CommentaryíLleweüyn: Elaborative encoding that this is one place where Freud did not really get it (Greenberg & Pearbnan 1978). French and Fromm (1964) pointed to dreams and their manifest content as containing important images related to the patient's "focal conflict." We (Greenberg & Pearlnian 1978) demonstrated how in Freud's own classical "Specimen dream," where he again talks about indifferent day residue, he misses the veiy emotionally important day residue. That dream, in die manifest content, actually portrays an event - a failed operation on a patient diat was so very important to Freud's self-esteem. We also presented findings from the sleep lab for a patient in psychoanalysis (Greenberg & Pearlnian 1975). Again die manifest images relate to emotionally significant issues for the patient. The results of our studies (Greenberg et al. 1992) suggest that what is in the dream is emotionally significant and that what is emotionally significant from waking life is what appears in die dream. If one considers these findings meaningful, then the statement "'frustrating dearth' of evidence on dream constmction and its possible functions" (sect. 1, para. 2) is missing die point. Only in the world of nonclinical research can one miss die connection (bridge) between the clearly demonstrated and pretfy much accepted role of REM sleep in memory and the idea diat the kind of memories integrated in human dreams are mainly connected with the organization of emotionally meaningful and active issues with which the dreamer has been struggling while awake and continues to try to resolve during dreaming. Dreams show clearly how the dreamer sometimes succeeds in integrating and resolving the waking issues or at odier times fails to integrate and has nightmares or repetitive dreams that faü to show any resolution (Greenberg et al. 1992). These ideas build on the early and much more cognitive proposals about REM sleep and memory consolidation. An example of how diis might be approached can be considered in relation to the "Quicksand" dream in the target article. This is presented as an example of a way to think about dreains and die day residue radier than a considered demonstration of the emotional salience of die dream. One should approach a dream widiin die context of its occurrence. In this case, Llewellyn has chosen to present the dream in die context of proposing an important, elaborate framework for understanding tlie operation of memory functions in dreams. Her effort is impressive both in the amount of hterature she has mastered and in the qualify of her ideas. I do not think it is any stretch to suggest that this effort has been a major preoccupation and coneem of hers (only she can confirm this) and that one might wonder how this might show up in the dream. Because of space limitations, I can only suggest that one might think about her efforts to create a new bridge in our thinking about dreams and perhaps her fear, as she stmggled with this enormous effort, diat she might fail and be swallowed by the quicksand - or, put another way, wiU anyone buy her new dieoretical house? 'The story in die dream and her associations certainly encompass great hopes and great fears. This commentary is a very sketchy presentation of ideas about a fuller approach to the understanding of dreams, which might be added to Llewellyn's extremely thorough and well-presented discussion. I hope these ideas will make the third leg as substantial as those of neurobiology and cognitive psychology.
The ancient art of memory doi:10.1017/S0140525X13001350 Allan Hobson Professor of Psychiatry Emeritus, Harvard Medical School, Boston, MA 02130. [email protected] www.dreamstage-museum.net/aiianhobson/index.html
Abstract: Revision of Freud's theory requires a new way of seeking dream meaning. With tlie idea of elahorative encoding. Sue Llewellyn has
provided a method of dream interpretation that takes into account both modem sleep science and the ancient art of memory. Her synthesis is elegant and compelling. But is her ^ipothesis testable?
