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Medicine » "Sleep and its Disorders Affect Society", book edited by Chris Idzikowski, ISBN 978-953-51-1725-4, Published: September 24, 2014 under CC BY 3.0 license. © The Author(s).

Chapter 3

An Essay on Sleep-Related Sexual Behaviours and Offences Related to Sexual Behaviours

By Chris Idzikowski
DOI: 10.5772/59140

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An Essay on Sleep-Related Sexual Behaviours and Offences Related to Sexual Behaviours

Chris Idzikowski1

1. Introduction

The aim of this chapter is to consider mainly the deep sleep parasomnias associated with sexual behaviour (known variously as sexsomnia, sleep sex, etc, see below) that may lead to non-consensual behaviour resulting in criminal charges.

Most jurisdictions will acquit a defendant if a court accepts that the criminal behaviour occurred whilst they were asleep-that is they were 'sleepwalking' or in a 'somnambulistic' state. It is said that Hippocrates and Aristotle were aware of the condition; that Galen wrote in De motu musculorum "that he once spent a whole night walking about in his sleep, awakening only after he struck a stone in his way" and that the philosopher Diogenes Laërtius "was said to read, to write, and to correct his works while asleep" [1], similar to one of John Polidori’s cases [2]. Umanath et al also note that Polish intellectual Joannes Jonstonus in his 1632 Thaumatographia naturalis had a section on “Of Walkers in the Night” [1]. In England King James II in the seventeenth century pardoned Colonel Cheyney Culpeper for shooting a guardsman and his horse with a blunderbuss [1, 3]. (It should be noted that blunderbusses are not very accurate though very effective at short range.)

Sexual relations are complex across a range of dimensions [4] which could impact on reporting of sexual crimes, both historically and now. Some may be clouded in confusion-as for example, with the ‘Old Hag’ (an incubus?) in sleep paralysis (when the muscles of the body are temporarily paralysed around the time of awakening) [5]. Schenck et al do cover sleep paralysis mainly in the context of narcolepsy though [6]. In their appendix they had to resort to quoting Tess’s experience in Thomas Hardy’s Tess of the d’Urbervilles (1891) [7] to provide some historical though literature-based context.

Putting forward a sleep-related sexual behaviour (SRSB) as a defence is relatively new and has emerged within the last two decades. Whilst the literature shows Bowden [8] reacting to Buchanan’s report of a case of somnambulistic indecent exposure [9] by pointing out that Motet in an 1897 article in the Annales d'Hygiène et de Médecine Légale described a similar case, this is not the type of sexual offence considered in this chapter (the advice generally being wear pyjamas or nighties if you are a sleepwalker). As a side note, Motet’s case was interesting as the court acquitted the defendant on the basis that a somnambulistic state was confirmed by hypnotism. Using the England and Wales Sexual Offences Act 2003 as a guide the type of offences considered are rape, sexual assault by penetration, sexual assault, etc, those offences where consent is as much of an issue as the behaviour. Both Shapiro (Canada) [10, 11] and Guilleminault (U.S.) [12] were the first to describe case series of SRSBs (though there had previously been sporadic case reports, e.g. Wong: masturbation [13] and forensic cases, e.g. Fenwick [14]), which eventually led to both Schenck et al’s 2007 comprehensive, thorough and critical review of the whole area [6].

Legal procedures have evolved to deal with sleep-related violent behaviour but SRSB has only recently been described so existing laws have to be applied to these cases. Given that courts have no experience with these cases inevitably means that expert guidance is needed. There are, however, as this essay flags problems, e.g.1) laws are inconsistent with respect to sleep-related violence and 2) sleep research is in its infancy and has difficulty answering the questions that courts may pose. To examine these problems the recently published 2014 3rd edition of the International Classification of Sleep Disorders [15] will be used as a springboard to explore SRSB. This is followed by an examination of existing SRSB literature, and the professional guidelines that have evolved to manage these cases. The problem of matching the different possible medical (mainly psychiatric) models of these disorders with the different legal models of a defendant [16] and the lack of an ontological basis with which to link these two professional domains will be deferred to another essay.

2. The international classification of sleep disorders 3rd edition [2014] [15]

The International Classification of Sleep Disorders Diagnostic and Coding Manual, 3rd edition [2014] (ICSD3) [15] lists more than 60 different sleep disorders. This is a reduction to the number of disorders listed in the previous manual, published 2007, which had 80 but more than the original manual published 1990. The reduction reflects refinements in the classification and pooling some categories which were better covered by umbrella terms.

The sleep disorders are roughly classified into insomnias (inability to sleep), hypersomnias (inability to remain awake), sleep-related breathing disorders (SRBs) and the parasomnias (unwanted or abnormal behaviours during sleep) see Table 1. The parasomnias are the main group of interest in ICSD3 [17]. There are overlaps (e.g. treatment of SRBs may trigger the (re-) emergence of a parasomnia [18] or SRBs may mimic parasomnias [19], or hypersomnias like narcolepsy [20, 21].

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Figure 1.

Sleep Disorders (ICSD3)

The parasomnias are further divided into REM (Rapid Eye Movement) and NREM (Non-REM) – Figure 1; and again there are overlaps such as Parasomnia Overlap Disorder. The NREM Disorders of Arousal include Confusional Arousals, Sleepwalking and Night Terrors. These disorders all have similar characteristics and are distinguished thus: Confusional arousals are characterised by mental confusion or confused behaviour that occurs while the person is in bed and there is an absence of terror or ambulation outside of the bed. Sleepwalking is associated with ambulation and other behaviours out of bed whilst Sleep (Night) Terrors are characterised “by episodes of abrupt terror, typically beginning with an alarming vocalization such as a frightening scream” and “There is intense fear and signs of autonomic arousal, including mydriasis, tachycardia, tachypnea, and diaphoresis during an episode.

Disorders of Arousal (From NREM Sleep) - confusional arousals, sleepwalking, sleep terrors (including SRSBs)
share similar
1genetic and familial patterns
2pathophysiology of partial arousals from deep sleep
3priming by sleep deprivation and bio-psychosocial stressors
and are
1not secondary to psychiatric disorders
2not generally secondary to neuropathology or head injury
3associated with absent or minimal cognitive functioning
4associated with amnesia for the prior episode
5may be triggered by sound, touch, or other stimuli

Table 1.

Disorders of Arousal (From NREM Sleep) — Confusional arousals, sleepwalking, sleep terrors (including SRSBs) share similar:

As with many diagnostic schemes the frequency of a sign or symptom leads to a classification rule. The problem in many legal cases is that all the signs and symptoms for a recognised (medical) mental disorder may be present but a single instance is insufficient to warrant a ‘diagnosis’.

3. Disorders of arousal

Disorders of arousal lead to behaviours that are usually initiated during partial arousals from (deep) slow wave (N3) sleep. "Most episodes are brief, but they may last as long as 30 to 40 minutes [in some children].” ICSD3 notes that most sleepwalking occurs in children. “They are especially prevalent among children and adults younger than 35 years.” Also: “The prevalence of confusional arousals in children three to 13 years of age in a large population-based study was 17.3%. Lifetime prevalence of confusional arousals has recently been reported as 18.5% (16.1-20.9 confidence interval). The prevalence among adults older than 15 years is 2.9% to 4.2%”.

The behaviours can be simple or complex, well-learned or automated or instinctive behaviour of which the person is thought to be unaware and usually is completely amnesic; there is either no, or relatively sparse mental content. Actions are not necessarily completed. Awakening is difficult and slow-this effect is known as sleep inertia (and has been called sleep drunkeness). “Sleep talking and shouting may accompany these events. The eyes are usually open during an episode and, not uncommonly, are wide open with a confused “glassy” stare." Someone with "a disorder of arousal may be very difficult to awaken and, when awakened, is often confused. There is usually amnesia for these episodes, although adults may remember fragments of episodes. Dream-like mentation is sometimes reported in adults. Other high-level cognitive functions such as attention, planning, social interaction, and intent are absent."

