Parasomnias are defined as unpleasant or undesirable behavioral or experiential phenomena that occur predominately or exclusively during the sleep period. They were initially thought to represent a unitary phenomenon, often attributed to psychiatric disease. Careful clinical and polysomnographic studies have revealed that parasomnias are not a unitary phenomenon, but rather represent a large number of completely different conditions, most of which are diagnosable and treatable. Moreover, most are not the manifestation of psychiatric disorders and are far more prevalent than generally appreciated. Many parasomnias trigger acute and emergent events in sleep because of injurious behavior posing a threat to self or others.
The parasomnias may conveniently be categorized as “primary parasomnias” (disorders of the sleep states per se) and “secondary” (disorders of other organ systems that interfere with the sleep process). The primary sleep parasomnias can be classified according to the sleep state of origin: rapid eye movement (REM) sleep, non-rapid eye movement (NREM) sleep, or miscellaneous (i.e., those not respecting sleep state). The secondary sleep parasomnias can be further classified by the organ system involved.1
The concept that sleep and wakefulness are not invariably mutually exclusive states, and that the various state-determining variables of wakefulness, NREM sleep, and REM sleep may occur simultaneously or oscillate rapidly, is key to the understanding of the primary sleep parasomnias. The admixture of wakefulness and NREM sleep explains confusional arousals (sleep-drunkenness), automatic behavior, or microsleeps.2 The admixture of wakefulness and REM sleep explains cataplexy, wakeful dreaming, hypnagogic hallucinations, lucid dreaming, and the persistence of motor activity during REM sleep (REM sleep behavior disorder).3
The primary sleep parasomnias are clinical phenomena that appear as the brain becomes reorganized across states and therefore are particularly apt to occur during transitions between states. In view of (1) the large number of neural networks, neurotransmitters, and other state-determining substances that must be recruited synchronously for full state declaration and (2) the frequent transitions among states during the wake/sleep cycle, it is surprising that errors in state declaration do not occur more frequently than they do.2
This chapter focuses on the emergent events in sleep triggered by the two most common forms of primary sleep parasomnias (disorders of arousal and REM sleep behavior disorder), followed by a discussion of the forensic issues engendered by these parasomnias.
Disorders of Arousal
Disorders of arousal are NREM sleep parasomnias that occur on a broad spectrum and include confusional arousals, sleepwalking, and sleep terrors. The underlying pathophysiology is state dissociation, whereby neither wake nor NREM has been completely declared. Simply stated, the brain is partially awake and partially in NREM sleep. The result of this mixed state of being is that the brain is awake enough to perform very complex and often protracted motor and/or verbal behaviors, yet asleep enough to not have conscious awareness, thereby abrogating responsibility for these behaviors.
Disorders of arousal share common features. They tend to arise from any stage of NREM sleep, most commonly from slow wave sleep (stage N3, formerly stages 3 and 4 of NREM sleep), and therefore they usually occur in the first third of the sleep cycle and hence rarely during naps. They are common in childhood, usually decreasing in frequency with increasing age.4
Disorders of arousal may be associated with febrile illness, prior sleep deprivation, physical activity, or emotional stress. Medication-induced cases have been reported with sedative–hypnotics, neuroleptics, minor tranquilizers, stimulants, and antihistamines, often in combination with each other.4 Contrary to popular opinion, there is no evidence that alcohol serves to trigger NREM parasomnias.5 Recently, there have been numerous reports of extremely complex behaviors attributed to sedative–hypnotic agents, often resulting in forensic issues.6–14 In some women, disorders of arousal may be exacerbated by pregnancy or menstruation, whereas in others, disorders of arousal may be alleviated by pregnancy, suggesting hormonal influences.4 Underlying predisposing, priming, and precipitating factors have been thoroughly reviewed elsewhere.15
Numerous other sleep disorders that result in arousals (obstructive sleep apnea, nocturnal seizures, or periodic limb movements) may provoke these disorders.16 Sleep-disordered breathing has been found to be more prevalent in both children and adults with disorders of arousal. One recent study found that sleep fragmentation induced by sleep-disordered breathing is more common in adults with disorders of arousal than in normal subjects.17 The combination of frequent arousals and sleep deprivation seen in these other sleep disorders provides fertile ground for the appearance of disorders of arousal. These represent a sleep disorder within a sleep disorder: the clinical event is a disorder of arousal, but the true culprit is a different, unrelated sleep disorder. This would explain the common clinical experience of improvement of disorders of arousal following identification and treatment of obstructive sleep apnea.18 Conversely, effective treatment of obstructive sleep apnea with nasal continuous positive airway pressure (CPAP) may result in disorders of arousal, presumably associated with deep NREM sleep rebound.19,20
Numerous studies have dispelled the myth that persistence of these behaviors beyond childhood or appearance in adulthood is suggestive of underlying psychopathology.21–23 In one study in children, there was an association between disorders of arousal and anxiety.24 These arousals may not be the culmination of ongoing psychologically significant mentation, in that somnambulism can be induced in normal children by standing them up during slow wave sleep, and sleep terrors can be precipitously triggered in susceptible individuals by sounding a buzzer during slow wave sleep.25–28
The mechanism of these disorders is not clear, but clearly both genetic and environmental factors are operant.29 It has been suggested that sleep terrors may be the manifestation of anomalous REM sleep admixed with NREM sleep.30
In addition to the phenomenon of state dissociation, in which two states of being overlap or occur simultaneously, there are likely additional underlying physiologic phenomena that contribute to the appearance of complex motor behaviors during sleep. These include locomotor centers, sleep inertia, and sleep state instability.
Locomotor centers (LMCs), present in multiple sites in the central nervous system, may play a role in the disorders of arousal, which represent motor activity that is dissociated from waking consciousness.31 These areas project to the central pattern generator of the spinal cord, which itself is able to produce complex stepping movements in the absence of supraspinal influence.32 This accounts for the fact that decorticate experimental and barnyard animals are capable of performing very complex, integrated motor acts.33 A biological substrate is further supported by the similarity between spontaneously occurring sleep terrors in humans and “sham rage” induced in animals.34–36 Indeed, human neuropathology may result in similar behaviors.37–41 Dissociation of the LMCs from the parent state of NREM sleep would explain the presence of complex motor behavior seen in disorders of arousal. Spontaneous locomotion following decerebration in cats clearly indicates that such centers, if dysfunctional, release motor activity into the sleeping state.42,43 Single photon emission computed tomography (SPECT) study of a sleepwalker suggested activation of thalamocingulate pathways and persisting deactivation of other thalamocortical arousal systems, resulting in a dissociation between body sleep and mind sleep.44
Sleep inertia (also termed sleep drunkenness) refers to a period of impaired performance and reduced vigilance following awakening from the regular sleep episode or from a nap. This impairment may be severe, last from minutes to hours, and be accompanied by polysomnographically recorded microsleep episodes.45 Support of a gradual disengagement from sleep to wakefulness comes from neurophysiologic studies in animals and cerebral blood flow studies in humans.46–49 There appears to be great inter-individual variability in the extent and duration of sleep inertia, both following spontaneous awakening after the major sleep period and following naps. Sleep inertia likely plays a role in the susceptibility to disorders of arousal.46
Sleep State Instability
The cyclic alternating pattern (CAP) may also play a role in the etiology of disorders of arousal.50 CAP is a physiological component of NREM sleep and is functionally correlated with long-lasting arousal oscillations. CAP is a measure of NREM instability with high level of arousal oscillation.51 More sophisticated monitoring techniques such as topographical EEG mapping suggest that there may be more delta EEG activity prior to the onset of sleep terrors.52 While there is no difference in the macrostructural sleep parameters between patients with disorders of arousal and controls, patients with disorders of arousal have been found to have increases in CAP rate, in the number of CAP cycles, and in arousals with EEG synchronization. An increase in sleep instability and in arousal oscillation is a typical microstructural feature of slow wave sleep-related parasomnias and may play a role in triggering abnormal motor episodes during sleep in these patients.53,54 Microarousals preceded by EEG slow wave synchronization during NREM sleep are more frequent in patients with sleep walking and sleep terrors than in controls. This supports the existence of an arousal disorder in these individuals.53 Although some have reported hypersynchronous delta activity on polysomnographs of young adults with sleepwalking, this has not been the experience of others.55,56 EEG spectral analysis studies indicate that patients with sleepwalking demonstrate an instability of slow wave sleep, particularly in the early portion of the sleep period.57 Impairment of efficiency of inhibitory cortical circuits during wakefulness has also been reported.58
Disorders of arousal occur on a broad spectrum ranging from confusional arousals, through somnambulism (sleepwalking), to sleep terrors (also termed pavor nocturnus and, erroneously, incubus or succubus). Some take the form of “specialized” behaviors (discussed later) such as sleep-related eating and sleep-related sexual activity, executed without conscious awareness.
These are often seen in children and are characterized by movements in bed, occasionally thrashing about, or inconsolable crying.59 “Sleep drunkenness” is probably a variation on this theme.60 The prevalence of confusional arousals in adults is approximately 4%.61
Sleepwalking is prevalent in childhood (1% to 17%), peaking at 11 to 12 years of age, and is far more common in adults (nearly 4%) than generally acknowledged.61–64 Sleepwalking may be either calm or agitated, with varying degrees of complexity and duration.
The sleep terror is the most dramatic disorder of arousal. It is frequently initiated by a loud, blood-curdling scream associated with extreme panic, followed by prominent motor activity such as hitting the wall, running around or out of the bedroom, even out of the house, resulting in bodily injury or property damage. A universal feature is inconsolability. Although the victim appears to be awake, he or she usually misperceives the environment, and attempts at consolation are futile and may serve only to prolong or even intensify the confusional state. Some degree of perception may be evident—for example, running for and opening a door or window. Complete amnesia for the activity is typical, but it may be incomplete.28,65,66 The intense endogenous arousal and exogenous unarousability constitute a curious paradox. As with sleepwalking, sleep terrors are much more prevalent in adults than generally acknowledged (4% to 5%).67 Although usually benign, these behaviors may be violent, resulting in considerable injury to the victim or others or damage to the environment, occasionally with forensic implications (see discussion below).
Specialized Forms of Disorders of Arousal
Sleep-Related eating disorder
The sleep-related eating disorder, characterized by frequent episodes of nocturnal eating, generally without full conscious awareness and often not associated with waking eating disorders, likely represents a specialized form of disorder of arousal. Formal sleep studies are indicated, as sleep-related eating may be the manifestation of other sleep disorders such as restless legs syndrome, periodic limb movements of sleep, or obstructive sleep apnea, all of which predispose to arousal.68 Nocturnal binging may be induced by benzodiazepine medication, and sleep-related eating has been associated with zolpidem and olanzapine administration.10,11,69,70 The sleep-related eating disorder is distinct from the night-eating syndrome, as the latter is characterized by morning anorexia, evening hyperphagia (while awake), and insomnia and is associated with hypothalamic-pituitary axis abnormalities.71–73
Inappropriate sexual behaviors occurring during the sleep state without conscious awareness, presumably the results of and admixture of wakefulness and sleep, have been reported.74 Such behaviors may be autoerotic or engage the bed partner, resulting in feelings of guilt, shame, or depression, and may have medicolegal implications.75
Isolated, often bizarre, sleep-related events may be experienced by perfectly normal people, and most do not warrant further extensive or expensive evaluation. The initial approach to the complaint of unusual sleep-related behavior is to determine whether further evaluation is necessary. The patient should be queried regarding the exact nature of the events. Because many of these episodes may be associated with partial or complete amnesia, additional descriptive information from a bed partner or other observer may prove invaluable. Home videotapes of the clinical event may be quite helpful. In general, indications for formal evaluation of parasomnias include behaviors that:1
• are potentially violent or injurious
• are extremely disruptive to other household members
• result in the complaint of excessive daytime sleepiness
• are associated with medical, psychiatric, or neurological symptoms or findings
Formal polysomnographic studies, appropriately performed, will provide direct or indirect diagnostic information in the majority of cases. This is of more than academic interest, as most of these conditions are readily treatable. Emphasis must be placed on the types of studies required; routine polysomnograms performed for conventional sleep disorders are inadequate. In addition to the physiologic parameters monitored in the standard polysomnogram, there must be an expanded EEG montage and continuous audiovisual monitoring.55,76 Observation by an experienced technologist is invaluable. Multiple night studies may be required to capture an event. Interpretation should be made by a polysomnographer experienced in these disorders. Sleep deprivation prior to formal polysomnographic study may increase the likelihood of capturing an event in the sleep laboratory.77 Unattended studies have no role in the evaluation of parasomnias.78 Formal sleep studies are indicated to establish a clinical diagnosis but are of no utility in forensic cases (discussed below).