Why are dreams strange? Why are they so difficult to remember? And what is their furiction? We still do not really know die answers to these fundamental questions, which Sue Llewellyn addresses in her provocative article on dreaming as elaborative encoding. Besides being a forceful reminder of die ancient art of memory, I appreciate the effort to tie diis tradition to modem science in an integrative way. For me, die approach links quantitative studies of dream bizarreness (Hobson et al. 1987), the neurophysiology of rapid eye movement (REM) sleep (Hobson et al. 2000), and the experimental study of sleep and memory (Stiekgold et al. 2001). In essence, Llewellyn is telling us that dreams are bizarre because their content is scrambled by the altered physiology of REM sleep (low aminergic, high choUnergic tone), which allows fragments of the dream to be reordered to facihtate the efficient storage of emotional sahent information. This theory is capital because it allows us to retain the idea that dreams are, somehow, meaningful whue setting aside the unlikely suggestion of Freud that die function of dreaming is to disguise and conceal unacceptable wishes to protect consciousness (Hobson and McGarley 1977; McGarley and Hobson 1977). Llewellyn's elaborative encoding dieory of is more compatible with the completely opposite view that REM sleep and dreaming are positive collaborators that shape and update waking consciousness (Hobson 2009). My own dieoiy of REM dreams as protoconsciousness is not entirely independent of the idea of elaborative encoding. In fact, die two ideas are not only theoretical cohesive but mutually enhancing by providing a dieoretical mechanism by which diumal waking experience could be integrated with what I take to be the evolutionary memory by .which die genome creates REM as an epigenetic program of virtual reality for the fetal brain. So die good news is theoretical coherence of an entirely novel sort. The bad news regards testability. For elaborative encoding to be more dian literary window dressing, it is essential to propose experimental tests to prove it wrong, and I must confess that I do not see how this can be done. Anecdotal selfanalysis wül not do here. We must not tolerate neo-Freudianism, no matter how brilliant. WiU Sue Llewellyn, the experimentalist, please stand up?
REi\/l sieep and dreaming functions beyond reductionism doi:10.1017/S0140525X13001362 Roumen Kirov Institute of Neurobiology, Bulgarian Academy of Sciences, SG-J 713 Sofia, Bulgaria. [email protected] [email protected] http://www.bio.bas.bg/neurobiology/EN/index.htm
Abstract: Brain activation pattems and mental, electrophysiological, and neurobiological features of rapid eye movement (REM) sleep suggest more functions tlian only elaborative encoding. Hence, the periodic occurrence of REM sleep episodes and dreaming may be regarded as a recurrent adaptive interference, which incorporates recent memories into a broader vital context comprising emotions, basic needs and individual genetic traits.
The target article makes a parallel between rapid eye movement (REM) sleep dreaming and principles of the ancient art of memory (AAOM), thus proposing a role for REM sleep dreaming state in elaborative encoding of episodic memories. First, in the target article, LleweUyii argues that REM sleep dreaming renders recent memories more distinctive through novel and meaningful associations with emotionally salient and remote BEHAVIORAL AND BRAIN SCIENCES (2013) 36:6
621
Commentary/ïAeweWyn: Elaborative encoding memories. Second, Llewellyn goes on to predict how recent episodic memories are furdier configured in die brain dirough dreaming imagery. This concept further challenges the enigmatic nature of REM sleep and its dreaming. Similar to previous dieories of sleep, the inevitable reductionism inherent in the concept of die target article leaves unresolved questions. The critical issue for milestone hypodieses for REM sleep dreaming is therefore to avoid as much as possible "suiprise," "free energy" costs, or redundant "prediction eiTors," as posited by another recent concept, according to which REM sleep dreaming and phenomenology may subserve basic adaptive functions beyond memory reprocessing such as free energy minimization (Hobson & Friston 2012, p. 87). Even if die AAOM principles are regarded as a focus in the cognitive domain in die context of already existing more fundamental theories of REM sleep (e.g., Hobson 2009; Hobson et al. 2000; Jouvet 1998), diere is still ex-perimentally driven and fact-based infonnation diat needs to be reconciled. Recent human studies indicate that REM sleep electroencephalographic (EEG) signatures are not merely associated widi memory encoding and consohdation. Whereas theta (5- to 7Hz) REM sleep electroencephalographic (EEG) activity has been associated with both dream recall from REM sleep (Marzano et al. 2011) and consolidation of only emotional memory (Nishida et al. 2009), gamma (more than 25- to 30-Hz) REM sleep EEG activity has been assumed to be associated with affective mental states (Marshall et al. 2011; van der Helm et al. 2011b). Hence, frequency-specific EEG activities of human REM sleep (Gantero et al. 2003; Lhnás & Ribary 1993) may support its functions dissimilarly. A recent rodent study indicates diat dieta oscillations during REM sleep may produce synaptic downscaling in die hippocampus (Grosmark et al. 2012). Along widi the observed association between human dieta EEG rhydim and successful dream recall in REM sleep (Marzano et al. 2011), Üiis finding conforms well widi either die kind of elaborative encoding proposed in die target article or the need for room to minimize die free energy (Hobson & Friston 2012). Yet, specifically regarding the target article's concept, a possibility remains diat sleep-dependent memory reprocessing may be an epiphenomenon of more basic functions of both non-REM sleep (Tononi & Güelli 2006) and REM sleep (Hobson & Friston 2012). Sleep studies of human insight have demonstrated that whereas early-night slow-wave sleep (SWS) and its EEG signatures support die transformation of implicit knowledge into ex-pUcit insight to a hidden regularity in a complex generation task, latenight REM sleep preserves only die previously generated impUcit knowledge widiout engaging specific REM sleep EEG signatures (Yordanova et al. 2008; 2012). These results show diat only SWS and its EEG signatures may be linked to successful human heuristic creativity and do not suggest memory reconstruction during REM sleep. GriticaUy, nearly all psychiatric disorders are characterized by a REM sleep overdrive, yet diese psychiatric conditions can not be linked to successful memory formation (Benca et al. 1992; Walker 2010). Furtlier, it has been shown that augmented REM sleep in children widi attention-deficit/liyperactivity disorder is associated witli die core psychiatric symptoms of inattention and hyperactivity/impulsivity, whereas die greater amount of REM sleep in normally developing children is associated witli better performance intelligence (Kirov et al. 2007; 2011). These findings suggest at least a bidirectional role of REM sleeps depending on presence or absence of psychopathology. From a developmental perspective, infants ex-perience much more REM sleep, which decreases dirough cMdliood and adolescence, dian adults (Roffwarg et al. 1966). Thus, considering that REM sleep neurobiology and die corresponding dream generation are tighdy coupled (Stickgold et al. 2001), explanations are needed for the following: (1) What memoiy sources may create tlie presumably enormous dreaming during infancy and early 622
BEHAVIORAL AND BRAIN SCIENCES (2013) 36:6
childliood? (2) What cognitive and/or adaptive functions does such dreaming subserve? (3) How does diis risk)' homeostatic state (e.g., Hobson & Friston 2012) predominant during early development relate to evolutionary advantages? (4) What kind of memoiy processes may be subseived by REM sleep dreams incoiporated in nightmares, a common feature of botli normal ontogenesis and developmental psychopathology (Brand & Kirov 2011; Kirov & Brand 2011)? Although it has been assumed diat REM sleep subserves brain maturation during ontogenesis dirough intemally generated and genetically grounded stimulation of neuronal assembles (Marks et al. 1995), this assumption mandates experimental updates by applying new paradigms accounting for REM sleep hypodieses such as genetic programming (Jouvet 1998), direat simulation (Revonsuo 2000), and protoconsciousness (simple awareness of perception and emotions provided by genetic equipment ensuring generation of a viitual world) or Bayesian leaming and inference (Hobson 2009; Hobson & Friston 2012). Human REM sleep occurs periodically, thus distinguisliing sleep cycles from one anodier, with the frequency and duration of REM sleep periods increasing progressively across ovemight sleep (Broughton 1987). These temporal dynamics of REM sleep and dreaming can not be readily linked to die concept of elaborative encoding dirough the AAOM principles forwarded in die target article. Instead, it seems more relevant that in combination widi concomitant neuroendocrine (Steiger 2002, 2007) and cardiorespiratory processes (Gastaut & Broughton 1964), die temporal dynamics of REM sleep and dreaming could supply vitally important homeostatic functions togedier widi many cognitive adaptive processes. I argue diat die periodic occurrence of REM sleep and its dreaming may be regarded as a recurrent adaptive interference that may incorporate previously encoded and consolidated memories into a broader vital context comprising residuals of hypotheses testing, related emotions, basic needs, and individual genetic traits.