Sleepwalking tends to run in families. A twin study looking at how genetic and environmental factors affect sleepwalking looked at 11, 220 subjects including 1, 045 monozygotic (genetically identical) twins and 1, 899 dizygotic (50% of gene factors shared) twins. Childhood sleepwalking was more frequent in women 9% saying they experienced it “sometimes” or “often” compared to 8%” of men. Childhood sleepwalkers can continue walking as adults. 24.6% of men and for 18.3% of women continued to walk if they had walked frequently as children [22]. Of adult men sleepwalkers 88.9% had a positive history of sleepwalking in childhood, and in women, 84.5%. For both men and women those who never walked in their sleep as children did so rarely has adults-0.6%.In a separate study, immediate relatives of sleepwalkers were shown to have at least a 10-fold increased likelihood of sleepwalking over that of the general population. There are no studies on genetic similarity. The highest correlations in both children and adults between parasomnias were between sleep talking with sleepwalking, nightmares, and bruxism (tooth grinding) [22].

It is not clear why sleepwalking should decline during adolescence. Certainly children have much more deep sleep than adults and the duration of deep sleep declines during adolescence.

What triggers sleepwalking is also an area of debate. During deep sleep the thalamus which is the main sensory relay in the brain goes into an idling or neutral state so less sensory information is passed up to the cortex. The cortex reacts to stimuli so with less stimuli the less there is to respond to. As the areas of brain that handle automatic or well-learned behaviour have not shut down but are also in a neutral state, the person just continues to sleep. However, if there is an interruption of breathing or some other stimulus then the learned behaviour may be triggered. As the rational part of the brain is switched off there is nothing to prevent the behaviour, the walk, beginning. Recent research on adult sleepwalkers showed that sleepwalkers thought that stressful events during the day triggered sleepwalking 52% of the time. Other important triggers that were reported were: strong positive emotions 42%, prior sleep deprivation 27%, alcohol 12% and intense physical activity 5% [23]. However, it has been suggested recall bias may have affected these results [24].

Zadra has highlighted some misconceptions concerning somnambulism that have arisen over time: 1) that it has no daytime consequences; apparently there are, patients are more somnolent and have daytime functioning anomalies, 2) somnambulism is characterised by episodic amnesia-this appears not to be the case and 3) somnambulism is an automatic behaviour arising in the absence of dreamlike mental activity-again untrue, it has always been known that dream mentation is not exclusively related to REM sleep and Montplaisir’s group has noted mentation in somnambulists [25]. These ambiguities lead to disagreements in classification and diagnostic committees. For legal cases this is a problem as factors that are considered as significant may in fact not be. There is also a problem with working clinician’s experience, particularly those who are not engaged at sleep centres and even those have the difficulty of not actually knowing what patients do in their homes as patients, on the whole, do not have the capacity to walk in sleep centres.

3.1. Sleep-related violence

NREM Disorders of arousal are not inevitably associated with (criminally) violent behaviour. In a cohort of 64 of his patients Moldofsky noted with 89% sensitivity, 80% specificity and 81% diagnostic accuracy violence was associated with being male and having less than 2% stage 4 sleep (similar to N3, refer to table 4) [26]. Also associated was experiencing more stressors, drinking excessive caffeinated beverages and abusing drugs. A UK population study on 2, 078 men and 2, 894 women reported 1997 noted a frequency of 2% [27]. A larger sample of 19, 961 participants was polled 2010 in Finland, Germany, Italy, Portugal, Spain and the UK and found the frequency was 1.7% of the population [28]. The perpetrators were younger than 35. 61.5% noted vivid dreams during the episodes, though the highest frequency was observed with subjects suffering from sleepwalking and sleep terrors. It is notable that only 12.3% of these subjects reported their problems to a physician. Guilleminault reviewed his violent cases in 1998 comprising of 48 patients with REM Behaviour Disorder (who will not be discussed in this essay), 44 young somnambulistic patients (mean age 18+/-5 years) and 27 older subjects [29]. His review is preceded with pertinent questions for the forensic area:”Is the subject ever ‘asleep’ during violent acts, do the events occur out of sleep, or is there an intermediate or borderland period between sleep and wake? At what point does full alertness occur? Is there a decrease or absence of judgment when violent actions occur within this ill-defined borderland between wake and sleep? Based on available data, if one accepts the existence of this borderland of sleep and abnormal states of alertness, how long could this "abnormal state" last? Is there some event during sleep that influences the violent behavior? Is the state of alertness during the abnormal behavior different from "normal" wake, and, if different, how and based on what objective information?” Perhaps the review not surprisingly could not answer the questions but characterise many of the behaviours that can occur and further noted instances of seizures, the impact of narcolepsy and sleep-related respiratory disorders. He does note:”The pattern of violence against others is mostly an unconstructed violence against a bystander who may not be recognized by the wandering subject The most likely bystander, given the time these nocturnal episodes occur, is a caregiver or family member, often leading to a heart breaking situation for the perpetrator of the violent act.” Siclari et al recently (2010) reviewed the violence in sleep literature [30]. They noted that apart from the NREM parasomnias (Confusional Arousals, Sleepwalking and Sleep Terror) and REM parasomnias (RBD) that epileptic conditions such as Nocturnal Paroxysmal Dystonia and Epileptic Nocturnal Wandering, Confusional States, Psychiatric dissociative states and malingering could also account for (apparently) sleep-related violence. They also listed numerous court cases which perhaps is less than desirable (see below) but amongst other topics usefully provided a summary distinguishing between arousal disorders and nocturnal seizures in nocturnal frontal lobe epilepsy. Ebrahim & Fenwick [31] provide the most comprehensive listing for differential diagnosis (see Table 2) and controversially use an alcohol provocation test in their sample case. Their work has led to some controversy [32-40].

Organic medical and neurologic disorders
Vascular
Mass lesions
Toxic/metabolic
Infectious (limbic encephalitis).
Central nervous system (CNS) trauma.
Seizure disorders e.g. partial complex seizures.
Nocturnal seizures
Narcolepsy and idiopathic hypersomnia.
Sleep apnoea.
Sleep deprivation.
Sleep schedule/circadian rhythm disorder (including jet-lag).
Psychogenic disorders (Dissociative states, Fugues. Multiple personality disorder)
Psychogenic amnesia.
Post-traumatic stress disorder.
Malingering.
Munchausen by proxy.

Table 2.

Ebrahim & Fenwick provide a comprehensive list of possible aetiologies to aid differential diagnosis [31]

4. Forensic guidelines for sleep-related violence

In forensic psychiatry it not unusual to consider a behaviour in terms of predisposing (e.g. heredity), priming (e.g. sleep deprivation) and precipitating (e.g. touch) factors. Pressman in a series of papers has examined reviewed the literature to consider variables such as touch, sleep deprivation, febrile illness, etc. [37, 41] with a particular focus on sleep recording correlates [42] and alcohol [24, 38]. He has also questioned whether in cases that involve alcohol, whether the amnesia associated with the alleged event is caused by the putative parasomnia or is merely the result of an alcohol blackout [43] and whether the apparent association is a result of a methodological bias in the way the data has been collected (i.e. if a sleepwalker says they walk more often but are amnesic then how do they know, and how reliable is a third-party’s information on the association) [24].

