Schizophrenia Bulletin vol. 42 no. 5 pp. 1098–1109, 2016 doi:10.1093/schbul/sbw076 Advance Access publication June 29, 2016 What Is the Link Between Hallucinations, Dreams, and Hypnagogic–Hypnopompic Experiences? Flavie Waters*,1,2, Jan Dirk Blom3–5, Thien Thanh Dang-Vu6, Allan J. Cheyne7, Ben Alderson-Day8, Peter Woodruff9, and Daniel Collerton10 1Clinical Research Centre, Graylands Hospital, North Metro Health Service Mental Health, Perth, Australia; 2School of Psychiatry and Clinical Neurosciences, The University of Western Australia, Perth, Australia; 3Parnassia Psychiatric Institute, The Hague, the Netherlands; 4Faculty of Social Sciences, Leiden University, Leiden, the Netherlands; 5Department of Psychiatry, University of Groningen, Groningen, the Netherlands; 6Center for Studies in Behavioral Neurobiology, PERFORM Center and Department of Exercise Science, Concordia University; and Centre de Recherches de l’Institut Universitaire de Gériatrie de Montréal and Department of Neurosciences, University of Montreal, Montreal, QC, Canada; 7Department of Psychology, University of Waterloo, Waterloo, ON, Canada; 8Department of Psychology, Durham University, Durham, UK; 9University of Sheffield, UK, Hamad Medical Corporation, Doha, Qatar; 10Clinical Psychology, Northumberland, Tyne and Wear NHS Foundation Trust, and Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, UK *To whom correspondence should be addressed; The School of Psychiatry and Clinical Neurosciences, The University of Western Australia (M708), 35 Stirling Highway, Crawley, WA 6009, Australia; tel: +61-8-9347-6650, fax: +61-8-9384-5128, e-mail: [email protected] By definition, hallucinations occur only in the full wak- evidence exists to fully support the notion that the major- ing state. Yet similarities to sleep-related experiences ity of hallucinations depend on REM processes or REM such as hypnagogic and hypnopompic hallucinations, intrusions into waking consciousness. dreams and parasomnias, have been noted since antiq- uity. These observations have prompted researchers to Key words: sleep/misperception/hypnopompic and suggest a common aetiology for these phenomena based hypnagogic hallucination/nightmare/parasomnia/ on the neurobiology of rapid eye movement (REM) sleep. REM/Parkinson’s disease/schizophrenia/ With our recent understanding of hallucinations in differ- eye disease/consciousness ent population groups and at the neurobiological, cogni- tive and interpersonal levels, it is now possible to draw Introduction comparisons between the 2 sets of experiences as never before. In the current article, we make detailed compari- Philosophers and scientists have long been fascinated sons between sleep-related experiences and hallucinations by perceptual phenomena occurring around and during in Parkinson’s disease, schizophrenia and eye disease, at sleep, such as the hypnagogic and hypnopompic hallu- the levels of phenomenology (content, sensory modali- cinations on the borders of sleep and the dreams and ties involved, perceptual attributes) and of brain function parasomnias of sleep. The similarities to “daytime” hal- (brain activations, resting-state networks, neurotransmit- lucinations received much scrutiny over the centuries. ter action). Findings show that sleep-related experiences The French researcher, Alfred Maury,1 noted a con- share considerable overlap with hallucinations at the level tinuum of form and cause between dreams and hallu- of subjective descriptions and underlying brain mecha- cinations, and the English neurologist, John Hughlings nisms. Key differences remain however: (1) Sleep-related Jackson,2 argued that strong “sensory discharges” were perceptions are immersive and largely cut off from reality, likely a common mechanism of dreams and hallucina- whereas hallucinations are discrete and overlaid on veridi- tions. Lhermitte3 elaborated further by designating the cal perceptions; and (2) Sleep-related perceptions involve midbrain structures associated with peduncular halluci- only a subset of neural networks implicated in hallucina- nations as the brain’s “dream centre.” Observations of tions, reflecting perceptual signals processed in a function- sleep disturbances in clinical disorders associated with ally and cognitively closed-loop circuit. In summary, both hallucinations (eg, schizophrenia and Lewy body disor- phenomena are non-veridical perceptions that share some ders) also prompted suggestions of a common aetiology phenomenological and neural similarities, but insufficient for both dreams and hallucinations,4,5 and the notion © The Author 2016. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: [email protected] 1098 Sleep and Hallucinations that hallucinations may be the results of “rapid eye movement (REM) intrusions” of visual imagery into wakefulness.5–7 Despite these suggestions of continuity at some level, a strict dichotomy between sleep-related perceptual phe- nomena and hallucinations is still central to definitions of hallucinations.8 The main objective of this article is to revisit the status of perceptual experiences that occur during sleep. This task will better distinguish the characteristics and properties specific to daytime hallu- cinations from those that are general to sleep percep- tions, and draw upon information regarding underlying mechanisms. We marshal empirical and theoretical work to address the questions: Fig. 1. Fuzzy forms of visual experience. There are no clear boundaries between perceptions. Here, sensory perceptions 1. What mental functions are active during sleep? overlap with illusions and voluntary internal images, 2. What are the similarities and differences in phe- hallucinations, and dreams. nomenological features, and in neuroanatomical and neurophysiological mechanisms, between sleep- (in which they are known as Charles Bonnet Syndrome related perception and hallucinations? Specifically, [CBS]), each showing a distinct character. are sleep-related perceptions closely related to hal- In schizophrenia, most hallucinations are auditory lucinations in psychosis, neurodegeneration, or eye (“voices”) although hallucinations in other modalities disease? also occur (Waters F, Collerton D, Jardri R, et al. Visual 3. Can hallucinations be conceptualized as REM dream hallucinations in the psychosis spectrum and compara- intrusions? Or conversely: might night-time percep- tive information from neurodegenerative disorders and tions be reclassified as hallucinations? eye disease. Schizophr Bull. 2014;40(suppl 4):S233–S245.). Hallucinations are often mistaken for veridical perceptions This knowledge has the potential to refine our under- and interpreted as symbolic and personally meaningful. standing of hallucinations, destigmatize hallucinations in Importantly, they are often laden with affect, and believed clinical disorders, and point the way towards new treat- to originate from external (nonself) sources.10 In PD, visual ment approaches. hallucinations are predominant, although auditory hallu- cinations and hallucinations of sensed presence are com- Hallucinations—Definition Issues mon. Visual hallucinations often comprise formed complex percepts (eg, people, faces, animals, objects), or, less com- Hallucinations are perceptual experiences that are primar- monly, simple percepts (flashes, dots).11 Hallucinations in ily defined by their subjective reports rather than by their PD are usually perceived to be real and unpleasant, but not underlying neurobiological mechanisms. Three criteria 12 9 frightening. Finally, visual hallucinations can occur in converge in the majority of definitions. Hallucinations healthy individuals with CBS. These individuals with eye are: (1) perceptions (in the auditory, visual and/or other disease commonly report simple hallucinations (shapes, sensory modalities), (2) not elicited by a correspond- lines, colors), but complex visual hallucinations also occur. ing stimulus from the outside world, and (3) unbidden, These are often of intense color and rich in detail, and may although this latter criterion is not a necessary criterion include panoramic hallucinations. They are usually recog- in all definitions. nized as non-veridical and do not lead to intense distress. There is no “archetype” for hallucinations. Halluc­ inations can occur in any sensory modality with fea- Consciousness and the Sleeping Brain tures that are markedly different between each other. Furthermore, there is no clear demarcation between sen- The notion of “clear consciousness” has been decisive sory perceptions and misperceptions and evidence exists in some definitions of hallucinations.9 Complicating this of a continuity between subjective perceptions (see exam- requirement, however, is the contemporary view that ple for visual experiences, figure 1). consciousness represents multiple and graded mental The auditory and visual modalities of hallucinations states,13,14 including several overlapping constructs such are the most commonly enquired about and reported, but as sensory discrimination, perceptual awareness, focused have a varied presentation depending on the population attention, introspection, and volitional actions.13,14 group in which they are studied. For example, hallucina- In sleep, many of these mental functions remain active. tions are prominent in people with schizophrenia spec- During REM sleep (Box 1), pontine nuclei and choliner- trum disorders,