The spaces left over between REM sleep, dreaming, hippocampal formation, and episodic autobiographical memory doi:10.1017/S0140525X13001374 Hans J. Markowitsch®''^ and Angelica Staniloiu^ ^Physiological Psychology, University of Bielefeld, D-33501 Bielefeld, Germany; "Center of Excellence Cognition Interaction Technology (CITEC), University of Bielefeld, D-33501 Bielefeld, Germany; '^Hanse Institute of Advanced Study, D-27753 Delmenhorst, Germany. [email protected] [email protected] http://www.uni-bieiefeld.de/psychoiogie/ae/AE14
Abstract: It is argued that Llewellyn's hypotliesis about die lack of rapid eye movement (REM)-sleep dreaming leading to loss of personal identity and deficits in episodic memory, affectixnty, and prospection is insufficiently grounded because it does not integrate data from neurodevelopmentiil studies and makes reference to an outdated definition of episodic memory.
The assumptions about relations between sleep and memory have changed considerably since Momzzi and Magoun (1949) proposed tliat sleep reinstates the function of synapses. About a decade ago, tlie biological significance of dreams was downplayed by some audiors, who called diem "spandrels of sleep" (e.g., Flanagan 2000). Llewellyn's target aiticle confirms a new impetus in sleep research, suggesting diat Freud's wish to develop a scientific dieory for "the interpretation of dreams" might not be a "lost dream" (Freud 1900). By emphasizing elaborative encoding (as opposed to consohdation) and a major role of rapid eye movement
Copyright of Behavioral & Brain Sciences is the property of Cambridge University Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
The ancient art of memory doi:10.1017/S0140525X13001350 Allan Hobson Professor of Psychiatry Emeritus, Harvard Medical School, Boston, MA 02130. [email protected] www.dreamstage-museum.net/aiianhobson/index.html
Abstract: Revision of Freud's theory requires a new way of seeking dream meaning. With tlie idea of elahorative encoding. Sue Llewellyn has
provided a method of dream interpretation that takes into account both modem sleep science and the ancient art of memory. Her synthesis is elegant and compelling. But is her ^ipothesis testable?
Why are dreams strange? Why are they so difficult to remember? And what is their furiction? We still do not really know die answers to these fundamental questions, which Sue Llewellyn addresses in her provocative article on dreaming as elaborative encoding. Besides being a forceful reminder of die ancient art of memory, I appreciate the effort to tie diis tradition to modem science in an integrative way. For me, die approach links quantitative studies of dream bizarreness (Hobson et al. 1987), the neurophysiology of rapid eye movement (REM) sleep (Hobson et al. 2000), and the experimental study of sleep and memory (Stiekgold et al. 2001). In essence, Llewellyn is telling us that dreams are bizarre because their content is scrambled by the altered physiology of REM sleep (low aminergic, high choUnergic tone), which allows fragments of the dream to be reordered to facihtate the efficient storage of emotional sahent information. This theory is capital because it allows us to retain the idea that dreams are, somehow, meaningful whue setting aside the unlikely suggestion of Freud that die function of dreaming is to disguise and conceal unacceptable wishes to protect consciousness (Hobson and McGarley 1977; McGarley and Hobson 1977). Llewellyn's elaborative encoding dieory of is more compatible with the completely opposite view that REM sleep and dreaming are positive collaborators that shape and update waking consciousness (Hobson 2009). My own dieoiy of REM dreams as protoconsciousness is not entirely independent of the idea of elaborative encoding. In fact, die two ideas are not only theoretical cohesive but mutually enhancing by providing a dieoretical mechanism by which diumal waking experience could be integrated with what I take to be the evolutionary memory by .which die genome creates REM as an epigenetic program of virtual reality for the fetal brain. So die good news is theoretical coherence of an entirely novel sort. The bad news regards testability. For elaborative encoding to be more dian literary window dressing, it is essential to propose experimental tests to prove it wrong, and I must confess that I do not see how this can be done. Anecdotal selfanalysis wül not do here. We must not tolerate neo-Freudianism, no matter how brilliant. WiU Sue Llewellyn, the experimentalist, please stand up?