Feature Violent behaviour SRSBs Comment
History Corroborated+For violent behaviours there is usually a history of childhood sleepwalking or other deep sleep parasomnias. For adult onset there should also be some evidence in the clinical history or support from observers (ideally independent). For sexual behaviours previous bed partners may corroborate the behaviour.
Defendant asleep +There should be evidence that the defendant was asleep.
Asleep for how long 30 mins - two hours?For cases of violence it is rare for the behaviour to occur around the time of sleep onset. More usually around the time that deep sleep occurs (the first three hours of the night). For sexual behaviours - the behaviour may occur later in the night (as it may with sleepwalking - Mwenge et al, 2013 [44)]
Sleep exceptionally deep Fatigue, drugs, alcohol, fever?Bonkalo[44] identifies this factor
Aroused/ (awoken) Touch, etc+ cf [36, 44]
Impulsive/short Behaviours occurs on arousal?Most guidelines suggest durations of a few minutes to 30 minutes.
Victim accidental ?The rarer form of sleep-related sexual assault is when the ‘somnambulist’ perambulates to the victim.
Amnesia None, or marginal?Sexual ‘RBD’ (see Schenck et al 2007 review) [8]
Return to awareness Incomprehension, possibly horror at act?In many cases both the victim and defendant remain asleep and the assault may not reported immediately.

Table 3.

Forensic sleep guidelines [11, 12, 30, 31, 44, 46-49]

Guidelines as to how to assess these cases have been available at least since Bonkalo (1974) [44] reviewed the literature. His guidelines which had a strong focus on Confusional Arousals and cases of violence have been adopted and amended by various authors since. Table 4 summarises these guidelines. With minor variations these guidelines are the same.

For my own part before considering the guidelines that are available the questions that need to be answered are: 1) is the defendant capable of this behaviour whilst asleep (i.e. is there a compatible history) and not affected by confounding factors (e.g. medicines, drugs, alcohol, et) and 2) is the alleged behaviour compatible with a sleep-related disorder (i.e. a parasomnia)?

Sleepwalking — Simple behaviours turning into longer duration wandering?

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Figure 2.

An illustration that attempts to show the decreasing incidence of a complex SRSB such as rape (though ejaculation is not noted).

4.1. Sleep-related sexual behaviour

ICDS3 lists SRSBs as a pathologic subtype under Confusional Arousals (A NREM parasomnia). However, not all SRSBs occur as NREM parasomnias (Table 5). SRSBs first emerged as a possible subtype of parasomnia with a description of masturbation by Wong [13]. This was followed by case reports of sleep-related sexual abuse of children [50] and subsequently more reports from Shapiro [10] and Rosenfeld [49] with Guilleminault [12] providing the largest, substantive, well-investigated case series with Shapiro [11] running roughly parallel. Schenck et al [6] subsequently provide the first major review of the area.

Sleep sex, sexsomnia, sexual behaviour in sleep
Sleep sex moaning, sleep sex talking, sleep-sex shouting
Sleepsex snoring
Hypersexuality with Kleine-Levin syndrome;
Epileptic sleep sex/sexsomnia/SBS, sleep related sexual seizures
Epileptic sleep sex moaning, sleep sex talking, sleep sex shouting
Chronic, severe insomnia;
Restless legs syndrome (RLS)
Sexual hypnagogic or hypnopompic;
Sexual REM-onset dream attack
Cataplectic orgasm, peri-orgasmic cataplexy
Sleep exacerbation of persistent sexual arousal syndrome
Hypersexuality with sleep related painful erections (SRPE)
Hypersexuality with sleep related dissociative disorders
Hypersexuality during nocturnal awakenings
Nocturnal sexual delusions and hallucinations

Table 4.

Sleep related abnormal sexual behaviours (alternate names)

[i] - (Terms used for searching for SRSBs in the published research literature by Schenk et al [6] for their 2007 review)

It is notable that the largest number of cases was derived from patients suffering from Kleine-Levine Syndrome (78 cases), follow by parasomniacs [31] and sleep-related seizures (7 cases).

Schenck et al [6] note that neither the Kinsey [51, 52], apart from male nocturnal emissions, or Hite Reports [53, 54] note SRSBs. In the section on “Individual Variation, ” Kinsey commented on the wide variety of human sexual behaviour which may have been a covert reference to nocturnal or sleep-related behaviour. They also note that their data, because of the sources contain cases that have led to criminal proceedings. Importantly they find that the greatest incidence of SRSBs is with patients suffering from Kleine-Levin syndrome, a rare disorder (probable incidence 1 in a million) characterised by periods of hypersomnia and mood changes, and with many patients suffering from hypersexuality and/or hyperphagia. Seventy-eight cases were reported. The next main group was the parasomnias-31 cases, followed by 7 cases of sleep-related seizures. Schenck et al [6] also question the existence of REM-related SRSBs or at least note there are no sleep laboratory confirmations of this behaviour and that the cases they reviewed did not involve dream-enactment. Parasomnia Overlap Disorder (a mixture of NREM and REM parasomnia was noted).

Kleine-Levin syndrome
Sleep related sexual seizures
Severe chronic insomnia
Restless legs syndrome
Narcolepsy
Sleep exacerbation of persistent sexual arousal syndrome
Sleep related painful erections and increased sexual activity
Sleep related dissociative disorders
Nocturnal psychotic disorders
Hypersexuality after nocturnal awakenings
Miscellaneous

Table 5.

Sleep Related Disorders and Abnormal Sexual behaviours and Experiences

[i] - (naps; [REM] sleep erections and sexual vulnerability; medication-induced states)

It is perhaps surprising that the published clinical literature has relatively few SRSB case studies, given that an internet survey [55-57] ? The answer may lie in dream mentation work. Nielsen found that the prevalence of various behaviours particularly sexual behaviours apparently increased if respondents were asked specific questions about the behaviour; subjects did not readily reveal their sexual behaviour without being asked. Overall Nielsen noted that “females reported more speaking, crying, fear and smiling/laughing than did males; males reported more sexual arousal” [58].

4.2. Sleep-related sexual violence

Andersen et al (2007) [59] provide a slightly more focussed review than Shenck et al, 2007 [6] on SRSBs but include the main datasets provided by Guilleminault [12] and Shapiro [11]. The total number of cases cited was 40 (9 women). If the cases that were involved in criminal or other legal proceedings are excluded the number falls to 22 (7 women) ; if alcohol is then excluded there remain 17 cases (6 women). Further, if cases of multiple substance abuse and indecent exposure are removed that leaves a dataset of 15 (6 women). Of these there were 3 cases of sexual intercourse (men). Interaction between two individuals which is an assault without consent occurred with 7/9 men, and 1/6 women. Moaning was reported for 3/6 women and 1/10 men; masturbation 3/6 women and 2/10 men.

Variable R&K 1968 [60] AASM 2007 [61] Comments
Scoring page/window length 15, 20 or 30 seconds30 seconds (compulsory) Originally sleep stages were scored on pages which consisted of 15-30 seconds data
Stages Wakefulness, stage 1 (drowsy), stage 2 (light), stage 3, stage 4, REM sleep, movement time.Stages W, N1, N2, N3, and R Combinations and alternative names:
NREM = N1+N2+N3;
REM sleep = Paradoxical sleep
Mental world
Wakefulness EEG alpha activity for ≥50% of an epochSame (W) Multiple variants Awake (full range)
N3 EEG slow-wave activity for ≥50% of the page for stage 4 sleep or ≥20% of the page for stage 3 sleep, 0.5-2.0 Hz and >75 μVSame, except that stages 3 and 4 are combined to N3Not all slow waves are the same. Some are very slow oscillations <1 Hz or classified according to different amplitudes Nil or dark and threatening (usually associated with amnesia upon awakening)
Deep sleep = Delta Sleep = SWS = Slow Wave Sleep, stages 3 and 4 combined.
N2 Sleep spindles or K-complexes; EEG slow-wave activity for <20% of the pageSame (N2) Not all sleep spindles or K-complexes are the same Identifies sleep onset in some systems.
Stage 2
(light sleep)
N1 Low-voltage, mixed-frequency activity; possibly slow eye movements; no sleep spindles or K-complexes; EEG alpha activity for <50% of the epochSame (N1) Identifies sleep onset in some systems.
Possible hallucinations
Stage 1
(drowsiness)
REM Low-voltage, mixed-frequency EEG activity; very low submental EMG activity; possible saw tooth EEG theta activity; >=1 rapid eye movement (unequivocal) Same (R) Phasic activity, sawtooth wavesDreaming (full range of possible, nil, black & white, colour, etc). Dream incorporation, Dream enactment
REM sleep

Table 6.

