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Nonviolent elaborate behaviors may alsooccur in REM sleep behavior disorder
D. Oudiette, MScV.C. De Cock, MD,PhDS. Lavault, MScS. Leu, MDM. Vidailhet, MDI. Arnulf, MD, PhD
ABSTRACT
Objective:
To document unusual, nonviolent behaviors during REM sleep behavior disorder (RBD)and evaluate their frequency in Parkinson disease (PD).
Background:
Most behaviors previously described during RBD mimic attacks, suggesting theyproceed from archaic defense generators in the brainstem. Feeding, drinking, sexual behaviors,urination, and defecation have not been documented yet in RBD.
Methods:
We collected 24 cases of nonviolent behaviors during idiopathic and symptomatic RBD(narcolepsy,dementiawithLewybodies,PD),reportedorobservedinvideopolysomnography.ThefrequencyofviolentandnonviolentbehaviorsduringRBDwasevaluatedbyfacetofaceinterviewof patients and their cosleepers in a prospective series of 100 patients with PD.
Results:
Incidental cases of nonviolent behaviors during RBD included masturbating-like behaviorand coitus-like pelvic thrusting, mimicking eating and drinking, urinating and defecating, display-ing pleasant behaviors (laughing, singing, dancing, whistling, smoking a fictive cigarette, clappingand gesturing “thumbs up”), greeting, flying, building a stair, dealing textiles, inspecting the army,searchingatreasure,andgivinglessons.Speechesweremumbledorcontainedlogicalsentenceswithnormalprosody.InPDwithRBD(n
60),18%ofpatientsdisplayednonviolentbehaviors.Inthis series (but not in incidental cases), all RBD patients with nonviolent behaviors also showedviolent behaviors.
Conclusions:
Although they are less frequent than violent behaviors, nonviolent behaviors duringREM sleep behavior disorder (RBD) fill a large spectrum including learned speeches and culture-specificbehaviors,suggestingtheyproceedfromthecortexactivation.SexualbehaviorsduringRBDmayexposepatientsandcosleeperstoforensicconsequences.
Neurology
®
2009;72:551–557GLOSSARY
PD
Parkinson disease;
RBD
REM sleep behavior disorder.
REM sleep behavior disorder (RBD) is characterized by abnormal behaviors corresponding toenacted dreams. These behaviors emerge during REM sleep and may cause injury or sleepdisruption. During RBD, there is a loss of the physiologic REM sleep-associated muscle atonia.Sleep monitoring demonstrates an excess of phasic or tonic muscle activity during REMsleep.
1,2
Chronic RBD can be idiopathic or associated with various neurologic conditions,including narcolepsy and neurodegenerative diseases.
3-6
In addition, idiopathic RBD fre-quently predates synucleopathies.
5,7
The behaviors during RBD are various, nonstereotyped, and complex. They include talking,laughing, shouting, swearing, yelling, crying, gesturing, reaching, grabbing, arm flailing,slapping, punching, kicking, jerking, strangulating, thrashing, sitting up, leaping frombed, crawling, and running.
8-11
Most descriptions emphasize on forceful motor behaviorsduring RBD, usually associated with an unpleasant, action-filled, violent aspect of dreams.
9,12
Typically, the individuals or their spouses are being pursued or attacked by
Supplementaldataatwww.neurology.org
Address correspondence andreprint requests to Dr. Isabelle Arnulf, Unite´ des Pathologies duSommeil, Hoˆpital Pitie´-Salpeˆtrie`re, 47-83 boulevard del’Hoˆpital, 75651 Paris Cedex 13,Franceisabelle.arnulf@psl.aphp.frFrom the Sleep Disorders Unit, Pitie´-Salpeˆtrie`re Hospital, APHP, Team 106, CRICM, and Paris 6 University, France.Supported by a grant from Fe´de´ration pour la Recherche sur le Cerveau, 2006-02.
Disclosure:
The authors report no disclosures.
Copyright © 2009 by AAN Enterprises, Inc.
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unfamiliar people or animals. In contrast,nonviolent RBD such as laughing or quietly gesturing are rarely reported. Moreover,chewing, feeding, drinking, urinating, defe-cating, or performing a sexual behaviorhave yet not been documented in patients,mirroring an animal model of RBD.
2,13
The abnormal motor behaviors duringREM sleep parallel abnormal dreaming. In-deed, patients with RBD remember an in-creased proportion of dreams with aggressivecontents compared to controls, despite nor-mal levels of daytime aggressiveness.
