Dreamlike Mentations during SleepWalking in Adults Dreamlike Mentations During Sleepwalking and Sleep Terrors in Adults Delphine Oudiette, MSc; Smaranda Leu, MD; Michel Pottier, MD; Marie-Annick Buzare, MD; Agnès Brion, MD; Isabelle Arnulf, MD, PhD Sleep Disorders Unit, Pitié-Salpêtrière Hospital, APHP, UMR 975, CRICM, and Paris 6 University, Paris, France Background: Sleep terrors and sleepwalking are described as arousals from slow wave sleep with no or poor mental recollection. Objective: To characterize the mental content retrospectively associated with sleep terrors or sleepwalking. Setting: University Hospital Design: Controlled prospective cohort Participants: Forty-three patients referred for severe sleepwalking/sleep terrors (age: 26 ± 7 y, 46% men, 5 with sleep terrors only, 8 with sleepwalking only, and 30 with both), matched with 25 healthy control subjects. Intervention: Thirty-eight of the 43 patients (88%) underwent an interview about the frequency, time, behaviors, and mental content associated with the episodes of sleepwalking and sleep terrors, whenever they occurred over a lifetime. The mental contents were classified for complexity (Orlinski score), and for characters, emotions, fortune/misfortune, and social interactions (Hall and Van de Castle categories). Patients and control subjects underwent an overnight video-polysomnogram. Results: Seventy-one percent of the patients reported at least 1 dreamlike mentation associated with the sleepwalking/sleep terrors episode. The dreamlike mentation action corresponded with the observed behavior. A total of 106 dreamlike mentations were collected (mean: 3 ± 3.4 dreamlike mentations/patient, range 0-17). Most (95%) dreamlike mentations consisted of a single visual scene. These dreamlike mentations were frequently unpleasant, with aggression in 24% (the dreamer being always the victim), misfortune in 54%, and apprehension in 84%. The patients with dream mentations reported more severe daytime sleepiness. Conclusion: Short, unpleasant dreamlike mentations may occur during sleepwalking/sleep terrors episodes, suggesting that a complex mental activity takes place during slow wave sleep. Sleepwalking may thus represent acting out of the corresponding dreamlike mentation. Keywords: Sleepwalking, sleep terror, dream Citation: Oudiette D; Leu S; Pottier M; Buzare MA; Brion A; Arnulf I. Dreamlike mentations during sleepwalking and sleep terrors in adults. SLEEP 2009;32(12):1621-1627. SLEEPWALKING AND SLEEP TERRORS CONSIST OF A SERIES OF COMPLEX BEHAVIORS THAT ARE INITIAT� ED DURING SUDDEN AROUSALS FROM SLOW WAVE sleep (SWS). Episodes often begin with sitting up in bed and looking about in a confused manner. Sleepwalking and sleep terrors show considerable overlap and share many features. In� deed, at least 1�������������������������������������������������� ��������������������������������������������������� of the following is present in both of the disor� ders: (1) difficulty arousing the person, (2) mental confusion when awakened from an episode, (3) complete or partial amne� sia for the episode, and (4) dangerous or potentially dangerous behaviors during the episode.1 Both disorders arise from SWS, frequently cooccur in the same family or patient, and have a strong genetic background.2 In contrast with SWS, rapid eye movement (REM) sleep has, for a long time, been considered as the neurobiologic basis of dreaming. Nevertheless, complex mentations are re� ported in 5% to 74% of non-rapid eye movement (NREM) sleep awakenings.3-8 The extent to which the reported men� tation may legitimately be described as “dreaming” is still debated.8,9 Indeed, there are qualitative and quantitative differ� ences between NREM- and REM-sleep dreams. NREM-sleep dreams, especially when elicited during the first half of the night, are usually reported as being shorter, less complex, less vivid, and more “thought like” than REM-sleep dreams.7,10-12 NREM sleep dreams can also be a recollection of the previous REM-sleep dreams. Although there are sporadic descriptions of the mental con� tent associated with sleepwalking or sleep terrors in the litera� ture,13-18 there is a general consensus against a complex dream activity associated with the sleepwalking/sleep terrors.19 More� over, some authors have proposed that the sleepwalking/sleep terrors is triggered by the physiologic changes occurring dur� ing the arousal state (e.g., accelerated heart rate and respira� tory changes) rather than by the mental activity preceding the arousal state.20 In a cohort of patients with sleepwalking/sleep terrors, we investigate whether dreamlike mentations are fre� quent at the very moment of the episode and compare the sleep structure and daytime sleepiness of these patients with those of healthy matched control subjects. METHODS Patients All patients with sleepwalking/sleep terrors