Sleep walking or somnambulism is a sleep disorder characterised by ambulation during sleep, the persistence of sleep and an altered state of consciousness. It is also characterized by recurrent events of complex motor behaviour mostly occurring during the first third of the night where NREM sleep is predominant. Sleepwalkers are difficult to arouse, confused when awakened and have complete or partial amnesia to the event. Sleep walking has been defined as “a series of complex behaviours that are usually initiated during arousals from slow-wave sleep and culminate in walking around with an altered state of consciousness an impaired judgement” (1). Together with confusional arousals and sleep terror, they form a group of parasomnias known as NREM parasomnias, which is based on the sleep state from which they arise from.
Sleep walking is a common occurrence during childhood, with a prevalence of up to 11% at 7 and 8 years of age (2). This prevalence decreases in adulthood to about 2-4% (3). Approximately 25% of children who have sleep walking will continue to have this disorder in adulthood. Childhood somnambulism is considered a benign condition and medical intervention is usually unnecessary, with only environmental modifications occasionally needed. However this is not true in adulthood, where it is the leading cause for sleep related violence or self-harm (4). Sleepwalkers may also complain of excessive daytime sleepiness and fatigue, insomnia, anxiety and depression symptoms (5).
Despite being the subject of more than 5 decades of scientific research, the underlying fundamental pathophysiology of somnambulism remains unclear. In this essay, we will briefly describe 3 of the more commonly held causal hypothesis and their supporting evidence. We will discuss which of these hypothesis is the most compelling and can best explain the occurrence of sleep walking.
Sleep walking as a disorder of arousal
Somnambulism was described by Broughton et al in 1969 as an arousal disorder (6). A sudden partial arousal from NREM sleep was believed to be the cause of sleepwalking. The theory of a partial arousal was due to the observation of autonomic and motor arousals associated with incomplete wakefulness. Sleep walking behavioural episodes were observed to occur from sudden but incomplete arousals from slow‐wave sleep initially. However, it was subsequently documented that such episodes may also occur from arousals from stage N2 sleep (7).
That sleepwalking was a disorder of arousal was an early hypothesis framework that was tied in with the developing understanding of the neurophysiological basis of sleepwalking.
In 1965 Kales and Jacobsen performed all night electroencephalogram (EEG) studies on 8 children and 3 adults with somnambulism. They demonstrated that sleep walking episodes occurred during slow-wave sleep. The episodes were not related to dream periods (REM sleep) and there was no evidence of wakefulness (8). In 1998, Schenck et al studied 252 arousals in 38 adult subjects with sleep walking and demonstrated 3 EEG postarousal patterns that characterise slow-wave sleep arousals and sleep walking episodes. There was no evidence of wakefulness detected on these EEG patterns. It was also noted that there were no discernible increase in the prearousal EEG patterns, nor heart rate increases, nor tonic/phasic EMG activation. This led the authors to conclude that sleepwalking was likely to arise from an arousal (likely an abrupt arousal) rather than leading to it (9). To characterise the distribution of postarousal EEG pattern in sleep walkers, Zadra et al studied 10 sleepwalkers during normal sleep and after a 38 hour sleep deprivation period. They detected EEG delta activity (indicative of sleep related processes) in 48% of the sleepwalking behavioural episodes emerging from slow-wave sleep. There was no EEG evidence of complete awakening during any of the sleepwalking episodes (10).
These findings led to the theory that sleepwalking episodes were triggered by a sudden arousal and sleepwalkers were in a state of partial arousal between NREM sleep and wakefulness. During sleepwalking episodes, subjects were neither fully awake (reduced awareness and responsiveness) nor were they fully asleep (complex behavioural motor activity).
There are other observations that support sleep walking as an arousal disorder. For instance, if sleepwalking is an arousal disorder, then arousals that occur from slow-wave sleep or N2 sleep should induce sleepwalking episodes in sleepwalking subjects. Also, conditions that increase arousals in slow-wave sleep should also worsen sleepwalking. Triggering arousals may be spontaneous in nature or are produced by other sleep disorders or external stimuli.