Numerous other conditions may perfectly mimic the disorders of arousal. These include obstructive sleep apnea, REM sleep behavior disorder, nocturnal seizures, psychogenic dissociative disorders, malingering, or psychopathy.79–81 NREM parasomnias may be particularly difficult to differentiate from nocturnal epileptic phenomena82 (see Chapter 16). There may be an association between disorders of arousal and migraine headache,83 neurofibromatosis type 1,84 or Tourette’s syndrome.85,86 In children unable to verbalize, nocturnal cluster or migraine headaches may mimic sleep terrors.87 Obstructive sleep apnea may be associated with and even present as disorders of arousal.81,88,89
Given the high prevalence of these disorders in normal individuals, formal sleep center evaluation should be confined to the situations listed above. Treatment is often not necessary. Reassurance of their typically benign nature, lack of psychological significance, and the tendency to diminish over time is often sufficient. Objective studies documenting medication efficacy are lacking. Tricyclic antidepressants and benzodiazepines may be effective and should be administered if the behaviors are dangerous to person or property or extremely disruptive to family members.60 Paroxetine and trazodone have been reported to be effective in isolated cases of disorders of arousal.90,91 Nonpharmacologic treatment such as psychotherapy,27 progressive relax-ation,92 or hypnosis93 is recommended for long-term management. Anticipatory awakening has been reported to be effective in treating sleepwalking in children.94 The avoidance of precipitants such as drugs and sleep deprivation is also important.
Sleep-related eating may respond to topiramate or dopaminergic agents.68
Systematic studies of pharmacologic treatment of sleep sex are lacking.
REM sleep behavior disorder
Numerous physiologic phenomena occur during REM sleep and fall into two categories: (1) tonic (appearing throughout a REM period) and (2) phasic (occurring intermittently during a REM period). Tonic elements include electromyographic (EMG) suppression, low voltage desynchronized EEG, high arousal threshold, hippocampal theta rhythm, elevated brain temperature, poikilothermia, olfactory bulb activity, and penile tumescence. Phasic elements include REMs, middle ear muscle activity, tongue movements, somatic muscle-limb twitches, variability of autonomic activity (cardiac and respiratory), and ponto-geniculo-occipital spikes (PGO). It is not known whether dreaming occurs tonically or phasically during REM sleep.95
The tonic and phasic neurophysiologic processes underlying each state can be variously dissociated and recombined across states.96 For REM sleep, the processes that generally occur in concert may also be seen in dissociated form—both experimentally (e.g., REM sleep-deprived animals with PGO spikes occurring in NREM sleep and wakefulness)97 and in human and animal disease (narcolepsy). In narcolepsy, the best-understood dissociated state, the sleep attacks, hypnagogic hallucinations, sleep paralysis, cataplexy, and automatic behavior each represent the intrusion or persistence of one state of being into another (i.e., cataplexy may be the inappropriate isolated intrusion of REM sleep atonia [REM atonia] into wakefulness, usually induced by an emotionally laden event).98,99
The most common and best-studied REM sleep parasomnia is the REM sleep behavior disorder (RBD). In patients with RBD, somatic muscle atonia, one of the defining features of REM sleep, is absent, permitting the acting out of dream mentation (or the dreaming out of fictive movements), often with violent or injurious results.100
A recent phone survey of over 4,900 individuals between the ages of 15 and 100 years of age indicated an overall prevalence of violent behaviors in general during sleep of 2%, one quarter of which were likely due to RBD, giving an overall prevalence of RBD at 0.5%.101 Another survey estimated the prevalence of REM sleep behavior to be 0.38% in elderly individuals.102
The generalized atonia of REM sleep results from active inhibition of motor activity by pontine centers of the peri-locus ceruleus region that exert an excitatory influence upon the reticularis magnocellularis nucleus of the medulla via the lateral tegmento-reticular tract. The reticularis magnocellularis nucleus, in turn, hyperpolarizes spinal motoneuron postsynaptic membranes via the ventrolateral reticulospinal tract.103,104 Loss of muscle tone during REM sleep is very complex and has been shown to be due to a combination of inactivation of brain stem motor inhibitory systems and inactivation of brain stem facilitatory systems.105,106 Normally, the atonia of REM sleep is briefly interrupted by excitatory inputs that produce the rapid eye movements and the muscle jerks and twitches characteristic of REM sleep.107–109 REM atonia is felt to be mediated by glycine and may be influenced by medullary enkephalinergic neurons.110,111 (The prevailing hypothesis that REM atonia is due to glycinergic inhibition has recently been questioned.112)
Neuroimaging studies indicate dopaminergic abnormalities in RBD. SPECT studies have found reduced striatal dopamine transporters,113,114 and decreased striatal dopaminergic innervation has been reported.115 Decreased blood flow in the upper portion of the frontal lobe and pons has been reported,116 as has functional impairment of brain stem neurons.117 PET and SPECT studies have revealed decreased nigrostriatal dopaminergic projections in patients with multiple system atrophy and RBD.118 Impaired cortical activation as determined by EEG spectral analysis in patients with idiopathic RBD supports the relationship between RBD and neurodegenerative disorders.119
RBD in humans occurs in both an acute and chronic form. Until recently, most reported cases of acute transient RBD fell in the toxic/metabolic category, with the best-studied conditions being the withdrawal states (most commonly involving ethanol).120 In 1881 Lasegue postulated that dreams and hallucinations may have a common mechanism.121 Wakeful dreaming has been considered as an etiology for the vivid visual hallucinations associated with delirium tremens.122–124 Although controversial, dissociated wakeful-REM phenomena may play a major role in delirium tremens. Japanese investigators in 1975 formally used the name “Stage 1-REM with tonic EMG” to describe a polysomnographic and behavioral condition seen in alcohol and meprobamate withdrawal that appeared to represent REM sleep without atonia.125 The polysomnographic and detailed clinical description of delirium tremens in 1966 by Gross et al122 resembles those observed in patients with RBD. Comparable patterns have been described with nitrazepam withdrawal and biperiden intoxication.126,127
Currently, the most common cause of acute REM sleep without atonia and RBD may be iatrogenic. Acute RBD is almost always induced by medications (most commonly tricyclic antidepressants, monoamine oxidase inhibitors, SSRIs, or SNRIs) or associated with withdrawal (alcohol, barbiturate, or meprobamate).100,128 Excessive caffeine ingestion has also been implicated,129 as has chocolate ingestion.130
The chronic form is most often either idiopathic or associated with neurological disorders. Each basic category of neurological disease (vascular, neoplastic, toxic/metabolic, infectious, degenerative, traumatic, congenital, and idiopathic) could be expected to result in RBD. Table 7–1 lists reported associations with RBD.131 A familial association has been documented.132 Interestingly, spontaneously occurring idiopathic RBD has been reported in dogs and cats.133,134
Table 7–1 Conditions Associated with RBD131
Amyotrophic lateral sclerosis
Brain stem parainfectious encephalitis (both RBD and narcolepsy)
Group A xeroderma pigmentosum
Implantation of subthalamic stimulator for Parkinson’s disease (isolated event)
Medication (particularly tricyclic antidepressants and SSRIs)
Machado-Joseph disease (spinocerebellar ataxia type 3)
Paraneoplastic (Anit-Ma2) encephalitis (both RBD and narcolepsy)
Parkinson’s disease associated with parkin mutations
Synucleinopathies (Parkinson’s disease, multiple system atrophy, dementia with Lewy
body disease, pure autonomic failure)
Tauopathies (Alzheimer’s disease, progressive supranuclear palsy, corticobasal degeneration)
Voltage-gated potassium channel antibody-associated limbic encephalitis
The overwhelming male predominance of REM sleep behavior disorder (not seen in the associated neurodegenerative disorders) raises the intriguing question of hormonal influences, as suggested in male-aggression studies in both animals and humans.135–137 Another possible explanation for the male predominance is sex differences in brain development and aging.138–140 There is evidence for a sex difference on the effects of sex steroids on the development of the locus ceruleus in rats.141 However, serum sex hormone levels are normal in idiopathic RBD or RBD associated with Parkinson’s disease.142,143 Recent studies suggest that RBD may be more common in women than previously thought.144,145
The cases reported to date indicate strikingly similar clinical features.100 The presenting complaint is vigorous sleep behaviors usually accompanying vivid striking dreams. These behaviors may result in repeated injury, including ecchymoses, lacerations, and fractures. Some of the self-protection measures taken by the patients (tethering themselves to the bed, using sleeping bags or pillow barricades, or sleeping on a mattress in an empty room) reveal the recurrent and serious nature of these episodes.146,147 The potential for injury to self or bed partner raises interesting and difficult forensic medicine issues.148 RBD may have serious psychological ramifications for the spouse: one woman threatened suicide because her husband with RBD could not share their bed.149
Idiopathic RBD is commonly a chronic progressive disorder, with increasing complexity, intensity, and frequency of expressed behaviors, but the symptoms may fluctuate over time.150 Although irregular jerking of the limbs may occur nightly, the major movement episodes appeared intermittently with a frequency minimum of once in 2 weeks to a maximum of four times nightly on 10 consecutive nights. Observed somniloquy runs the spectrum from short and garbled to long-winded and clearly articulated. Angry speech with shouting, but also laughter, can emerge. One patient appeared to have a dissociated RBD-lucid dream state in that he could carry on lengthy and coherent conversations with his wife and family while dreaming and incorporate the conversational material into his dreams. Most patients complained of sleep injury but rarely of sleep disruption.
In RBD patients, arousal from sleep to alertness and orientation is usually rapid and accompanied by complete dream recall (very unlike the confusional arousals observed in the disorders of arousal such as sleepwalking or sleep terrors). After awakening, behavior and social interactions are appropriate, mitigating against a NREM sleep relationship, delirious states, or ictal/post-ictal phenomena, but rather further supporting a REM sleep phenomenon. It should be emphasized that the behaviors, although complex and violent, are of briefer duration than those seen in the disorders of arousal. In some individuals, the clinical features contain elements of both RBD and disorders of arousal (see the section on RBD variations below).
