Article Don't count your chickens before they're hatched: Elaborative encoding in REM dreaming in face of the physiology of sleep stages DELIENS, Gaétane, SCHWARTZ, Sophie, PEIGNEUX, Philippe Abstract Llewellyn suggests that episodic memories undergo "elaborative encoding" during rapid eye movement (REM) dreams, generating novel associations between recent and remote memories that are then instantiated during non-REM (NREM) sleep. This hypothesis conflicts with our knowledge of the physiology of NREM and then REM sleep stages and their ordered succession. Moreover, associations during sleep might also involve the extraction of hidden patterns rather than de novo associations. Reference DELIENS, Gaétane, SCHWARTZ, Sophie, PEIGNEUX, Philippe. Don't count your chickens before they're hatched: Elaborative encoding in REM dreaming in face of the physiology of sleep stages. Behavioral and Brain Sciences, 2013, vol. 36, no. 6, p. 613-4 PMID : 24304753 DOI : 10.1017/S0140525X1300126X Available at: http://archive-ouverte.unige.ch/unige:33963 Disclaimer: layout of this document may differ from the published version. 1 / 1 BEHAVIORAL AND BRAIN SCIENCES (2013) 36, 589–659 doi:10.1017/S0140525X12003135 Such stuff as dreams are made on? Elaborative encoding, the ancient art of memory, and the hippocampus Sue Llewellyn Faculty of Humanities, University of Manchester, Manchester M15 6PB, United Kingdom http://www.humanities.manchester.ac.uk [email protected] Abstract: This article argues that rapid eye movement (REM) dreaming is elaborative encoding for episodic memories. Elaborative encoding in REM can, at least partially, be understood through ancient art of memory (AAOM) principles: visualization, bizarre association, organization, narration, embodiment, and location. These principles render recent memories more distinctive through novel and meaningful association with emotionally salient, remote memories. The AAOM optimizes memory performance, suggesting that its principles may predict aspects of how episodic memory is configured in the brain. Integration and segregation are fundamental organizing principles in the cerebral cortex. Episodic memory networks interconnect profusely within the cortex, creating omnidirectional “landmark” junctions. Memories may be integrated at junctions but segregated along connecting network paths that meet at junctions. Episodic junctions may be instantiated during non–rapid eye movement (NREM) sleep after hippocampal associational function during REM dreams. Hippocampal association involves relating, binding, and integrating episodic memories into a mnemonic compositional whole. This often bizarre, composite image has not been present to the senses; it is not “real” because it hyperassociates several memories. During REM sleep, on the phenomenological level, this composite image is experienced as a dream scene. A dream scene may be instantiated as omnidirectional neocortical junction and retained by the hippocampus as an index. On episodic memory retrieval, an external stimulus (or an internal representation) is matched by the hippocampus against its indices. One or more indices then reference the relevant neocortical junctions from which episodic memories can be retrieved. Episodic junctions reach a processing (rather than conscious) level during normal wake to enable retrieval. If this hypothesis is correct, the stuff of dreams is the stuff of memory. Keywords: elaborative encoding; episodic memory; hippocampus; neocortical junctions; REM dreams 1. Introduction these memory sources reflect emotional concerns (Domhoff 1996; Hartmann 1998; Schredl 2003). Memories The idea that sleep and dreaming complement memory are not replayed in dreams (Fosse et al. 2003); instead, function in wake has a long history (for broad reviews, memory elements are merged and fused to construct see Hobson 1999a; 2002; Winson 1986; 1993). More visual scenes (cf. Hartmann 1996; Hobson 1988, pp. 36– recently, there is interest in the synergistic roles of rapid 38; Walker & Stickgold 2010). The significance (if any) of eye movement (REM) and non–rapid eye movement why memory elements unite in dream image composition (NREM) in memory processes (see, e.g., Diekelmann remains elusive. This requires explanation in any account et al. 2009; Ribeiro & Nicolelis 2004; Stickgold 2005; of the mnemonic function of dreaming. Stickgold et al. 2009). The relationship, if any, between dreams and (2001) pinpoint a “frustrating dearth” of evidence on “ memory has remained enigmatic, however. Why do we dream construction and its possible functions. The article fi fl need to create an arti cial world of ine and spend two aims to make a contribution in this area. ” hours a day in it? (Hobson 1999a, p. 73). Possibly