who were moni� tored with video-polysomnography (including an extensive 8-electroencephalographic channel montage) in our sleep dis� order unit during the last 2 years were prospectively evaluated. This is an adult unit with occasional investigations of children younger than 15 years of age. The patients were referred be� cause of severe nocturnal behaviors that were dangerous, dis� turbing, or frequent. Patients with parasomnia overlap disorders (when sleepwalking/sleep terrors is combined with REM sleep behavior disorder [RBD]), nocturnal epilepsy, sleep sex, and sleep-related eating disorder (as the exclusive symptoms) and patients with psychosis were excluded. There were 43 patients with sleepwalking/sleep terrors (sleepwalking only, n = 8; sleep Submitted for publication March, 2009 Submitted in final revised form August, 2009 Accepted for publication August, 2009 Address correspondence to: Isabelle Arnulf, Unité des Pathologies du Sommeil, Hôpital Pitié-Salpêtrière, 47-83 boulevard de l’Hôpital, 75651 Paris Cedex 13; Tel: 01 42 16 77 04; Fax: 01 42 16 77 00; E mail: isabelle. [email protected] SLEEP, Vol. 32, No. 12, 2009 1621 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al terrors only, n = 5; and both, i.e. displaying either sleep terrors some nights, sleepwalking some other nights, or night terrors followed by sleepwalking, n = 30). Sleepwalking was defined as (1) a history of ambulation during sleep; (2) the persistence of sleep or impaired judgment during ambulation; and (3) the disturbance was not better explained by another sleep, medi� cal, mental, neurological disorder, or medication/drug use.1 Sleep terrors were defined as (1) a history of a sudden episode of terror occurring during sleep, usually initiated by a cry or loud scream with sympathetic and behavior manifestations of intense fear; (2) difficulty in arousing the person, or mental con� fusion when awakened from an episode, or complete or partial amnesia for the episode, or dangerous or potentially dangerous behaviors; (3) the disturbance was not better explained by an� other sleep, medical, mental, neurological disorder, or medica� tion/drug use.1 In addition to these clinical criteria, we observed in all patients at least 1���������������������������������������� ����������������������������������������� of the following features on the video� polysomnography (although they are neither totally sensitive nor specific, they are supportive in the context of a systematic study): (1) at least 1������������������������������������������ ������������������������������������������� arousal during NREM sleep stage 4 associ� ated with an abnormal motor behavior suggesting surprise, con� fusion, or fear (startling, sitting in the bed, or looking around surprised); (2) numerous sudden arousals during NREM sleep stage 4; or (3) hypersynchronous delta waves before an arousal in NREM sleep stage 4. Because sleepwalking and sleep terror share many features, we pooled patients with sleepwalking with those with sleep terrors in the next part of this article. Their demographic, clinical (body mass index, Epworth Sleepiness Scale score), and sleep characteristics during polysomnogra� phy were compared with those from 25 age- and sex-matched healthy controls without sleep disorders. The control subjects were retrospectively selected from our database after they took part in another paid study. dreamlike mentation if the score ranged from 2 to 7. We used the nominal categories (characters; emotions; social interac� tions including aggression, friendliness, and sexuality; misfor� tune and good fortune; and success and failure) of the Hall and Van De Castle method to qualify each mental-content compo� nent.23 We determined the presence or absence of any given cat� egory, in accordance with the “at least 1” procedure. Because most dreamlike mentation contents in sleepwalking/sleep ter� rors contained fewer than 50 words, we used only the categories of this method, but not the normative values, which have been established for 50- 350-word dream contents. Whenever pos� sible, family members were also interviewed. A demonstrative case report of dreamlike mentation contents obtained during sleepwalking/sleep terrors is presented in the Appendix. Sleep was monitored for 1 night in all subjects using videoelectroencephalography (8 channels) in patients and 3 electro� encephalographic channels in control subjects, and we used classic channels (eyes movements, chin and leg electromyog� ������������ raphy, nasal pressure, body position, thoracic and abdominal respiratory efforts, pulse oximetry, electrocardiography, and sounds) in all participants. The sleep stages, arousals, periodic leg movements, and respiratory events were scored using the international criteria, as previously described.24 Statistics Data are presented as mean ± SD, unless