A common sleep disorder is that of sleep disordered breathing. Several studies in the literature have shown the association of sleep disordered breathing and sleepwalking episodes. Espa et al performed polysomnographic studies on 10 subjects with NREM parasomnias (sleepwalking, sleep terrors or both) and 10 control subjects for 3 consecutive nights. They measured respiratory effort with an oesophageal pressure monitor. The authors found that respiratory events in the parasomnia subjects led to more frequent arousals as compared to the control group. They also found that respiratory events were precipitated parasomnia episodes (11). Guilleminault et al performed a study on 84 prepubertal children with parasomnias and found that 61% of these children had a concomitant sleep disorder. 49 had sleep disordered breathing and 2 had restless leg syndrome. 43 of the 49 children with sleep disordered breathing were treated for their condition through surgical management and the 2 children with restless leg syndrome were treated with medications as well. They reported that after adequate treatment of the concomitant sleep disorder, parasomnia events in all 45 children were eliminated (12). Pilon et al in 2008 precipitated sleep walking events using a combination of sleep deprivation and auditory stimuli in 10 sleep walkers. They managed to induce at least 1 episode in 100% of the subjects by presenting an auditory stimuli during recovery slow-wave sleep following sleep deprivation. In contrast, no control subjects exhibited these behaviours under similar conditions (13).
These studies and their findings suggest that sleepwalkers have an abnormal reaction to arousals, leading to sleepwalking episodes. It may also suggest that (at least in children) treatment of sleep disorders that trigger arousal may prevent these episodes.
In summary, the strength of the hypothesis that sleepwalking may arise from a disorder of arousals rests mainly on studies showing that sleep walkers have incomplete awakenings from sleep. This is established by characteristic post-arousal EEG patterns and abnormal arousal reactions despite the persistence of sleep. The supporting evidence for this theory is that conditions or disorders that increases arousals in slow-wave sleep worsen sleep walking.
Sleep walking as a disorder of slow-wave sleep
The hypothesis of a slow-wave sleep disorder as the mechanism for sleepwalking is built along 2 lines. One is the observation of innate abnormalities of slow-wave sleep seen in sleep walkers. This is also commonly referred to as NREM instability. The second is the abnormal response of sleep walkers to sleep deprivation.
There are established differences seen in the slow-wave sleep EEG patterns of sleep walkers compared to healthy controls. One such difference is that sleep walkers have an increased amounts of hypersynchronous delta waves during NREM sleep as compared to healthy controls. Hypersynchronous delta waves was first described in 1965 by Jacobson et al as occurring prior to sleepwalking episodes (8). These patterns are characterised by several continuous high voltage delta waves (>150 μV). Pilon at al in 2006 demonstrated significant higher ratios of hypersynchronous delta waves in sleepwalkers as compared to healthy controls regardless of the occurrence of sleepwalking episodes (14). However, unlike what was described by Jacobson, Pilon et al found that sleep walking episodes were not preceded by a build-up of hypersynchronous delta waves. Jaar et al performed a study in 2010 to determine the slow-wave activity prior to sleep walking events in 22 adult sleep walkers. They found, using time course comparisons, that there was a sudden increase in the density of high amplitude very slow oscillations (<1 Hz) during the final 20 seconds immediately preceding a sleep walking episode onset. Hypersynchronous delta waves were not observed. These findings were not seen in normal subjects. The exact pre-event EEG parameters that characterise a sleepwalking episode remains undetermined (15).
Sleepwalkers also exhibit reduced slow-wave activity and reduced consolidated NREM sleep (ie, more awakenings) as compared to healthy controls. Gaudreau et al performed power spectral analysis on the polysomnograms recorded from 15 sleepwalkers and 15 healthy controls. They found that sleepwalkers had significantly more awakenings from slow wave sleep as compared to control subjects. Sleepwalkers were also found to have lower levels of slow-wave sleep activity during the first NREM sleep cycle (16). These findings were consistent to Guilleminault and colleague’s 2001 spectral analysis study of the EEG slow-wave activity recorded on 12 sleepwalking subjects and 12 controls. They too reported sleepwalking subjects as having more disturbed sleep than controls during the first sleep cycle. This was evidenced by a greater number of arousals and lower levels of slow-wave activity during the first sleep cycle. The lower level of slow-wave activity at the start of the night correspondingly led to a lower rate of slow-wave activity decline through the night (17). These findings led to the theory of NREM instability. As a consequence of frequent arousals during the early sleep cycles of slow-wave sleep seen in sleep walkers, the normal consolidation of slow-wave activity is impaired leading to NREM instability. NREM instability in turn is seen as a precipitating factor for sleep walking episodes.