Showing classification rules and nomenclature of sleep staging systems.

[i] - AASM, American Academy of Sleep Medicine; EEG, electroencephalogram; EMG, electromyogram; R&K, Rechtschaffen and Kales [60].

It is now becoming clear that slow wave sleep consists of not only different types of slow wave but these types have different functions [103-109]. It follows that when generalisations are made about deep sleep, those generalisations may not apply to all type of deep sleep. That degree of inaccuracy is below that usually required by courts that are seeking the truth. Spindles have the same problem [110-113].

The table is provided to enable comparison of older research with the new American Academy guidelines. That main point is that precisely what the sleep stages are is still a matter of research, debate and discussion. The original committee had difficulty in deciding on the stages (Oswald, personal communication, 1978 and others on the committee) and the 2007 still had similar problems. However it is notable that the professional sleep societies continue to monitor and refine the definitions (e.g. [62]). New ‘stages’ continue to be found, e.g. Koch et al [63]. For applied purposes like legal cases though the stages that cause most problems are REM and deep sleep. Further discussion in Idzikowski (2014) [64].

Sleep research and sleep medicine using electroencephalography (‘brainwaves’) as the primary measures grew with the discovery that ‘dreaming’ could be measured objectively [65]. Unfortunately, over time it turned out that the correlation between electrophysiological measures that lead to a particular classification of sleep stages was just a correlation (see Table 5 for definitions) ; dreaming generally occurs during REM but may occur in other stages, etc. Also, awkwardly both subjective appreciation, or behavioural responses do not directly map on to sleep stage. So in ‘light sleep’, (stage 2/N2) which is generally regarded as ‘sleep’ behavioural responses are still possible (depending on the time of night) [66].

The problem of identifying the stages accurately as indexed by the difficulties in producing automatic computer algorithms to do the staging and the disagreements between human scorers when sleep records are compared. Rosenberg et al, found sleep stage agreement averaged 82.6%. Agreement was highest for stage R sleep with stages N2 and W approaching the same level. Scoring agreement for stage N3 sleep was 67.4% and was lowest for stage N1 at 63.0% (the stages that are important with regard to NREM parasomnias. Scorers had particular difficulty with the last epoch of stage W before sleep onset, the first epoch of stage N2 after stage N1 and the first epoch of stage R after stage N2. Discrimination between stages N2 and N3 was particularly difficult for scorers [62].

In addition to compartmentalising sleep into page lengths of 20-30 seconds there have been other attempts to quantify sleep that are less reliant on page size and that may be important in the definition of sleep, deep sleep and sleepwalking. For example, spectral analysis (looking at the frequency domains) [67, 68, 69, 70] and Cyclic Alternating Pattern CAP [69].

In humans sleep has a 90 minute cyclicity [71, 72], and in normal individuals there is a preponderance of deep (N3) sleep early in the night, with progressively more REM sleep occurring late in the sleep period. The 90 minute cycle is punctuated with REM sleep and possibly wakefulness. Deep sleep is homeostatically controlled as is REM sleep, but REM sleep also has a circadian component with more REM sleep occurring in the morning.

AREA DEEP SLEEP REM SLEEP
Lateral frontal cortex
Medial prefrontal +
orbitofrontal cortex
↑ ↓
Lateral parietal cortex
Medial parietal cortex +precuneus
Temporal-occipital cortices
Anterior cingulate cortex
Medial temporal lobe, hippocampal regions, amygdala
Thalamus
Basal ganglia
Pons, midbrain
Cerebellum

Table 7.

Provides an overview of brain imaging studies that show both the decreases and increases in brain activity during the major sleep stages [73-77].

It is important to note that when the hypothalamic and lower brain sleep centres are most active, the wake centres are generally quiescent. The interplay between the two orchestrates some of the changes seen in the brain. Loss of conscious awareness occurs some time during stage 2 when functional MRI signals decrease in the tale thalamic and hypothalamic regions, the cingulate cortex, right insula, nearby temporal regions, the inferior parietal lobules and the inferior/middle frontal gyri [78]. Bassetti et al [79] have observed in one subject during sleepwalking that a disassociation between an activation in thalamocingulate pathways coupled with deactivation of thalamocortical arousal systems is associated with sleepwalking. It is almost important to note though that within cortical regions there can be both increases and decreases of activity within “sleep” which are presumed to reflect local energy requirements [80, 81]

Sleep is an orchestrated state with hypothalamic centres strongly controlling which areas of brain remain active and which become quiescent-see Table 7. Diminution of activity in areas such as the prefrontal cortex underpin the scientific arguments that the brain centres that might be involved in the determining whether a behaviour is ‘right or wrong’, appropriate or not are not active. That coupled with evidence from sleep deprivation work that points to degraded moral judgement with sleep loss [82].

Whilst this section and sleep classifications describe sleep states as mutually exclusive, in reality they are not. The stages are an amalgam of different physiological signs that have been lumped together as stages (by committee and consensus). That does not mean that all aspects associated with a particular stage will necessarily remain within that stage. For example a penile erection which is usually associated with REM sleep may continue, for a period of time, into light sleep or wakefulness? Moreover, there is still debate as to what the functional significance of sleep stages. Pharmacological disassociations have occasionally been noted, e.g. changes in deep sleep duration without apparent impact on waking function [83]. Mahowald and Schenck [84] describe the extreme states of wakefulness whilst apparently asleep (according to electrophysiological characteristics). Mahowald and Schenck identify the three basic states of being as wakefulness, NREM sleep and REM sleep.

5. Alcohol and sleep

Bonkalo notes alcohol amongst factors that may increase deep sleep and thus facilitate violent confusional arousals [44]. ICSD3 explicitly states [17] “… Disorders of arousal should not be diagnosed in the presence of alcohol intoxication. The behavior of the alcohol-intoxicated individual may superficially resemble that of the sleepwalker. …“ This is within a section on differential diagnosis but it also may have an undue impact in the forensic area. Why this sort of policy statement should be placed in a scientific document is not entirely clear. It is correct to note that there are difficulties, but an instance of a behaviour that may occur without alcohol could be repeated within sleep, irrespective of whether alcohol is present or not? However, there is confusion in the literature as alcohol has been suggested as a priming factor, partly on the basis of self-reports, rejected by Pressman et al [24] because of recall bias, and partly as early hypotheses noted that: 1) deep sleep is associated with sleepwalking, 2) alcohol facilitates deep sleep (not currently, wholly accepted) and 3) they hypothesis, so alcohol must promote sleepwalking? No formal experiments have been published either refuting or accepting this hypothesis and in fact given the reported complex effects of alcohol on sleep [36] and the variables involved, e.g. Carskadon and colleagues [85-88], it may be quite some time before an adequate experiment on sleepwalkers is conducted. Answering the question as to how alcohol might affect sexual response [89, 90] during sleep exacerbates the complexities.

6. Wakefulness and violence

Sleep and wakefulness are two sides of the same coin. Sleep-related legal cases need to be balanced by considering what can happen when a person is awake. Humans are inherently a violent species, both in terms of physical aggression and aggression directed sexually [91]. Sleep-related violence has only a loose overlap with WHO’s typology of violence. The overlap is interpersonal violence which may be physical or sexual. It is unknown whether self-directed violence in the form of suicidal behaviour occurs during sleep as it is assumed that sleepwalkers who have perished did not intend to commit suicide. The links between violent assaults and wakefulness are broad and will not be considered here.