otherwise specified. The comparisons between the patients and the control subjects were performed using the student t test. RESULTS Clinical Characteristics of Patients with NREM Sleep Parasomnia The 43 patients with sleepwalking/sleep terrors were aged 11 to 72 years at the time of the videopolysomnography (mean age: 26 ± 7 years). Only 1 patient was a child, the other patients being adult. Forty-six percent were male, with a mean body mass index of 22.7 ± 3.4 kg/m2 (not different from controls). Patients were 4 to 61 years old at the onset of parasomnia (mean age: 12 ± 12). They experienced sleepwalking/sleep terrors for 20 ± 12 years. They had great difficulties estimating the fre� quency of their episodes. Most patients said the episodes came irregularly, with clusters for several days to weeks. The events occurred during the first 2 hours of sleep in 88% patients. When they occurred, there was a single event per night in 55% and more than 1 event per night in 45%. The precipitating factors were alcohol intake in 14%, sleep deprivation in 28%, stress or argument in 58%, a specific context from the preceding day (such as watching a horror film or an action-filled film or read� ing a thriller) in 16%, sleeping at someone else’s house in 5%, and unknown in 16%. Investigations All patients underwent a semistructured interview admin� istered by a sleep specialist that included assessments of the medical history, any family history of parasomnia, the age at sleepwalking/sleep terrors onset, the frequency and timing of the sleepwalking/sleep terrors episodes, and predisposing fac� tors (such as alcohol intake, sleep deprivation, stress, or change of room). In addition, we asked the patients about their men� tal content during the episodes of sleepwalking or sleep terrors using the following question: ”What was going through your mind at the very moment of the episodes, whenever the night?” Our data had been gathered retrospectively, so that the dream� like mentation collection covered a lifetime span for each pa� tient. Most patients had the greatest difficulty precisely dating the time of the sleep terrors/sleepwalking-associated dreamlike mentation. After obtaining the spontaneous mentation report, we interviewed the patient more pointedly to elicit additional information, including characters, emotions, and bizarre ele� ments. We classified the mental contents according to their complexity using the Orlinski score21,22 (0: No dream recall; 1: Feeling of having dreamt but no memory of it; 2: One scene; 3: More than 1 scene; 4: Coherent dream; 5: Coherent and detailed dream with the dreamer as an actor; 6: Prolonged, image-filled scenario resembling real life; 7: Prolonged, image-filled sce� nario with bizarreness). The mental content was defined as a SLEEP, Vol. 32, No. 12, 2009 Mental Content During Sleepwalking or Sleep Terrors Thirty-eight out of 43 patients (88%, including 2/5 patients with sleep terrors only, 6/8 patients with sleepwalking only, and 30/30 patients with sleep terrors and sleepwalking) could re� liably answer questions about their mental content during the parasomnia episodes. The mental content was classified using the Orlinski score (Table 1). Among them, 27 of 38 (71%) re� ported at least 1 incidence of mental content associated with 1622 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al an episode. Four additional patients had the feeling of hav� ing dreamt during at least 1 episode but had no clear memory about the dreamlike mentation. Most mental contents (95%) were brief, corresponding with the vision of a single scene. A single patient (a child, 11 years old) experienced a prolonged, image-filled, and complex dreamlike mentation, with several scenes and odd features. An example of dreamlike mentations reported by a patient with sleepwalking and sleep terrors is detailed in Appendix. According to the categories of the Hall and Van de Castle method, 39% of patients described the pres� ence of at least 1 person. The people seen during sleepwalking/ sleep terrors were mostly unknown by the dreamer (uncertain identity: 33%, strangers: 24%), whereas only 33% were rela� tives of the dreamer. Eleven percent of patients saw animals, generally aggressive or frightening, during sleepwalking/sleep terrors. A dreamlike mentation was classified as containing ag� gression when the situation involved a deliberate intentional act on the part of 1���������������������������������������������� ����������������������������������������������� character to harm or annoy some other charac� ter. The classification of misfortune was used to handle those situations in which injury, mishap, or adversity occurred to a character through chance or environmental circumstances over which it was impossible to exert personal control (“something bad happens”). During sleepwalking/sleep terrors, most mental