A singular feature of the dream-enacted episodes in this group of patients is that customary dreams are generally not being played out; rather, distinctly altered, stereotypical, repetitive, and “action-packed” dreams are put on display. The violence of the sleep-related behavior is often discordant with the waking personality. The increased aggressive dream content experienced by patients with RBD is not associated with increased daytime aggressiveness.151
RBD and extrapyramidal disease
As more patients with “idiopathic” RBD are carefully followed over time, it is becoming clear that the majority will eventually develop neurodegenerative disorders, most notably the synucleinopathies (Parkinson’s disease, multiple system atrophy—including olivopontocerebellar degeneration and the Shy-Drager syndrome, dementia with Lewy body disease, or pure autonomic failure). RBD may be the first manifestation of these conditions and may precede any other manifestation of the underlying neurodegenerative process by more than 10 years.152
Systematic longitudinal study of patients with such neurological syndromes indicates that RBD and REM sleep without atonia may be far more prevalent than previously suspected. Although the prevalence of RBD in Parkinson’s disease is unknown, subjective reports indicate that 25% of patients with Parkinson’s disease have behaviors suggestive of RBD or sleep-related injurious behaviors, and polysomnographic studies found RBD in up to 47% of patients with Parkinson’s disease with sleep complaints.153–156 In one large series of patients with multiple system atrophy, 90% were found to have REM sleep without atonia and 69% had clinical RBD,157 and in another, nearly half had RBD.158 The presence of RBD may differentiate pure autonomic failure from multiple system atrophy with autonomic failure.159 The finding of incidental Lewy body disease in one patient asymptomatic for Parkinson’s disease suggests that this condition may explain idiopathic RBD in some older patients.160 The presentation of RBD and dementia is suggestive enough of dementia with Lewy body disease that RBD has been proposed as one of the core diagnostic features of dementia with Lewy body disease.161 The relationship between neurodegenerative disorders and RBD has been recently thoroughly reviewed.152
The waking motor impairments of Parkinson’s disease may improve or even normalize during REM sleep-related movements in Parkinson’s disease-RBD patients. In a study of 53 patients with Parkinson’s disease-RBD who slept with bed partners, 100% reported improvement of at least one of the following during RBD episodes: faster, stronger or smoother movements; more intelligible, louder, or better-articulated speech; or normalization of facial expression. Furthermore, 38% of bed partners reported that movements were “much better” even in the most disabled Parkinson’s disease patients. The responsible mechanisms for these fascinating observations remain obscure.162
RBD and Narcolepsy
RBD may also be yet another manifestation of narcolepsy: it is present in over half of patients with narcolepsy, may be an early symptom in childhood narcolepsy, and may even be the presenting symptom in narcolepsy.163–167 Furthermore, tricyclic antidepressants, MAOIs, SSRIs, and SNRIs, prescribed to treat cataplexy, can trigger or exacerbate RBD in this population. The demographics (age and sex) of RBD in narcolepsy conform to those of narcolepsy, indicating that RBD in these patients is yet another manifestation of the state boundary dyscontrol seen in narcolepsy.168
Routine medical history-taking should include questions that screen for abnormal sleep movements and altered dreams, especially in older adults, patients of any age with acute or chronic central nervous system disorders (particularly those who have neurological conditions that predispose to RBD such as Parkinson’s disease or multiple system atrophy), and patients receiving psychoactive medications known to trigger RBD. The diagnosis of RBD may be suspected on clinical grounds, but polysomnographic confirmation is mandatory. The complaint of sleep-related injurious or violent behaviors should be taken very seriously. Reported injuries in our series include lacerations and fractures to the patient and/or bed partner. RBD has also resulted in subdural hematomas and other serious injuries.169–171
Detailed polysomnographic data in these patients have been reported elsewhere.95 The overall sleep architecture is usually normal, with the expected cycling of NREM and REM sleep. Most of our subjects had excessive slow wave sleep for age. The conventional scoring parameters of Rechtschaffen and Kales172 must be modified to allow for the persistence of EMG tone during epochs that are otherwise clearly REM sleep. In addition to the intermittent absence of atonia, there are varying amounts of limb twitching (usually far in excess of that observed in normal REM sleep), gross body movements, and complex, often violent behaviors that correlate with reported dream mentation.
A curious feature of the chin EMG and extremity movements seen during the REM period is the variability of involvement and distribution. The submental EMG may be augmented without body movements or may be atonic despite flailing extremities. The arms and legs often move independently, necessitating monitoring of all limbs. Some patients demonstrated persistent (over the span of several years) lateralization of limb EMG activity or also predominant upper or lower extremity movements. Most all patients displayed prominent aperiodic movements of all extremities in every conceivable combination during all stages of NREM sleep. RBD patients may also show conventional periodic movements of sleep usually involving the legs during both NREM and REM sleep, infrequently associated with arousals. Prolonged periods of aperiodic and periodic movements restricted to the arms were noted occasionally.
The polygraphic marker of RBD is REM without atonia (RWA) (Fig. 7–1). It must be remembered that RWA is a polysomnographic observation and that RBD is a clinical syndrome of dream-enacting behavior associated with RWA. RWA often occurs without clinical symptoms and therefore, of itself, does not establish a diagnosis of RBD. The diagnosis of RBD requires both the clinical history of dream-enacting behavior coupled with the polysomnographic finding of RWA. Some cases of RWA may represent “preclinical” RBD, and RWA is most commonly seen in association with medications, particularly SSRIs and SNRIs.
The minimum diagnostic criteria for RBD we formulated can be satisfied in either of two ways:
a) History of problematic sleep behavior that is
i) harmful or potentially harmful, or
ii) disruptive of sleep continuity, or
iii) annoying to self and/or bed partner
AND any polysomnographic abnormality listed below.
b) No history of problematic sleep behaviors AND
POLYSOMNOGRAPHY: At least one of the following during REM sleep:
i) excessive augmentation of chin EMG tone
ii) excessive chin and/or limb EMG twitching, irrespective of chin EMG tone
VIDEOTAPING OF BEHAVIOR: record at least one of the following during REM sleep:
i) excessive limb and/or body jerking
ii) complex movements
iii) vigorous or violent movements
The determination of what constitutes either excessive EMG augmentation, EMG twitching, or limb jerking requires both meticulous execution of standard recording techniques and an experienced polysomnographer. Studies are underway to quantify RWA.
1. Review of sleep/wake complaints (from patient and/or bed partner)
2. Neurologic and psychiatric examinations
3. Sleep laboratory study that includes continuous videotaping of behavior during standard polygraphic monitoring of the electro-oculogram (EOG), EEG, EMG (chin, bilateral extensor digitorum and anterior tibialis muscles), electrocardiogram (EKG), and nasal air flow.172 An experienced and formally trained technician makes written observations of ongoing behaviors. It is encouraged that such technicians be certified by the American Board of Registered Polysomnographic Technologists (RBPT).
4. Because of the association between RBD and narcolepsy, a Multiple Sleep Latency Test is routinely administered the day following the overnight sleep study.173
More extensive neurological evaluations including multimodal evoked potentials, brain imaging by magnetic resonance imaging (MRI) or computerized axial tomography (CAT), or comprehensive neuropsychological testing by methods previously reported174 are indicated only if there is a suggestion of neurological dysfunction by history or neurological examination.
RBD can masquerade as many other conditions. Most conditions in this differential diagnosis represented an initial clinical misdiagnosis in our series, leading to inappropriate and ineffective treatment. The differential diagnosis of these disorders has been reviewed elsewhere.78 Nocturnal seizures and movement disorder are discussed elsewhere in this volume (Chapters 16 and 17). It should be remembered that the clinical event (arousal) may not be primary, but rather triggered by another, underlying sleep disorder (i.e., apnea leading to arousal leading to sleep terror). Nocturnal behaviors induced by obstructive sleep apnea or sleep-related seizures can perfectly mimic those of RBD.175–177 “Overlap” parasomnias (discussed below) are characterized by the clinical history suggestive of sleepwalking/sleep terrors with polysomnographic features of motor disinhibition during both REM and NREM sleep.178 Nocturnal panic disorder is poorly understood and requires more study. It is well established that psychogenic dissociative disorders may arise predominately or exclusively from the sleep period.179 Finally, our group has seen extremely violent sleep-period behavior felt to represent malingering.180
The acute form is self-limited following discontinuation of the offending medication or completion of withdrawal. About 90% of patients with chronic RBD respond well to clonazepam administered a half-hour prior to sleep time. The dose ranges from 0.5 to 2.0 mg, and there has been little, if any, tendency to develop tolerance, dependence, abuse, or adverse sleep effects despite years of continuous administration and efficacy.146,181 Melatonin at doses up to 12 mg at bedtime or pramipexole may also be effective.182–185 Although tricyclic antidepressants may sometimes induce or potentiate RBD, imipramine has been reported effective in three clonazepam-resistant cases.186 Likewise, there are reports of response to an SSRI (paroxetine).187,188 Carbamazepine has been effective in one case.189 Levodopa may be effective, particularly in cases where RBD is the harbinger of Parkinson’s disease.190 There have been anecdotal reports of response to gabapentin, MAOIs, donepezil, and clonidine.191,192 In RBD associated with narcolepsy, the tricyclic antidepressants or MAOIs administered for cataplexy may be continued and clonazepam added.168 The treatment of medication-induced or Parkinson’s disease-associated RBD is the same as for idiopathic RBD.193 Pallidotomy has been effective in one case of RBD associated with Parkinson’s disease, whereas chronic bilateral subthalamic stimulation was not.194–196 Interest-ingly, an isolated episode of RBD has been reported immediately following left subthalamic electrode implantation for the treatment of Parkinson’s disease.197
Underlying obstructive sleep apnea should be ruled out before prescribing clonazepam.198 Despite the often-dramatic clinical improvement with medications, the effect of clonazepam or melatonin on the polysomnographic features of RBD is unimpressive. (Melatonin may restore some of the tonic REM atonia, and clonazepam may reduce excessive phasic EMG activity during REM sleep—but clearly incompletely).199,200 This raises the possibility that these medications may act preferentially upon the locomotor systems rather than those affecting REM atonia.201
The other essential therapeutic intervention concerns environmental safety. Clonazepam is not failsafe: one patient injured himself during a violent dream one year after initiating very satisfactory pharmacotherapy. There was no recurrence during the ensuing 5 months, even though the dose was not increased. Therefore, potentially dangerous objects, particularly firearms, should be removed from the bedroom, cushions positioned around the bed, consideration given to place the mattress upon the floor, and windows protected. We anticipate some cases in which drug intolerance or ineffectiveness will lead to discontinuation, requiring maximal environmental safety.
Parasomnia overlap syndrome
There is a subgroup of parasomnia patients with both clinical and polysomnographic features of both RBD and disorders of arousal (sleepwalking/sleep terrors). These cases demonstrate motor–behavioral dyscontrol extending across NREM and REM sleep and suggest the possibility of a unifying hypothesis for disorders of arousal and RBD. The primary underlying feature is motor disinhibition during sleep—when predominately during NREM sleep manifesting as disorders of arousal, and when predominately during REM sleep manifesting as RBD—with the parasomnia overlap syndrome occupying an intermediate position, with features of both.178
This condition is characterized by generalized overactivity associated with loss of slow wave sleep, mental oneiricism (inability to initiate and maintain sleep with wakeful dreaming), and marked motor and autonomic sympathetic activation seen in such diverse conditions as delirium tremens, Morvan’s fibrillary chorea, and fatal familial insomnia.202 Oneiric dementia is likely a related condition.203 Agrypnia excitata is similar to “status dissociatus,” which may be the most extreme form of RBD, appearing to represent the complete breakdown of state-determining boundaries. Clinically, patients with status dissociatus, by behavioral observation, appear to be either awake or asleep; however, clinically, their outward expression of sleep is very atypical, characterized by frequent muscle twitching, vocalization, and reports of dream-like mentation upon spontaneous or forced awakening. Polysomnographically, there are no features of either conventional REM or NREM sleep; rather, there is the simultaneous admixture of elements of wakefulness, REM sleep, and NREM sleep. “Sleep” may be perceived as “normal” and restorative by the patient despite the nearly continuous motor and verbal behaviors and absence of polysomnographically defined REM or NREM sleep. Conditions associated with status dissociatus include protracted withdrawal from alcohol abuse, narcolepsy, olivopontocerebellar degeneration, and prior open heart surgery.204
The fact that violent or injurious behaviors may arise in the absence of conscious wakefulness raises the crucial question of how such complex behaviors can occur. The widely held concept that the brain stem and other more “primitive” neural structures primarily participate in elemental/vegetative rather than behavioral activities is inaccurate: there is clear evidence that highly complex emotional and motor behaviors may originate from these more primitive structures, without involvement of more rostral neural structures.
Ethology is the study of whole patterns of animal behavior under natural conditions in a manner that highlights the functions and the evolutionary process of those patterns. With an ever-increasing physiological approach through the application of refined and elegant laboratory research techniques to animal behavior, opportunities of cross-fertilization of neurobiology and ethology have coalesced to develop neuroethology.205 An important behavior type in ethology is the fixed action pattern (FAP), which is an instinctive indivisible behavioral sequence that when initiated will run to full completion. FAPs are invariant and are produced by a neural network known as the innate releasing mechanism in response to an external stimulus known as a sign stimulus. FAPs are ubiquitous in the animal kingdom and are seen from invertebrates to higher primates. Movements resulting in FAPs may be initiated by central pattern generators (CPGs), an anatomic entity well recognized by neurologists.
Tassinari et al, in their neuroethologic approach, recognized that motor events related to certain epileptic seizures and parasomnias share very similar features suggestive of stereotyped inborn FAPs perhaps initiated by CPGs.206 Furthermore, Tassinari recognized CPGs as genetically determined neuronal aggregates in the mesencephalon, pons, and spinal cord that from an evolutionary perspective were linked with innate primal behaviors essential for survival (e.g., feeding, locomotion, reproduction). In higher primates, CPGs are inhibited by the influence of neocortical control. Keep in mind that many of the CPGs are located in the brain stem and in proximity to processes that govern the wake, NREM sleep, and REM sleep transitions. Despite diurnal neocortical inhibition, Tassinari et al provide a neuroethologic model whereby both epilepsy and sleep can lead to a temporary loss of control of the neo-mammalian cortex that is provided a pathway through a common arousal platform initiated by CPGs, which in turn triggers these FAPs, resulting in the abrupt onset of bizarre motor and/or emotional expressions that are uncharacteristic of the awake neocortical-mediated diurnal behaviors.