12,14
These observations led several authors to sug-gest that RBD would proceed from archaicdefense generators and other locomotor gen-erators in the brainstem.
6,15
We wondered whether violent RBD may be more easily de-tected and referred to a physician than nonvi-olent behaviors. Hence, nonviolent RBDcould be underestimated. We recently ob-served several cases of nonviolent RBD, in-cluding eating and sexual behaviors. They arereported here. In addition, we used our sys-tematic interview of a series of 100 consecu-tive patients with PD to determine thefrequency of nonviolent RBD.
METHODS
We retrospectively collected 24 cases of nonvio-lent RBD observed in the Sleep Disorders Clinic during the last2 years. Nonviolent RBD were defined as behaviors that wouldbe usual and perceived as nonaggressive in normal, awake life(e.g., eating, clapping, smoking) whether associated with adream recall or not. When a given behavior was not previously experienced during normal life (e.g., flying, being a police-duck),the perception by the patient that the dream/behavior was non-violent was sufficient. All cases had a history of clinical RBD if their bed partners reported purposeful limb or body movements(as if patients were acting out their dreams) associated with adream recall. RBD was proved on videopolysomnography (en-hanced chin muscle tone or complex movements during REMsleep) in 18 of 24 patients, while 6 patients with PD had notbeen monitored. We determined in a previous PD series, using atwo-step procedure, that our face-to-face interview had a 97.2%positive predictive value for the diagnosis of polysomnography-proved RBD.
16
In order to minimize the risk of including pa-tients with RBD combined with sleepwalking (the overlapsyndrome,
17
which has been reported in rare, isolated cases of PD),
18
we checked for any abnormal behaviors emerging fromslow wave sleep in monitored patients. In the other patients withPD, we requested 1) no history of sleepwalking even as a child;2) no behavior of getting out of bed or walking at home; 3) aclear memory of the corresponding, elaborated dream scenario;and 4) age greater than 50 years. We also estimated the prevalence of nonviolent RBD in aprospective series of 100 unselected patients with PD and theirspouses, who were systematically interviewed about clinical RBD(60 positive patients). Among them, 36 of 60 patients under- went a videopolysomnography which documented either en-hanced chin muscle tone or RBD. All enacted dream reports were collected, which brought a median of two dreams per pa-tient. Patients with clinical RBD were split into two groups:those with exclusively violent RBD and those with at least onereport of nonviolent RBD. We compared the demographic, clin-ical, and treatment characteristics in both groups. The clinicalevaluation included RBD severity,
19
depression (Beck Depres-sion Inventory),
20
cognition (Mini-Mental State Evaluation andFrontal Assessment Battery),
21,22
motor disability (Unified Par-kinson’s Disease Rating Scale–III while treated),
23
daytime ag-gressiveness (evaluated by bed partner), and daytime sleepiness(Epworth Sleepiness Scale score).
24
The patients signed an in-formed consent for the prospective study that was approved by the local ethics committee. The case reports and videos of RBD were shown to the patients, who gave written consent for theirpublication in this journal. The demographic, clinical, and treat-ment characteristics of patients with PD were compared usingthe
2
test for qualitative measures (with Yates correction whenappropriate) and Student
t
test for quantitative measures.
RESULTS
Patient 1.
A 74-year-old retired carpenterhad typical narcolepsy/cataplexy for 51 years. He hadthree sleepwalking episodes as a child but neverdeambulated as an adult. He was referred to theSleep Disorders Unit when sleepiness and hallucina-tions worsened. He was treated with modafinil andclomipramine. Incidentally, his wife reported sometypical, nonviolent nocturnal behaviors. He wouldfrequently enact behaviors related to his former job,giving orders to his employees. Once he pushed his wife out of the bed, digging in the sheets, while he was dreaming that he was digging up a treasure. Thecouple never consulted a doctor for these behaviors.During the videopolysomnography, REM sleep wasa single, 115-minute-long episode at the end of thenight, with a complete loss of atonia (figure). Thenext morning, he reported having drawn and thenbuilt a stair with a plank in a dream. On the video,his eyes were closed and he exhibited sequences of complex, nonstereotyped behaviors during REMsleep (video, patient 1). He would shake an invisiblehand, while he introduced himself as “I am Mr. Do.”Later, he seemed to draw while whistling, to mea-sure, pull, and then hit something with a fictive ham-mer. He said in Spanish (his mother tongue) “One,two, three” and moved his arms as if he were danc-ing. He whistled and said in French “Get up! Eh, eh(laughing).” Although he quit smoking 4 years ago(ex-heavy smoker for 60 years), he quietly mimickedsmoking during the RBD, expired the smoke, andscratched a fictive cigarette, with a relaxed attitude(crossed legs and rocking foot). He also scratchedhimself in his pajamas and seemed to briefly mastur-bate, with regular, 25-second lasting, backwards andforwards motions of the hand in the pajamas. He did
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Neurology 72 February 10, 2009
not report any associated sexual dream, but was notawakened at that very moment.
Patient 2.
A 76-year-old retired civil servant at theDepartment of Defense had a mild, probable de-mentia with Lewy bodies for 1 year. He had ab-normal movements several times per night, every night for 2 years, gesticulating, speaking about hisfamily, and grumbling. He never injured himself but had already hit his wife while asleep. He usedto play basketball and football and many of hisnight behaviors were linked to his sport activity.His wife reported he would urinate at home twicea month while asleep, and had defecated twice ayear, although he had no prostatism, nocturia, orpolyuria and did not take clonazepam. He indeeddreamed that he was urinating, as a young man, inthe Senegal River. During the videopolysomnog-raphy, there were three episodes of REM sleep, allof them without atonia, but movements occurredmainly during the last episode. These behaviors, which occurred with eyes closed, were complex,various, and usually accompanied with sentencesresembling a teacher with children (first sequence)or a captain inspecting his troop (second se-quence): “(Professorial) Can we all return to ourseats! (pause) (Overbearing) What do you do,standing there in the middle? (pause) Removeyour finger away from the switch! (pause) Well, if that’s so, I’ll take the numbers. (Ironic) And . . .late! (pause). (Professorial) Get back to your seats.I’m going to start.” Mumbles for 6 minutes. Then:“(bossy) Raise your hands, raise your hands, raiseyour hands, I said raise! I didn’t say to pull away! Isaid: raise your hands!” Here the patient quickly raised his left arm and waved his hand it as if he were showing something. “(Bossy and rhythmic)Halt! (pause) Halt! (pause) Halt!” Three minuteslater, he shouted “(Bossy, like in a military parade) Attention! Gentleman, please, attention! (pause)Halt, halt, I said! (pause) Halt, I said!” (video, pa-tient 2). Patient 2 spoke here with a loud and clearvoice, but other speeches were shorter or muttered. Hedid not urinate during the polysomnography.
Nonviolent RBD in clinical practice.
In our RBD da-tabase, we found 11 additional patients (aged 33 to76 years) with nonviolent RBD (table 1 and video).They did not complain of these behaviors, contrary to the violent behaviors. RBD was idiopathic in fourpatients, associated with parkinsonism in six pa-tients, and associated with narcolepsy in one patient.There were newly described behaviors, included eat-ing a fictive soup (video, patient 3), making businessand deal, collecting apples, greeting friends, clappingat a show (video, patient 10), and displaying pelvic,coitus-like thrusting (video, patient 12). This last pa-tient also swore profanities at home during the night,but he did not remember any sexual dreams for sev-eral years, and did not attempt to rape or have sex with his wife.
FrequencyandcharacteristicsofnonviolentRBDinPD.
Inthe group of 60 patients with PD and clinical RBD,11 (18%) patients exhibited nonviolent enacteddreams (examples in table 2). Among them, 6 pa-tients had no videopolysomnography, but their clin-ical history strongly supported the diagnosis of RBDin the context of PD, including elaborate movements with closed eyes and inappropriate use of the envi-
FigurePolysomnographicrecordings
Two examples of the polysomnographic recordings while patient 1 (A) and patient 2 (B)exhibited nonviolent behaviors during REM sleep. They include from the top to the bottomthe EEG (Fp1-A2, C3-A2, C3-O1), eye movements (EOG1, EOG2), and EMG (chin, left andrightanteriortibialismuscles).(A)Two-minuteperiodofREMsleep.Thereisanintermittentlossofchinmuscleatonia,withmuscleburstscorrespondingtospeeches(givesorders).(B)Thirty-second period of REM sleep, including sawtooth waves, eyes in opposition of phase,andintermittentlossofatonia,duringwhichthepatientspeaks.
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