Cyclic alternating pattern analysis studies performed on sleep walkers yield similar findings. Cyclic alternating pattern is seen as a marker for NREM sleep instability. Guilleminault and colleagues performed 2 studies using cyclic alternating patterns 2 groups of sleepwalkers. One on young adults and one on pre-purbertal children. Both studies showed that sleepwalkers demonstrated, using cyclic alternating pattern analysis, instability of NREM sleep on nights with no sleep walking episodes (18) (19). Zucconi et al showed that although classic sleep macrostructure in patients with sleep walking and sleep terrors were unchanged, cyclic alternating pattern rates and cycles were increased in this group of subjects (20). Slow-wave sleep fragmentation is then thought as a predisposing factor for the occurrence of sleepwalking.
Sleepwalkers also show an abnormal response to sleep deprivation. In normal healthy subjects, sleep deprivation induces a rebound of slow wave sleep and also consolidates NREM sleep (21). Sleepwalkers do not exhibit this normal physiological response. Sleep deprivation in sleep walkers results in more awakenings from slow-wave sleep during recover sleep (13) (22). Zadra et al also demonstrated in 40 sleepwalkers that 25 hours of sleep deprivation resulted in an increase in frequency and complexity of sleepwalking events. The authors concluded that the mechanisms responsible for sustaining stable slow-wave sleep are disrupted in sleep walkers (22). These findings were consistent with other investigations on the effect of sleep deprivation in sleepwalkers (23). In these studies, sleep deprivation did not induce any sleepwalking episodes in normal healthy controls. Sleep deprivation was not the cause for sleepwalking.
In summary, the strength of the hypothesis that sleep walking arises as a consequence of a disorder of slow-wave sleep rests heavily on the presence of intrinsic abnormalities of slow-wave sleep seen in sleepwalkers. These include increased spontaneous arousals, decreased slow-wave activity, increased cyclic alternating pattern rate (NREM instability) and hypersynchronous delta waves or very slow oscillations just before sleepwalking episodes. The supporting evidence is the abnormal response of sleep walkers to sleep deprivation, leading to an absence of normal rebound of slow-wave sleep and an increase in the frequency and complexity of sleep walking episodes.
Sleep walking as a disorder of state dissociation
The most recent mechanistic hypothesis for sleep walking is the theory that sleepwalkers may exhibit a simultaneous coexistence states of wakefulness and NREM sleep. This is based on the concept of state dissociation. The traditional concept that sleep and wakefulness states occur in an either “all or none” global state in the entire brain has been challenged. Evidence now shows that wakefulness, REM sleep and NREM sleep may coexist in the brain in different topographical regions (24). The theory is that sleep is not a global or whole brain situation but can and does exist as a local regional situation. Therefore, the interplay of wakefulness, NREM sleep, and REM sleep states may exist, and in varying combinations. Sleepwalking may occur as a consequence of a dysfunction or an imbalance between these states.
There are growing studies that have provided evidence to support this theory making it a viable neurophysiological model and potentially a neurobiochemical model. This current model proposes that there is concurrent deactivation of the frontal associative areas of the brain with a concurrent activation of the cingulate motor cortex of the brain during sleepwalking episodes. The activation of cingulate motor areas would enable the complex behavioural motor activities observed in sleepwalking. The paradoxical deactivation of frontal cortex areas would be consistent with the reduction of awareness and mentation also seen in sleepwalking. We present the evidence for this working model.