6.1. Wakefulness and sexual violence

There are multiple risk factors that increase the risk of a man committing rape. These include individual factors such as alcohol and drug use; coercive sexual fantasies, attitudes and beliefs supportive of sexual violence; impulsive and antisocial tendencies; preference for impersonal sex; hostility towards women; history of sexual abuse as a child; witnessing family violence as a child. Additionally, relationship factors (e.g. associating with sexually aggressive and delinquent peers), community factors (e.g. lack of employment opportunities, general tolerance of sexual assault within the community) and societal factors (e.g. societal norms supportive of sexual violence, male superiority and sexual entitlement). Conservative estimates suggest that at least 25 percent of American women have been assaulted in adolescence or adulthood and that 18 percent have been raped. Furthermore, at least 20 percent of American men report having perpetrated sexual assault and 5 percent report having committed rape [92].

In the United Kingdom (North London, 1993) 6% assaulted in the past 12 months, and 23% attempted or completed forced sex by an intimate partner [93, 94]. The comparable figures for the U.S. are 0.7% and 7.7% but these may be skewed as the sample group did not include women who had been in a relationship [91].

6.2. Alcohol and sexual violence

The biological links between alcohol and violence are complex. Even the impact of alcohol on sexual potency needs further research as results currently still need clarification-e.g. high doses of alcohol which might render some men impotent do not appear to have the same effects on rapists [95]. Alcohol does though have a disinhibiting role in sexual assaults, it reduces inhibitions, clouds judgements and impairs ability to interpret cues [91]. As lack of reporting causes a problem in identifying the precise incidence of alcohol being associated with rape, the estimates are similar to violent crime in general and range between 34-74% [92]. The role of alcohol is complex [96].

7. Discussion

It is perhaps not surprising that there are calls for more considered opinions and further research into the whole area of sleep-related violence, let alone sleep-related sexual violence [97]. Extrapolating what is known about parasomnias, given the limited evidence base, which at best is still only at the data-collection phase, to applied situations such as legal cases have to be fraught. There are varying degrees of certainty with respect to what we know: 1) in NREM deep sleep, associated with short-duration somnambulism (within the confines of one sleep cycle), there is a) limited or fragmentary connection with the external world, b) some mental activity that may be concordant with behaviour, and c) behaviours including ambulation that are relatively simple. 2) It is not clear, particularly with longer duration, more complex behaviours, whether deep sleep continues, or whether sleep either moves into a more wakeful but disassociated state, or to drowsiness and/or light sleep but still possibly in a disassociated state. 3) The normal cyclicity of sleep is disturbed. The main hypotheses dealing with sleep control posit an interaction between a sleep homeostat and the circadian system. There is curiously little evidence that the circadian system is involved, other than most (if not all) NREM parasomnias occur at night? However, circadian displacement is being increasingly implicated [115]. The homeostat increases the pressure for sleep, particularly deep sleep, in parallel with the duration of prior wakefulness. However, in sleepwalkers this system appears to be faulty [25], with their deep sleep being more broken with arousals and wakefulness (which could be a circadian system effect, with circadian time being affected by the sleep deprivation?).With SRSBs there is a range of possibilities ranging from simple caresses to sexual intercourse, all of which may lead to legal action if occurring inappropriately and without consent. The current database of recorded sexual activity is sparse and what there is has been with consenting adults dressed for sleep. Apart from sexual intercourse rape may involve unclothing a possibly unfamiliar victim, and also possibly in unfamiliar circumstances. Whilst erection and ejaculation are underpinned by primarily reflexive mechanisms, more complex control is required to achieve full intercourse with ejaculation.

It is perhaps not surprising that the emerging (sub-?) speciality of 'forensic sleep' or 'forensic sleep medicine', given the limited database, ambiguities over the function of sleep or its staging, that the area has little theoretical underpinning. Perhaps though the time has come to start theorising or creating testable models against which to run hypotheses? This has already started thought at a basic level. Cramer Bornemann and Mahowald [114] leaning on the concept of central pattern generators provide some ideas as to how simple, reflexive and instinctive behaviours may arise in humans during sleep. Zadra et al [25] consider the existing evidence to assemble a model describing somnambulistic behaviour. This suggests that there are two main dimensions to sleepwalking: a dysfunctional “deep sleep” system, and b) a dysfunctional arousal (wake-promoting) system.

7.1. What can sleep science & sleep medicine tell the law?

Sleep research has identified various stages of sleep though there are still debates as to scoring of the stages and their functional significance. As noted earlier, there are also ambiguities as to when sleep onset actually occurs and very little work on what cognitive capacity remains-(insight, problem-solving, etc.) (dreams are a special case, where a mixture of brain imaging and self-report identities what brain regions appear inactive, and provides more information e.g. reduced firing in the locus coeuruleus would lead external stimuli having less impact on attention-which may account for a dream narrative incorporating external stimuli as opposed to breaking the narrative (and awakening the subject?) [98].

For forensic work the main issues are how (particular stages of) sleep can affect cognitive capacity, and control of behaviour. The impact of sleep deprivation and sleep restriction on waking sleepiness and cognitive capacity is not dealt with in this chapter. This needs further consideration as the complexity of behaviour in an alleged crime is important, e.g. what capacity is required for a defendant to appreciate consent, what capacity is required for a ‘sleeping?’ rapist to seek out and locate a victim? At which point does apparent capacity preclude the possibility that the defendant is in fact not asleep (they may be awake but may be in a different state, a disassociated state of some sort (not necessarily sleep-related)).

In normal REM sleep the muscles are paralysed so movement is more or less impossible. However penile tumescence is normal and in some circumstances the meaning of an erection can be misconstrued (leading to legal action). Given that sleep is a usually coordinated state the tumescence would normally subside prior to or when entering other stages, like wakefulness (with the possibility of sleep inertia) or drowsiness or light or even deep sleep. At sleep onset, the precise determination of the onset of mental sleep is unclear, occurring sometime during N2 (light sleep). ‘Wet dreams’ are not regarded as pathological, when ejaculation occurs during [REM?] sleep. Clearly, some movements occur during sleep to maintain comfort (either avoiding pain or maintaining an appropriate temperature, etc), but even these if someone is sleeping nearby, these movements may accidentally impact on the other sleeper which in some circumstances can lead to complaints of assault.

Sleep medicine can describe somnambulistic episodes only roughly (virtually no helpful home recordings), quite roughly-both duration and timing of episodes are subject to dispute. Consider Mwenge et al’s sleepwalker whose latest episode was 06.45-using home recordings [45].

7.2. What can the law tell sleep science and medicine?

Judicial systems have had to manage sleep-related states considerably a lot longer than the time that sleep science and medicine have existed (considerably longer than the Royal College of Psychiatrists!). Understanding the nuances where they are not policy driven can be a useful area to explore. Unfortunately though, reliable data as to individual cases is rarely available. Media misreporting is common. Attention demanding headlines or misreporting by legal correspondents creates difficulties that may ultimately influence professional opinions and misguide the opinions experts may give in court. Furthermore, publishing of case studies is fraught with difficulty if reference is made to court proceedings. Case material acquired during a court case is not in the public domain. A defendant whether convicted or not retains their human rights and although the confidentiality between practitioner and client is broken in relation to the court, that does not necessarily (arguable) make the material available to the public domain.

8. Future agendas

Basic science research: arousal thresholds, sensory/cognitive processing capability, classical/operant conditioning potential. Better models of human sexual behaviour. Development of home recording equipment (video, ambulatory systems (e.g. like the Zeo [99-102]. There is also a need for better models of describing the relationship of sleep and wakefulness with cognition and behaviour (the subject of another paper).

