1997).
In a group of combat-veteran patients with PTSD
studied with PSG, trauma-related nightmare complaints
were not associated with an effect on sleep latency but
instead with effects on wake after sleep onset. In the
discussion, the authors suggest that in their sample of
chronic, severe, combat-related PTSD patients, trauma-
related nightmares were associated with increased wake
after sleep onset, whereas other types of nightmares were
not (Woodward et al., 2000).
AUTONOMIC NEUROPHYSIOLOGIC STUDIES
PTSD
IN NIGHTMARES WITH
Assessing arousal response, heart rate, skin conductance,
and facial EMG reactions (corrugator and lateralis
frontalis muscle) in trauma-exposed individuals suffer-
ing from chronic nightmares, investigators found facial
EMG reactions and heart rate were associated with
increased global sleep problems, fewer hours slept per
night, and panic upon waking (Rhudy et al., 2008). Skin
conductance correlated with time to fall asleep and panic
upon awakening. The authors demonstrated that auto-
nomic reactions were the most reliable correlates of pure
sleep and health and concluded that autonomic reactions
to nightmare imagery appear related to sleep disturbance
and health symptomatology. Reducing nightmare-
related autonomic arousal could improve sleep and
health (Rhudy et al., 2008).
Another study in individuals with frequent night-
mares but not PTSD demonstrated similar sleep distur-
bances compared to those with PTSD (Germain and
Nielsen, 2003).
PSGs performed on patients with PTSD and comorbid
panic and nightmare did not show the normal differences
in respiratory rates between non-REM and REM sleep;
PTSD patients with trauma-related nightmare complaints
exhibited higher sleep respiration rates in both REM and
non-REM sleep (Woodward et al., 2003).
PTSD AND PSG
In combat-exposed military veterans, eveningness influ-
enced PTSD symptoms (greater lifetime PTSD symp-
toms) and sleep, with more disturbed sleep, and more
frequent and intense nightmares. (Hasler et al., 2013).
In women with PTSD, the heart-rate response signif-
icantly correlated with Clinician-Administered PTSD
Scale (CAPS) total score and with CAPS nightmares.
The authors discussed that the association of night-
mares with greater heart-rate response in the absence
of association with larger skin conductance response
likely reflects reduced parasympathetic tone (Tanev
et al., 2017).
The association of PTSD and sleep apnea was inves-
tigated in PTSD. Overall nightmare severity was similar
in PTSD with and without OSA (van Liempt et al., 2011).
The frequency of an apnea-hypopnea index (AHI) > 10/h
was similar among all groups, but the mean CAPS score
was significantly higher in patients with sleep apnea
compared to those without sleep apnea. These findings
suggested that comorbid OSA leads to an increase in
PTSD complaints (van Liempt et al., 2011).
A study of patients with PTSD, frequent nightmares,
and sleep disturbance after administration of prazosin
found that prazosin compared with placebo increased
total sleep time by 94 min, and increased REM sleep time
and mean REM period duration without altering sleep
onset latency (Taylor et al., 2008). A study using a rodent
model of PTSD found acute increases in REM sleep and
transition to REM sleep, which significantly correlated
with PTSD severity. They also reported that reductions
in delta and sigma pent power during transition to
REM sleep also correlated with impaired fear-associated
memory processing in rodents. The author suggested
 CLINICAL NEUROPHYSIOLOGY OF REM
that changes in REM sleep and transition to REM
sleep may serve as sleep biomarkers to identify
increased susceptibility to PTSD following trauma
exposure (Vanderheyden et al., 2015).
Nightmares in other disorders
Nightmares also occur in other settings such as physio-
logic dreaming and lucid dreaming. Disturbed dreaming
is also observed in sleep terrors, terrifying hypnagogic
hallucinations, nightmares in PTSD, dreams in narco-
lepsy, sleep paralysis, and RBD (reviewed in Nielsen
and Zadra, 2000).
In a series of 20 patients with temporal lobe epilepsy
screening positive for parasomnias and undergoing
PSG, 16 had confusional arousals, 14 had recurrent
nightmares, 2 had sleepwalking episodes, and 4 had
night terrors in different combinations (Silvestri and
Bromfield, 2004). Half the patients had documented
episodes during PSG (again confusional arousals, night
terrors, sleepwalking, and nightmare out of stage 2).
SLEEP APNEA AND NIGHTMARES
One study of patients with PSG-confirmed OSA found
that respiratory parameters, as a measure of sleep apnea
severity, did not correlate with nightmare frequency,
thereby refuting a simple oxygen hypothesis for night-
mares (Schredl et al., 2006).
Another study investigated clinical and PSG charac-
teristics and response to positive airway pressure therapy
in 99 patients with comorbid OSA and nightmares
(BaHammam et al., 2013). The study found that OSA
patients with nightmares had a significantly higher
AHI during REM sleep compared with the OSA patients
without nightmares (51.7 vs 39.8); REM AHI and inter-
rupted sleep were independent predictors of nightmares
in the OSA patients. Nightmares disappeared in 91% of
the patients who accepted CPAP treatment, compared
with 36% of those who refused CPAP (BaHammam
et al., 2013).
CPAP-therapy reduced PTSD-associated nightmares
and PTSD symptoms in a group of patients with OSA,
PTSD, and nightmares (Tamanna et al., 2014).
A PSG study investigated female patients with
borderline personality disorder, with comorbid post-
traumatic stress response in 33%. Borderline personality
patients compared with controls had only slightly
decreased sleep efficiency, but the number of awaken-
ings, time awake, and number of arousals were signi-
ficantly increased. The patients also had shorter
REM latencies, higher REM densities, and more non-
REM or awake epochs during REM periods (Schredl
et al., 2012).
391
OTHER COMORBIDITIES
Nightmares appear to be significantly more prevalent in
both narcolepsy type 1 and 2, while PSG showed more
wakefulness and a higher percentage of non-REM stage
N1 sleep in narcolepsy type 1 (Pisko et al., 2014).
The term trauma associated sleep disorder (TASD)
has been proposed to describe disruptive nocturnal
behaviors and nightmares following traumatic experi-
ences (Mysliwiec et al., 2014). In one PSG study,
REM without atonia was present in 4 patients with
TASD, and the SINBAR EMG activity index ranged
from 13.7% to 37.6%, with only one patient exceeding
the cut-off for RBD (Frauscher et al., 2012a). TSAD
could be distinguished as a unique sleep disorder because
patients were young, had a precipitating event, and had
nightmares with a specific topic. In contrast to RBD,
in TASD an overdrive phenomenon appears to occur,
resulting in loss of REM atonia and loss of sympathetic
suppression (Mysliwiec et al., 2014).
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