Intracerebral EEG investigations by Nobili et al demonstrated that wakefulness and sleep patterns may coexist in different areas during normal sleep in subjects without sleep. The authors goal was to investigate the coexistence of wakefulness and sleep electrophysiological behaviours in the brain during normal sleep. The subjects were 5 patients with drug treatment resistant focal epilepsy. These patients had no sleep disturbances. These patients had presurgical intracerebral EEG localisation investigations and recordings were obtained after informed consent. The authors analysed both EEG data obtained from scalp and intracerebral electrodes placed within the motor cortex and the prefrontal cortex. Readings were taken during normal sleep. The findings were that the motor cortex showed increased activations hallmarked by an a sudden disruption of EEG slow wave pattern and by a wakefulness-like high frequency EEG pattern. Local activations in the motor cortex coexisted with EEG patterns of deep sleep in other regions, as evidenced by the concurrent increase in slow-wave activity in the prefrontal cortex. These results revealed that the coexistence of wakefulness and sleep EEG patterns in different cortical areas takes place in normal sleep. The authors proposed that an imbalance of the 2 states of wakefulness and sleep could result in NREM parasomnias (30).
Studies using multiple modalities to study local electrophysiological activity conducted in sleepwalkers would reveal this exact process. In 2000, Bassetti et al reported the use of single photon emission computed tomography (SPECT) brain imaging in a 17 year old subject with a history of sleep walking. During a sleep walking episode, SPECT analysis of regional cerebral blood flow revealed that there was persistent deactivation of the frontoparietal associative cortices. This was indicative and typical of a sleep state. However, paradoxically, there was also concomitant activation of posterior cingulate and anterior cerebellum pathways. This activation was consistent with motor activity during wakefulness (25). The authors also demonstrated that these perfusion patterns were different as compared to normal subjects. In normal sleeping subjects, there was a reduction in regional cerebral perfusion in both the associative frontoparietal cortex as well as the motor cingulate areas.
In 2009, Terzaghi et al obtained intracerebral EEG recordings of a sleepwalking episode in a young adult. The recording demonstrated wakefulness EEG patterns in the motor and cingulate cortices with increased delta activity (indicating slow-wave sleep) concurrently in the frontal and parietal cortices. This proved the neurophysiological coexistence of local states of wakefulness and sleep in different regions of the brain. The activation of cingulate and motor cortices would be able to explain the complex behaviours seen in sleep walking and the deactivation of the frontoparietal cortices would be able to explain the reduction of environmental awareness and mentation that is also seen in these episodes (26). These findings were also demonstrated in confusional arousals. In 2012 Terzaghi and colleagues reported on the intracerebral EEG findings of a 7 year old boy with confusion arousals. They demonstrated EEG patterns of persistent sleep in the frontal associative cortices, as well as the concurrent coexistence of EEG patterns of awakening in the motor and cingulate cortices. The conclusion was that the clinical parasomniac features of confusional arousal was likely as a result of disordered coexistence of local cortical wakefulness and local cortical sleep (27).
A recent high density EEG (256 channels) study was conducted by Castelnovo et al in 2016 on 15 adult subjects with sleep arousal disorders and 15 healthy controls (age and gender matched). This study found that subjects with sleep arousal disorders had a localised reduction in slow-wave activity in the cingulate and motor cortices as compared to normal subjects (28). These findings are consistent with earlier studies done by Bassetti et al (25). The frontoparietal areas demonstrated increased slow-wave activity but this was found to not be significant after multiple comparison correction tests. Nevertheless, the implication was the presence of localised NREM instability or excitability in a brain area responsible for motor control.
Januszko et al utilized a non-invasive EEG neuroimaging (eLORETA) technique to investigate local arousal pattern activity immediately preceding a sleepwalking event in 15 adult subjects with sleepwalking. In these subjects, they compared the neuroimaged current density distribution in the 4 seconds immediately preceding a sleepwalking episode with the current density distribution during earlier 4 second epochs not associated with a sleepwalking episode. They found that there were significant brain activations in Brodmann areas 33 and 24 (corresponding to the beta 3 frequencies of 24-30 Hz) just before the onset of a sleep walking episode. Brodmann areas 33 and 24 are subdivisions of the cingulate region of cerebral cortex. This was again consistent with previous neurophysiological findings that sleepwalking episodes are associated with activation of cingulate motor areas (29).