REi\/l sieep and dreaming functions beyond reductionism doi:10.1017/S0140525X13001362 Roumen Kirov Institute of Neurobiology, Bulgarian Academy of Sciences, SG-J 713 Sofia, Bulgaria. [email protected] [email protected] http://www.bio.bas.bg/neurobiology/EN/index.htm
Abstract: Brain activation pattems and mental, electrophysiological, and neurobiological features of rapid eye movement (REM) sleep suggest more functions tlian only elaborative encoding. Hence, the periodic occurrence of REM sleep episodes and dreaming may be regarded as a recurrent adaptive interference, which incorporates recent memories into a broader vital context comprising emotions, basic needs and individual genetic traits.
The target article makes a parallel between rapid eye movement (REM) sleep dreaming and principles of the ancient art of memory (AAOM), thus proposing a role for REM sleep dreaming state in elaborative encoding of episodic memories. First, in the target article, LleweUyii argues that REM sleep dreaming renders recent memories more distinctive through novel and meaningful associations with emotionally salient and remote BEHAVIORAL AND BRAIN SCIENCES (2013) 36:6
621
Commentary/ïAeweWyn: Elaborative encoding memories. Second, Llewellyn goes on to predict how recent episodic memories are furdier configured in die brain dirough dreaming imagery. This concept further challenges the enigmatic nature of REM sleep and its dreaming. Similar to previous dieories of sleep, the inevitable reductionism inherent in the concept of die target article leaves unresolved questions. The critical issue for milestone hypodieses for REM sleep dreaming is therefore to avoid as much as possible "suiprise," "free energy" costs, or redundant "prediction eiTors," as posited by another recent concept, according to which REM sleep dreaming and phenomenology may subserve basic adaptive functions beyond memory reprocessing such as free energy minimization (Hobson & Friston 2012, p. 87). Even if die AAOM principles are regarded as a focus in the cognitive domain in die context of already existing more fundamental theories of REM sleep (e.g., Hobson 2009; Hobson et al. 2000; Jouvet 1998), diere is still ex-perimentally driven and fact-based infonnation diat needs to be reconciled. Recent human studies indicate that REM sleep electroencephalographic (EEG) signatures are not merely associated widi memory encoding and consohdation. Whereas theta (5- to 7Hz) REM sleep electroencephalographic (EEG) activity has been associated with both dream recall from REM sleep (Marzano et al. 2011) and consolidation of only emotional memory (Nishida et al. 2009), gamma (more than 25- to 30-Hz) REM sleep EEG activity has been assumed to be associated with affective mental states (Marshall et al. 2011; van der Helm et al. 2011b). Hence, frequency-specific EEG activities of human REM sleep (Gantero et al. 2003; Lhnás & Ribary 1993) may support its functions dissimilarly. A recent rodent study indicates diat dieta oscillations during REM sleep may produce synaptic downscaling in die hippocampus (Grosmark et al. 2012). Along widi the observed association between human dieta EEG rhydim and successful dream recall in REM sleep (Marzano et al. 2011), Üiis finding conforms well widi either die kind of elaborative encoding proposed in die target article or the need for room to minimize die free energy (Hobson & Friston 2012). Yet, specifically regarding the target article's concept, a possibility remains diat sleep-dependent memory reprocessing may be an epiphenomenon of more basic functions of both non-REM sleep (Tononi & Güelli 2006) and REM sleep (Hobson & Friston 2012). Sleep studies of human insight have demonstrated that whereas early-night slow-wave sleep (SWS) and its EEG signatures support die transformation of implicit knowledge into ex-pUcit insight to a hidden regularity in a complex generation task, latenight REM sleep preserves only die previously generated impUcit knowledge widiout engaging specific REM sleep EEG signatures (Yordanova et al. 2008; 2012). These results show diat only SWS and its EEG signatures may be linked to successful human heuristic creativity and do not suggest memory reconstruction during REM sleep. GriticaUy, nearly all psychiatric disorders are characterized by a REM sleep overdrive, yet diese psychiatric conditions can not be linked to successful memory formation (Benca et al. 1992; Walker 2010). Furtlier, it has been shown that augmented REM sleep in children widi attention-deficit/liyperactivity disorder is associated