contents (80%) were bad dreamlike mentations with aggression (26% of the total number of dreamlike mentations) and mis� fortune (54%). In the case of aggression dreamlike mentations, the patient was never the first aggressor, except for one patient who “was ordered to stab the flesh of somebody on pain of be� ing killed.” In addition, 12% of the dreamlike mentation reports contained at least 1 act of friendliness. In all cases, the patient was a befriender who attempted to protect someone (generally a relative) from danger. In contrast, no patient in a dangerous situ� ation was befriended or rescued. There were no sexual elements in the dreamlike mentation reports. The majority of dreamlike mentations (84%) were negatively perceived, with apprehen� sion, fear, or terror at the heart of them. The 4 patients with no clear dreamlike mentation recall had only a feeling of pure fear, with no associated images (Table 2). Seventeen patients acted out nonaggressive behaviors such as laughing, singing a dirty song, or saying “how nice are the bees” with no associated dreamlike mentation recall. All patients had some additional, more usual, “good,” and classic dreams that they would recall the following morning. We tried to distinguish patients with isolated sleep terrors (n = 5), with isolated sleepwalking (n = 8), and with both phenom� ena (n = 30). Unfortunately, only 2 of 5 patients with isolated sleep terrors were appropriately interviewed, and only 1 of these 2 patients remembered at least 1 mentation (2 frightening images) associated with the sleep terrors. As for isolated sleep� walking, 6 of 8 patients were appropriately interviewed and only 2 of the 6 remembered at least 1 mentation associated with the sleepwalking. These 2 patients reported 6 different menta� tions, with 2 of 6 containing a frightening image (Supplemental Table 1 available online at www.journalsleep.org). Table 1—Characteristics of Mental Content Associated with Sleepwalking or Sleep Terrors Patients Patients with sleepwalking/sleep terrors, No. 43 Patients appropriately interviewed, No. 38 Patients with at least one mental content recall, % 71% (27 of 38) Total number of dreamlike mentations 106 Number of dreamlike mentations per person (mean ± SD) 3.0 ± 3.6 Number of dreamlike mentations per person (range) 0-17 Type of mental content: Orlinski scale No real mental content (% of 38 patients) 0. No dream recall 18% (7 of 38) 1. Feeling of having dreamt but no memory of it 11% (4 of 38) Mental content recall (% of all dreams obtained) 2. Vision of one scene 95% (101 of 106) 3. Vision of more than one scene 0% (0 of 106) 4. Coherent dream 4% (4 of 106) 5. Coherent and detailed dream, with the 0% dreamer as an actor 6. Prolonged, image-filled scenario, resembling 0% real life 7. Prolonged, image-filled scenario, with bizarre- 1% (1 of 106) ness Dreamlike mentations (% of all dreams obtained) with at least one Character People 40% (42 of 106) Animals 11% (12 of 106) Social interaction Aggression 24% (25 of 106) Dreamer as a victim, % of aggression dreams 100% (25 of 25) Dreamer as an aggressor, % of aggression dreams 4% (1 of 25) Friendliness 11% (12 of 106) Befriender, % of friendliness dreams 100% (12 of 12) Befriended, % of friendliness dreams 0% (0 of 12) Sexuality 0% (0 of 106) Fortune and misfortune Fortune 0% (0 of 106) Misfortune 54% (57 of 106) Emotions Anger 2% (2 of 106) Apprehension 84% (89 of 106) Sadness 0% (0 of 106) Confusion 0% (0 of 106) Happiness 0% (0 of 106) stages, arousal index, apnea-hypopnea index, and periodic leg movements. The number of sudden arousals from SWS varied from 1 to 13 in patients and 0 to 4 in control subjects. It was 4 times higher in patients than in control subjects. The sudden arousals from SWS were not preceded by any respiratory event, including flow limitation. The patients had an Epworth Sleepi� ness Scale score of 10 ± 4, and 47% of them had an abnormal sleepiness score (greater than 10). Their mean sleepiness score was higher than in the control group, but the control subjects were selected for having no abnormal sleepiness. Thirty-five of the 43 (81%) patients exhibited at least 1 arousal during non-REM sleep stage 4 associated with an Sleep Measures in Sleepwalkers and in Controls With regard to the sleep architecture (Table 3), there was no difference between the patient and control groups for sleep duration and efficacy, sleep-onset latency, percentages of sleep SLEEP, Vol. 32, No. 12, 2009 1623 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al Table 2—Examples of the Mental Content During Sleepwalking/Sleep Terrors and Associated Behaviors Patient Mental content Patient 4, F, 34 y Patient 4 Patient 5, F, 32 y Patient 7, F, 66 y Patient 9, F, 27 y Patient 14, F, 26 y Patient 18, F, 32 y Patient 18 She was going to get run over by a truck. Patient 19, M, 11 y Patient 25, F, 