Clinical science research: improved classifications systems; the need to distinguish between somnambulism, sleep inertia and disassociated states.

Forensic: Some definition of standards and methodologies driven not only by a reaction to legal needs but also by consideration of basic pathophysiology. The effect of alcohol needs to be explored both in a laboratory and non-laboratory setting (initially outside of a legal context).

Legal: Reform and uniformity across jurisdictions with respect to insanity and automatism laws. Ideally a mechanism to record accurately court proceedings and the data associated with these cases, so that it is possible to court cases as data.

9. Conclusion

This essay focused on NREM parasomnias that might lead to SRSB that in turn might lead to legal proceedings. A considerable amount of work needs to be done so that expert opinion in court is based on science that has substantive forensic value.

10. Acknowledgements

Former colleagues of Sleep Medicine Centre Ltd (Edinburgh Sleep Centre-Heriot Row and the London Sleep Centre – Harley Street) especially Ewan Crawford, Lizzie Hill, Stevie Williams, Heather Engleman, Laura Bolton, Christine Auld, Susan Fifer, Mario Alfredo Parra-Rodriguez, Marios Kittenis, and Elvina Gountouna.

Prisons: HMPs Belmarsh, Swansea, Peterborough, Holloway, Durham, Exeter and Edinburgh (at the Edinburgh Sleep Centre – Heriot Row)