In 2007, Oliviero et al performed a study using transcranial magnetic stimulation to examine the excitability of the motor cortex of sleep walkers during wakefulness. 8 sleep walkers were studied along with 12 age matched normal controls. Using 3 measures of motor cortex activity, the authors found that there was reduction in short interval intracortical inhibition, cortical silent period and short latency afferent inhibition in sleep walkers as compared to normal subjects. This impaired inhibition of excitability in the motor cortex during wakefulness could explain the abnormal neurophysiological activation of these areas during sleep and sleep walking episodes (31). The authors further proposed the involvement of gamma-aminobutyric acid A (GABAA) and cholinergic (ACH) transmission in the pathogenesis of sleep walking episodes. GABAA has been reported to have a role in voluntary movement suppression during sleep. (32). GABAA function and transmission is strongly associated with short interval intracortical inhibition expression, which was measured in this study. Cholinergic (ACH) transmission is involved in the reactivity of cortical neurons to sensory stimuli. An impairment of ACH transmission is associated with increased excitability measures. The authors hypothesised that the impaired inhibition of excitability of the motor cortex could be due to GABAA and ACH dysfunction. This would wold explain the features of lack of suppression of movements as well as reduced responsiveness to sensory stimuli observed in sleep walkers.
If there were neurophysiological functional differences in the cortices of sleepwalkers, would there also be neuroanatomical differences in these regions? In 2017, a study using 3 Tesla magnetic resonance imaging (MRI) was performed on 14 sleep walkers and 14 healthy controls who were age and gender matched. They found statistically significant reduction of gray matter volume in the left dorsal posterior cingulate cortex and posterior mid-cingulate cortex in sleep walkers as compared to the control group. The authors proposed that these changes may represent a neuroanatomical basis for the dissociative state theory of sleep walking (33).
These current research studies establishes the presence of neurophysiologic abnormalities in the brains of sleep walkers that are present both during sleep and wakefulness. Only one paper has reported possible neuroanatomical abnormalities. Consistently, these studies show a general consensus in the observations of the deactivation of the frontoparietal areas with concurrent activation cingulate motor cortex in sleep walkers.
Discussion
Sleepwalking has long been recognised as an abnormal behaviour and has been culturally documented throughout history. Authors such as William Shakespeare, Vincenzo Bellini and Charles Brockden Brown have incorporated somnambulism into their plays, operas, and novels. Early theories of somnambulism included demonic possession as well as the unconscious re-enactment of suppressed traumatic memories (34).
We do know that there is a likely genetic basis for sleepwalking. The Finnish Twin Cohort study in 1997 of 1045 monozygotic twins and 1899 dizygotic twins showed a 1.6 times greater concordance rate in monozygotic as compared to dizygotic twins for childhood sleepwalking. For adult sleepwalking, this rate was 5.3 times (35). In Kales et al study on hereditary factors in sleepwalking, they found that compared to the general population, first-degree relatives of sleepwalkers had a 10-fold increased risk of sleepwalking (36). Licis et al studied 4 generations of a single family with 9 sleepwalkers and 13 normal family members. Using DNA parametric linkage analysis, they found that sleepwalking could be inherited as an autosomal dominant trait with reduced penetrance. They also described a possible genetic locus at chromosome 20q12-q13.12 (37).
In this essay, we have laid out the current theories for the cause of sleepwalking. The evidence for each theory have been discussed and remain viable explanations for each hypothesis. Although initially described as distinct pathophysiological processes, they can be viewed as a common mechanistic pathway. Therefore most compelling mechanistic hypothesis would be consistent with all three theories and the findings of all the studies mentioned above.
The evidence in the studies mentioned propose that in genetically predisposed individuals, the presence of NREM instability (as evidenced by increased arousal, reduced slow-wave activity in the initial sleep cycles, increased cyclic alternating patterns) leads to increased events of arousal from slow-wave sleep. It is these arousals that trigger a concomitant dissociative state of wakefulness and sleep in localised areas of the brain. The post-arousal EEG patterns seen in the associative frontoparietal areas and cingulate motor areas then explain the clinical phenomenon of complex behavioural motor activities with reduced responsiveness and awareness. Consistent with this mechanism would be the abnormal response of sleep deprivation in sleepwalkers which increases the NREM instability and worsens the condition. Also consistent with this hypothesis is the observation that conditions that increase arousals in slow-wave sleep also worsen sleepwalking. Taken individually, the separate hypothesis would not be able to explain the total body of neurophysiological and clinical findings seen in sleepwalking subjects. Taken collectively, there is consistency in these observations.
