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Lucid dreaming: A new pathway for learning

"We are asleep. Our life is a dream. But we wake up, sometimes, just enough to know that we are dreaming."

By

Quirine Tordoir

0569097

Supervisor

Ysbrand van der Werf

Co-assessor

Winni Hofman

LITERATURE THESIS for the degree of MASTER OF SCIENCE

in Brain and Cognitive Sciences, University of Amsterdam Track: Cognitive Neuroscience

30th of January, 2015 Word count: 8332

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1. Introduction

A normal healthy person sleeps approximately 8 hours a day, meaning that throughout our lives we sleep for about 30% of the time. Of those 8 hours, we spend around 1,5 hours in Rapid Eye Movement (REM) sleep (Hobson, 2009), a stage of sleep in which most of our dreams occur. Hence you could say that we spend roughly 6% of our lives dreaming. That is a fairly large amount of time and for centuries people have been fascinated by the meaning and purpose of dreaming.

Several studies have investigated the purpose of sleep and dreaming (Hobson, Pace-schott, & Stickgold, 2000; Nir & Tononi, 2010; Peigneux et al., 2003; Walker & Stickgold, 2006) while others have explored the possibilities of using the time spent sleeping for learning purposes (Antony, Gobel, O’Hare, Reber, & Paller, 2012; Arzi et al., 2012; Rasch, Büchel, Gais, & Born, 2007; Rudoy, Voss, Westerberg, & Paller, 2009). Mostly these studies were done by exposing participants to external stimuli, such as sounds (Antony et al., 2012; Rudoy et al., 2009) or odours (Arzi et al., 2012; Rasch et al., 2007) to test whether they were able to learn from these stimuli during the different stages of sleep. However, even though these studies revealed that the brain is certainly capable of processing sensory information during sleep and that sensory information during sleep can enhance memory traces (Antony et al., 2012) or even create new memory (Arzi et al., 2012), findings have been inconsistent and have not yet resulted in a successful method for active learning.

In this review a different and potentially useful way to look at the possibility of learning during sleep will be discussed, not by using external input but by using internal processes; by so called lucid dreaming. A dream is called lucid when the dreamer becomes aware of the fact that he/she is dreaming, making it possible to influence the content and control the script of the dream (LaBerge, Nagel, Dement, & Zarcone, 1981). Moreover, lucid dreamers can be aware of information from waking life and even appear to be able to carry out prearranged tasks within their dream (Erlacher, Schädlich, Stumbrys, & Schredl, 2014; Erlacher & Schredl, 2008; LaBerge et al., 1981). This gives rise to an exciting possibility of using lucid dreaming as a new method for rehearsal. It has been shown that mental rehearsal

improves performance and increases learning (Feltz & Landers, 1983; Driskell, Copper &

Moran, 1994). Thus, if it is possible to rehearse something that was learned in waking life within a dream, it could possibly even improve performance in waking life. Imagine learning a new piece on the piano and practicing it over night? Rehearsing those

Spanish words that you learn before you went to bed? Moreover, by using a lucid dream

to practice a skill, you could practice things that are usually difficult or dangerous to practice in real life, e.g. speaking in public, driving a car, difficult conversations, confronting a problem, parachute jumping.

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The suggestion of using lucid dreaming as a field of practice is not new but has been around for decades (LaBerge et al., 1981; LaBerge & Rheingold, 1990; Tholey, 1983). A comparison has been made with mental rehearsal, suggesting that lucid dream rehearsal might be a very strong form of mental rehearsal (Erlacher, 2005). Yet research on this subject has been limited. This thesis will provide a literature review, investigating the current state of affairs of scientific research on lucid dream rehearsal. Initially it will

provide an understanding of the current neuroscientific knowledge behind lucid dreaming, starting off with some background information on dreaming in general. The different stages of sleep, their connection to dreaming and several explanations on why we dream from a neurophysiological and phenomenological/ psychological point of view will be discussed. This will be followed by a section defining the phenomenon of lucid dreaming and its neural correlates. Then a comparison will be made between mental rehearsal and lucid dream rehearsal, possible implications of lucid dreaming will be discussed and an explanation will be given on the lack of experimental studies on the field of lucid dreaming.

In sum, this thesis will provide an integrated view on dream functioning and neurophysiology for understanding the current state of affair of the investigation of lucid dream rehearsal as a possible method for learning.

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2. Dreaming

In the Oxford Dictionary the definition of a dream is “A series of thoughts, images, and sensations occurring in a person’s mind during sleep; A state of mind in which someone is or seems to be unaware of their immediate surroundings”. A dream is defined as a state of mind during sleep in which a person can experience envisioned images, sounds and emotions (Nir & Tononi, 2010). They are usually very visual and vivid, and range from very normal and realistic to bizarre and surreal. They are experienced as extremely sensory and outside of control of the dreamer. Sometimes dreams have such a strong effect on emotions that they terrify or scare the dreamer: these dreams are knows as nightmares.