72 y Patient 28, M, 30 y Patient 34, M, 28 y She plunged into death. Behaviors (observed by a cosleeper or by the dreamer) She leapt out of bed and out of the mezzanine to avoid it. She spat in her bed to drown them. She grabbed her baby and ran out of the room with it. She yelled. She was locked in a box she could not escape. She felt herself suffocating. She pushed back the walls around her. She broke a vial containing a lethal virus. She shouted. She saw Death with its dark cape and an emaciated hand coming up close to her face and about to kill her. She saw a crack above her bed containing dead flesh. Cockroaches crawled on the dead flesh, then fell in her bed and hair. She rubbed her hair to remove them and saw a cockroach drop and run on the floor She yelled and ran away. There were spiders. Her baby was jeopardized. He went to the roof of the house because people were following him and his little brother. He forbade his brother to climb on the roof because of the danger. On the way, he picked up luminous balls. There were also people at the bottom of the house. The ceiling was collapsing. He was skiing and hurtling down an icy steep slope, with a ravine at the end of the slope. He could not stop from falling in the abyss His girlfriend was in danger. abnormal motor behavior suggesting surprise, confusion, or fear (startling, sitting in the bed, or looking around sur� prised). Most of the episodes were minor and much less im� portant than those described at home. Because these patients were first referred to our sleep unit for a clinical (and not a research) purpose, they were not interviewed by the nurse just after the brief parasomnia to collect their mentations. No pa� tient reported any dreamlike mentation when interviewed in the morning after the videopolysomnography night. A video of a patient with sleep terror (opening the eyes and looking scared before screaming) is displayed as supplemental video available online at www.journalsleep.org. On the next morn� ing, she did not remember any mental content. During similar events at home, she had the vision of being locked in a box and suffocating or being attacked by something or somebody unknown. She shouted, jumped out of the bed, and pushed the wall. He shouted and leaped out of the bed. He pulled his girlfriend out of the bed to save her. This study highlights the presence of dreamlike mentation content during an episode of sleepwalking/sleep terrors in adults. These results are concordant with those from a study of a group of 12 patients with sleep terrors who slept with elec� troencephalographic and heart rate monitoring during 4 to 23 nights.18 In this group, a mean of 58% recall of mental content was obtained after spontaneous arousals from NREM sleep as� sociated with heart rate acceleration (but not necessarily with a scream). Apart from this case series reported in 1974, dreamlike mentations associated with a sleepwalking/sleep terror episode have been described incidentally. A young patient rushed into the room where his parents were sitting and threw the butter dish out of the window, believing it to be a bomb.17 A sleepwalker threw his wife on the floor, ran to his 2 children, took them into his arms, and ran outside. He afterwards said he believed that the house was on fire.14 A father took his baby girl from her cradle, brought her into the attic and tied her, while dreaming that officials from child welfare wanted to deprive him of the custody of the baby.16 These cases illustrate that a complex mental content can be syn� chronous with elaborate motor behavior erupting from SWS, sug� gesting a mind-behavior isomorphism. One may notice, however, that the patients reported at least 1 dreamlike mentation associated with a sleepwalking/sleep terrors episode. They could not be pre� cise enough to determine how many sleepwalking/sleep terrors episodes were associated with dreamlike mentations, as they were frequently amnesic of numerous episodes. In this study, we did DISCUSSION In this group of 43 adults with sleepwalking/sleep terrors, as many as 71% of patients reported at least ������������������ 1����������������� dreamlike menta� tion associated with a nocturnal motor episode. The dreamlike mentations were mostly short and frequently unpleasant. There was no major difference regarding the frequency and nature of the dreamlike mentation content in sleepwalkers compared with patients with sleep terrors. Compared with healthy controls, the patients with sleepwalking/sleep terrors had more frequent arousals from SWS (despite a similar percentage of SWS) and reported more severe daytime sleepiness. SLEEP, Vol. 32, No. 12, 2009 She ran out of her bed, rubbed her hair, and saw the cockroach and needed time to realize that she was in the dark without any insects. He climbed onto the roof of the house. 