References

1 - Umanath S, Sarezky D, Finger S. Sleepwalking through history: Medicine, arts, and courts of law. J Hist Neurosci 2011, Oct; 20 (4); 253-76.
2 - Petrain DE. An english translation of john william polidoris (1815) medical dissertation on oneirodynia (somnambulism). European Romantic Review 2010; 21 (6); 775-88.
3 - Ekirch AR, Shneerson JM. Nineteenth-Century sleep violence cases: A historical view. Sleep Med Clin 2011, Dec; 6 (4); 483-91.
4 - Rubin G. The" political economy" of sex. Feminist Anthropology: A Reader 2009:87.
5 - Kompanje EJO. ‘The devil lay upon her and held her down’ hypnagogic hallucinations and sleep paralysis described by the dutch physician isbrand van diemerbroeck (1609–1674) in 1664. J Sleep Res 2008; 17 (4); 464-7.
6 - Schenck CH, Arnulf I, Mahowald MW. Sleep and sex: What can go wrong? A review of the literature on sleep related disorders and abnormal sexual behaviors and experiences. Sleep 2007, Jun; 30 (6); 683-702.
7 - Hardy T. Tess of the d'urbervilles. New York: Nelson Doubleday; 1891 f.
8 - Bowden P. Sleepwalking and indecent exposure. Med Sci Law 1991, Oct; 31 (4); 359.
9 - Buchanan A. Sleepwalking and indecent exposure. Med Sci Law 1991, Jan; 31 (1); 38-40.
10 - Shapiro CM, Fedoroff JP, Trajanovic NN. Sexual behavior in sleep: A newly described parasomnia. Sleep Res 1996; 25:367.
11 - Shapiro CM, Trajanovic NN, Fedoroff JP. Sexsomnia--a new parasomnia? Can J Psychiatry 2003, Jun; 48 (5); 311-7.
12 - Guilleminault C, Moscovitch A, Yuen K, Poyares D. Atypical sexual behavior during sleep. Psychosom Med 2002; 64 (2); 328-36.
13 - Wong KE. Masturbation during sleep--a somnambulistic variant? Singapore Med J 1986, Dec; 27 (6); 542-3.
14 - Fenwick P. Sleep and sexual offending. Med Sci Law 1996, Apr; 36 (2); 122-34.
15 - Medicine AAOS. International classification of sleep disorders, 3rd edition. Darien, IL: American Academy Of Sleep Medicine; 2014f.
16 - Eastman N. Psychiatric, psychological, and legal models of man. Int J Law Psychiatry 1992; 15 (2); 157-69.
17 - ICSD nrem-related parasomnias. In: International Classification of Sleep Disorders. American Academy of Sleep Medicine, ; 2014g. p. 228-39.
18 - Pressman MR, Meyer TJ, Kendrick-Mohamed J, Figueroa WG, Greenspon LW, Peterson DD. Night terrors in an adult precipitated by sleep apnea. Sleep 1995, Nov; 18 (9); 773-5.
19 - Iranzo A, Santamaría J. Severe obstructive sleep apnea/hypopnea mimicking REM sleep behavior disorder. Sleep 2005, Feb; 28 (2); 203-6.
20 - Ohayon MM, Priest RG, Caulet M, Guilleminault C. Hypnagogic and hypnopompic hallucinations: Pathological phenomena? Br J Psychiatry 1996, Oct; 169 (4); 459-67.
21 - Ohayon MM. Prevalence of hallucinations and their pathological associations in the general population. Psychiatry Res 2000, Dec 27; 97 (2-3); 153-64.
22 - Hublin C, Kaprio J, Partinen M, Koskenvuo M. Sleeptalking in twins: Epidemiology and psychiatric comorbidity. Behav Genet 1998, Jul; 28 (4); 289-98.
23 - Lopez R, Jaussent I, Scholz S, Bayard S, Montplaisir J, Dauvilliers Y. Functional impairment in adult sleepwalkers: A case-control study. Sleep 2013, Mar; 36 (3); 345-51.
24 - Pressman MR. Sleepwalking, amnesia, comorbid conditions and triggers: Effects of recall and other methodological biases. Sleep 2013, Nov; 36 (11); 1757-8.
25 - Zadra A, Desautels A, Petit D, Montplaisir J. Somnambulism: Clinical aspects and pathophysiological hypotheses. Lancet Neurol 2013, Mar; 12 (3); 285-94.
26 - Moldofsky H, Gilbert R, Lue FA, MacLean AW. Sleep-related violence. Sleep 1995, Nov; 18 (9); 731-9.
27 - Ohayon MM, Caulet M, Priest RG. Violent behavior during sleep. J Clin Psychiatry 1997, Aug; 58 (8); 369-76; quiz 377.
28 - Ohayon MM, Schenck CH. Violent behavior during sleep: Prevalence, comorbidity and consequences. Sleep Med 2010, Oct; 11 (9); 941-6.
29 - Guilleminault C, Leger D, Philip P, Ohayon MM. Nocturnal wandering and violence: Review of a sleep clinic population. J Forensic Sci 1998, Jan; 43 (1); 158-63.
30 - Siclari F, Khatami R, Urbaniok F, Nobili L, Mahowald MW, Schenck CH, et al. Violence in sleep. Brain 2010, Dec; 133 (Pt 12); 3494-509.
31 - Ebrahim O, Fenwick P. Sleep-related automatism and the law. Med Sci Law 2008, Apr 1; 48 (2); 124-36.
32 - Pressman MR. Alcohol does not increase slow wave sleep. Alcohol Clin Exp Res 2012, Aug; 36 (8); 1474; author reply 1475.
33 - Pressman MR, Mahowald MW, Cramer–Bornemann M. Reply to Ebrahim and Fenwick. Sleep Med Rev 2007, Jun; 11 (3); 244-7.
34 - Mahowald MW, Schenck CH, Cramer Bornemann MA. Response to Ebrahim and Fenwick. Sleep Med Rev 2007, Jun; 11 (3); 247.
35 - Ebrahim I, Fenwick PB. Response to pressman: "Factors that predispose, prime and precipitate NREM parasomnias in adults: Clinical and forensic implications" sleep med. Rev. 2007; 11:5-9. Sleep Med Rev 2007, Jun; 11 (3); 241-3; author reply 244-7.
36 - Ebrahim IO, Shapiro CM, Williams AJ, Fenwick PB. Alcohol and sleep I: Effects on normal sleep. Alcohol Clin Exp Res 2013, Apr; 37 (4); 539-49.
37 - Pressman MR. Factors that predispose, prime and precipitate NREM parasomnias in adults: Clinical and forensic implications. Sleep Med Rev 2007, Feb; 11 (1); 5-30; discussion 31-3.
38 - Pressman MR, Mahowald MW, Schenck CH, Bornemann MC. Alcohol-induced sleepwalking or confusional arousal as a defense to criminal behavior: A review of scientific evidence, methods and forensic considerations. J Sleep Res 2007, Jun; 16 (2); 198-212.
39 - Pressman MR, Schenck CH, Mahowald MW, Bornemann MC. Sleep science in the courtroom. J Forensic Leg Med 2007, Feb; 14 (2); 108-11; author reply 111-3, discussion 114-8.
40 - Ebrahim I, Fenwick P. Letter to the editor re: Pressman et al. Alcohol-induced sleepwalking or confusional arousal as a defense to criminal behavior: A review of scientific evidence, methods and forensic considerations. J. Sleep res. (2007) 16, 198-212. J Sleep Res 2008, Dec; 17 (4); 470-2; author reply 473-4.
41 - Pressman MR. Disorders of arousal from sleep and violent behavior: The role of physical contact and proximity. Sleep 2007, Aug; 30 (8); 1039-47.
42 - Pressman MR. Hypersynchronous delta sleep EEG activity and sudden arousals from slow-wave sleep in adults without a history of parasomnias: Clinical and forensic implications. Sleep 2004, Jun 15; 27 (4); 706-10.
43 - Pressman MR, Caudill DS. Alcohol-induced blackout as a criminal defense or mitigating factor: An evidence-based review and admissibility as scientific evidence. J Forensic Sci 2013, Jul; 58 (4); 932-40.
44 - Bonkalo A. Impulsive acts and confusional states during incomplete arousal from sleep: Criminological and forensic implications. Psychiatr Q 1974; 48 (3); 400-9.
45 - Mwenge B, Brion A, Uguccioni G, Arnulf I. Sleepwalking: Long-term home video monitoring. Sleep Med 2013, Nov; 14 (11); 1226-8.
46 - Buchanan PR. Sleep sex. Sleep Med Clin 2011, Dec; 6 (4); 417-28.
47 - Ebrahim I, Wilson W, Marks R, Peacock KW, Fenwick P. Violence, sleepwalking and the criminal law: (1) the medical aspects. Criminal Law Review 2005:601-13.
48 - Mahowald MW, Bundlie SR, Hurwitz TD, Schenck CH. Sleep violence--forensic science implications: Polygraphic and video documentation. J Forensic Sci 1990, Mar; 35 (2); 413-32.
49 - Rosenfeld DS, Elhajjar AJ. Sleepsex: A variant of sleepwalking. Arch Sex Behav 1998, Jun; 27 (3); 269-78.
50 - Hurwitz TD, Mahowald MW, Schluter JL. Sleep-related sexual abuse of children. Sleep Res 1989; 18:246.
51 - Kinsey AC. Sexual behavior in the human female. Indiana University Press; 1953f.
52 - Kinsey AC, Pomeroy WB, Martin CE. Sexual behavior in the human male. 1948.
53 - Hite S. The hite report: A nationwide study of female sexuality. Seven Stories Press; 2004h.
54 - Hite S. The hite report on male sexuality. Knopf New York; 1981i.
55 - Mangan MA. A phenomenology of problematic sexual behavior occurring in sleep. Arch Sex Behav 2004, Jun; 33 (3); 287-93.
56 - Mangan MA, Reips UD. Sleep, sex, and the web: Surveying the difficult-to-reach clinical population suffering from sexsomnia. Behav Res Methods 2007, May; 39 (2); 233-6.
57 - Trajanovic NN, Mangan M, Shapiro CM. Sexual behaviour in sleep: An internet survey. Soc Psychiatry Psychiatr Epidemiol 2007, Dec; 42 (12); 1024-31.
58 - Nielsen T, Svob C, Kuiken D. Dream-enacting behaviors in a normal population. Sleep 2009, Dec; 32 (12); 1629-36.
59 - Andersen ML, Poyares D, Alves RS, Skomro R, Tufik S. Sexsomnia: Abnormal sexual behavior during sleep. Brain Res Rev 2007, Dec; 56 (2); 271-82.
60 - Rechtschaffen A, Kales A. A manual of standardized terminology, technique and scoring system for sleep stages of human sleep. NIH publication no. 204. Washington DC: US Government Printing Office; 1968k.
61 - Medicine AAOS, Iber C. The AASM manual for the scoring of sleep and associated events: Rules, terminology and technical specifications. American Academy of Sleep Medicine; 2007l.