Further research would be needed to establish the exact pathophysiology of sleepwalking. One such area would be the use of functional neuroimaging modalities to study the patterns of cerebral perfusion and metabolism during normal sleep in normal subjects and in normal sleep in sleepwalker subjects. This could be extended during wakefulness as well. More detailed neuroanatomical imaging studies may be able to shed light on the exact anatomical substrate responsible in sleepwalkers. These studies may also be able to offer a non-polysomnographic based diagnosis of sleepwalking. Lastly, more molecular studies are required to identify the genes that predispose to sleepwalking.
Conclusion
A exact neurophysiological and neurobiological mechanism of sleepwalking remains unclear. However current evidence posts to several components of this mechanism. The most compelling mechanistic hypothesis would need to be consistent to all these components, and this is the hypothesis that a synthesis of all 3 theories of disorders of arousals, disorders of slow-wave sleep and a disorder of simultaneous dissociative states of sleep and wakefulness. Further research is required to elucidate the exact genetic basis, neuroanatomical, neurophysiological and neurobiochemical mechanism for sleepwalking.
References
American Academy of Sleep Medicine. ICSD-II: the international classification of sleep disorders: diagnostic and coding manual, 2nd edn. Westchester: American Academy of Sleep Medicine, 2005.
Petit D, Paquet J, Touchette E, Montplaisir J. Sleep: an unrecognized actor in child development. Montreal: Institut de la Statistique du Québec, 2010.
Ohayon MM, Mahowald MW, Dauvilliers Y, Krystal AD, Leger D. Prevalence and comorbidity of nocturnal wandering in the U.S. adult general population. Neurology 2012; 78: 1583–89.
Moldofsky H, Gilbert R, Lue FA, MacLean AW. Sleep-related violence. Sleep 1995; 18: 731–39.
Lopez R, JaussentI, Scholz S, Bayard S, Montplaisir J, Danvilliers Y. Functional impairment in adult sleepwalkers: a case-control study. Sleep. 2013:36:345-51
Broughton RJ. Sleep disorders: disorders of arousal? Enuresis, somnambulism, and nightmares occur in confusional states of arousal, not in “dreaming sleep”. Science 1968; 159: 1070–78.
Joncas S, Zadra A, Paquet J , Montplaisir J. The value of sleep deprivation as a diagnostic tool in adult sleepwalkers. Neurology, 2002, 58:936-940.
Jacobson, A., Kales, A., Lehmann, D. and Zweizig, J. R. Somnambulism: all‐night electroencephalographic studies. Science, 1965, 148: 975–977.
Schenck CH, Pareja JA, Patterson AL, Mahowald MW. Analysis of polysomnographic events surrounding 252 slow-wave sleep arousals in thirty-eight adults with injurious sleepwalking and sleep terrors. J Clin Neurophysiol 1998; 15: 159–66.
Zadra A, Pilon M, Joncas S, Rompre S, Montplaisir J. Analysis of postarousal EEG activity during somnambulistic episodes.
J Sleep Res 2004; 13: 279–84.Espa F, Dauvilliers Y, Ondze B, Billiard M, Besset A. Arousal reactions in sleepwalking and night terrors in adults: the role of respiratory events. Sleep 2002; 25: 871–75.
Guilleminault C, Palombini L, Pelayo R, Chervin RD. Sleepwalking and sleep terrors in prepubertal children: what triggers them? Pediatrics 2003; 111: e17–25.
Pilon M, Montplaisir J, Zadra A. Precipitating factors of somnambulism: impact of sleep deprivation and forced arousals. Neurology 2008; 70: 2284–90.
Pilon M, Zadra A, Joncas S, Montplaisir J. Hypersynchronous delta waves and somnambulism: brain topography and effect of sleep deprivation. Sleep 2006; 29: 77–84.
Jaar O, Pilon M, Carrier J, Montplaisir J, Zadra A. Analysis of slow-wave activity and slow-wave oscillations prior to somnambulism. Sleep 2010; 33: 1511–16.
Gaudreau H, Joncas S, Zadra A, Montplaisir J. Dynamics of slow-wave activity during the NREM sleep of sleepwalkers and control subjects. Sleep 2000; 23: 755–60.