In essence, the behaviors of primary sleep parasomnias are FAPs that are mediated through CPGs, which may in turn result in serious injury to self or to others. Importantly, the victim is almost always someone in proximity: victims are not “sought” out. The behaviors associated with sleepwalking may be protracted, whereas those associated with RBD tend to be very quick and brief. Sleepwalkers have their eyes open, allowing them to navigate complex paths; patients with RBD have their eyes closed, so they tend not to get very far before hitting something, which causes them to awaken. Upon awakening, sleepwalkers tend to be confused, disoriented, and unable to remember complex dream imagery, while those with RBD are immediately awake, alert, and oriented, often with vivid recall of a dream corresponding to the observed behavior.
Prevention of injury with medication and environmental safety measures is most important. Sleeping in a room on the first floor or in the basement and alarming the room or dwelling are prudent actions. It must be remembered that previously benign sleepwalking episodes are no guarantee that a violent event may not occur in the future. Also, medication is not failsafe. Lastly, once the individual has left the bedroom and steps out of the home, the compromise in safety involves not just the individual patient but now the general public, and proactive measures should be accordingly considered.
Individuals seeking medical attention for any type of injury should be queried as to the circumstances of the event. Could the car crash have been related to falling asleep at the wheel or to an episode of sleep-driving? Could the fall down the stairs or out the window have occurred while sleepwalking? Inasmuch as sleep is an anesthetic state, very painful injuries may not be appreciated until awakening after completion of the behavior. Some fatal parasomnias are undoubtedly deemed suicides, rather than correctly attributed to an untoward tragic consequence of sleepwalking.207
It should be noted that RBD and other parasomnias may appear in the hospital setting. In one series of 20 patients experiencing parasomnias in intensive care units, 17 had RBD (3 developed RBD during admission for neurological disorders, 1 was admitted as a consequence of RBD, and 13 displayed pre-existing RBD during the course of hospitalization for other medical conditions).208
Definition: “The application of the principles and tools of neuroscience as applied to Somnology and Sleep Medicine that have been widely accepted under international scientific peer-review to the investigation in understanding unusual, irrational, and/or bizarre human behaviors associated with alleged criminal behavior which is to undergo further examination in a conflict resolution legal atmosphere and/or courtroom”
M.A. Cramer Bornemann
WORLDSLEEP 07, Fifth Congress of the WFSRSMS, Cairns, Australia
Sleep disorders, most notably parasomnias, have become increasingly invoked as a legal defense to explain violent, reckless, or asocial behaviors that have resulted in a broad spectrum of criminal allegations. Sleep medicine professionals are often asked to render an opinion as to whether a given alleged criminal act could possibly have been committed during an admixed period of wake/sleep, and therefore have been performed without conscious awareness and hence ultimately without culpability. Alternatively, a prosecutor may request a medical expert opinion to combat an opposing counsel’s attempt to use a largely improbable, if not entirely bogus, sleepwalking defense as a means to secure a full acquittal in a criminal case.
Recent advances in neuroscience are providing clues regarding how our brains affect our minds and behaviors. Neuroscience has developed powerful tools to investigate the neural activity underlying elementary aspects of physiology and behavior, which has been extended to encompass research into memory, executive function, and higher levels of cognition. Such innovative tools have also been applied to understanding the pathophysiology, diagnosis, and management of many clinical conditions, including those found in sleep medicine.
Unfortunately, conflicts arise with escalating tension as law in many ways is the polar opposite of neuroscience. Law usually requires dichotomies with an exacting all-or-none approach, whereas the modern scientist is comfortable describing non-static systems in multiple intersecting dimensions. Courts reach decisions savoring the adversarial bipartisan environment, while much of science is consensus-driven and prepared with statistics on groups. Law covets tradition embodying centuries of thought and beliefs that resists change; science values rapidly accelerating innovation. Lastly, law accepts cultural assumptions and common sense that is largely based upon casual observation and unexamined conjecture.
Advances in cognitive neuroscience have clearly established that consciousness (not unlike wakefulness and sleep) exists on a broad spectrum and certainly is not dichotomous. The element of consciousness is an essential feature addressed in the courtroom of every criminal case, placing neuroscientific principles at the core of criminal law. In many ways the admixed states resulting from incomplete transitions between sleep and wakefulness are unique experiments in nature, providing the clinician scientist a direct window into the evanescent spectrum of consciousness with its associated expressions of human behavior. Thus, those asked to become engaged in sleep forensics would appear to be well poised at this intersection of law and neuroscience. But to be adequately equipped for the developing field of sleep forensics, a medical expert called upon to investigate criminal allegations should not only be well versed in clinical sleep medicine but also be familiar with (1) the evolution of legal thought, (2) the neuroscience of consciousness, (3) the clinical guidelines to assist in the determination of purported acts of violence arising from sleep, and (4) the guidelines for the role of sleep medicine in expert witness testimony. Such an approach will not only enhance the role of the sleep medicine specialist as a resource to the legal community but will also begin to develop the framework for further research, particularly in parasomnias, and to facilitate the discourse related to the social implications concerning advances in cognitive neuroscience.
Evolution of Legal Thought
The first appearance of the “sleepwalking defense” in an American court of law came in Tirrell v Massachusetts in 1846.209 In the mid- to late-1800s there were no plausible medical explanations to account for sleepwalking, let alone complex violent behaviors apparently arising from sleep that led to misfortune. Though such tragic circumstances resulting in death appear to be exceedingly rare, when presented to a court of law, as in HMS Advocate v Fraser (1878)210 and Fain v Commonwealth (1879),211 a homicide charge may be acquitted by defense pleas of a temporary “defect of reason” or “disease of mind.”
The legal community’s perspective towards sleep began to shift in 1968 with Roger Broughton’s seminal publication characterizing the relationship between somnambulism, nightmares, confusional states of arousal, and REM sleep.25 By creating a clear demarcation between sleep disorders and other medical or psychiatric conditions, this appears to be the first scientific sleep-related publication with direct legal implications—as supported by Regina v Parks (1992).212 It was documented in this criminal case that the defendant drove in the early morning hours to the house of his wife’s parents. Apparently while still sleepwalking, he was provoked to attack due to the in-laws’ physical contact; he attacked both of them with a kitchen knife, killing the mother and leaving the father seriously injured.213 The defendant was acquitted in a complete defense of all criminal charges, including homicide, in a courtroom jury trial; the rendering was eventually upheld by a landmark Supreme Court of Canada decision not to characterize sleepwalking as a mental health disorder.
Regina v Park helped to usher the sleepwalking defense into the modern era, but the interface between law and science remains contentious due in part to conflicting philosophies, methodologies, and goals. Nonetheless, there is now a greater degree of civic responsibility placed upon the field of sleep medicine, given the legal community’s growing recognition of sleep’s broad implications on behavior (or lack thereof) ranging from parasomnias, to cognitive impairment related to sleep deprivation, to pharmaceutical toxicity, just to name a few. Thus, sleep forensics was born of the need to address civic responsibility while appreciating that advances in neuroscience have social implications. It thereby attempts to facilitate discourse between the two disparate disciplines of law and sleep medicine within currently held rules and regulations of the legal system.
Anglo-American law has traditionally defined criminal offenses as requiring both an actus reus (guilty act) and a mens rea (guilty mind). The state (or prosecution) must prove both elements to secure a conviction. Regrettably, it has proven exceedingly difficult to establish either the precise meaning of these terms or the relationships connecting them. Criminal law presumes that most human behavior is voluntary and that individuals are consciously aware of their acts. As voluntariness is to mens rea, consciousness is to voluntary conduct.
Neuroscience of Consciousness
A comprehensive review toward a neuroscience of consciousness is well beyond the scope of this chapter. Consciousness is a term that has varied and evolving meanings to neuroscientists, though in the legal realm its definition has held steadfast. In science, for example, consciousness may be used to indicate whether or not an individual is in a conscious state, as in whether it has been altered, reduced, or even lost. On the other hand, consciousness may be a trait or an attribute of a psychological process, as in the ability to think, see, and feel consciously. With trait consciousness, further distinctions may be made between conscious representations, which are usually phenomenal, and required conscious access. Unfortunately, a direct objective marker for the neural basis of state and trait consciousness that is independent of an individual’s external expressions or behavior has yet to be determined.
There have been seismic shifts in cognitive neuroscience, which the legal system has yet to appreciate and incorporate into the legal arena. Rather confusingly, the terms “conscious” and “unconscious” are still used in the lexicon of neuroscience, but the ideas and principles behind these terms have been substantially altered and continue to be refined, with one such example being Tononi’s information integration theory of consciousness.214,215 Advances in neuroscience within the past 30 years support the existence of a continuum of conscious and unconscious processes, and it has dispensed with Freudian-influenced psychoanalytic concepts and theories. The boundaries between our conscious and unconscious, as between wake and sleep, are permeable, dynamic, and interactive, and there is no valid scientific support for the sharp dichotomy as currently held by the legal community. It is this model of permeability, or state dissociation, that will also assist in the explanation of unusual, irrational, and/or bizarre human behaviors in sleep forensics.
Violent sleep-related behaviors have been reviewed in the context of automatic behavior in general, with many well-documented cases resulting from a wide variety of disorders.216 Conditions associated with sleep period-related violence fall into two major categories: neurologic and psychiatric. Behaviors arising from a primary neurologic condition can be explained by applying conceptual approaches based upon models of evanescent consciousness, the overlapping physiology of clinical disorders, and the platform of CPGs supported by semiotic neuroethology.
Despite considerable attention in the popular media in the United States and the United Kingdom given to the association between alcohol and sleepwalking, there are no compelling scientific research data to support that a reasonable amount of alcohol will either prime or trigger such an admixture of states such as sleepwalking or sexsomnia.5217
The application of sleep forensics is best based upon an adaptable conceptual approach using the most current neuroscientific and clinical principles, as opposed to a static condition that simply lists or highlights clinical disorders and extrapolates associations with criminal behavior. Such a dynamic approach would apply current neuroscientific concepts of consciousness and sleep–wake state dissociation to sleep medicine. As a result, to effectively translate this information into the courtroom, attention must be given to the controversy between dynamic neuroscientific principles of consciousness that contrast with static definitions put forth by the U.S. Model Penal Code. To assist in the determination of the putative role of an underlying sleep disorder in a specific violent act, guidelines should be proposed that are based upon international clinical experience that have undergone peer-reviewed publication. Lastly, the role of the sleep medicine specialist and recommendations for expert witness qualifications and testimony should be addressed to ensure that those who practice sleep forensics optimize dialogue and maintain ethical behavior for the process of law to proceed without hindrance.
Tassinari’s concept of the role of CPGs and FAPs provides a physiologic explanation for parasomnias. As a neuroethologic concept, it also sets a framework for future research by promoting a naturalistic approach through behavioral observation, including methodical data collection, to better understand the spectrum of parasomnias for which the duration and complexity of behaviors remain ill defined. Lastly, this concept is particularly useful in sleep forensics as parasomnias and epileptic seizures tend to have patterned stereotyped behaviors—without conscious awareness. When addressing criminal allegations and their potential association with sleep-related conditions, behavior pattern recognition applying neuroethologic concepts, indicative of process fractionation and neurobehavioral investigative techniques, could be particularly beneficial and would be consistent with the direction of current mainstream science.
Clinical Guidelines to Assist in the Determination of Purported Violence Arising from Sleep
Legal implications of automatic behavior have been discussed and debated in both the medical and legal literature.218–222 As with non-sleep-related automatisms, the identification of a specific underlying organic or psychiatric sleep/violence condition does not establish causality for any given deed. Two questions accompany each case of purported sleep-related violence: (1) directly addressing mens rea, is it possible for behavior this complex to have arisen in a mixed state of wakefulness and sleep without consciousness? And, (2) is that what happened at the time of the incident? The answer to the first is usually “yes.” The second can never be determined with certainty after the fact.
1. There should be reason by history to suspect a bona fide sleep disorder. Similar episodes, with benign or morbid outcome, should have occurred previously. (It must be remembered that disorders of arousal may begin in adulthood.)
2. The duration of the action is usually brief (seconds), though action of longer duration (minutes) does not necessarily exclude a sleep disorder or a sleep-related behavior.