witli die core psychiatric symptoms of inattention and hyperactivity/impulsivity, whereas die greater amount of REM sleep in normally developing children is associated witli better performance intelligence (Kirov et al. 2007; 2011). These findings suggest at least a bidirectional role of REM sleeps depending on presence or absence of psychopathology. From a developmental perspective, infants ex-perience much more REM sleep, which decreases dirough cMdliood and adolescence, dian adults (Roffwarg et al. 1966). Thus, considering that REM sleep neurobiology and die corresponding dream generation are tighdy coupled (Stickgold et al. 2001), explanations are needed for the following: (1) What memoiy sources may create tlie presumably enormous dreaming during infancy and early 622
BEHAVIORAL AND BRAIN SCIENCES (2013) 36:6
childliood? (2) What cognitive and/or adaptive functions does such dreaming subserve? (3) How does diis risk)' homeostatic state (e.g., Hobson & Friston 2012) predominant during early development relate to evolutionary advantages? (4) What kind of memoiy processes may be subseived by REM sleep dreams incoiporated in nightmares, a common feature of botli normal ontogenesis and developmental psychopathology (Brand & Kirov 2011; Kirov & Brand 2011)? Although it has been assumed diat REM sleep subserves brain maturation during ontogenesis dirough intemally generated and genetically grounded stimulation of neuronal assembles (Marks et al. 1995), this assumption mandates experimental updates by applying new paradigms accounting for REM sleep hypodieses such as genetic programming (Jouvet 1998), direat simulation (Revonsuo 2000), and protoconsciousness (simple awareness of perception and emotions provided by genetic equipment ensuring generation of a viitual world) or Bayesian leaming and inference (Hobson 2009; Hobson & Friston 2012). Human REM sleep occurs periodically, thus distinguisliing sleep cycles from one anodier, with the frequency and duration of REM sleep periods increasing progressively across ovemight sleep (Broughton 1987). These temporal dynamics of REM sleep and dreaming can not be readily linked to die concept of elaborative encoding dirough the AAOM principles forwarded in die target article. Instead, it seems more relevant that in combination widi concomitant neuroendocrine (Steiger 2002, 2007) and cardiorespiratory processes (Gastaut & Broughton 1964), die temporal dynamics of REM sleep and dreaming could supply vitally important homeostatic functions togedier widi many cognitive adaptive processes. I argue diat die periodic occurrence of REM sleep and its dreaming may be regarded as a recurrent adaptive interference that may incorporate previously encoded and consolidated memories into a broader vital context comprising residuals of hypotheses testing, related emotions, basic needs, and individual genetic traits.
The spaces left over between REM sleep, dreaming, hippocampal formation, and episodic autobiographical memory doi:10.1017/S0140525X13001374 Hans J. Markowitsch®''^ and Angelica Staniloiu^ ^Physiological Psychology, University of Bielefeld, D-33501 Bielefeld, Germany; "Center of Excellence Cognition Interaction Technology (CITEC), University of Bielefeld, D-33501 Bielefeld, Germany; '^Hanse Institute of Advanced Study, D-27753 Delmenhorst, Germany. [email protected] [email protected] http://www.uni-bieiefeld.de/psychoiogie/ae/AE14
Abstract: It is argued that Llewellyn's hypotliesis about die lack of rapid eye movement (REM)-sleep dreaming leading to loss of personal identity and deficits in episodic memory, affectixnty, and prospection is insufficiently grounded because it does not integrate data from neurodevelopmentiil studies and makes reference to an outdated definition of episodic memory.
The assumptions about relations between sleep and memory have changed considerably since Momzzi and Magoun (1949) proposed tliat sleep reinstates the function of synapses. About a decade ago, tlie biological significance of dreams was downplayed by some audiors, who called diem "spandrels of sleep" (e.g., Flanagan 2000). Llewellyn's target aiticle confirms a new impetus in sleep research, suggesting diat Freud's wish to develop a scientific dieory for "the interpretation of dreams" might not be a "lost dream" (Freud 1900). By emphasizing elaborative encoding (as opposed to consohdation) and a major role of rapid eye movement
Copyright of Behavioral & Brain Sciences is the property of Cambridge University Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