Stages of sleep

During sleep, the brain goes through different stages of activity which can be roughly divided into two types: Rapid Eye Movement (REM) and Non Rapid Eye Movement (NREM). Dreaming is mostly related to REM sleep (Dement & Kleitman, 1957), although there have also been reports of dreams during NREM sleep (Manni, 2005). A normal night of sleep is built up in sleep cycles of approximately 90-100 minutes long and within each cycle a person will alternate between periods of NREM and REM sleep (Walker & Stickgold, 2006). NREM sleep can be divided in 3 stages, namely N1, N2 and N3 with each stage having its own specific electroencephalographic (EEG) characteristics (Nir & Tononi, 2010). A cycle usually starts in stage N1, passing through all the NREM stages and ending in REM. Stage N1 is considered light sleep; muscle activity slows down, eyes move slowly and people are easily woken up in this stage. Brain oscillations seem to slow down and transitions start to occur from alpha (8–13 Hz) waves to theta (4–8 Hz) waves. When entering the second stage N2, the eyes stop moving and EEG brain waves slow down even more. Sleep stage N2 EEG is characterized by complete transition to theta waves combined with K-complexes (occasional large electrical sharp waves) and sleep spindles (short bursts of increased frequency oscillatory waves). The last stage N3 is also known as deep- or slow-wave sleep (SWS) due to the prevalence of low frequency delta (<4Hz) oscillations with high amplitude. By this stage it becomes very difficult to wake people up and they are usually disorientated when doing so. The time spent in deep sleep N3 is highest during the first half of the night with short periods of REM. As the night progresses, light sleep stages of NREM predominate and periods of REM sleep increase (see figure 1) (Stickgold, Hobson, Fosse, & Fosse, 2001).

REM sleep stage got its name from the involuntary rapid saccadic eye movement that clearly differentiates this stage from other sleep stages (Dement & Kleitman, 1957; Hobson, Stickgold, & Pace-schott, 1998; Nir & Tononi, 2010). During this stage EEG activity shows brain activity similar to that of the waking brain but with inhibition of muscle tone, preventing the dreamer from acting out his/her dreams (Hobson et al., 2000; Muzur, Pace-schott, &

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Hobson, 2002). Alpha waves and higher frequency waves predominate in the EEG activity of REM sleep. When woken up in this stage, people are most likely to report long vivid and bizarre dreams.

The manifestation of sleep stages and wakefulness seem highly influenced by neuromodulatory control of the pontine brainstem (Hobson et al., 1998). Reciprocal interconnections between aminergic inhibitory neurons and cholinergic excitatory neuron determine onset of the different sleep stages. Activation of aminergic cells, such as serotonin and norepinephrine, is high during waking, decreases during NREM and becomes very low in REM sleep. The reverse is true for the cholinergic cells, such as acetylcholine, showing highest activity during REM sleep. Shifts between stages happen when the activity of aminergic and cholinergic switch dominance in activity, with respectively wakefulness and REM sleep arising at the peaks and with NREM sleep being the transition between the two stages (Hobson et al., 1998; Stickgold et al., 2001).

When do we dream?

Although dream reports appear to be more abundant in REM sleep, there has been evidence that also during NREM sleep it is possible to dream (Manni, 2005). However, these dreams seem to be shorter, fragmentary, thought-like, less vivid and less memorable than those occurring during REM sleep (Hobson, 2009). Most of these reports come from light sleep, stage N1, where people experience short lived hallucinatory dreams, so-called ‘hypnagogic hallucinations’ (Nir & Tononi, 2010). Due to sleep inertia when woken up from deep sleep, it is difficult to assess dream reports from stages of NREM sleep (Hobson, 2009; Nir & Tononi, 2010). For this reason, REM sleep has been a better candidate for dream studies. Consequently current neurophysiological and phenomenological knowledge of dreams are mainly derived from studies of REM-sleep (Desseilles, Dang-Vu, Sterpenich, &

Figure 1: from Stickgold et al. (2001). A schematic overview of sleep cycles during a normal night of sleep of 8 hours of sleep. Cycles go through stages of REM, NREM and SWS with SWS prevailing in the first half of the night, and REM sleep during the second half. When comparing the activity of acetylcholine to the onset of REM sleep, it shows a clear interaction; REM sleep arises at peak activity of acetylcholine.

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Schwartz, 2011). Therefore the underpinning of this review will be restricted to the understanding of dreaming during REM sleep.

REM sleep neuronal activation and modulation

EEG studies have shown that REM-sleep is characterized with heightened neuronal activity, more similar to wakening then to other stages of sleep (Dement & Kleitman, 1957). More recently also neuroimaging studies have been able to confirm this notion (Schwartz & Maquet, 2002) and were able to give more insight on where this cortical activity originates from. Although the activation of the brain during REM-sleep shows similarities to the waking brain there are some specific activity differences between the two brain states (Desseilles et al., 2011).

When comparing REM sleep to wakefulness, diminished activation is shown in some brain regions, specifically in the dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex, posterior cingulate gyrus, precuneus, and the inferior parietal cortex (Vandekerckhove & Cluydts, 2010). These regions are known for their importance in executive and attentional functions during wakefulness (Desseilles et al., 2011). Therefore these findings suggest a decrease in functioning of cognitive processes that depend on these brain regions during REM sleep when comparing to wakefulness.

An increase of neuronal activity has been found in the pontine tegmentum, thalamus, basal forebrain, as well as in limbic and paralimbic structures, including the amygdala, hippocampus, anterior cingulate cortex (ACC) and parietal operculum (Vandekerckhove & Cluydts, 2010). Especially the amygdala and the hippocampus are highly active during this stage. These brain structures are considered to be responsible for emotion processing, regulation and integration into memory. These findings support a role for REM-sleep in emotional memory consolidation (Vandekerckhove & Cluydts, 2010; Walker & Stickgold, 2006), since designated areas seem to be involved in processes of consolidation (Stickgold et al., 2001).

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Furthermore, several motor regions, such as the primary motor and premotor cortices, but also primary visual cortex, show increased activity during REM (Walker & Stickgold, 2006). The reactivation of memory traces during REM sleep from learned motor information prior to sleep have been proposed to be the cause of this activity (Peigneux et al., 2003). Another REM sleep phenomenon, the so called ponto-geniculo-occipital (PGO) waves are thought to play part in the activation of these areas. PGO waves seem to originate from the pontine brainstem (P), but since they propagate via the lateral geniculate body of the thalamus (G) to the occipital visual cortex (O) PGO waves can also be measured in those brain structures (Manni, 2005). As noted earlier in the section “stages of sleep”, the transition between sleep and wakening is largely regulated by the reciprocal interaction between aminergic- and cholinergic systems (Hobson et al., 1998). The PGO waves also seem to be affected by this reciprocal interaction. PGO waves are typically measured during the transition from NREM to REM sleep, where activation of cholinergic activity is high, and during REM co-occur with the saccadic eye movements that characterize REM sleep (Desseilles et al., 2011). Activation of the visual and motor cortices, as well as the amygdala and hippocampus, during REM sleep are thought to be triggered by PGO waves. Therefore it has been suggested that PGO waves play an important role in memory consolidation by reactivating memory traces during REM sleep (Stickgold et al., 2001).

Figure 2: from Desseilles & Dang-Vu (2011). A regional brain pattern showing activation and deactivation during REM sleep compared to wakefulness.

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Why do we dream?

There have been various theories on the purpose of dreaming (Desseilles et al., 2011; Franklin & Zyphur, 2005; Hobson, 2009; Revonsuo, 2000; Stickgold et al., 2001). Some claim that dreaming is just the mere side effect of activation processes occurring during REM sleep physiology (Desseilles et al., 2011; Revonsuo, 2000). Since REM sleep is claimed to be involved in reprocessing and optimizing information learned during daytime (Peigneux et al., 2003) it is thought that memory traces get reactivated during sleep. When this happens, the brain simply tries to make sense of the electric involuntary stimuli it perceives and combines the reactivated traces into a ‘story’ which we experience as a dream. Many dream features can be attributed to diminished or heightened activity of particular brain regions. The increased activity of amygdala and hippocampus, as described above, could explain the emotional nature of most dreams (Vandekerckhove & Cluydts, 2010; Walker & Stickgold, 2006) whereas the decreased functioning of the DLPFC could account for the lack of self-awareness and control over the dream (Desseilles et al., 2011; Hobson et al., 2000, 1998; Maquet et al., 1996). The PGO waves, as discussed above, are thought to represent the main mechanism for the internal neuronal activation that create dreamlike visual experiences (Hobson et al., 1998; Stickgold et al., 2001).

However, aside from the fact that dream experiences have also been reported outside of REM sleep (Manni, 2005), it seems too narrow to state that dreams are just a random by-product of the neuronal activity during REM sleep. Revonsuo (2000) proposed that dreams have an evolutionary purpose. They serve as a preparation for the real world, by simulating threat in an entirely harmless situation, namely during sleep while lying in bed, in order to rehearse endangered encounters without the risk of getting hurt. Based on waking experiences our dreams teach us how to recognize and deal with possible threats (Revonsuo, 2000). Psychological theories on dream functioning have proposed a similar role, posing that dreams help the individual cope with personal concerns or problems in waking life up to the point that they promote emotional resolution and positively influence mood (Desseilles et al., 2011). Where Revonsuo restricts his view to threat rehearsal, Franklin and Zyphur (2005) broaden this view to a more general virtual rehearsal mechanism. They suggest that especially the developing brain could learn from the vivid experiences during dreams by a form of mental rehearsal so that we can act in an appropriate manner based on the perceived stimuli (Franklin & Zyphur, 2005). The fact that REM sleep is most prominent in new-born babies and infants support this argument. Franklin and Zyphur believe that these adaptive qualities of dreaming help the individual by restructuring and optimizing newly received information in cortical networks in order to maintain psychological wellbeing. Helm and Walker (2010) elaborated on the link between sleep and emotional wellbeing. They discussed the interaction between dreaming and emotional regulation, in which they link

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recovery of an emotional trauma to dreaming and even introduce REM sleep as an “overnight therapy”.

If we stay with the latter theory on dream purpose, suggesting that dreams prepare us for the outside world or help us cope with the outside world, then what would that mean if we could control what we dream about? If dreaming teaches us how to adapt and respond to stimuli we receive, then by becoming aware in our dreams we could be able to direct the occasions we want to be prepared for in real life. Becoming aware whilst dreaming is known as lucid dreaming. In the next chapter, the phenomenon of lucid dreaming will be discussed, building up to possible implications of lucid dreaming such as exploiting the theory of using a lucid dream to prepare ourselves for the real world.

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3. Lucid Dreaming

In the Oxford Dictionary lucid is defined as expressed clearly and in the context of dreaming it defines the following: (Of a dream) experienced with the dreamer feeling awake, aware of dreaming, and able to control events consciously. During lucid dreaming, the dreamer becomes aware that he/she is dreaming (LaBerge et al., 1981). The realization of being in a dream gives rise to the possibility to consciously influence various actions or features that are present in the dream (Erlacher, 2009). Lucid dreaming mostly occurs during REM sleep but there have been reports of lucid dreaming in NREM sleep stage N1 and during transition from N2 to REM sleep (LaBerge et al., 1981) although most studies on lucid dreaming have reported only REM sleep lucid dreaming (Mota-Rolim & Araujo, 2013).

What makes a dream lucid?

What differentiates a lucid dream from a non-lucid dream is the level of consciousness (LaBerge et al., 1981) As described earlier, non-lucid dreams are an internal world in which events and characters can be vivid and surreal and everything happens beyond the dreamer’s control. What is remarkable is that during the event of dreaming there is no realization of the surrealism of the perceived world. The dreamer can feel part of this world even if the content is inexplicable and inconsistent/incongruent. The dream is experienced as real and only upon awakening the dreamer is able to realize it was in fact a dream (Desseilles et al., 2011). It has been opted that this is due to deactivation of the prefrontal cortex during REM sleep. The prefrontal cortex is thought to be involved in self-reflective awareness, attention control, internal goals and decision-making (Desseilles et al., 2011; Hobson et al., 2000, 1998; Maquet et al., 1996) Therefore deactivation of this area affects the ability to think logically and make critical judgments, resulting in the lack of control of dream actions and events and in the failure of noticing the bizarreness and inconsistency of the dream. This delusional character of a dream is a feature of primary consciousness (Hobson, 2009). Primary consciousness can be simply put as “the subjective awareness of perception and emotion” (Hobson, 2009). The dreamer is merely aware of the immediate presence, without a sense of the past or the future (Edelman, 2005). Upon awakening, it is believed that the dreamer enters secondary consciousness giving rise to features such as self-reflective awareness, abstract thinking and volition (Hobson, 2009). Secondary consciousness makes it possible to reflect on the past and helps the dreamer to realize that the bizarre world he/she just experienced was only a dream. When awake, humans are aware of their environment, their bodies and their selves; they are even aware of their awareness.

According to the primary-secondary hypothesis by Hobson and Voss (2011), in a lucid dream, the dreamer enters secondary consciousness making it possible to become

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self-aware within the dream but without actually waking up. It is a remarkable state of sleep in which elements of secondary consciousness coexist with the primary state of consciousness (Voss, Schermelleh-Engel, Windt, Frenzel, & Hobson, 2013). The dreamer can be aware of the dream state he/she is in and to some extent even influence dream events. Sometimes lucid dreamers can even take control over the plot and decide to do things that are physically impossible like flying or being invisible. The dream world does not obey laws of physics, giving rise to incredible possibilities when gaining control. Both lucid insight and plot control are functions of secondary consciousness (Edelman, 2005; Hobson, 2009). In lucid dreams, part of the brain operates in the primary mode while other parts have access to secondary consciousness. This makes lucid dreaming a very good candidate to investigate states of consciousness and their neurological correlates (Hobson, 2009; Voss, Holzmann, & Hobson, 2014).

Neurophysiology of lucid dreaming

As described in the previous section, a dream is considered lucid when the dreamer experiences awareness of being in a dream-state and is capable of self-reflection, insight, judgment or abstract thoughts (Hobson & Voss, 2011); attributes that constitute secondary consciousness (Edelman, 2005). For these functions to arise, it is expected that the essential cortical structures get modulated while sleeping. The brain should be activated enough to enter a higher level of consciousness, but not upon full awakening. The idea has been postulated that lucid dreaming is a brain-mind-state between REM-sleep and waking (Hobson, 2009; Voss, Holzmann, Tuin, & Hobson, 2009).

Hobson and colleagues (2000) underpin this idea by capturing lucid dreaming within their so called AIM-model. This neurocognitive model is represented by a three dimensional space that plots activation (A), input source (I), and neuromodulation (M) as the x, y, and z dimensions (Hobson et al., 2000). In their article, Hobson and colleagues (Hobson et al., 2000; see also Hobson, 2009a) describe how consciousness evolves in brain-mind-states like NREM-, REM-sleep and waking in terms of these three factors. (A) Several cortical areas are activated during wakefulness while deactivated during NREM-sleep, but get reactivated when entering REM-sleep (see section “REM sleep neuronal activation and modulation”). High levels of activity, corresponding with a high value of “A” in the aim model, correlate to the ability of the mind to access information stored in the brain during wakefulness and during synthesis of dreams. (I) The factor input-output gating corresponds to the amount of internal or external sensory input, resulting in a low or high value of “I” respectively. In state of wakefulness the brain is open for external sensory input, but external input gets blocked when entering a state of sleep. However during REM sleep PGO waves emerge, functionally replacing the external sensory input from the inside out, simulating the external world during

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dreams. As described earlier, PGO waves are thought to be responsible for the activation of the visual and motor cortices during REM (Stickgold et al., 2001). (M) The shift from aminergic to cholinergic neuromodulation is represented in the AIM model as the “M” factor. As described earlier, aminergic and cholinergic neurons are reciprocally connected and are thought to be responsible for the onset of different sleep stages. When the activity curves of these neurons cross changes in the sleep stages occur. Aminergic neurons are most active during wakefulness while cholinergic cells show peak activity during REM-sleep (Stickgold et al., 2001). It has been suggested that the shift from aminergic to cholinergic alter the ability of remembering an event and reduces reliability of cortical circuits. This could explain the acceptance of bizarre temporal and illogical events and associations that characterize most dreams during REM-sleep (Hobson et al., 2000; Hobson, 2009).

Only the mind-states waking, NREM and REM sleep were described above according to this model of brain-mind-states but besides these three cardinal states of consciousness there are many more mental states (abnormal conditions such as coma or psychosis and other psychiatric syndromes) that can be placed within the AIM state-space-model (Hobson et al., 2000). Also lucid dreaming can be placed within this three dimensional model (Hobson et al., 2000; Hobson, 2009; Voss et al., 2009). For lucid dreaming to occur, Hobson (2000) predicts that the deactivated dorsolateral prefrontal cortex (DLPFC) during REM-sleep should be reactivated similar to waking but just enough not to interfere with the pontolimbic systems signals. Input should still come from an internal source to remain in a dream-state, but the reduced self-awareness should be enhanced in order for the dreamer not to perceive the dream-world as the real world. When positioning lucid dreaming within the AIM state space, it suggest that lucid dreaming “is a hybrid state lying across the wake-REM interface” (Hobson et al., 2000).

In a study by Ursula Voss and colleagues (2009) participants were recorded with EEG while sleeping, with the aim of measuring physiological correlates of lucid dreaming. They were able to show that lucid dreaming is significantly different from both non-lucid dreaming and waking when comparing EEG power and coherence profiles. Differences in oscillatory power and coherence were found between lucid sleep, REM-sleep, and waking with eyes closed (Voss et al., 2009). In the low frequencies (below 28 Hz) lucid dreaming appeared to be REM-like, but differed from REM-sleep state at higher frequencies. During lucid dreaming a higher power was measured starting at 28 Hz and peaking at 40 Hz; all within the gamma frequency range. The highest significant difference in gamma power for lucid dreaming occurred frontolaterally and frontally. Lucid dreaming together with REM-sleep differentiated from waking state by a higher power in low frequencies, except for alpha as was expected. Alpha power is predominantly higher in state of waking, because alpha activity is a typical feature of waking with eyes closed (Voss et al., 2009).

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When looking at coherence over the whole frequency spectrum, waking and lucid dreaming appear to be more similar and both significantly higher than REM-sleep. When considering specific frequency bands in the comparison between waking and lucid dreaming, waking showed higher coherence for alpha frequencies whereas in lucid dreaming coherence was higher in the delta and theta band. Furthermore coherence was larger for lucid dreaming compared to waking in frontolateral regions and when compared to REM, coherence was larger at frontal regions (Voss et al., 2009).

This study data indicates that lucid dreaming is indeed highly correlated to waking and is not just a form of REM-sleep. The results suggest that lucid dreaming has features of both REM sleep and waking. For lucid dreaming to occur, brain activity during REM-sleep will shift to a more wake-like brain pattern (Voss et al., 2009). These findings nicely correspond with the placement of lucid dreams within the AIM model as an intermediate position between REM sleep and waking (Hobson et al., 2000; Hobson, 2009).

Furthermore his study partially supports Hobson’s prediction about the reactivation of the DLPFC during lucid dreaming. Although the EEG data did not support highly localized analysis, coherence did show a clear increase in frontal and frontolateral areas for lucid dreaming when compared to REM sleep. In addition, a recent fMRI study, with the same aim of investigating lucid dream neural correlates, was able to provide localized data. In line with Voss’ EEG data, they found increased activity during lucid dreaming in areas that are normally deactivated during REM sleep. Reactivation was measured in several brain region, including the bilateral precuneus, cuneus, parietal lobules, and prefrontal and occipitotemporal cortices (Dresler et al., 2012). As mentioned before, it has been hypothesized that deactivation of the frontal cortex during REM sleep causes the loss of features of secondary consciousness (Desseilles et al., 2011; Hobson et al., 2000, 1998; Maquet et al., 1996). Thus reactivation of these areas might explain or even cause the recovery of higher order cognitive skills involved in lucid dreaming.

In sum, neurophysiological findings strongly support the notion that lucidity is related to the reactivation of areas which are normally deactivated during REM sleep, most prominently in frontal brain areas. Lucid dreaming is an extraordinary state of mind, between waking and dreaming, that gives rise to functions of secondary consciousness on top of the already existing features of primary consciousness while dreaming.

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4. Application of lucid dreams

Lucid dreams have been used for scientific research of consciousness (Desseilles et al., 2011; Hobson & Voss, 2011; Hobson, 2009; Voss et al., 2013), as well as for the understanding of other mental states or illnesses (Mota-Rolim & Araujo, 2013). But aside from the scientific significance of understanding the mind, lucid dreaming has also been used in a more practical sense, such as in nightmare therapy and in sport performance enhancement.

Nightmare therapy

In nightmare therapy psychotherapists have applied lucid dreaming with the idea that patients that suffer from recurring nightmares can benefit from the awareness of being in a dream. By becoming lucid, dreamers can become aware of the fact that they are indeed dreaming, thus making it possible to alter the nightmare storyline in order to stop the dream from frightening them. Spoormaker and van den Bout (2006) investigated the validity of lucid dreaming in the treatment of patients suffering from chronic nightmares. The Lucid Dreaming Treatment (LDT) consisted of three components: exposure to the idea, mastery of the technique, and lucidity exercises. Results showed a decrease of nightmares frequency after treatment but it remains unclear which part of the LDT was responsible for this alleviation because alleviation occurred also in patients who did not reach lucidity. This suggests that perhaps the idea of gaining control of the nightmare can already be enough to reduce nightmares. Nonetheless LDT appears to be promising as a treatment for nightmares, even though the successfulness of this form of nightmare therapy cannot be fully ascribed to the state of lucidity (Spoormaker & Van Den Bout, 2006).

Sport performance enhancement

Lucid dreaming has also been applied within sport science and has been thought to be of great value for sport performance enhancement (Erlacher & Chapin, 2010). Already in 1981, scientists came up with the idea to use dream, or more specifically lucid dreams to practise sport skills in athletes (Tholey, 1981). Paul Tholey, a sports psychologist and pioneer in dream research investigating the use of lucid dreaming for motor skill training, did a qualitative study where lucid dreamers were instructed to perform complex sport skills. Participants were asked to execute a difficult skill, that they already mastered in waking life, when they become lucid. Participant reported that they were perfectly capable of remembering the given instruction and were able to execute the complex sport skill in their lucid dream. Furthermore, participants claimed that they improved during practice within the dream and that this improvement persistent even in waking life. Unfortunately there was no

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measurement done to test sport performance after lucid dreaming, so these findings remain subjective (Tholey, 1981; Erlacher & Schredl, 2008).

More recently, in a small online experimental pre-post design study Erlacher (2005) showed the influence of lucid dream practice on an aiming task. The task had to be performed twice, once before sleeping and once after waking. In this aiming task, participants had to throw a coin into a cup and each time they had 20 tosses. They were instructed to practice the task in their lucid dream overnight. Hit rate increased for the group that was instructed to practice within their lucid dream, while the other group without lucid practice instructions showed no increase (Erlacher, 2005). Although this experiment does not exclude confounding variables, results indicate a possible significance for lucid dreams as a place for skill enhancement in wakefulness (Erlacher & Schredl, 2008).

Furthermore several anecdotal studies showed successful use of lucid dreaming in sport performance. LaBerge and Rheingold (1990) discussed reports of several amateur athletes who improved their skills during lucid dreams. In their book they describe a long distance runner who practiced his running technique, a tennis novice who learned his tennis serve and a woman who enhanced her skating skills. Examples of professional athletes (Alpine skiing, equestrian and martial arts) who used lucid dreaming as a practice ground were reported by Tholey (1990). Aside from researching other lucid dreamers, Tholey also used himself as an study subject and became a very skilled lucid dreamer. He practiced sport techniques in his lucid dreams and claimed that this helped him improve in waking life (Erlacher, 2005). More recently, Erlacher (2005) collected some anecdotal reports from professional athletes of which two are cited there as examples:

Spring board diving (female, 33): „I practice complex twists and somersaults in my lucid dreams. When I do my lucid dream practice the movements feel real but if I want to I can slow down the whole sequence to focus on important details of the dive.”

Winter sport (male, 26): „I dreamed lucidly about snowboarding, I was in a fun park and I practiced several tricks on my board. I couldn‘t do those tricks in waking life but the practice in my dreams helped to get better.“ (both quotes are cited from Erlacher & Schredl, 2008)

Lucid rehearsal versus mental rehearsal

The explanation on why lucid dreaming would be a valuable place for practicing motor skills is because it can be compared with mental imagery (Erlacher, 2005). Practicing a motor skill in a lucid dream is equivalent to mental rehearsal in wakefulness. In mental rehearsal or imagery “movements are rehearsed with an imagined body on a cognitive level” (cited from Erlacher et al., 2014). Mental imagery is a successful and well-known method

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within sport science and several meta-analyses (Feltz & Landers, 1983; Driskell et al., 1994) have confirmed that mental rehearsal in general has significant positive effects on performance. Studies investigating the effect of mental rehearsal on motor performance showed that repeated imagination of muscle movement resulted in an increase of muscular strength (Yue & Cole, 1992), that it improves the acquisition of new motor skills (Hall, Buckolz, & Fishburne, 1992; Yágüez et al., 1998) and that it increases sport performance (Lejune, Decker & Sanchez, 1994).

It has been suggested that mentally simulating a movement activates the same neural activity as the actual preparation and execution of that movement (Jeannerod, 1994). In a research study, Decety (1996) investigated this notion based on three lines of evidence: mental chronometry, measurement of central nervous activity and autonomic responses. He found that neural activity and autonomic responses during imagery of physical activity were almost equivalent to the neural activation and the autonomic responses of actual exercise (Roland, Larsen, Lassen, & Skinhoj, 1980; Decety, Jeannerod, Germain, & Pastene, 1991). The same accounted for mental chronometry; the timing of imagined and actual motor actions closely mimicked actual movement times (Munzert, 2002). These findings provide evidence that imagined and executed actions to some extent share the same central neural structures (Decety, 1996).

A parallel comparison can be made between dreamed actions in REM sleep and executed actions in wakefulness (Fenwick et al., 1984). Erlacher and Schredl (2008) wrote an extensive review addressing the correlation between dreamed and real life action. They demonstrate that dreamed action is comparable to actual action, similar to mental imagery. The strongest evidence was found in measurements of central nervous activity of REM dreams. Several lucid dream studies revealed a correlation between dreamed limb movements and an increase in EMG activity in the corresponding limb (Fenwick et al., 1984; Hearne, 1983; LaBerge et al., 1981). In a more recent study, Dresler and colleagues (2011) provided first (preliminary) evidence that lucid dreaming content can be visualized by neuroimaging. In the experiment, they were able to measure activation in the sensorimotor cortex elicited by predefined motor task performed during lucid dreaming (Dresler et al., 2011).

Autonomic responses and mental chronometry findings were less convincing due to inconsistent results (Erlacher & Schredl, 2008). For example, regarding mental chronometry, LaBerge (1985) showed in a pilot study that counting to ten in a lucid dream takes about the same amount of time as during waking. Erlacher en Schredl (2004) replicated this finding, but they had added another task to the experiment namely a motor task in which participants had to perform a number of squats. Surprisingly, this motor task took up to 44.5% more time in lucid dreams than in wakefulness. The authors speculated that this disproportional effect

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was caused by the modality of the activity (cognitive vs. motor activity). Fortunately, a recent study by Erlacher and colleagues (2014) reveals new insights on this subject. In this study they confirm the earlier findings of prolonged duration of motor action in lucid dreaming (Erlacher & Schredl, 2004) but moreover they discovered that the relative time structure is not disproportionally longer during lucid dreaming. The authors hypothesized that the prolonged duration of dream action could be related to the absence of muscular feedback or perhaps due to slower neural processing during REM-sleep. This study offers additional evidence of mental chronometry in lucid dreaming, thus supporting the notion of correspondence between action in lucid dreams and executed action in waking life.

Lucid rehearsal: a new pathway for learning?

Based on these findings it is permitted to claim that practicing in lucid dreaming can be seen as a novel type of mental rehearsal, making it plausible for lucid dreaming practice to be an effective method of performance enhancement (Erlacher & Schredl, 2008). Similar to mental rehearsal (Decety, 1996), this enhancement can be explained by the strengthening of neuronal pathways, required for the skill, that are similar for waking and dreamed actions (Erlacher & Schredl, 2008).

These two types of mental rehearsal (waking mental rehearsal and lucid dream rehearsal) both simulate movements at a cognitive level, without physically executing the action. However there are some properties that differentiate lucid dream- from waking mental rehearsal. One being the state of consciousness in which they occur; mental practice in perform during wakefulness whereas lucid practice can only be executed while sleeping (Erlacher & Chapin, 2010). This dream state gives rise to “an extraordinarily vivid form of mental imagery during lucid rehearsal” (LaBerge & Rheingold, 1990). Dream images are stronger sensory imitations than waking mental images (LaBerge & Rheingold, 1990). A lucid dream is an imaginary world that the dreamer can control, where boundaries of the physical world don’t exist. The more realistic the imagination, the closer the neuronal activation during the dream resembles the neuronal pattern that is activated during the actual event. Therefore lucid dreaming practice is expected to be more effective as a tool for rehearsal than waking mental imagery (Erlacher & Chapin, 2010).

Secondly, there is another important difference between dreamed action and imagined action that supports the idea that lucid rehearsal is a more effective type of mental rehearsal. When mentally rehearsing a movement during waking, neuronal input to the muscles must be inhibited to stop you from acting out your imagination (LaBerge & Rheingold, 1990). During dreaming the neuronal impulses do not have to be attenuated, due to muscle atonia which already prevents the dreamer from acting out his or her dreams (Hobson et al., 2000; Muzur et al., 2002). Therefore there is no need for the neuronal input

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that comes from the dream action to be actively attenuated. Instead the input can have the same neuronal strength as in waking. A study by Jouvet (1979) provides evidence for this unimpaired neural strength of dreamed action. He developed a cat model without muscle atonia causing the cats to perform complex behaviour while sleeping. The movements were interpreted as enactments of dreams (Arnulf, 2011; Erlacher & Schredl, 2008). This same enactment of dreams was found in humans with certain sleep disorders that alter or damage the muscle inhibition in REM sleep (Sforza, Krieger & Petiau, 1997). Thus during lucid rehearsal, dreamed actions are performed at least at the higher-order neuronal level similarly to real live actions, making lucid rehearsal potentially a strong form of mental rehearsal.

Limited research

Noteworthy is that while the empirical data on mental imagery are abundant, the amount of research done on rehearsal in lucid dreaming is extremely small. Although scientists seem to agree on the statement that practicing during lucid dreaming is a novel type of mental rehearsal, only very few studies were done investigating the effect that lucid dreaming has on waking performance systematically. Studies that have been done in this field were either anecdotal or of low experimental value (as described above in section “Sport performance enhancement”). Nevertheless results were promising therefore further empirical research would be expected. Evidently, there have been some obstacles around the study of lucid dreams that make it a challenging field for experimental research.

One difficulty was the measurability of lucid dreams. Because there was no measure of lucidity other than subjective report, it was problematic to set up an experimental study. LaBerge was the first to show that it was possible to detect a lucid dream and thus verify the existence of the phenomenon (LaBerge et al., 1981). Lucid dreamers were given the task to perform a specific ocular movement the moment they realized they were dreaming. Unlike other muscles, the eyes are not in atonia during REM (Dement & Kleitman, 1957). The eye movement, usually two consecutive left and right horizontal eye movements left–right–left– right, produced a distinct electrooculagram (EOG) recording during REM sleep, making it possible for the researchers to get an objective measure of a lucid dream. Furthermore this also proves that it is possible for lucid dreamers to execute a prearranged task within their dream, meaning they have access to their waking memory (Erlacher, 2009; LaBerge et al., 1981). This is a prerequisite for exploring the idea of lucid dreaming as a place for mental rehearsal.

But despite the progress that has been booked in lucid dreaming research, still the overall number of lucid dreaming studies remains small. Fundamental reason for this is because it is difficult to find proficient lucid dreamers (Erlacher & Schredl, 2008). The main obstacle is to find participants that firstly are experienced lucid dreamers and secondly can

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induce a lucid dream on the specific night spent in the laboratory (Dresler et al., 2012; Voss et al., 2009). Although lucid dreaming is a cognitive skill that can be developed (LaBerge et al., 1981; Paulsson & Parker, 2006; Purcell, Mullington, Moffit, Hoffman, & Pigeau, 1986) until recently it was not possible to effectively and consistently induce lucid dreams. In the following section several induction techniques will be discussed together with a new promising technique that might provide a solution for this induction problem.

Induction techniques

As explicated previously, lucid dreaming is considered to be a hybrid state between dreaming and waking and dreamers often report losing their lucidity either by waking up or by falling back into a non-lucid dream. Thus, to obtain a state of lucidity spontaneously is very rare and evanescent but it has been shown that lucidity can be trained. Lucid dreaming is thought to be a cognitive skill that can be developed (LaBerge et al., 1981; Paulsson & Parker, 2006; Purcell et al., 1986). Stumbrys and Erlacher (2012) wrote a systematic overview assessing the effectiveness of lucid dreaming induction techniques used in dream research. They categorized the techniques in three main categories: Cognitive techniques, external stimulation and drug application. Only the techniques with the most promising results will be discussed here.

Cognitive techniques focus on deploying cognitive skills to increase the likelihood of lucid dreams. The technique that was used most often was Mnemonic Induction of Lucid Dreams technique (MILD). It requires that the dreamer, before falling asleep imagines a dream and reminds himself of the intention of becoming lucid. This technique was most successful in the morning after 30–120 min of wakefulness. Another method is reflection/reality testing, where the dreamer trains himself to do reality check on a regular basis during waking. By doing so, the dreamer is more likely to do the same during a dream and therefore gives the possibility of realization of a dream state. The intention technique is quite similar to MILD. It requires the dreamer, prior to sleep, to imagine himself being in a dream and recognizing it as such. However, in MILD the focus is on memory, the dreamer has to remember that he is dreaming, whereas in the intention technique the dreamer should recognize that he is dreaming.

The method that was most successful appeared to be Tholey’s combined technique. This technique combines several techniques in one namely: intention, reflection and autosuggestion. Pre-sleep autosuggestion means that the dreamer suggests to himself, before falling asleep, that he will become lucid (Tholey, 1983). It has been proposed that autosuggestion primes the prefrontal cortex that is involved in self-reflective awareness thus increasing the likelihood of lucidity (Hobson et al., 2000). Whereas other techniques increase

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the frequency of lucid dreams only in lucid dreamers, this combined technique also aided people that were inexperienced in lucid dreaming to get to a lucid state (Tholey, 1983).

External stimulation techniques are based on the idea that an external stimulus can be recognized during sleep by the dreamer in order to trigger awareness of the dream state. These external stimuli can be tactile, visual or auditory (Stumbrys & Erlacher, 2012). Most studies were of low quality and results were not conclusive but even though some study results were promising, they should be viewed with some scepticism since effectiveness of this method was only achieved within one research group (for an overview see Stumbrys & Erlacher, 2012) and has not been replicated by others.

As a drug application method, only the drug donepezil was empirically tested (LaBerge, 2004). By altering the cholinergic system and enhancing the acetylcholine levels in the brain during sleep, it is thought that lucid dreaming can be induced. Although this method was successful, unpleasant side effects were present. Further research should be done to investigate these adverse effects and to test other substances that are suggested to induce lucidity by altering the cholinergic system, e.g. DMAE (2-dimethylaminoethanol), rivastigmin, galantamine, huperzine (Stumbrys & Erlacher, 2012).

Unfortunately, although several techniques showed promising results, especially the cognitive methods, research groups remained small and the methodological quality was in most studies quite low. Abovementioned induction methods indeed had an effect on the frequency of lucid dreaming but, there has not been an induction technique that actually induces lucid dreaming reliably, consistently and with a high success rate, up until now,

Recently scientists discovered an effective way of inducing lucidity by applying low-current stimulation to the scalp during REM sleep (Voss et al., 2014). Based on previous studies, that investigated neuronal correlates for lucid dreaming (Dresler et al., 2012; Voss et al., 2009), it was hypothesized that gamma-band activity around 40 Hz in frontal and temporal brain areas could have a causal relationship with dream lucidity. Voss and colleagues looked at the involvement of the prefrontal cortex in lucid dreaming by stimulating the prefrontal areas of 27 participants with transcranial alternating current stimulation (tACS) at a range of different frequencies. What they observed was that only stimulation at 25 Hz and 40 Hz induced further gamma frequency activity in the frontal and temporal lobes, a frequency that was already found to be correlated to lucid dreaming (Voss et al., 2009). These results provide a strong causal relationship between prefrontal high gamma oscillations and increased conscious awareness (Voss et al., 2014). The authors speculate that high gamma oscillatory activity could even be a necessary condition for the emergence of secondary consciousness, in dreaming but perhaps also in waking.

What is striking in this research, is that this experiment had a large sample size because, unlike most lucid dreaming research, the participants were inexperienced in lucid

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dreaming (Voss et al., 2014). Moreover, lucid dreams were reported by participant after being stimulation with 25 Hz (58%) and even more after stimulation with 40 Hz (77%). These findings are astonishing and therefore very promising for lucid dreaming research and for potential applications of lucid dreaming.

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5. Conclusion

In this thesis the goal was to provide an extensive review on lucid dreaming and its possible application as a method for learning/rehearsal. Research on mental rehearsal together with studies implying a similarity between real and dreamed action, strengthen the notion that lucid dreaming could be a strong form of mental rehearsal and presumably even more effective than mental rehearsal while awake. During mental rehearsal, there must be active inhibition to stop/refrain the person from acting out their imagination. Lucid dream rehearsal does not need this active inhibition because of muscle atonia during REM sleep. Thus dream actions are not performed physically but the neuronal pattern is activated in the same way as in real life, suggesting that lucid dream rehearsal could have a strong effect on waking performance. Yet, research investigating the possibility of lucid dream rehearsal has been limited, even though the idea has been around for decades.

Up until recently it was not possible to investigate lucid rehearsal properly due to a lack of effective lucid induction techniques. Experimental research on lucid dreaming has been limited because it remains difficult to recruit experienced lucid dreamers, and moreover to test them while they are successfully experiencing a lucid dream during the nights in the sleep laboratory. There are many lucid induction techniques but none are effective on inexperienced lucid dreamers. Fortunately, Voss and colleagues recently developed a new induction technique that could make any participant into a lucid dreamer. They were able to reactivate the frontal cortex and with that effectively and consistently induce lucidity. This paves a way for lucid dreaming research on a larger scale and moreover gives rise to the possibility of systematically investigating lucid rehearsal.

The idea of lucid dreaming being the method to use to practice skills for waking live coincides nicely with Revonsuo’s theory of dream purpose. Revonsuo (2000) postulates that dreams are a simulation of the real world, helping us to “practice” and prepare us for situations in real life. Lucid rehearsal takes this dream purpose to the next level and provides the possibility of consciously deciding what one wants to prepare for with one’s dream. The advantage of the dream world is that there are no limitations like in our real physical world; practicing newly mastered skills goes without the possible dangers of the real world. Now, with the new induction technique, the time has come to investigate lucid dreaming on a larger scale and explore the potentials of lucid rehearsal as a new pathway of learning.

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