3. The behavior is usually abrupt, immediate, impulsive, and senseless— without apparent motivation. Although ostensibly purposeful, it is completely inappropriate to the total situation, out of (waking) character for the individual, and without evidence of premeditation.
5. Immediately following return of consciousness, there is perplexity or horror, without attempt to escape, conceal, or cover up the action. There is evidence of lack of awareness on the part of the individual during the event.
6. There is usually some degree of amnesia for the event; however, this amnesia need not be complete.
7. Sleep is an analgesic state. The sensory pathway for pain for the most part is considered “off-line” during sleep. Consequently, pain associated with acts committed during disorders of arousal may not be perceived until awakening after the event.
8. In the case of sleep terrors/sleepwalking or sleep inertia, the act:
A. May occur upon awakening (rarely immediately upon falling asleep)—usually at least 1 hour after sleep onset
B. Occurs upon attempts to awaken the subject
C. Has been potentiated by sedative–hypnotic administration, or prior sleep deprivation
9. Polysomnographic studies performed “after the fact” are of absolutely no value in determining whether a parasomnia accounted for the remote act in question. Even capturing a parasomnia event during a sleep would indicate behavior at the time of the recording, not remotely. Furthermore, there is no scientific basis for attempting to replicate conditions surrounding the event in question (sleep deprivation, alcohol or other substance ingestion) during a sleep study. Provocation tests to trigger parasomnias by any intoxicants or mind-altering agents would appear to be ethically challenged until well-controlled validated research studies have been performed.
10. Voluntary intoxication by alcohol, or other illicit mind-altering intoxicants, precludes the sleepwalking defense.
It should be emphasized that these guidelines are purely meant to provide direction when beginning the review process to gauge whether or not a medicolegal case has merit for consideration of a sleep disorder to be used as a possible defense. Once determined, the strength of the argument to either support or refute the defendant’s claim should be used alongside current neuroscientific models of consciousness and behavior and further sustained with the medical expert’s wealth of specialized clinical experience.
Recent interest in the forensic aspects of parasomnias provides sleep medicine professionals with an opportunity to educate and assist the legal profession in cases of sleep-related violence. One infrequently used tactic to improve scientific testimony is to use a court-appointed “impartial expert.”226 When approached to testify, volunteering to serve as a court-appointed expert, rather than one appointed by either the prosecution or defense, may encourage this practice. Other proposed measures include the development of a specific section in scientific journals dedicated to expert witness testimony extracted from public documents with request for opinions and consensus statements from appropriate specialists, or the development of a library of circulating expert testimony that could be used to discredit irresponsible professional witnesses.226 Good science is not determined by the credentials of the expert witness, but rather by scientific consensus.227
To address the problem of junk science in the courtroom, many professional societies are calling for and some have developed guidelines for expert witness qualifications and testimony. The American Academy of Sleep Medicine’s stance on expert witness testimony is to accept those opinions as held by the American Medical Association (AMA) in their 2004 Report of the Council on Ethical and Judicial Affairs.228 Similarly, influenced by both American Academy of Neurology and the AMA, the following guidelines should serve as a compass:229–231
A. Expert witness qualifications
1. Must have a current, valid, unrestricted medical license
2. Must be a Diplomat of the American Board of Sleep Medicine, or have passed the American Board of Internal Medicine specialty examination in sleep medicine
3. Membership in the Sleep Research Society is strongly encouraged
4. Must be a recognized resource within the sleep medicine community and should have been actively involved in clinical practice in a manner consistent with the requirement of the criminal case at the time of the event
5. Given the essential position of mens rea in criminal law and the pivotal role of levels of consciousness, must have significant direct experience in either neurology and/or neuroscience
B. Guidelines for expert testimony
1. Must be impartial: ultimate test for accuracy and impartiality is a willingness to prepare testimony that could be presented unchanged for use by either the plaintiff or the defendant.
2. Fees should relate to time and effort, not contingent upon the outcome of the claim. Fees should not exceed 20% of the practitioner’s annual income.
3. Practitioner should be willing to submit such testimony for peer review.
5. The expert witness must not become a partisan or advocate in the legal proceeding.
It is not the role of the medical expert to win the case for his or her client, though it is not uncommon to use irrelevant disingenuous technicalities in an attempt to deceive to attain an advantage to secure the decision. Instead, the salient ethical decision for those who assume this mantle of medical expert witness is to recognize and value the privileged position given within our society as an educator inside the legal system by promoting current published peer-reviewed science while all along minimizing bias while rendering an opinion. The role of the expert witness is therefore to attempt to succinctly and clearly communicate scientifically valid information to the jury, who in turn determines culpability based upon this information. The weight of the decisions of either guilt or innocence should never rest in the hands of medical experts, whose task is to contribute to the due process of an efficient and functional legal system by ensuring that the jury is educated and well informed.232
Advances in neuroscience are increasing our understanding of how the brain enables “action” from everything from simple movement, to thought, to the diurnal and nocturnal variability of wake–sleep processing. All this seems to be occurring at a pace never before seen as we appear to be closing in on the idea that humans are a determined system. Such scientific advance certainly comes at a cost, as the societal and cultural implications have yet to be understood—or even conceived.233 However, the legal community is all too aware of the implications of this “new neuroscience,” as it directly challenges its currently held constructs of consciousness as defined by mens rea and the voluntary act requirements. To study these problems, the John D. and Catherine T. MacArthur Foundation has established the Law and Neuroscience Project (www.lawandneuroscienceproject.org) comprising 40 neuroscientists, legal specialists, and philosophers, with funding that began in 2007.234 One most important concept to be incorporated into the legal community is the fact that consciousness is not all-or-none, but rather occurs on a spectrum, and that consciousness can be dissociated from behavior.
Sleep forensics involves more than providing medical expert testimony in individual legal cases. Here we provide a definition and a conceptual approach for the formal development of the field of sleep forensics so that it not only serves as a resource to the legal community but also so that we can appreciate its complex and important position at the intersection of neuroscience and law. With this appreciation comes significant social responsibility. Applying process fractionation, much can be learned about consciousness from sleep physiology, particularly in admixed states. The growth of cognitive neuroscience will continue to change our understanding of what it means to be human, and as a result the justice will have to change in conformity with it. Lastly, the conceptual approach to sleep forensics encourages further research to define and characterize admixed states of wake/sleep and parasomnias, all of which are beneficial in understanding the spectrum of complex human behavior. Close collaboration among basic neuroscientists, sleep medicine clinicians, and the legal community will facilitate the development of a commonly shared concept of consciousness and culpability.
1. Mahowald MW, Ettinger MG. Things that go bump in the night—the parasomnias revisited. J Clin Neurophysiol. 1990;7:119–143.Find this resource:
2. Mahowald MW, Schenck CH. Evolving concepts of human state dissociation. Archives Italiennes de Biologie. 2001;139:269–300.Find this resource:
3. Mahowald MW, Schenck CH. REM sleep behavior disorder. In: Kryger MH, Dement W, Roth T, eds. Principles and Practice of Sleep Medicine, 2nd ed. Philadelphia: Saunders; 1994:574–588.Find this resource:
4. Mahowald MW, Schenck CH. NREM sleep parasomnias. Neurol Clin. 2005;23:1077–1106.Find this resource:
5. Pressman MR, Mahowald MW, Schenck CH, et al. Alcohol-induced sleepwalking or confusional arousal as a defense to criminal behavior: review of scientific evidence, methods and forensic considerations. J Sleep Res. 2007;16:198–212.Find this resource:
6. Zolpidem:sleepwalking and automatic behaviours. Prescrire International. 2007;16:200.Find this resource:
7. Canaday BR. Amnesia possibly associated with zolpidem administration. Pharmacotherapy. 1996;16:687–689.Find this resource:
8. Harazin J, Berigan TR. Zolpidem tartrate and somnambulism. Military Med. 1999;164:669–670.Find this resource:
9. Mendelson WB. Sleepwalking associated with zolpidem. J Clin Psychopharmacol. 1994;14:150.Find this resource:
10. Morgenthaler TI, Silber MH. Amnestic sleep-related eating disorder associated with zolpidem. Sleep Med. 2002;3:323–327.Find this resource:
11. Najjar M. Zolpidem and amnestic sleep related eating disorder. J Clin Sleep Med. 2007;3:637–638.Find this resource:
12. Sansone RA, Sansone LA. Zolpidem, somnambulism, and nocturnal eating. Gen Hosp Psychiatry. 2008;30:90–91.Find this resource:
13. Schenck CH, Connoy DA, Castellanos M, et al. Zolpidem-induced amnestic sleep-related eating disorder (SRED) in 19 patients. Sleep. 2005;28 (abstract supplement):A259.Find this resource:
14. Yang W, Dollear M, Muthukrishnan SR, et al. One rare side effect of zolpidem—sleepwalking: a case report. Arch Phys Med Rehab. [Case Reports] 2005;86:1265–1266.Find this resource:
15. Pressman MR. Factors that predispose, prime, and precipitate NREM parasomnias in adults: clinical and forensic implications. Sleep Med Rev. 2007;11:5–30.Find this resource:
16. Guilleminault C, Silvestri R. Disorders of arousal and epilepsy during sleep. In: Sterman MB, Shouse MN, Passouant PP, eds. Sleep and Epilepsy. New York: Academic Press, 1982:513–531.Find this resource:
18. Lateef O, Wyatt J, Cartwright R. A case of violent non-REM parasomnias that resolved with treatment of obstructive sleep apnea. Chest. 2005;128:461S (abstract).Find this resource:
19. Millman RP, Kipp GR, Carskadon MA. Sleepwalking precipitated by treatment of sleep apnea with nasal CPAP. Chest. 1991;99:750–751.Find this resource:
20. Fietze I, Warmuth R, Witt C, et al. Sleep-related breathing disorder and pavor nocturnus. Sleep Res. 1995;24A:301.Find this resource:
21. Schenck CH, Hurwitz TD, Bundlie SR, et al. Sleep-related injury in 100 adult patients: a polysomnographic and clinical report. Am J Psychiatry. 1989;146:1166–1173.Find this resource:
22. Guilleminault C, Moscovitch A, Leger D. Forensic sleep medicine: nocturnal wandering and violence. Sleep. 1995;18:740–748.Find this resource:
23. Llorente MD, Currier MB, Norman S, et al. Night terrors in adults: phenomenology and relationship to psychopathology. J Clin Psychiatry. 1992;53:392–394.Find this resource:
24. Laberge L, Tremblay RE, Vitaro F, et al. Development of parasomnias from childhood to early adolescence. Pediatrics. 2000;106:67–74.Find this resource:
25. Broughton RJ. Sleep disorders: disorders of arousal? Science 1968;159:1070–1078.Find this resource:
26. Kales A, Jacobson A, Paulson MJ, et al. Somnambulism: psychophysiological correlates. I. All-night EEG studies. Arch Gen Psychiatry. 1966;14:586–594.Find this resource:
27. Kales JD, Cadieux RJ, Soldatos CR, et al. Psychotherapy with night-terror patients. Am J Psychother. 1982;36:399–407.Find this resource:
28. Fisher C, Kahn E, Edwards A, et al. A psychophysiological study of nightmares and night terrors. I. Physiological aspects of the stage 4 night terror. J Nerv Ment Dis. 1973;157:75–98.Find this resource:
29. Hori A, Hirose G. Twin studies on parasomnias. Sleep Res. 1995;24A:324.Find this resource:
30. Arkin AM. Night-terrors as anomalous REM sleep component manifestation in slow-wave sleep. Waking and Sleeping. 1978;2:143–147.Find this resource:
31. Tassinari CA, Rubboli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias. A neuroethologic approach. Neurol Sci. 2005;26:s225–s32.Find this resource:
32. Mori S, Nishimura H, Aoki M. Brain stem activation of the spinal stepping generator. In: Hobson JA, Brazier MAB, eds. The Reticular Formation Revisited. New York: Raven Press, 1980:241–259.Find this resource:
33. Rossignol S, Dubuc R. Spinal pattern generation. Curr Opin Neurol. 1994;4:894–902.Find this resource:
34. Elliott FA. Neuroanatomy and neurology of aggression. Psychiatric Ann. 1987;17:385–388.Find this resource:
35. Siegel A, Pott CB. Neural substrates of aggression and flight in the cat. Progr Neurobiol. 1988;31:261–283.Find this resource:
36. Bandler R. Brain nechanisms of aggression as revealed by electrical and chemical stimulation: suggestion of a central role for the midbrain periaqueductal region. Prog Psychobiol Physiol Psychol. 1988;13:67–154.Find this resource:
37. Kelts KA, Hoehn MM. Hypothalamic atrophy. J Clin Psychiatry. 1978;39:357–358.Find this resource:
38. Kelleffer FA, Stern WE. Chronic effects of hypothalamic injury. Arch Neurol. 1970;22:419–429.Find this resource:
39. Reeves AG. Hyperphagia, rage, and dementia accompanying a ventromedial hypothalamic neoplasm. Arch Neurol. 1969;20:616–624.Find this resource:
40. Haugh RM, Markesbery WR. Hypothalamic astrocytoma. Syndrome of hyperphagia, obesity, and disturbances of behavior and endocrine and autonomic function. Arch Neurol. 1983;40:560–563.Find this resource:
41. Sano K, Mayanagi Y. Posteromedial hypothalamotomy in the treatment of violent, aggressive behavior. Acta Neurochirurgica. 1988;44(Suppl):145–151.Find this resource:
42. Lai YY, Siegel JM. Brainstem-mediated locomotion and myoclonic jerks. I. Neural substrates. Brain Res. 1997;745:257–264.Find this resource:
44. Bassetti C, Vella S, Donati F, et al. SPECT during sleepwalking. Lancet. 2000;356:484–485.Find this resource:
45. Tassi P, Muzet A. Sleep inertia. Sleep Med Rev. 2000;4:341–353.Find this resource:
46. Horner RL, Sanford LD, Pack AI, et al. Activation of a distinct arousal state immediately after spontaneous awakening from sleep. Brain Res. 1997;778:127–134.Find this resource:
47. Koboyama T, Hori A, Sato T, et al. Changes in cerebral blood flow velocity in healthy young men during overnight sleep and while awake. EEG Clin Neurophysiol. 1997;102:125–131.Find this resource:
48. Balkin TJ, Wesensten NJ, Braun AR, et al. Shaking out the cobwebs: changes in regional cerebral blood flow (rCBF) across the first 20 minutes of wakefulness. J Sleep Res. 1998;21:411.A.Find this resource:
49. Balkin TJ, Braun AR, Wesensten NJ, et al. The process of awakening: a PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness. Brain Res Bull. 2002;12:2308–2319.Find this resource:
50. Parrino L, Halasz P, Tassinari CA, et al. CAP, epilepsy and motor events during sleep: the unifying role of arousal. Sleep Med Rev. 2006;10:267–285.Find this resource:
51. Terzano MG, Parrino L, Spaggiari MC. The cyclic alternating pattern sequences in the dynamic organization of sleep. EEG Clin Neurophysiol. 1988;69:437–447.Find this resource:
52. Zadra AL, Nielsen TA. Topographical EEG mapping in a case of recurrent sleep terrors. Dreaming. 1998;8:67–74.Find this resource:
53. Halasz P, Ujszaszi J, Gadoros J. Are microarousals preceded by electroencephalographic slow wave synchronization precursors of confusional awakenings? Sleep. 1985;8:231–238.Find this resource:
54. Zuccone M, Oldani A, Ferini-Strambi L, et al. Arousal fluctuations in non-rapid eye movement parasomnias: the role of cyclic alternating pattern as a measure of sleep instability. J Clin Neurophysiol. 1995;12:147–154.Find this resource:
55. Blatt I, Peled R, Gadoth N, et al. The value of sleep recording in evaluating somnambulism in young adults. EEG Clin Neurophysiol. 1991;78:407–412.Find this resource:
56. Schenck CH, Pareja JA, Patterson AL, et al. An analysis of polysomnographic events surrounding 252 slow-wave sleep arousals in 38 adults with injurious sleepwalking and sleep terrors. J Clin Neurophysiol. 1998;15:159–166.Find this resource:
57. Bruni O, Ferri R, Novelli L, et al. NREM sleep instability in children with sleep terrors: the role of slow wave activity interruptions. Clin Neurophysiol. 2008;119:985–992.Find this resource:
58. Oliviero A, Della Marca G, Tonali PA, et al. Functional involvement of cerebral cortex in adult sleepwalking. J Neurol. 2007;254:1066–1072.Find this resource:
59. Rosen G, Mahowald MW, Ferber R. Sleepwalking, confusional arousals, and sleep terrors in the child. In: Ferber R, Kryger M, eds. Principles and Practice of Sleep Medicine in the Child. Philadelphia: Saunders, 1995:99–106.Find this resource:
60. Nino-Murcia G, Dement WC. Psychophysiological and pharmacological aspects of somnambulism and night terrors in children. In: Meltzer HY, ed. Psychopharmacology: The Third Generation of Progress. New York: Raven Press, 1987:873–879.Find this resource:
61. Ohayon M, Guilleminault C, Priest RG. Night terrors, sleepwalking, and confusional arousal in the general population: their frequency and relationship to other sleep and mental disorders. J Clin Psychiatry. 1999;60:268–276.Find this resource:
62. Hublin C, Kaprio J, Partinen M, et al. Prevalence and genetics of sleepwalking; a population-based twin study. Neurology. 1997;48:177–181.Find this resource:
63. Klackenberg G. Somnambulism in childhood: prevalence, course and behavior correlates. A prospective longitudinal study (6–16 years). Acta Paediatr Scand. 1982;71:495–499.Find this resource:
64. Bixler EO, Kales A, Soldatos CR, et al. Prevalence of sleep disorders in the Los Angeles metropolitan area. Am J Psychiatry. 1979;136:1257–1262.Find this resource:
65. Fisher C, Kahn E, Edwards A, et al. A psychophysiological study of nightmares and night terrors. III. Mental content and recall of stage 4 night terrors. J Nerv Ment Dis. 1974;158:174–188.Find this resource:
66. Kahn E, Fisher C, Edwards A. Night terrors and anxiety dreams. In: Ellman SD, Antrobus JS, eds. The Mind in Sleep Psychology and Psychophysiology. 2nd ed. New York: John Wiley & Sons, 1991:437–447.Find this resource:
67. Crisp AH. The sleepwalking/night terrors syndrome in adults. Postgrad Med J. 1996;72:599–604.Find this resource:
68. Howell MJ, Schenck CH, Crow SJ. A review of nighttime eating disorders. Sleep Med Rev. 2009;13:23–34.Find this resource:
69. Paquet V, Strul J, Servais L, et al. Sleep-related eating disorder induced by olanzapine. J Clin Psychiatry. [Case Reports Letter] 2002;63:597.Find this resource:
70. Menkes DB. Triazolam-induced nocturnal bingeing with amnesia. Aust NZ J Psychiatry. 1992;26:320–321.Find this resource:
71. Birketvedt GS, Florholmen J, Sundsfjord J, et al. Behavioral and neuroendocrine characteristics of the night-eating syndrome. JAMA. 1999;282:657–663.Find this resource:
72. Birketvedt GS, Sundsfjord J, Florholmen JR. Hypothalamic-pituitary-adrenal axis in the night eating syndrome. Am J Physiol Endocrinol Metab. 2001;282:E366–E369.Find this resource:
73. Stunkard A, Allison KC. Two forms of disordered eating in obesity: binge eating and night eating. Int J Obesity. 2003;27:1–12.Find this resource:
74. 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;2007:683–702.Find this resource:
75. Guilleminault C, Moscovitch A, Yuen K, et al. Atypical sexual behavior during sleep. Psychosom Med. 2002;64:328–336.Find this resource:
76. Aldrich MS, Jahnke B. Diagnostic value of video-EEG polysomnography. Neurology. 1991;41:1060–1066.Find this resource:
77. Zadra A, Pilon M, Montplaisir J. Polysomnographic diagnosis of sleepwalking: effects of sleep deprivation. Ann Neurol. 2008;63:513–519.Find this resource:
78. Mahowald MW, Schenck CH. Parasomnia purgatory: the epileptic/non-epileptic interface. In: Rowan AJ, Gates JR, eds. Non-Epileptic Seizures. Boston: Butterworth-Heinemann, 1993:123–139.Find this resource:
79. Schenck CH, Mahowald MW. REM parasomnias. Neurol Clin. 1996;14:697–720.Find this resource:
80. Mahowald MW, Schenck CH. NREM parasomnias. Neurol Clin. 1996;14:675–696.Find this resource:
81. Goodwin JL, Kaemingk KL, Fregosi RF, et al. Parasomnias and sleep disordered breathing in Caucasian and Hispanic children: the Tucson children’s assessment of sleep apnea study. BMC Medicine. 2004;2 [on line].Find this resource:
82. Tinuper P, Provini F, Bisulli F, et al. Movement disorders in sleep: guidelines for differentiating epileptic from non-epileptic motor phenomena arising from sleep. Sleep Med Rev. 2007;11:255–267.Find this resource:
83. Casez O, Dananchet Y, Besson G. Migraine and somnambulism. Neurology. 2005;65:1334–1335.Find this resource:
84. Johnson H, Wiggs L, Stores G, et al. Psychological disturbance and sleep disorders in children with neurofibromatosis type 1. Devel Med Child Neurol. 2005;47:237–242.Find this resource:
85. Barabas G, Matthews WS, Ferrari M. Disorders of arousal in Gilles de la Tourette’s syndrome. Neurology. 1984;34:814–817.Find this resource:
86. Wand RR, Matazow GS, Shady GA, et al. Tourette syndrome: associated symptoms and most disabling features. Neurosci Biobehav Rev. 1993;17:271–275.Find this resource:
87. Isik U, D’Cruz OF. Cluster headaches simulating parasomnias. Pediatr Neurol. 2002;27:227–229.Find this resource:
88. Espa F, Dauvilliers Y, Ondze B, et al. Arousal reactions in sleepwalking and night terrors in adults: the role of respiratory events. Sleep. 2002;25:871–875.Find this resource:
90. Lillywhite AR, Wilson SJ, Nutt DJ. Successful treatment of night terrors and somnambulism with paroxetine. Br J Psychiatry. 1994;164:551–554.Find this resource:
91. Balon R. Sleep terror disorder and insomnia treated with trazodone: a case report. Ann Clin Psychiatry. 1994;6:161–163.Find this resource:
92. Kellerman J. Behavioral treatment of night terrors in a child with acute leukemia. J Nerv Ment Dis. 1979;167:182–185.Find this resource:
93. Hauri P, Silber MH, Boeve BF. The treatment for parasomnias with hypnosis: a 5-year follow-up study. J Clin Sleep Med. 2007;3:369–373.Find this resource:
94. Tobin JD, Jr. Treatment of somnambulism with anticipatory awakening. J Pediatr. 1993;122:426–427.Find this resource:
95. Schenck CH, Mahowald MW. REM sleep parasomnias. Neurol Clin. 2005;23:1107–1126.Find this resource:
96. Steriade M, Ropert N, Kitsikis A, et al. Ascending activating neuronal networks in midbrain core and related rostral systems. In: Hobson JA, Brazier MAB, eds. The Reticular Formation Revisited. New York: Raven Press, 1980:125–167.Find this resource:
97. Dement WC. The biological role of REM sleep (circa 1968). In: Kales A, ed. Sleep Physiology and Pathology. Philadelphia: Lippincott, 1969:245–265.Find this resource:
98. Hishikawa Y, Nan’no H, Tachibana M, et al. The nature of sleep attack and other symptoms of narcolepsy. EEG Clin Neurophysiol. 1968;24:1–10.Find this resource:
99. Guilleminault C, Wilson RA, Dement WC. A study on cataplexy. Arch Neurol. 1974;31:255–261.Find this resource:
100. Schenck CH, Mahowald MW. REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in Sleep. Sleep. 2002;25:120–130.Find this resource:
101. Ohayon MM, Caulet M, Priest RG. Violent behavior during sleep. J Clin Psychiatry. 1997;58:369–376.Find this resource:
102. Chiu HF, Wing YK. REM sleep behaviour disorder: an overview. Int J Clin Pract. 1997;51:451–454.Find this resource:
103. Sakai K, Sastre J-P, Kanamori N, et al. State-specific neurons in the ponto-medullary reticular formation with special reference to the postural atonia during paradoxical sleep in the cat. In: Pompeiano O, Ajmone Marsan C, eds. Brain Mechanisms and Perceptual Awareness. New York: Raven Press, 1981:405–429.Find this resource:
104. Webster HW, Frideman L, Jones BE. Modification of paradoxical sleep following transections of the reticular formation at the pontomedullary junction. Sleep. 1986;9:1–23.Find this resource:
105. Mileykovskiy BY, Kiyashchenko LI, Kodama T, et al. Activation of pontine medullary motor inhibitory regions reduces discharge in neurons located in the locus coeruleus and the anatomical equivalent of the midbrain locomotor region. J Neurosci. 2000;20:8551–8558.Find this resource:
106. Mileykovskiy BY, Kiyashchenko LI, Siegel JM. Cessation of activity in red nucleus neurons during stimulation of medial medulla in decerebrate rats. J Physiol. 2002;543:997–1006.Find this resource:
107. Chase MH. The motor functions of the reticular formation are multifaceted and state-determined. In: Hobson JA, Brazier MAB, eds. The Reticular Formation Revisited. New York: Raven Press, 1980:449–472.Find this resource:
108. Askenasy JJ, Weitzman ED, Yahr MD. Rapid eye movements: expression of a general muscular phasic event of the REM state. Sleep Res. 1983;12:172.Find this resource:
109. Chase MH, Morales FR. Subthreshold excitatory activity and motoneurone discharge during REM periods of active sleep. Science. 1983;221:1195–1198.Find this resource:
110. Fort P, Rampon C, Gervasoni D, et al. Anatomical demonstration of a medullary enkephalinergic pathway potentially implicated in the oro-facial muscle atonia of paradoxical sleep in the cat. Sleep Res Online. 1998;1:102–108.Find this resource:
111. Lopez-Rodriguez F, Kohlmeier K, Morales FR, et al. State dependency of the effects of microinjection of cholinergic drugs into the nucleus pontalis oralis. Brain Res. 1994;649:271–281.Find this resource:
112. Brooks PL, Peever JH. Glycinergic and GABAA-mediated inhibition of somatic motoneurons does not mediate rapid eye movement sleep motor atonia. J Neurosci. 2008;28:3535–3545.Find this resource:
113. Eisensehr I, Linke R, Noachtar S, et al. Reduced striatal dopamine transporters in idiopathic rapid eye movement sleep behavior disorder. Comparison with Parkinson’s disease and controls. Brain. 2000;123:1155–1160.Find this resource:
114. Eisensehr I, Linke R, Tatsch K, et al. Increased muscle activity during rapid eye movement sleep correlates with decrease of striatal presynaptic dopamine transporters. IPT and IBZM SPECT imaging in subclinical and clinically manifest idiopathic REM sleep behavior disorder, Parkinson’s disease, and controls. Sleep. 2003;26:507–512.Find this resource:
115. Albin RL, Koeppe RA, Chervin RD, et al. Decreased striatal dopaminergic innervation in REM sleep behavior disorder. Neurology. 2000;55:1410–1412.Find this resource:
116. Shirakawa S-I, Takeuchi N, Uchimura N, et al. Study of image findings in rapid eye movement sleep behavioral disorder. Psychiatry Clin Neurosci. 2002;56:291–292.Find this resource:
117. Miyamoto M, Miyamoto T, Kubo J, et al. Brainstem function in rapid eye movement sleep behavior disorder: the evaluation of brainstem function by proton MR spectroscopy (1H-MRS). Psychiatry Clin Neurosci. 2000;54:350–351.Find this resource:
118. Gilman S, Koeppe RA, Chervin R, et al. REM sleep behavior disorder is related to striatal monoaminergic deficit in MSA. Neurology. 2003;61:29–34.Find this resource:
119. Fantini ML, Gagnon JF, Petit D, et al. Slowing of electroencephalogram in rapid eye movement sleep behavior disorder. Ann Neurol. 2003;53:774–780.Find this resource:
120. Tachibana M, Tanaka K, Hishikawa Y, et al. A sleep study of acute psychotic states due to alcohol and meprobamate addiction. Adv Sleep Res. 1975;2:177–205.Find this resource:
121. Lasegue C. Le delire alcoolique n’est pas un delire, mais un reve. Arch Gen Med. 1881;88:513–586.Find this resource:
122. Gross MM, Godenough D, Tobin M, et al. Sleep disturbances and hallucinations in the acute alcoholic psychoses. J Nerv Ment Dis. 1966;142:493–514.Find this resource:
123. Greenberg R, Pearlman C. Delirium tremens and dreaming. Am J Psychiatry. 1967;124:37–46.Find this resource:
124. Hishikawa Y, Sugita Y, Teshima Y, et al. Sleep disorders in alcoholic patients with delirium tremens and transient withdrawal hallucinations: reevaluation of the REM rebound and intrusion theory. In: Karacan I, ed. Psychophysiological Aspects of Sleep. Park Ridge, NJ: Noyes Medical Publishers, 1981:109–122.Find this resource:
125. Tachibana M, Tanaka K, Hishikawa Y, et al. A sleep study of acute psychotic stated due to alcohol and meprobamate addiction. Adv Sleep Res. 1975;2:177–205.Find this resource:
126. Atsumi Y, Kojima T, Matsu’ura M, et al. Polygraphic study of altered consciousness: effect of biperiden on EEG and EOG. Ann Report Res Psychotropic Drugs. 1977;9:171–178 [in Japanese].Find this resource:
127. Sugano T, Suenaga K, Endo S, et al. Withdrawal delirium in a patient with nitrazepam addiction. Jpn J EEG EMG. 1980;8:34–35 [in Japanese].Find this resource:
128. Parish JM. Violent dreaming and antidepressant drugs: or how paroxetine made me dream that I was fighting Saddam Hussein. J Clin Sleep Med. 2007;3:529–531.Find this resource:
129. Stolz SE, Aldrich MS. REM sleep behavior disorder associated with caffeine abuse. Sleep Res. 1991;20:341.Find this resource:
130. Vorona RD, Ware JC. Exacerbation of REM sleep behavior disorder by chocolate ingestion: a case report. Sleep Med. 2002;3:365–367.Find this resource:
131. Mahowald MW, Schenck CH. The REM sleep behavior disorder odyssey. Sleep Med Rev. 2009;13:381-384.Find this resource:
132. Schenck CH, Bundlie SR, Smith SA, et al. REM behavior disorder in a 10-year-old girl and aperiodic REM and NREM sleep movements in an 8-year-old brother. Sleep Res. 1986;15:162.Find this resource:
133. Hendricks JC, Lager A, O’Brien D, et al. Movement disorders during sleep in cats and dogs. J Am Vet Med Assoc. 1989;194:686–689.Find this resource:
134. Hendricks JC, Morrison AR, Farnbach GL, et al. Disorder of rapid eye movement sleep in a cat. J Am Vet Med Assoc. 1980;178:55–57.Find this resource:
135. Goldstein M. Brain research and violent behavior. Arch Neurol. 1974;30:1–34.Find this resource:
136. Moyer KE. Kinds of aggression and their physiological basis. Commun Behav Biol. 1968;2 (part A):65–87.Find this resource:
137. Ramirez JM. Hormones and aggression in childhood and adolescence. Aggression Violent Behavior. 2003;8:621–644.Find this resource:
138. Coffey CE, Licke JF, Saxton JA, et al. Sex differences in brain aging. A quantitative magnetic resonance imaging study. Arch Neurol. 1998;55:169–179.Find this resource:
139. Patwardhan AJ, Eliez S, Bender B, et al. Brain morphology in Klinefelter syndrome. Neurology. 2000;54:2218–2223.Find this resource:
140. Cosgrove KP, Mazure CM, Staley JK. Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry. 2007;62:847–855.Find this resource:
141. Guillamon A, de Blas MR, Segovia S. Effects of sex steroids on the development of the locus coeruleus in rats. Devel Brain Res. 1988;40:306–310.Find this resource:
142. Iranzo A, Santamaria J, Vilaseca I, et al. Absence of alterations in serum sex hormone levels in idiopathic REM sleep behavior disorder. Sleep. 2007;30:803–806.Find this resource:
143. Chou KL, Moro-de-Casillas ML, Amick MM, et al. Testosterone not associated with violent dreams or REM sleep behavior disorder in men with Parkinson’s. Movement Disorders. 2007;22:411–414.Find this resource:
144. Teman PT, Tippmann-Peikert M, Silber MH, et al. Idiopathic rapid-eye-movement sleep disorder: Associations with antidepressants, psychiatric diagnoses, and other factors, in relation to age of onset. Sleep Med. 2009;10:60–65.Find this resource:
145. Bonakis A, Howard RS, Ebrahim IO, et al. REM sleep behavior disorder (RBD) and its associations in young patients. Sleep Med. 2009;10:641–645.Find this resource:
146. Schenck CH, Mahowald MW. Polysomnographic, neurologic, psychiatric, and clinical outcome report on 70 consecutive cases with REM sleep behavior disorder (RBD): sustained clonazepam efficacy in 89.5% of 57 treated patients. Cleveland Clinic J Med. 1990;57(Suppl):S9–S23.Find this resource:
147. Mahowald MW, Schenck CH. REM sleep behavior disorder. In: Thorpy MJ, ed. Handbook of Sleep Disorders. New York: Marcel Dekker, 1990:567–593.Find this resource:
148. Cramer Bornemann MA, Mahowald MW, Schenck CH. Parasomnias. Clinical features and forensic implications. Chest. 2006;130:605–610.Find this resource:
149. Yeh S-B, Schenck CH. A case of marital discord and secondary depression with attempted suicide resulting from REM sleep behavior disorder in a 35-year-old woman. Sleep Med. 2004;5:151–154.Find this resource:
150. Gjerstad MD, Boeve B, Wentzel-Larsen T, et al. Occurrence and clinical correlates of REM sleep behaviour disorder in patients with Parkinson’s disease over time. J Neurol Neurosurg Psychiatry. 2008;79:387–391.Find this resource:
151. Fantini ML, Corona A, Clerici S, et al. Increased aggressive dream content without increased daytime aggressiveness in REM sleep behavior disorder. Neurology. 2005;65:1010–1015.Find this resource:
152. Iranzo A, Santamaria J, Tolosa E. The clinical and pathophysiological relevance of REM sleep behavior disorder in neurodegenerative diseases. Sleep Med Rev. 2009 Apr [epub ahead of print].Find this resource:
153. Comella CL, Nardine TM, Diederich NJ, et al. Sleep-related violence, injury, and REM sleep behavior disorder in Parkinson’s disease. Neurology. 1998;51:526–529.Find this resource:
154. Eisensehr I, v Lindeiner H, Jager M, et al. REM sleep behavior disorder in sleep-disordered patients with versus without Parkinson’s disease: is there a need for polysomnography? J Neurol Sci. 2001;186:7–11.Find this resource:
155. Gagnon J-F, Bedard M-A, Fantini ML, et al. REM sleep behavior disorder and REM sleep without atonia in Parkinson’s disease. Neurology. 2002;59:585–589.Find this resource:
156. Scaglione C, Vignatelli L, Plazzi G, et al. REM sleep behaviour disorder in Parkinson’s disease: a questionnaire-based study. Neurol Sci. 2005;25:316–321.Find this resource:
157. Plazzi G, Corsini R, Provini F, et al. REM sleep behavior disorders in multiple system atrophy. Neurology. 1997;48:1094–1097.Find this resource:
158. Ghorayeb I, Yekhlef F, Chrysosotome V, et al. Sleep disorders and their determinants in multiple system atrophy. J Neurol Neurosurg Psychiatry. 2002;72:798–800.Find this resource:
159. Plazzi G, Cortelli P, Montagna P, et al. REM sleep behavior disorder differentiates pure autonomic failure from multiple system atrophy with autonomic failure. J Neurol Neurosurg Psychiatry. 1998;64:683–685.Find this resource:
160. Uchiyama M, Isse K, Tanaka K, et al. Incidental Lewy body disease in a patient with REM sleep behavior disorder. Neurology. 1995;45:709–712.Find this resource:
161. Ferman TJ, Boeve BF, Smith GE, et al. Dementia with Lewy bodies may present as dementia and REM sleep behavior disorder without parkinsonism or hallucinations. J Int Neuropsychol Soc. 2002;8:904–914.Find this resource:
162. De Cock VC, Vidailhet M, Leu S, et al. Restoration of normal motor control in Parkinson’s disease during REM sleep. Brain. 2007;130:450–456.Find this resource:
163. Bonakis A, Howard RS, Williams A, et al. Narcolepsy presenting as REM sleep behaviour disorder. Clin Neurol Neurosurg. [Case Reports] 2008;110:518–520.Find this resource:
164. Mattarozzi K, Bellucci C, Campi C, et al. Clinical, behavioural and polysomnographic correlates of cataplexy in patients with narcolepsy/cataplexy. Sleep Med. 2008;9:425–433.Find this resource:
165. Nightingale S, Orgill JC, Ebrahim IO, et al. The association between narcolepsy and REM behavior disorder (RBD). Sleep Med. 2005;6:253–258.Find this resource:
166. Dauvilliers Y, Rompre S, Gagnon J-F, et al. REM sleep characteristics in narcolepsy and REM sleep behavior disorder. Sleep. 2007;30:844–849.Find this resource:
167. Nevsimalova S, Prihodova I, Kemlink D, et al. REM sleep behavior disorder (RBD) can be one of the first symptoms of childhood narcolepsy. Sleep Med. 2007;8:784–786.Find this resource:
168. Schenck CH, Mahowald MW. Motor dyscontrol in narcolepsy: rapid-eye-movement (REM) sleep without atonia and REM sleep behavior disorder. Ann Neurol. 1992;32:3–10.Find this resource:
169. Dyken ME, Lin-Dyken DC, Seaba P, et al. Violent sleep-related behavior leading to subdural hemorrhage. Arch Neurol. 1995;52:318–321.Find this resource:
170. Gross PT. REM sleep behavior disorder causing bilateral subdural hematomas. Sleep Res. 1992;21:204 [abstract].Find this resource:
171. Morfis L, Schwartz RS, Cistulli PA. REM sleep behavior disorder: a treatable cause of falls in elderly people. Age Ageing. 1997;26:43–44.Find this resource:
172. Rechtschaffen A, Kales A. A Manual of Standardized Terminology: Techniques and Scoring System for Sleep Stages of Human Subjects. Los Angeles: UCLA Brain Information Service/Brain Research Institute, 1968.Find this resource:
173. Carskadon MA, Dement WC, Mitler MM, et al. Guidelines for the multiple sleep latency test (MSLT): a standard measure of sleepiness. Sleep. 1986;9:519–524.Find this resource:
174. Schenck CH, Bundlie SR, Patterson AL, et al. Rapid eye movement sleep behavior disorder. A treatable parasomnia affecting older adults. JAMA. 1987;257:1786–1789.Find this resource:
175. Nalamalapu U, Goldberg R, DePhillipo M, et al. Behaviors simulating REM behavior disorder in patients with severe obstructive sleep apnea. Sleep Res. 1996;25:311.Find this resource:
176. D’ Cruz OF, Vaughn BV. Nocturnal seizures mimic REM behavior disorder. Am J END Technol. 1997;37:258–264.Find this resource:
178. Schenck CH, Boyd JL, Mahowald MW. A parasomnia overlap disorder involving sleepwalking, sleep terrors, and REM sleep behavior disorder in 33 polysomnographically confirmed cases. Sleep. 1997;20:972–981.Find this resource:
179. Schenck CS, Milner DM, Hurwitz TD, et al. Dissociative disorders presenting as somnambulism: polysomnographic, video, and clinical documentation (8 cases). Dissociation. 1989;4:194–204.Find this resource:
180. Mahowald MW, Schenck CH, Rosen GR, et al. The role of a sleep disorders center in evaluating sleep violence. Arch Neurol. 1992;49:604–607.Find this resource:
181. Schenck CH, Mahowald MW. Long-term, nightly benzodiazepine treatment of injurious parasomnias and other disorders of disrupted nocturnal sleep in 170 adults. Am J Med. 1996;100:333–337.Find this resource:
182. Anderson KN, Jamieson S, Graham AJ, et al. REM sleep behaviour disorder treated wtih melatonin in a patient with Alzheimer’s disease. Clin Neurol Neurosurg. 2008;110:492–495.Find this resource:
183. Boeve BF, Silber MH, Ferman JT. Melatonin for treatment of REM sleep behavior disorder in neurologic disorders: results in 14 patients. Sleep Med. 2003;4:281–284.Find this resource:
184. Fantini ML, Gagno J-F, Filipini D, et al. The effects of pramipexole in REM sleep behavior disorder. Neurology. 2003;61:1418–1420.Find this resource:
185. Schmidt MH, Koshal VB, Schmidt HS. Use of pramipexole in REM sleep behavior disorder. Sleep Med. 2006;7:418–423.Find this resource:
186. Matsumoto M, Mutoh F, Naoe H, et al. The effects of imipramine on REM sleep behavior disorder in 3 cases. Sleep Res. 1991;20A:351.Find this resource:
187. Takahashi T, Mitsuya H, Murata T, et al. Opposite effect of SSRIs and tandospirone in the treatment of REM sleep behavior disorder. Sleep Med. 2008;9:317–319.Find this resource:
188. Yamamoto K, Uchimura N, Habukawa M, et al. Evaluation of the effects of paroxetine in the treatment of REM sleep behavior disorder. Sleep and Biological Rhythms. 2006;4:190–192.Find this resource:
189. Bamford C. Carbamazepine in REM sleep behavior disorder. Sleep. 1993;16:33.Find this resource:
190. Tan A, Salgado M, Fahn S. Rapid eye movement sleep behavior disorder preceding Parkinson’s disease with therapeutic response to levodopa. Movement Disorders. 1996;11:214–216.Find this resource:
191. Mike ME, Kranz AJ. MAOI suppression of R.B.D. refractory to clonazepam and other agents. Sleep Res. 1996;25:63[abstract].Find this resource:
192. Ringman JM, Simmons JH. Treatment of REM sleep behavior disorder with donepezil: a report of three cases. Neurology. 2000;55:870–871.Find this resource:
193. Schenck CH, Bundlie SR, Mahowald MW. Delayed emergence of a parkinsonian disorder in 38% of 29 older men initially diagnosed with idiopathic rapid eye movement sleep behavior disorder. Neurology. 1996;46:388–393.Find this resource:
194. Rye DB, Dempsay J, Dihenia B, et al. REM-sleep dyscontrol in Parkinson’s disease: case report of effects of elective pallidotomy. Sleep Res. 1997;26:591[abstract].Find this resource:
195. Iranzo A, Valldeoriola F, Santamaria J, et al. Sleep symptoms and polysomnographic architecture in advanced Parkinson’s disease after chronic bilateral subthalamic stimulation. J Neurol Neurosurg Psychiatry. 2002;72:661–664.Find this resource:
196. Arnulf I, Bejjani BP, Garma L, et al. Improvement of sleep architecture in PD with subthalamic stimulation. Neurology. 2000;55:1732–1734.Find this resource:
197. Piette T, Mescola P, Uytdenhoef P, et al. A unique episode of REM sleep behavior disorder triggered during surgery for Parkinson’s disease. J Neurol Sci. 2007;253:73–76.Find this resource:
198. Schuld A, Kraus T, Haack M, et al. Obstructive sleep apnea syndrome induced by clonazepam in a narcoleptic patient with REM-sleep-behavior disorder. J Sleep Res. 1999;8:321–322.Find this resource:
200. Lapierre O, Casademont A, Montplaisir J, et al. Tonic and phasic features of REM sleep behavior disorder. Sleep Res. 1991;20:276.Find this resource:
201. Watanabe T, Sugita Y. REM sleep behavior disorder (RBD) and dissociated REM sleep. Nippon RTNSHO Jpn J Clin Med. 1998;56:433–438.Find this resource:
202. Montagna P, Lugaresi E. Agrypnia excitata: a generalized overactivity syndrome and a useful concept in the neurophysiology of sleep. Clin Neurophysiol. 2002;113:552–560.Find this resource:
203. Cibula JE, Eisenschenk S, Gold M, et al. Progressive dementia and hypersomnolence with dream-enacting behavior. Oneiric dementia. Arch Neurol. 2002;59:630–634.Find this resource:
204. Mahowald MW, Schenck CH. Status dissociatus: a perspective on states of being. Sleep. 1991;14:69–79.Find this resource:
205. Lehner PN. Handbook of Ethological Methods, 2nd ed. New York: Cambridge University Press, 1996.Find this resource:
206. Tassinari CA, Rubolli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias. A neuroethologic approach. Neurol Sci. 2005;26:s225–s32.Find this resource:
207. Mahowald MW, Schenck CH, Goldner M, et al. Parasomnia pseudo-suicide. J Forens Sci. 2003;48:1158–1162.Find this resource:
208. Schenck CH, Mahowald MW. Injurious sleep behavior disorders (parasomnias) affecting patients on intensive care units. Intensive Care Med. 1991;17:219–224.Find this resource:
209. Knappman EW. Great American Trials: From Salem Witchcraft to Rodney King. Gale Group, 1994.Find this resource:
210. Yellowless D. Homicide by a somnambulist. J Mental Sci. 1878;24:451–458.Find this resource:
211. Fain v Commonwealth. 1879. 78 Ky.183Find this resource:
212. Regina v Parks, 2 S.C.R. 871. Canada; 1992.Find this resource:
213. Broughton R, Billings R, Cartwright R, et al. Homicidal somnambulism: a case report. Sleep. 1994;17:253–264.Find this resource:
214. Tononi G, Koch C. The neural correlates of consciousness: an update. Ann NY Acad Sci. 2008;1124:239–261.Find this resource:
215. Tononi G. The information integration theory of consciousness. In: Max Velmans SS, ed. The Blackwell Companion to Consciousness. 1st ed. Blackwell Publishing Ltd., 2007:287–299.Find this resource:
216. Mahowald MW, Schenck CH. Parasomnias: sleepwalking and the law. Sleep Med Rev. 2000;4:321–339.Find this resource:
217. Pressman MR, Mahowald MW, Schenck CH, et al. No scientific evidence that alcohol causes sleepwalking. J Sleep Res. 2008;17:473–474 [letter to editor].Find this resource:
218. Whitlock FA. Criminal Responsibility and Mental Illness. London: Butterworths, 1963.Find this resource:
219. Prevezer S. Automatism and involuntary conduct. Criminal Law Review. 1958:361–367.Find this resource:
220. Fitzgerald PJ. Voluntary and involuntary acts. In: Guest AG, ed. Oxford Essays in Jurisprudence. Oxford University Press, 1961:1–28.Find this resource:
221. Shroder O, Mather NJ. Forensic psychiatry. In: Camps FE, ed. Gradwohl’s Legal Medicine. Chicago: A. John Wright & Sons, 1976:505.Find this resource:
222. Schopp RF. Automatism, Insanity, and the Psychology of Criminal Responsibility. New York: Cambridge University Press, 1991.Find this resource:
223. Bonkalo A. Impulsive acts and confusional states during incomplete arousal from sleep: criminological and forensic implications. Psychiatric Q. 1974;48:400–409.Find this resource:
224. Mahowald MW, Bundlie SR, Hurwitz TD, et al. Sleep violence-forensic science implications: polygraphic and video documentation. J Forensic Sci. 1990;35:413–432.Find this resource:
225. Pressman MR. Disorders of arousal from sleep and violent behavior: the role of physical contact and proximity. Sleep. 2007;30:1039–1047.Find this resource:
227. Weintraub MI. Expert witness testimony: a time for self-regulation? Neurology. 1995;45:855–858.Find this resource:
228. Goldrich MS. Report of the Council on Ethical and Judicial Affairs. CEJA Report 12-A-04 (Committee on Constitution and Bylaws). JAMA. 2004.Find this resource:
229. American Sleep Disorders Association. ASDA Guidelines for expert witness qualifications and testimony. APSS Newsletter. 1993;8:23.Find this resource:
230. Sagsveen MG. American Academy of Neurology policy on expert medical testimony. Neurology. 2004;63:1555–1556 [editorial].Find this resource:
231. Freeman JM, Nelson KB. Expert medical testimony. Responsibilities of medical societies. Neurology. 2004;63:1557–1558.Find this resource:
232. Cramer Bornemann M. Health law: role of the expert witness in sleep-related violence trial. AMA J Ethics. 2008;10:571–577.Find this resource:
233. Churchland PS. The impact of neuroscience on philosophy. Neuron. 2008;60:409–411.Find this resource:
234. Gazzaniga MS. The law and neuroscience. Neuron. 2008;60:412–415.Find this resource: