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Sleep Medicine 19 (2016) 150–152

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Dissociated rapid eye movement sleep dream experiences in type 1 narcolepsy: a case report C. Bellucci a, S. Vandi b,c, M. Iloti b, F. Pizza b,c, P.M. Russo a, G. Tuozzi d, C. Cipolli a, G. Plazzi b,c,* a

DIMES, Alma Mater Studiorum University of Bologna, Bologna, Italy DIBINEM, Alma Mater Studiorum University of Bologna, Bologna, Italy c IRCCS, Istituto delle Scienze Neurologiche, Bologna, Italy d QUVI, Alma Mater Studiorum University of Bologna, Bologna, Italy b

A R T I C L E

I N F O

Article history: Received 27 April 2015 Received in revised form 23 June 2015 Accepted 23 July 2015 Available online 1 October 2015 Keywords: Narcolepsy type 1 REM sleep behavior disorder Video-polysomnography Dream content analysis

1. Introduction

2. Case description

Clinical and polygraphic hallmarks of type 1 narcolepsy (NT1) are the occurrence of episodes of rapid eye movement (REM) sleep at the onset of nocturnal or daytime sleep (SOREMP) and dissociated wake–REM sleep manifestations (cataplexy, sleep paralysis, hallucinations) [1]. Some recent neurophysiological findings, demonstrating that SOREMP in NT1 lacks the typical sympathetic activation of REM sleep [2], support that SOREMP per se may also be an REM sleep–wakefulness dissociation in NT1. Moreover, several behavioral and cognitive phenomena may surface during SOREMPs: REM sleep behavior disorder (RBD), characterized by loss of REM sleep muscle atonia coupled with dream-enacting behaviors [3]; cataplexy (episodes of sudden muscular weakness triggered by emotions) [4]; dream lucidity (maintenance of reality testing and volitional control of thinking while dreaming) [5,6]; hallucinatory phenomena such as flying sensation [7]; and out-of-body experiences (OBE; metamorphosis or exit of the self from the body) [8]. We report here an NT1 patient showing the co-occurrence of several dissociated mental and motor features of REM sleep during the same daytime SOREMPs.

The patient is an otherwise healthy, drug-naive, 27-year-old woman. Since the age of 10 years, she has suffered from sleep attacks, episodes of sudden muscular weakness triggered by laughing, vivid dreaming, and sleep paralysis. At our observation, the polysomnographic investigation (her multiple sleep latency test [MSLT] showed a pathological mean sleep latency of three minutes 40 seconds, and 5/5 SOREMPs), and the undetectable (0 pg/mL) cerebrospinal hypocretin-1 level confirmed NT1 diagnosis. During the MSLT procedure, the patient, who underwent standardized interview to collect dream report after the awakening from each nap, displayed RBD episodes. REM sleep atonia index calculated in the whole SOREMPs time recorded during the MSLT was 0.76, below the proposed cut-off of 0.8 for RBD [9].

* Corresponding author. Department of Biomedical and Neuromotor Sciences, University of Bologna, Via Ugo Foscolo 7, 40123 Bologna, Italy. Tel.: +39 051 4966926; fax: +39 0514966176. E-mail address: [email protected] (G. Plazzi). http://dx.doi.org/10.1016/j.sleep.2015.07.036 1389-9457/© 2015 Elsevier B.V. All rights reserved.

3. Video and dream report analysis The video-polysomnographic (v-PSG) recordings collected during the MSLT showed that SOREMPs were characterized by clear-cut REM sleep PSG activity intermingled by fragments of wakefulness and sleep stage N1. The patient provided extensive reports of dream experiences after awakening in four of five MSLT trials. Four RBD episodes were also documented during the first (n = 1) and fourth (n = 3) trials (see Videos S1–S4 in the Supplementary material). During those episodes, the patient either talked or displayed nonexplosive and nonviolent (although sometimes fast), simple