62 - Rosenberg RS, Van Hout S. The american academy of sleep medicine inter-scorer reliability program: Sleep stage scoring. J Clin Sleep Med 2013, Jan 15; 9 (1); 81-7.
63 - Koch H, Christensen JA, Frandsen R, Zoetmulder M, Arvastson L, Christensen SR, et al. Automatic sleep classification using a data-driven topic model reveals latent sleep states. J Neurosci Methods 2014, Jul 9; 235C:130-7.
64 - Idzikowski C. The pharmacology of human sleep, a work in progress? Curr Opin Pharmacol 2014, Feb; 14:90-6.
65 - Aserinksy E, Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 1953, Sep 4; 118 (3062); 273-4.
66 - Ogilvie RD, Wilkinson RT, Allison S. The detection of sleep onset: Behavioral, physiological, and subjective convergence. Sleep 1989, Oct; 12 (5); 458-74.
67 - Guilleminault C, Poyares D, Aftab FA, Palombini L, Abat F. Sleep and wakefulness in somnambulism: A spectral analysis study. J Psychosom Res 2001, Aug; 51 (2); 411-6.
68 - Pilon M, Zadra A, Joncas S, Montplaisir J. Hypersynchronous delta waves and somnambulism: Brain topography and effect of sleep deprivation. Sleep 2006, Jan; 29 (1); 77-84.
69 - Guilleminault C. Hypersynchronous slow delta, cyclic alternating pattern and sleepwalking. Sleep 2006, Jan; 29 (1); 14-5.
70 - Guilleminault C, Kirisoglu C, da Rosa AC, Lopes C, Chan A. Sleepwalking, a disorder of NREM sleep instability. Sleep Med 2006, Mar; 7 (2); 163-70.
71 - Dijk DJ. Regulation and functional correlates of slow wave sleep. J Clin Sleep Med 2009, Apr 15; 5 (2 Suppl); S6-15.
72 - Kishi A, Yasuda H, Matsumoto T, Inami Y, Horiguchi J, Tamaki M, et al. NREM sleep stage transitions control ultradian REM sleep rhythm. Sleep 2011, Oct; 34 (10); 1423-32.
73 - Braun AR, Balkin TJ, Wesenten NJ, Carson RE, Varga M, Baldwin P, et al. Regional cerebral blood flow throughout the sleep-wake cycle. An H2 (15) O PET study. Brain 1997, Jul; 120 (Pt 7); 1173-97.
74 - Maquet P, Péters J, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 1996, Sep 12; 383 (6596); 163-6.
75 - Maquet P, Degueldre C, Delfiore G, Aerts J, Péters JM, Luxen A, Franck G. Functional neuroanatomy of human slow wave sleep. J Neurosci 1997, Apr 15; 17 (8); 2807-12.
76 - Maquet P. Positron emission tomography studies of sleep and sleep disorders. J Neurol 1997, Apr; 244 (4 Suppl 1); S23-8.
77 - Maquet P, Phillips C. Functional brain imaging of human sleep. J Sleep Res 1998; 7 Suppl 1:42-7.
78 - Kaufmann C, Wehrle R, Wetter TC, Holsboer F, Auer DP, Pollmächer T, Czisch M. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: An EEG/fmri study. Brain 2006, Mar; 129 (Pt 3); 655-67.
79 - Bassetti C, Vella S, Donati F, Wielepp P, Weder B. SPECT during sleepwalking. Lancet 2000, Aug 5; 356 (9228); 484-5.
80 - Terzaghi M, Sartori I, Tassi L, Didato G, Rustioni V, LoRusso G, et al. Evidence of dissociated arousal states during NREM parasomnia from an intracerebral neurophysiological study. Sleep 2009, Mar; 32 (3); 409-12.
81 - Dang-Vu TT, Schabus M, Desseilles M, Sterpenich V, Bonjean M, Maquet P. Functional neuroimaging insights into the physiology of human sleep. Sleep 2010, Dec; 33 (12); 1589-603.
82 - Killgore WD, Killgore DB, Day LM, Li C, Kamimori GH, Balkin TJ. The effects of 53 hours of sleep deprivation on moral judgment. Sleep 2007, Mar; 30 (3); 345-52.
83 - Idzikowski C, Mills FJ, Glennard R. 5-Hydroxytryptamine-2 antagonist increases human slow wave sleep. Brain Res 1986, Jul 16; 378 (1); 164-8.
84 - Mahowald MW, Schenck CH. Status dissociatus--a perspective on states of being. Sleep 1991, Feb; 14 (1); 69-79.
85 - Rupp TL, Acebo C, Seifer R, Carskadon MA. Effects of a moderate evening alcohol dose. II: Performance. Alcohol Clin Exp Res 2007, Aug; 31 (8); 1365-71.
86 - Rupp TL, Acebo C, Van Reen E, Carskadon MA. Effects of a moderate evening alcohol dose. I: Sleepiness. Alcohol Clin Exp Res 2007, Aug; 31 (8); 1358-64.
87 - Van Reen E, Rupp TL, Acebo C, Seifer R, Carskadon MA. Biphasic effects of alcohol as a function of circadian phase. Sleep 2013, Jan; 36 (1); 137-45.
88 - Van Reen E, Tarokh L, Rupp TL, Seifer R, Carskadon MA. Does timing of alcohol administration affect sleep? Sleep 2011, Feb; 34 (2); 195-205.
89 - George WH, Stoner SA. Understanding acute alcohol effects on sexual behavior. Annu Rev Sex Res 2000; 11:92-124.
90 - George WH, Cue Davis K, Schraufnagel TJ, Norris J, Heiman JR, Schacht RL, et al. Later that night: Descending alcohol intoxication and men's sexual arousal. Am J Mens Health 2008, Mar; 2 (1); 76-86.
91 - Krug EG, Mercy JA, Dahlberg LL, Zwi AB. The world report on violence and health. The Lancet 2002; 360 (9339); 1083-8.
92 - Abbey A, Zawacki T, Buck PO, Clinton AM, McAuslan P. Alcohol and sexual assault. Alcohol Research and Health 2001; 25 (1); 43-51.
93 - Mooney J. The hidden figure: Domestic violence in north london. Middlesex University, School of Sociology and Social Policy; 1993ae.
94 - Lancet Editorial. Opening the door on gender-based violence. Lancet 2012, Aug 25; 380 (9843); 703.
95 - The effects of alcohol on penile erection. Electronic ed. New York: Routledge; 2014ad.
96 - Johnson SA. Understanding the role of alcohol during rape: The perfect storm of attention, emotion, & expectancies. International Journal of Emergency Mental Health and Human Resilience 2014; 16 (1); 30-8.
97 - Morrison I, Rumbold JM, Riha RL. Medicolegal aspects of complex behaviours arising from the sleep period: A review and guide for the practising sleep physician. Sleep Med Rev 2014, Jun; 18 (3); 249-60.
98 - Maquet P, Ruby P, Maudoux A, Albouy G, Sterpenich V, Dang-Vu T, et al. Human cognition during REM sleep and the activity profile within frontal and parietal cortices: A reappraisal of functional neuroimaging data. In: ; 2005ag. p. 219-595.
99 - Gumenyuk V, Roth T, Korzyukov O, Jefferson C, Bowyer S, Drake CL. Habitual short sleep impacts frontal switch mechanism in attention to novelty. Sleep 2011, Dec; 34 (12); 1659-70.
100 - Marshall JC, Malerba JR, Schroeder JA. Use of personal EEG monitors in a behavioral neuroscience course to investigate natural setting sleep patterns and the factors affecting them in college students. J Undergrad Neurosci Educ 2011; 10 (1); A65-70.
101 - Shambroom JR, Fábregas SE, Johnstone J. Validation of an automated wireless system to monitor sleep in healthy adults. J Sleep Res 2012, Apr; 21 (2); 221-30.
102 - Griessenberger H, Heib DP, Kunz AB, Hoedlmoser K, Schabus M. Assessment of a wireless headband for automatic sleep scoring. Sleep Breath 2013, May; 17 (2); 747-52.
103 - Dang-Vu TT, Schabus M, Desseilles M, Albouy G, Boly M, Darsaud A, et al. Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci U S A 2008, Sep 30; 105 (39); 15160-5.
104 - Mongrain V, Carrier J, Paquet J, Bélanger-Nelson E, Dumont M. Morning and evening-type differences in slow waves during NREM sleep reveal both trait and state-dependent phenotypes. PLoS One 2011; 6 (8); e22679.
105 - Feinberg I, de Bie E, Davis NM, Campbell IG. Topographic differences in the adolescent maturation of the slow wave EEG during NREM sleep. Sleep 2011, Mar; 34 (3); 325-33.
106 - Viola AU, Chellappa SL, Archer SN, Pugin F, Götz T, Dijk DJ, Cajochen C. Interindividual differences in circadian rhythmicity and sleep homeostasis in older people: Effect of a PER3 polymorphism. Neurobiol Aging 2012, May; 33 (5); 1010.e17-27.
107 - Mistlberger R, Bergmann B, Rechtschaffen A. Period-amplitude analysis of rat electroencephalogram: Effects of sleep deprivation and exercise. Sleep 1987, Dec; 10 (6); 508-22.
108 - Carrier J, Viens I, Poirier G, Robillard R, Lafortune M, Vandewalle G, et al. Sleep slow wave changes during the middle years of life. Eur J Neurosci 2011, Feb; 33 (4); 758-66.
109 - Saletin JM, van der Helm E, Walker MP. Structural brain correlates of human sleep oscillations. Neuroimage 2013, Dec; 83:658-68.
110 - Schabus M, Dang-Vu TT, Heib DP, Boly M, Desseilles M, Vandewalle G, et al. The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front Neurol 2012; 3:40.
111 - Ruch S, Markes O, Duss SB, Oppliger D, Reber TP, Koenig T, et al. Sleep stage II contributes to the consolidation of declarative memories. Neuropsychologia 2012, Aug; 50 (10); 2389-96.
112 - Astori S, Wimmer RD, Lüthi A. Manipulating sleep spindles--expanding views on sleep, memory, and disease. Trends Neurosci 2013, Dec; 36 (12); 738-48.
113 - Thomas Andrillon YNRJSFFCCGTIF. Sleep spindles in humans: Insights from intracranial EEG and unit recordings. The Journal of Neuroscience 2011, Dec 7; 31 (49); 17821.
114 - Cramer Bornemann, Michel A, Mahowald MW. Sleep forensics. In: Principles and Practice of Sleep Medicine. St. Louis: Saunders, Elsivier; 2011. p. 725-33.
115 - Ohayon MM, Mahowald MW, Leger D. Are confusional arousals pathological? Neurology 2014, Aug 26; 83 (9); 834-41.