1624 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al not systematically interview the patient spouse, Table 3—Sleep Measures in Patients with NREM Sleep Parasomnia and Controls who could possibly recall many more episodes than the patient. All in all, dreamlike mentation Patients Controls recalls were occasionally associated with sleep� Number 43 25 walking/sleep terrors, but the exact frequency of Nighttime sleep this association is still unknown. Total sleep period, min 522 ± 82 543 ± 73 The mental content associated with sleepwalk� Total sleep time, min 460 ± 76 491 ± 78 ing/sleep terrors in our patients was mostly short Sleep efficiency, % 88 ± 8 90 ± 6 and contained 1������������������������������� �������������������������������� single scene, except for 5 pa� Latency to sleep onset, min 28 ± 21 30 ± 23 tients (Patients 4, 15, 21, 18, and 1 child climbing Sleep duration, min on the roof as he followed a long and movie-like Stage 1 21 ± 12 (4.6%) 19 ± 12 (3.9%) inner scenario). This scene was visual. Similar to Stage 2 221 ± 56 (47.9%) 242 ± 55 (47.5%) our patients, a patient with sleepwalking/sleep Stage 3-4 117 ± 33 (25.7%) 123 ± 28 (25.3%) terrors in another series attempted to flee or fight REM sleep 107 ± 54 (21.7%) 105 ± 37 (21.0%) in self-defense during the night because he felt Sleep fragmentation threatened or attacked by individuals with “blank Periodic leg movements index 4.6 ± 5.1 3.4 ± 11.7 eyes” and by a cow with a knife hidden in its Apnea-hypopnea index 3.4 ± 6.9 2.0 ± 2.7 mouth as a tongue.13 One may discuss whether Arousals index 14.0 ± 9.2 15.5 ± 5.1 these brief scenes are closer to a hypnagogic hal� Number of arousals from SWS 4.8 ± 3.0* 1.2 ± 1.0 lucination from SWS than a more classic dream. Epworth Sleepiness Scale score 10 ± 4 Patient 9 (video) opened her eyes and turned her Percentage of patients with a score > than 10 47 0 head, while still in quiet SWS and then dread� NREM refers to non-rapid eye movement sleep; REM, rapid eye movement sleep; SWS, slow fully screamed. She behaved as somebody dis� wave sleep. covering a frightening scene. These brief, visual, mental contents during sleepwalking/sleep ter� rors suggest that the episodes could be either the terminal part with nonviolent sleepwalking/sleep terrors are less likely to of a longer dream forgotten at time of arousal or a phasic, short, seek medical advice. There could be a bias in our series towards mental creation elicited before or just at the time of arousal. One violent, unpleasant, or more disturbing cases. The association may wonder if these phasic visions could be triggered by ponto� of a dreamlike mentation (or a nightmare) recall with violent geniculooccipital waves that occur as rare isolated events during frightened behavior in sleepwalkers suggests that the distinc� SWS in cats, whereas they are numerous and grouped in bursts tion between sleepwalking and RBD can be difficult when it is during REM sleep.25 Some authors have proposed that sleepwalk� based only on a sleep interview. Confusion during an interview ing/sleep terrors episodes are triggered by accelerated heart and could lead to the misclassification of nocturnal violence during respiratory rates occurring during the arousal state rather than by epidemiologic surveys29 or case-reports.30 Some elements in the 20 the mental activity preceding the arousal state. Patient 9 here, interview may however direct the clinician toward a diagnosis however, does not fit the model, as she quietly opened her eyes of sleepwalking rather than RBD. They include the age (young with a normal heart rate before screaming. in NREM parasomnias, middle-aged or old in patients with The subject of scenes associated with sleepwalking/sleep ter� RBD), the occurrence of walking (frequent in NREM parasom� rors is mostly frightening, to the point that many patients call nias, exceptional in RBD),31 the frequency (low in patients with them nightmares in our clinical experience. As many as 54% NREM parasomnias, high in patients with RBD), and nature of the reports contained elements of misfortune (whereas none (a single brief scene in NREM parasomnias vs a long detailed contained fortune), 24% were aggressive, and 84% were appre� dream in RBD) of the dreamlike mentation associated with the hensive. In addition, 4 patients had “blank” dreams (the feeling behavior and, to some extent, its content. In our study, sleep� of having dreamt before arousal but with no recall) associated walkers report misfortune, whereas patients with RBD report with a pure intense fear. The strongly negative emotions associ� aggression.32 Misfortune is defined by any injury, mishap, or ated with sleepwalking/sleep terrors suggest that the emotional adversity occurring to a character through chance or environ� network, and especially the amygdala, would be activated during mental circumstances (e.g., collapsing ceiling) over