linked to the conflation of memory elements Aristotle (350 B.C./1996) argued that experiences, like (Cicogna & Bosinelli 2001) is the, often, bizarre nature of projectiles set in motion during wake, continue as mem- dream imagery (Fosse et al. 2004; Hobson 2002; Scarone ories in dreams. Freud (1899/1999, p. 12) claimed that et al. 2008). McCarley and Hoffman (1981) report that “all the material” in dreams derives “in some way” from remembered waking experiences; he also identified the memory sources for dreams (see, e.g., those for “Wolf Man” [Freud 1963, pp. 214–16]). Stickgold (2002) states that, in the absence of external sensory input, memories SUE LLEWELLYN, professor of accountability in the Faculty of Humanities at the University of Manchester, with derived meanings and symbols must be the source UK, has published widely on the delivery of health ser- material for dreams. Many have argued that memory vices. In recent years she has researched and published sources are key to dream construction (Baylor & Cavallero on the relationships between REM dreaming, memory 2001; Cicogna & Bosinelli 2001; Foulkes 1985; Kramer processes, and psychopathology. 2007; Nielsen & Stenstrom 2005). Some contend that © Cambridge University Press 2013 0140-525X/13 $40.00 Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 20:12:47, subject to the Cambridge Core terms of use, available at 589 https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X1300126X Llewellyn: Elaborative encoding 67% of REM dreams exhibit bizarreness. Indeed, the word micro, meso, and macro levels. At the micro level, “bizarre” is used to characterize a person/object/place that nodes/junctions may be said to be constituted by individ- takes on multiple (apparently inconsistent) elements. Bizar- ual neurons; at macro level, decisions are required over reness is constrained in dreams, however. Bizarre dream the parcellation of grey matter into regional nodes characters/objects conform to “bizarreness rules” (Ritten- (Zalesky et al. 2010). Neuronal assemblies may represent house et al. 1994). These rules limit bizarreness to incon- meso-level phenomena of particular relevance for gruities (inconsistent or fused features of people/objects/ memory networks (cf. Basaŗ et al. 2000; Miller 1996). At places), discontinuities (sudden changes in these features the meso level in episodic memory networks, junction/ of people/objects/places), and indeterminacy (where the node and connection/edge are not well understood. identity of a person/object/place remains explicitly vague). Segregation and integration are fundamental to the The constrained nature of dream bizarreness excludes organization of the cerebral cortex (Tononi et al. 1994; many possibilities. For example, typical adult dreams do Zeki 1978; Zeki & Shipp 1988). Buzsáki (2006, p. 65) not feature monsters or people who transmogrify into argues that pattern completion and pattern separation are walking pink blancmanges (cf. Hobson 2011, p. 163; Rit- the basic functions of neuronal networks, expressed tenhouse et al. 1994). Moreover, most of dream content though the concepts of integration and differentiation, is not bizarre and conforms to waking expectations respectively. Fuster (1999, p. 33) states that segregation (Domhoff 2011; Domhoff & Scheider 2008; Snyder 1970; and integration characterize memory networks; he uses Snyder et al. 1968). Dreams do not resemble abstract art, the concepts of divergence and convergence. The answer for example. to the problem of how episodic memories are both inte- This article argues that the sometimes bizarre (but rule grated and segregated in cortical networks may be that a bound) visually associative nature of a dream (along with REM dream, composed of associated memory elements, other dream characteristics) can, at least partially, be is a junction/node, thus enabling integration at the junction understood through the principles underlying what has but segregation between the episodic memory represen- been termed the “ancient art of memory” (henceforth, tations along the connecting paths/edges that “meet,” and AAOM). The article integrates knowledge of the AAOM, share elements, at a junction. from the humanities, into work on dreams and memory In support of this hypothesis, the structure of the article in neurobiology and psychology. The AAOM is elaborative is as follows. The next subsection sets out the article’s encoding in wake engendering a visual composition using underlying assumptions about dreaming and memory. imagery (which is often bizarre), association (particularly The second section describes the AAOM and explains to place), organization, and narration and forming the why this constitutes elaborative encoding. The third basis