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Fig. 1. From top to bottom the figure displays the Story Dygraph derived from the analysis of a dream reported by the patient, a frame extracted from the videopolysomnography and the coinciding hypnogram of MSLT’s first nap (9 AM). Abbreviations from Story Grammar System (Story Dygraph): BEG, beginning; DEV, development; END, ending; CR, complex reaction; GP, goal path; SR, simple reaction; GL, goal; ATT, attempt; OUT, outcome; ACT, action; ES, external state; EE, external event; IE, internal event; IS, internal state; numbers refer to statements (S1, S2, S3, . . ..in the text); 0, constituent not realised in report structure. Other abbreviations (Story Dygraph): RBD, REM sleep behavior disorder; VB, verbal behavior; MB, motor behavior; DA; dream awareness; VC, volitional control; FE, flying experience; OBE, out-of-body experience. Other abbreviations (Hypnogram): REM, Rapid-eye movements sleep; W, wake; N1, non-REM stage 1 sleep; N2, non-REM stage 2 sleep. Report Statements, Story 1. EE S1 I was hearing a song from Miley Cyrus, it played faster than usual; IE S2 (and) this was quite traumatic, it annoyed me; IE S3 I thought “No, I can’t fall asleep with a song from Miley Cyrus stuck in my head” (DA); IE S4 so I tried to change things (VC), EE S5 I was seeing the song’s music video where Miley Cyrus sits half naked on a swinging ball while singing; EE S6 in the end, there was I instead of the ball. I was spinning around clinging to this rotating chain (OBE); EE S7 (then) I took a running leap and flew away. (FE); EE S8 I landed in the middle of the water at a beach; ES S9 there were two black children alone, one might have been 7 years old, the other one 12; EE S10 they called me “Aunt” because I was their mother’s best friend; EE S11 they tried to find any excuses; IE S12 to spend more time with me. EE S13 From the beach we went to their house; ES S14 they lived nearby. EE S15 As soon as I entered the house the dream started to become sexually explicit, involving a man of my same age. IE S16 At that point I thought “No, I can’t have a sexually explicit dream while I’m undergoing sleep monitoring!” (DA); EE S17 (therefore) I said “Stop!” (and I waved the arm) (VC – RBD-MB+VB). EE S18 (Then) the children caught up with me in the house.

task-oriented behaviors (ie, raising and extending an arm as to intimate a stop, putting trousers on hastily). Two scorers analyzed independently the dream reports to identify the following: a) the structural components (statements and nodes) of the reported dreams using the story-grammar rules [10]; and b) the presence of lucid dreaming, flying experiences, and OBE. The scorers then evaluated which specific statements of either report corresponded to the verbal and/or motor features of the RBD episodes (which they saw as isolated and untagged clips) (Fig. 1 and Supplemental Fig. S1). Interscorer agreement was complete.

4. Discussion The present report showed that RBD episodes can occur repeatedly during SOREMPs of the same daytime nap [4], and can also be accompanied by dissociated REM–dreaming phenomena such as volitional control and awareness of dreaming, flying experiences, and OBE. The enacted behaviors were nonviolent (ie, taskoriented or reminiscent of lively interactions with other persons), similar to those of RBD episodes observed in the first part of the night in NT1 patients [3]. Moreover, RBD episodes occurred in

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largely fragmented periods of SOREMP, namely a highly transitional state that also fosters lucid dreaming [5,6], flying experiences [7], and OBE appearance [8]. Taken together, these findings suggest some considerations. First, the nonstereotyped fashion, the lack of electroencephalographic epileptic activity, the associated vivid and coherent dream recall, and the exclusive onset during REM sleep can easily steer the differential diagnosis with other complex behaviors appearing during sleep (eg, paroxysmal arousals) [11]. Second, the co-occurrence of objective (RBD episodes, likely to be observed by family members) and subjective (dream lucidity and OBE, easily recalled by patients) features of daytime SOREMP may be considered as a reliable clue of narcolepsy. Third, SOREMP may offer a unique natural opportunity to render the time course of dreaming by connecting mental to motor activity within a psychophysiological paradigm [12]. Indeed, a meticulous comparison of video-PSG and dream report allowed the identification of motor behaviors reminiscent of some statements of dream reports. Finally, further studies are needed to understand whether RBD and intense mental activity in NT1 may represent a discrete form of REM sleep–wakefulness dissociation due to a pathophysiology different from the idiopathic and neurodegenerative RBD forms [13].

Funding sources This work was supported in part by a grant from the Fondazione del Monte di Bologna e Ravenna (to P.R.) (RF 2013-14).

Conflict of interest The authors declare that there are no conflicts of interest in regard to this work.

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