which it the event. A single functional imaging session in a sleepwalker was impossible to exert personal control.23 In most dreamlike showed that the posterior cingulate cortex (which is part of the mentations reported by patients with RBD and pseudo-RBD as� emotional processing network) and the anterior cerebellum are sociated with severe obstructive sleep apnea syndrome,33 the activated during sleepwalking, whereas the frontoparietal corti� dreamers (or their loved ones) are a victim of an aggression ces are deactivated.26 Whether patients with sleepwalking/sleep (attack, rape, theft) by a human or an animal and fight back.32,34 terrors exhibit an abnormal processing of emotion, even during There is, however, possible an overlap between the contents of the daytime, as was recently shown in patients with narcolepsy/ dreamlike mentations in NREM parasomnia and RBD, so that a cataplexy, should be determined.27 videopolysomnography will be helpful in doubtful cases. Some sleepwalkers in our series, however, experienced not This study confirms previous observations that sudden only misfortune, but also sang dirty or childish songs and qui� arousals from SWS are frequent in patients with sleepwalking/ etly spoke while asleep. Similar to the previous report of non� sleep terrors and shows that the arousals are 4����������������� ��������������� times more com� violent behaviors during RBD,28 one may imagine that people mon than in healthy control subjects. Half of the patients with SLEEP, Vol. 32, No. 12, 2009 1625 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al sleepwalking/sleep terrors reported abnormal levels of daytime sleepiness. Sleepiness as a symptom of sleepwalking/sleep ter� rors has not been previously specifically highlighted. Because there is no difference other than the arousals from SWS between the patients’ and control subjects’ sleep structures (especially no more respiratory events during stage 4 sleep), we wonder whether long confused arousals from stage 4 sleep would not affect the restorative properties of sleep. These data should be considered with a number of important limitations. Sleep terrors and sleepwalking are usually described as 2 distinct parasomnias. They are pooled here, which can be considered as a limitation. They indeed show considerable over� lap, as 70% patients here have sleep terrors and sleepwalking at different periods of the night or the year or as a terror first (scream) followed by an attempt to flee out of the bed. Frightening images are not specific to sleep terrors (or sleep terrors/sleepwalking), however, as they occurred here in 2 patients with isolated sleep� walking. This result is observed in a small subsample, but it fur� ther suggests that the boundary between sleepwalking and sleep terrors is very thin. Another limitation in our study is that the dreamlike mentations have been gathered retrospectively, over a lifetime span, so that recall bias is possible. All studies on dreams are by definition retrospective, as the subject cannot at the same time experience the dream and report it to someone else. It is probable, however, that the time elapsed between the dreamlike mentation experience and the report alters the memory of the dreamlike mentation, so that an immediate recall would further enhance the percentage and the length of dreamlike mentations reported by our patients, as it is the case in normal subjects. This bias would underestimate (and not overestimate) the frequency of dreamlike mentations in our study. Also, healthy subjects tend to remember more easily the dreamlike mentations with strik� ing rather than ordinary content.35 To avoid this bias, one should perform a systematic, nightly based interview after each NREM parasomnia in a series of patients, which would be a costly but fascinating future study. Notably, because none of our 43 pa� tients had any dreamlike mentation recall the next morning in the sleep-unit settings, such a large study may require either home monitoring, staying a week in the sleep unit, or using provocative methods to increase the number of parasomnia events. In conclusion, dreamlike mentations (mostly brief, frighten� ing visual images) may occasionally exist during sleepwalking and sleep terrors, suggesting that a complex mental activity takes place during SWS. Sleepwalking may thus represent act� ing out of the corresponding dreamlike mentations. A previous study proposed that awakening serves as an indirect measure of nightmare intensity, the emotions during nightmares being more intense than during bad dreams.36 Similarly, the emotional character of the frightening image could be 1 of the proximal trigger of the sleepwalking and sleep terror. and has participated in speaking engagements for UCB. The other authors have indicated no financial conflicts of interest. References 1. International Classification of Sleep Disorders, 2nd ed: Diagnostic and Coding Manual. Westchester, IL: American Academy of Sleep Medicine; 2005. 2. Lecendreux M, Bassetti C, Dauvilliers Y, Mayer G, Neidhart E, Tafti M. HLA and genetic susceptibility to sleepwalking. Mol Psychiatry 2003;8:114-7. 3. Dement W, Kleitman N. Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencepha� logr Clin Neurophysiol 1957;9:673-90. 4. Dement W, Kleitman N. 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APPENDIX Case Report A Patient 21 was a 23-year-old 1 employee in a school who had ex� R perienced severe sleepwalking 2 and sleep terrors for 16 years. Her grandfather was a sleepwalker (he 3 jumped through the window into 4 a rosebush when he was young), and her mother still talks and walks while asleep. The patient had no 20:33 22:00 00:00 02:00 04:00 06:00 history of depression or psychologi� cal trauma. She had frequent night� Figure 1—Hypnogram of Patient 21 (case report) with 10 sudden awakenings from slow wave sleep (shown mares, several times per night, but by arrows) with corresponding behavior of surprise, sitting, and talking evoking a “status parasomnicus.” they occurred in clusters for several days or weeks at a time and then disappeared for several weeks. Fa� tions, she had to do something to survive. For example, she had tigue, stress, changes in altitude, and horror films precipitated to stay under the duvet because a superior power ordered it, she the episodes. She had fewer episodes during the holidays and had to wash her feet in the bathroom, and she had to plug the when she did not sleep at home. She complained of daytime bathroom door with clothes. Once, she saw her aggressor as a sleepiness, with an Epworth Sleepiness Scale score of 14. She Chinese dragon. In a recurrent dreamlike mentation, she was hurt herself several times during the sleepwalking episodes, in� in a large white room with many Smarties (colored chocolate cluding a broken clavicle, a twisted ankle, a head injury, and an candies) on the floor. She had to sort and pile them up accord� ear wound. During the nighttime videopolysomnography, the ing to their colors, but the stack always fell and she had to start sleep architecture was normal (without epileptiform activity), again. She required several minutes after awakening to admit except for 10 sudden awakenings from non-rapid eye move� that nothing bad had happened. When she resumed sleep, she ment sleep stage 4 (Figure 1). During these awakenings, she experienced the same dreamlike mentation again. She also ex� opened the eyes and looked, with a scared expression, around perienced dreamlike mentations resembling horror films (“the her. She sat twice on the bed and spoke shortly. At home dur� living-dead type”). She saw dead heads falling, people hanged ing the sleepwalking episodes, she was agile, opening doors, in her room, acid falling from the roof, thieves, killers, and and avoiding routine obstacles. Only unforeseeable obstacles, children from her school slaughtered by a madman. When she such as a bag left unattended on the floor the previous evening, had these types of dreamlike mentations, she screamed (wak� would cause her to fall. If someone awoke her at that time, she ing up her neighborhood), ran to the bathroom, and locked the would have superhuman strength and be very aggressive to� door. In addition, she had a recurrent dreamlike mentation in ward the intruder. She reported vivid mental imagery during the which a gorilla came into her house, grabbed her by the hair, sleepwalking episodes. She experienced recurrent nightmares and dragged her down the stairs. During this dreamlike menta� with short scenarios including floods, collapsing buildings, tion, she was partly aware but could not refrain from screaming fires, and 2 walls getting closer to the point of crushing her. and taking part in her dreamlike mentation, while she simulta� In these cases, she had to escape and felt extreme apprehen� neously thought “Oh no, not the gorilla again!” Her dreamlike sion. She shouted loudly, ran away from the bed, and hid in the mentation could also be influenced by daytime context. During bathroom or under the living room table. She was able to dress the rugby world cup 2007 in Paris, she dreamt that an army of within a few seconds to get out of the apartment and hurtle rugbymen wanted to kill her. Of note, she also had good dreams down the stairs before being aware that it was just a nightmare. but did not remember a sleepwalking episode associated with She also experienced other types of mental content, that she good dreams, nor did her boyfriend report such occurrences. herself called “the mission dreams.” In these dreamlike menta� SLEEP, Vol. 32, No. 12, 2009 1627 Dreamlike Mentations and Sleep Terrors in Adults—Oudiette et al
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