Guilleminault C, Poyares D, Aftab FA, Palombini L. Sleep and wakefulness in somnambulism: a spectral analysis study. J Psychosom Res 2001; 51: 411–16.
Guilleminault C, Kirisoglu C, da Rosa AC, Lopes C, Chan A. Sleepwalking, a disorder of NREM sleep instability. Sleep Med 2006; 7: 163–70.
Guilleminault C, Lee JH, Chan A, Lopes MC, Huang YS, da Rosa A. Non-REM-sleep instability in recurrent sleepwalking in pre-pubertal children. Sleep Med 2005; 6: 515–21.
Zucconi M, Oldani A, Ferini-Strambi L, Smirne S. 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: 147–54.
Borbely AA, Baumann F, Brandeis D, Strauch I, Lehmann D. Sleep deprivation: effect on sleep stages and EEG power density in man. Electroencephalogr Clin Neurophysiol 1981; 51: 483–95.
Zadra A, Pilon M, Montplaisir J. Polysomnographic diagnosis of sleepwalking: effects of sleep deprivation. Ann Neurol 2008;
63: 513–19.Joncas S, Zadra A, Paquet J, Montplaisir J. The value of sleep deprivation as a diagnostic tool in adult sleepwalkers. Neurology 2002; 58: 936–40
Mahowald MW, Schenck CH. Dissociated states of wakefulness and sleep. Neurology 1992;42(7 Suppl. 6):44e51. discussion 52.
Bassetti C, Vella S, Donati F, Wielepp P, Weder B. SPECT during sleepwalking. Lancet 2000; 356: 484–85.
Terzaghi M, Sartori I, Tassi L, et al. Evidence of dissociated arousal states during NREM parasomnia from an intracerebral neurophysiological study. Sleep 2009; 32: 409–12.
Terzaghi M, Sartori I, Tassi L, Rustioni V, Proserpio P, Lorusso G, et al. Dissociated local arousal states underlying essential clinical features of non- rapid eye movement arousal parasomnia: an intracerebral stereo- electroencephalographic study. J Sleep Res 2012;21(5):502e6.
Castelnovo A, Riedner BA, Smith RF, Tononi G, Boly M, Benca RM. Scalp and source power topography in sleepwalking and sleep terrors: a high-density EEG study. Sleep 2016;39(10):1815e25.
Januszko P, Niemcewicz S, Gajda T, Wolynczyk-Gmaj D, Piotrowska AJ, Gmaj B, et al. Sleepwalking episodes are preceded by arousal-related acti- vation in the cingulate motor area: EEG current density imaging. Clin Neurophysiol 2016;127(1):530e6.
Nobili L, Ferrara M, Moroni F, et al. Dissociated wake-like and sleep-like electro-cortical activity during sleep. Neuroimage 2011; 58: 612–19.
Oliviero A, Della Marca G, Tonali PA, Pilato F, Saturno E, Dileone M, et al. Functional involvement of cerebral cortex in adult sleepwalking. J Neurol 2007;254(8):1066e72.
Sohn YH, Wiltz K, Hallett M. Effect of volitional inhibition on cortical inhibitory mechanisms. J Neurophysiol 2002;88(1):333e8.
Heidbreder A, Stefani A, Brandauer E, Steiger R, Kremser C, GizewskiE R, et al. Gray matter abnormalities of the dorsal posterior cingulate in sleep walking. Sleep Med 2017;36:152e5.
Pressman M, Broughton R. NREM arousals parasomnias. In: Chokroverty S, Billiard M, editors. Sleep Medicine: a comprehensive guide to its development, clinical milestones and advances in treatment; 2015. p. 375e90.
Hublin C, Kaprio J, Partinen M, Heikkila¨ K, Koskenvuo M. Prevalence and genetics of sleepwalking: a populationbased twin study. Neurology 1997;48:177–181.
Kales A, Soldatos CR, Bixler EO, et al. Hereditary factors in sleepwalking and night terrors. Br J Psychiatry 1980; 137:111–118.
Licis AK, Desruisseau DM, Yamada KA, Duntley SP, Gurnett CA. Novel genetic findings in an extended family pedigree with sleepwalking. Neurology 2011 Jan 4; 76(1): 49–52.