How the Brain Learns While You Sleep

From BBC Future, this is a cool and in-depth examination of what the research shows on how the brain consolidates learning in sleep (and in dreams, but that another study).

Below this long article is a related piece from BBC News.

Can you learn in your sleep?

David Robson | BBC
22 July 2014



(Getty Images)
Sleep learning used to be a pipe dream. Now neuroscientists say they have found ways to enhance your memory with your eyes closed, says David Robson.
Just before you climb under your duvet, you carefully prepare your room. You sprinkle a few drops of incense on your pillow, put on some headphones, and place a strange-looking band over your scalp. Then you go to sleep. The ritual takes just a few minutes, but you hope this could accelerate your learning of a diverse range of skills: whether you are trying to master the piano, tennis or fluent French. You won’t recall a single aspect of the night’s “training” – but that doesn’t matter: your performance the next morning should be better, all the same.

The idea of learning as you sleep was once thought very unlikely, but there are several ways – both low- and hi-tech – to try to help you acquire new skills as you doze. While there is no method that will allow you to acquire a skill completely from scratch while you are unconscious, that doesn’t mean that you still can’t use sleep to boost your memory. During the night, our brain busily processes and consolidates our recollections from the day before, and there could be ways to enhance that process.

Given that we spend a third of our lives in the land of nod, it is little wonder that sleep learning has long captured the imagination of artists and writers. In most incarnations, it involved the unconscious mind absorbing new information from a recording playing in the background. In Aldous Huxley’s Brave New World, for instance, a Polish boy learns English after having slept through a radio lecture by George Bernard Shaw; the authoritarian government soon uses the same technique to brainwash its subjects. More recently, in The Simpsons, Homer buys a tape to subliminally reduce his appetite as he sleeps, only to find that it is instead changing his vocabulary. When his wife, Marge, asks if his diet is working, the normally inarticulate Homer replies: “Lamentably, no. My gastronomic rapacity knows no satiety”.

Bad science

In reality, this particular kind of sleep learning is almost certainly impossible. Although some early studies suggested that subjects could pick up some facts as they slept, the researchers couldn’t be sure that they hadn’t just awoken to listen to the recording. To test those suspicions, Charles Simon and William Emmons attached electrodes on the scalps of their subjects, allowing them to be sure that they only played the tapes once the subjects were dozing. As they had suspected, the subjects learnt nothing once they had dropped off. The results were published in the 1950s, but entrepreneurs over the years have still tried to cash-in on the attraction of effortless learning with various products – even though their methods had no scientific basis.

Monitoring brain activity of sleeping people suggests they can't learn new skills while unconscious (SPL)

Despite being blind and deaf to new information, however, the sleeping brain is far from idle: it mulls over the day’s experiences, sending memories from the hippocampus – where memories are first thought to form – to regions across the cortex, where they are held in long-term storage. “It helps stabilise the memories and integrate them into a network of long-term memory,” says Susanne Diekelmann at the University of Tubingen in Germany. Sleep also helps us to generalise what we’ve learnt, giving us the flexibility to apply the skills to new situations. So although you can’t soak up new material, you might instead be able to cement the facts or skills learned throughout the day.

Smell enhancer

So far, at least four methods have shown promise. The simplest strategy harks back to the research of a 19th Century French nobleman named the Marquis d’Hervey de Saint-Denys. As he explored ways to direct his dreams, the Marquis found that he could bring back certain memories with the relevant smells, tastes or sounds. In one experiment, he painted a scantily clad woman while chewing an orris root; when his servant then placed the root in his mouth as he slept, the tart flavour brought back visions of the same beautiful lady in the foyer of a theatre. She was wearing “a costume that would have hardly been acceptable to the theatre committee”, he wrote with delight in his book, Dreams and How to Guide Them. Another time, he asked the conductor of an orchestra to play certain waltzes whenever he danced with two particularly attractive women. He then rigged up a clock to a music box, so that it played the same tunes during the night, which apparently brought their handsome figures to his sleeping mind.

The Marquis simply wanted to seed his slumbers with pleasant (and sometimes lustful) experiences, but it now looks like the same approach can also trigger the sleeping brain to replay the learning of skills or facts, reinforcing the memory in the process.

(Thinkstock)

Diekelmann, for instance, asked her volunteers to play a variation of the game Concentration, in which they had to learn a specific pattern of objects in a grid before going to sleep in her lab. Some of the subjects were exposed to a subtle, artificial, odour as they played, and Diekelmann then wafted the same scent into their noses as they slept. Brain scans showed that these subjects had greater communication between the hippocampus and several cortical areas, compared to those without the cue – just the kind of activity that should lead to enhanced memory consolidation. Sure enough, those subjects remembered about 84% of the object locations when they awoke, while a control group remembered just 61%.

It’s not just sweet smells that could boost learning; as the Marquis found with his night-time waltzes, sounds might also be able to trigger recall, provided they do not wake you up in the process. In one study, volunteers found it easier to master a musical game (a little like Guitar Hero) if they heard soft strains of the melody as they slept. Bjorn Rasch at the University of Zurich, Switzerland, meanwhile, found that the same setup helped Swiss German speakers learning Dutch vocabulary, allowing them to remember about 10% more.

Tech upgrade

In the near future, technology may offer further ways of upgrading the brain’s sleep cycles. Memory consolidation is thought to occur during specific, slow, oscillations of electrical activity, so the idea here is to subtly encourage those brain waves without waking the subject. Jan Born, at the University of Tubingen, has been at the forefront of these experiments. In 2004, he found that he could help amplify those signals using transcranial direct current stimulation (tDCS), which passes a small electric current across the skull, successfully improving his subjects’ performance on a verbal memory test.

More recently, he has turned to an even less-invasive form of stimulation, which uses a skullcap of electrodes to measure neural activity, while headphones deliver sounds that are in sync with the brain waves. Born compares the auditory stimulation to the tiny push that you might give a child on a swing, so that it gently enhances neural activity that is already present in the brain. “You deepen the slow wave sleep and make it more intense,” says Born. “It’s a more natural way of getting the system into a rhythm,” he says.

 

(Thinkstock)

If the idea of going to sleep with a cumbersome headset doesn’t appeal, Miriam Reiner at the Technion Institute of Technology in Haifa, Israel may have a more attractive solution. She hopes to use a form of neurofeedback, which allows subjects to control their neural activity while awake. In her setup, an electrode attached to the subject’s head feeds into a simple computer game, in which the subject is advised to drive a car with the power of their thoughts.

When the electrode records the right frequency of brainwaves, normally associated with memory consolidation during sleep, they accelerate; when they don’t, it slows down. It typically takes just a few minutes for the subjects to start revving up the right brainwaves – and the change in mind set is palpable, says Reiner. “I feel kind of relaxed – like when you’re in a garden or walking along beach. It’s just like being in a serene beautiful place.” The idea is to kick-start memory consolidation straight after learning, which then gives the sleeping brain a head-start as it sets about reorganising the day’s events. “You create a seed that then grows during the night,” says Reiner.

Play a tune

To test the impact on learning, her subjects first learned a complex sequence of finger movements – a little like learning to play a tune on the piano – before taking 30 minutes of neurofeedback. The benefits were immediate – straight after the training they were about 10% better than the controls, suggesting the computer game really had begun to stabilise their memories as if they were actually asleep. Importantly, the improvements continued to grow as they were tested throughout the following week, supporting her theory that neurofeedback could help memories to blossom as you sleep.

Needless to say, we will need to see bigger trials with many more subjects before these techniques should be recommended for everyday use. Since the experiments have so far used somewhat artificial tests of learning and memory, it would also be useful to see how they fare on more useful tasks; Reiner is beginning to take a few steps in this direction by testing whether her neurofeedback can help students learn the guitar. Diekelmann also thinks that we need to confirm that these memory hacks don’t have unexpected consequences. “If you enhance one set of memories, maybe you’d impair another set,” she says.

Sounds and melodies can consolidate memory (Thinkstock)

And we shouldn’t shy away from the problems highlighted by fiction like Brave New World and The Simpsons, she says. Although she doesn’t think that these methods could be used for brainwashing people against their will, she thinks we still need to question whether it would be right to start manipulating their children’s memories, for instance, in these ways. “Sleep is a vulnerable state.” But she’s keen to stress that these potential issues shouldn’t deter interest in sleep learning. “It’s very worthwhile. We just need to use it as responsibly as possible.”

Easy tricks

Once those questions have been addressed, there shouldn’t be too many practical hurdles for people who wish to use the techniques for themselves, says Diekelmann. Many of her students and colleagues have already found that sensory cues during sleep can help them swat-up for exams. “It’s very easy to apply,” she says. And you can now buy EEG kits that work with your smartphone, potentially opening the door for games that help you boost memory consolidation. Even the hardware for certain forms of tDCS became commercially available last year, which could lead to kits designed to improve sleep learning.

Further evidence will be needed to show that the commercial kits can provide the benefits seen in the laboratory experiments, but Born is optimistic. “I think it’s just a matter of time before it is used as a cognitive enhancer,” he says.

At the very least, the research could change the way we view this often under-appreciated part of our lives. Sleep tends to be considered an unnecessary down-time that we try to conquer with coffee or Red Bull; we are all driven by the need to squeeze the day for every last drop of productivity. But we may take more time to catch 40 winks if we know that the most profitable part of the day really could involve doing nothing at all.

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* * * *

Sleep's memory role discovered

By James Gallagher Health and science reporter, BBC News

5 June 2014

  

The mechanism by which a good night's sleep improves learning and memory has been discovered by scientists.

The team in China and the US used advanced microscopy to witness new connections between brain cells - synapses - forming during sleep.

Their study, published in the journal Science, showed even intense training could not make up for lost sleep.

Experts said it was an elegant and significant study, which uncovered the mechanisms of memory.

It is well known that sleep plays an important role in memory and learning. But what actually happens inside the brain has been a source of considerable debate.

Researchers at New York University School of Medicine and Peking University Shenzhen Graduate School trained mice in a new skill - walking on top of a rotating rod.

They then looked inside the living brain with a microscope to see what happened when the animals were either sleeping or sleep deprived.

Their study showed that sleeping mice formed significantly more new connections between neurons - they were learning more.

 

A connection between two brain cells

And by disrupting specific phases of sleep, the research group showed deep or slow-wave sleep was necessary for memory formation.

During this stage, the brain was "replaying" the activity from earlier in the day.

Prof Wen-Biao Gan, from New York University, told the BBC: "Finding out sleep promotes new connections between neurons is new, nobody knew this before.

"We thought sleep helped, but it could have been other causes, and we show it really helps to make connections and that in sleep the brain is not quiet, it is replaying what happened during the day and it seems quite important for making the connections."


Analysis

This is just the latest piece of science to highlight the importance of sleep.

A new reason for sleep was discovered last year when experiments showed the brain used sleep to wash away waste toxins built up during a hard day's thinking.

However, there are concerns that people are not getting enough sleep.

As part of the BBC's Day of the Body Clock, Prof Russell Foster argued that society had become "supremely arrogant" in ignoring the importance of sleep, leading to "serious health problems".

These include:

• cancer
• heart disease
• type-2 diabetes
• infections
• obesity

The reward for more sleep, Prof Foster argues, is we would all be "better human beings."

Further tests showed how significant sleep was.

Mice doing up to an hour's training followed by sleep were compared with mice training intensively for three hours but then sleep deprived.

The difference was still stark, with the sleepers performing better and the brain forming more new connections.

Prof Gan added: "One of the implications is for kids studying, if you want to remember something for long periods you need these connections.

"So it is probably better to study and have good sleep rather than keep studying."

Commenting on the findings, Dr Raphaelle Winsky-Sommerer, from the University of Surrey, told the BBC: "This is very impressive, carefully crafted and using a combination of exquisite techniques to identify the underlying mechanisms of memory.

"They provide the cellular mechanism of how sleep contributes to dealing with experiences during the day.

"Basically it tells you sleep promotes new synaptic connections, so preserve your sleep."

From Scientific American, this is an excerpt from a new book by Penelope Lewis, The Secret World of Sleep: The Surprising Science of the Mind at Rest. I'm not convinced based on this short section that there is anything new in the book, but it seems worth sharing nonetheless.

What Is Dreaming and What Does It Tell Us about Memory?

Dreams may play a role in memory incorporation and influence our long-term moods, physiology and creativity

Jul 18, 2014 | By Penelope A. Lewis

Excerpted with permission from The Secret World of Sleep: The Surprising Science of the Mind at Rest, by Penelope A. Lewis. Available from Palgrave Macmillan Trade. Copyright © 2013. (Scientific American and Palgrave Macmillan are part of the Holtzbrinck Publishing Group.)

You are terrified and running along a dark, narrow corridor. Something very evil and scary is chasing you, but you’re not sure why. Your fear is compounded by the fact that your feet won’t do what you want—it feels like they are moving through molasses. The pursuer is gaining, but when it finally catches you, the whole scene vanishes...and you wake up.

Almost by definition, a dream is something you are aware of at some level. It may be fragmentary, disconnected, and illogical, but if you aren’t aware of it during sleep then it isn’t a dream. Many people will protest, “I never remember my dreams!,” but that is a different matter entirely. Failing to remember a dream later on when you’re awake doesn’t mean you weren’t aware of it when it occurred. It just means the experience was never really carved into your memory, has decayed in storage, or isn’t accessible for easy call back.

We all intuitively know what a dream is, but you’ll be surprised to learn there’s no universally accepted definition of dreaming. One fairly safe catch-all is “all perceptions, thoughts, or emotions experienced during sleep.” Because this is very broad, there are also several different ways of rating, ranking, and scoring dreams. For example, one uses an eight-point rating system from 0 (no dream) to 7 (“an extremely long sequence of 5 or more stages”).

Physical Bases of Dreams

But let me backtrack. One aim of neuroscience is to map the brain loci of thoughts and mental experiences. Everything we see, imagine, or think about is linked to neural responses somewhere in the brain. Dreams also have a home. Neural activity in the primary sensory areas of the neocortex produces the impression of sensory perception. This means that neurons firing in the primary visual cortex create the illusion of seeing things, neurons firing in the primary auditory area create the illusion of hearing things, and so forth. If that firing occurs at random, these perceptions can feel like crazy, randomly fragmented hallucinations. It is easy to imagine that the random imagery and sensations created in this way could be woven together to create a complex, multisensory hallucination which we might call a dream.

Do Dreams Serve a Purpose?

In contrast to an activation-synthesis model, which views dreams as epiphenomena—a simple by-product of neural processes in sleep—other scientists have suggested that dreams serve an important function. As usual in psychology, there are lots of different ideas about what this function could be. Sigmund Freud’s suggestion that dreams express forbidden desires is of course the most famous of these, but there are lots of other theories about what dreams might do, many with more empirical support than the Freudian view. For example, the threat simulation hypothesis suggests that dreams may provide a sort of virtual reality simulation in which we can rehearse threatening situations, even if we don’t remember the dreams. Presumably, this rehearsal would lead to better real-life responses, so the rehearsal is adaptive. Evidence supporting this comes from the large proportion of dreams which include a threatening situation (more than 70 percent in some studies) and the fact that this percentage is much higher than the incidence of threats in the dreamer’s actual daytime life. Furthermore, studies of children in two different areas of Palestine show that those who live in a more threatening environment also have a much higher incidence of threat in their dreams. Reactions to these threats are almost always relevant and sensible, so the rehearsal (if that’s what it is) clearly involves plausible solutions, again suggesting that they provide a kind of valid simulation of potential real-life scenarios.

Another suggestion is that dreams influence the way you feel the next day, either in terms of mood or more basic bodily states. Forcing people to remember the nastier dreams from their REM sleep definitely puts them in a foul mood, and nightmares (defined as very negative dreams which can wake you up) may even lead to ongoing mood problems. On the other hand, there is also evidence that dreams could help to regulate long-term mood. For instance, a study of dreams in divorced women showed that those who dreamed about their ex-husbands more often were better adapted to the divorce. Amazingly enough, dreams also seem able to influence physiological state: One study showed that people who were deprived of water before they slept, but then drank in their dreams, felt less thirsty when they woke up.

The content of dreams can be influenced in lots of different ways. For instance, recent work has shown that sleepers tend to initiate pleasant dreams if nice smells are wafted at them in REM sleep, and they have negative or unhappy dreams if stinky, unpleasant smells are sent their way. Some people can achieve lucid dreaming, in which they control the sequence of events in their dream, and evidence suggests that these techniques can be learned by intensive practice and training. All of this is highly tantalizing, of course, because (though it tells us nothing at all about the original evolved purpose of dreams) it suggests we might not only be able to set ourselves up for pleasant experiences while we sleep, but we might also eventually be able to use these techniques to treat mood disorders, phobias, and other psychological problems. We already know that hypnotic suggestion can cause people to incorporate snakes, spiders, or other things about which they have phobias into their dreams, and—when combined with more benign forms of these menacing objects—such incorporation helps to remove the phobia. Hypnotic suggestion can also make dreams more pleasant, and mental imagery practiced during the day can be used to modify (and often nullify) persistent nightmares.

There is little evidence that people actually learn during their dreams. The fact that they can learn during sleep is a different matter, but dreams themselves don’t appear to be a good forum for imprinting new information into the hippocampus (after all, we don’t even remember our dreams most of the time). Studies of language learning illustrate this well. Although learning efficiency is predicted by an increase in the percentage of the night that is spent in REM, the dreams which are experienced during this extra REM don’t have much to do with language. If they relate to it at all they are most often about the frustration of not being able to understand something and not about the mechanics of how to construct or decode a sentence.

Memories in Dreams

What’s the most recent dream you can remember? Was anyone you know in it? Did it happen in a place you know well? Were you doing something familiar? Most dreams incorporate fragments of experiences from our waking lives. It’s common to dream about disconnected snippets like a particular person, place, or activity. But do dreams ever replay complete memories—for instance, the last time you saw your mother, including the place, activities, and people? Memories like this are called episodic because they represent whole episodes instead of just fragments; studies the secret world of sleep of dreaming show that these types of memories are sometimes replayed in sleep, but it is quite rare (around 2 percent of dreams contain such memories, according to one study). Most of our dreams just recombine fragments of waking life. These fragments are relatively familiar and reflect the interests and concerns of the dreamer. This means cyclists dream about cycling, teachers dream about teaching, and bankers dream about money.

Some researchers have capitalized upon dream reports to gain insight into the process by which memories are immediately incorporated (i.e., in the first night after they were initially experienced). Freud famously referred to this as “day-residues.” One study showed day residues appear in 65 to 70 percent of single dream reports. On the other hand, a more recently described phenomenon called the dream-lag effect refers to the extraordinary observation that, after its initial appearance as a day residue, the likelihood that a specific memory will be incorporated into dreams decreases steadily across the next few nights after the memory was formed, then increases again across the following few nights (Fig. 20).

Thus, it is very common for memories to be incorporated into dreams on the first night after they were initially experienced (if I have a car crash today, I’m likely to dream about it tonight). The likelihood of such incorporation decreases gradually across the next few nights, with few memories incorporated into dreams three to five days after they occurred. Extraordinarily, however, the probability that a memory will be incorporated into a dream increases again on nights six and seven after it was initially experienced. What is going on here? Why are memories less likely to be incorporated into dreams three to five days after they originally occurred than six to seven days afterward? One possibility relates to the need for consolidation. Memories may be inaccessible at this stage because they are being processed in some way which takes them temporarily “offline.” Notably, this effect is only true for people who report vivid dreams, and it also appears to only be true of REM dreams. As with most research, the dream-lag effect raises more questions than it answers.

Why Do We Have Different Kinds of Dreams at Different Stages of the Night?

Dreams aren’t all the same. Everyone is aware of the difference between good and bad dreams, but we don’t tend to notice that some dreams are more logical and structured while others are more bizarre. Some dreams are so highly realistic that it is difficult to convince ourselves they aren’t real, while others are fuzzy and indistinct. Some dreams are fragmented, jumping rapidly from one topic to another, while others move forward in a more coherent story. Recent analyses have suggested that these differences are far from random; instead they may be driven by the physiology of various brain states and the extent to which structures like the hippocampus and neocortex are in communication during different sleep stages.

Dreams occur in all stages of sleep, but they seem to become increasingly fragmented as the night progresses. In general, they appear to be constructed out of a mishmash of prior experience. As mentioned above, dreams contain disconnected memory fragments: places we’ve been, faces we’ve seen, situations that are partly familiar. These fragments can either be pasted together in a semi-random mess or organized in a structured and realistic way. The dreams that occur in non-REM sleep tend to be shorter but more cohesive than REM dreams, and often they relate to things that just happened the day before. REM dreams that occur early in the night often also reflect recent waking experiences, but they are more fragmented than their non-REM counterparts. Conversely, REM dreams that occur late in the night are typically much more bizarre and disjointed.

Simply thinking about where these memory fragments are coming from and how they are connected together may provide an explanation for the difference between early and late-night dreams. The various elements of an episode are thought to be stored in the neocortex, but they are not necessarily linked together to form a complete representation. For example, if your memory of having dinner last night involves memories about a specific place, specific sounds, specific actions, and maybe even memories about other people who were there, each of these bits of information is represented by a different area of the neocortex. Even though they combine together to make up a complete memory, these various neocortical areas may not be directly interlinked. Instead, the hippocampus keeps track of such connections and forms the appropriate linkages, at least while the memory is relatively fresh. However, communication between the neocortex and hippocampus is disrupted during sleep, so this process is also disrupted. During REM sleep, both the hippocampus and those parts of the neocortex which are involved in a current dream are strongly active—but they don’t appear to be in communication. Instead, responses in the neocortex occur independently, without hippocampal input, so they must relate to memory fragments rather than linked multisensory representations. Essentially, when memories which have been stored in the neocortex are accessed or activated during REM, they remain fragmentary instead of drawing in other aspects of the same memory to form a complete episodic replay. These fragments aren’t linked together in the way they might be if you thought of the same place while you were awake (or indeed in non-REM sleep). For instance, cortical representations of both someone who was present for your dinner last night and of the place where it was held may be triggered, but these will not necessarily be linked together, and they may not be linked to the idea of dinner or eating at all. Instead, seemingly unrelated characters and events may be activated in conjunction with the memory of this place. One possible driver for this is the stress hormone cortisol, which increases steadily across the night. High cortisol concentrations can block communication between the hippocampus and neocortex, and since concentrations are much higher early in the morning, this could provide a physiological reason for the disjointed properties of late-night (early morning) dreams.

Irrespective of how it happens, it is clear that dreams not only replay memory fragments but also create brand-new, highly creative mixtures of memories and knowledge. This process has led to the creation of many works of literature, art, and science, such as Mary Shelley’s Frankenstein, the molecular formula of benzene, and the invention of the light bulb. An especially good demonstration of this somnolent creativity comes from a study of 35 professional musicians who not only heard more music in their dreams than your normal man-on-the-street but also reported that much of this (28 percent) was music they had never heard in waking life. They had created new music in their dreams!

Although we don’t quite understand how dreams achieve this type of innovative recombination of material, it seems clear that the sleeping brain is somehow freed of constraints and can thus create whole sequences of free associations. This is not only useful for creativity, it is also thought to facilitate insight and problem solving. It may even be critical for the integration of newly acquired memories with more remote ones (see chapter 8). In fact, this facilitated lateral thinking could, in itself, be the true purpose of dreams. It is certainly valuable enough to have evolved through natural selection.

This is wonderful to see, finally - even if it is less than honest about the existing evidence for lifestyle interventions to affect depression levels. Drugs for depression are not treating the depression, they are creating an effect of feeling better through making people, for lack of a better word, stoned.

I have seen, firsthand, a client start walking 3-5 days a week (exercise and nature/environment), begin practicing contemplative prayer (meditation), spend more time with her dog (animal therapy - goes on the walk, then fetch in the park), and start spending less time at home by joining church activities and spending time with her kids and granddaughter (socializing). These synergy of these simple changes have been more effective than years of medications and various attempts at therapy.

Lifestyle medicine for depression

Jerome Sarris, Adrienne O'Neil, Carolyn E Coulson, Isaac Schweitzer, and Michael Berk
Author Affiliations | For all author emails, please log on.

Published: 10 April 2014

Abstract (provisional)

The prevalence of depression appears to have increased over the past three decades. While this may be an artefact of diagnostic practices, it is likely that there are factors about modernity that are contributing to this rise. There is now compelling evidence that a range of lifestyle factors are involved in the pathogenesis of depression. Many of these factors can potentially be modified, yet they receive little consideration in the contemporary treatment of depression, where medication and psychological intervention remain the first line treatments. "Lifestyle Medicine" provides a nexus between public health promotion and clinical treatments, involving the application of environmental, behavioural, and psychological principles to enhance physical and mental wellbeing. This may also provide opportunities for general health promotion and potential prevention of depression. In this paper we provide a narrative discussion of the major components of Lifestyle Medicine, consisting of the evidence-based adoption of physical activity or exercise, dietary modification, adequate relaxation/sleep and social interaction, use of mindfulness-based meditation techniques, and the reduction of recreational substances such as nicotine, drugs, and alcohol. We also discuss other potential lifestyle factors that have a more nascent evidence base, such as environmental issues (e.g. urbanisation, and exposure to air, water, noise, and chemical pollution), and the increasing human interface with technology. Clinical considerations are also outlined. While data supports that some of these individual elements are modifiers of overall mental health, and in many cases depression, rigorous research needs to address the long-term application of Lifestyle Medicine for depression prevention and management. Critically, studies exploring lifestyle modification involving multiple lifestyle elements are needed. While the judicious use of medication and psychological techniques are still advocated, due to the complexity of human illness/wellbeing, the emerging evidence encourages a more integrative approach for depression, and an acknowledgment that lifestyle modification should be a routine part of treatment and preventative efforts.

The complete article is available as a provisional PDF. The fully formatted PDF and HTML versions are in production.

Full Citation:
Sarris, J, O'Neil, A, Coulson, CE, Schweitzer, I, and Berk, M. (2014, Apr 10). Lifestyle medicine for depression. BMC Psychiatry, 14:107 doi:10.1186/1471-244X-14-107

Introduction

While modernity has provided multiple technological and medical advances including increased life-expectancy, it has come at a cost, in that a range of lifestyle issues are now negatively affecting our mental health [1]. As Hidaka [1] and Walsh [2] comment, in Western society people are increasingly becoming more sedentary and eating a poorer diet than previous generations. This, in combination with sleep/wake cycle pressures, substance misuse, and psychosocial factors such as more competition and time pressure, social isolation and less intimate engagement with the family unit, may exert a cost on mental health. Further, the combination of stress, fatigue, inactivity, and sleep deficiency in people who are “timepoor”, may advance obesity, and this in turn may promote a sedentary life with potential for resultant depression.

Due to the afore-mentioned challenges of modern urbanity, there is now the need to consider a “Lifestyle Medicine” approach for the potential prevention, promotion and management of depression. While medication and psychological interventions are first-line treatments for depression, Lifestyle Medicine offers a potentially safe and low-cost option for augmenting the management of the condition. While the evidence base remains patchy, many lifestyle or environmental factors are mutable and can provide the basis of practical interventions for the management of depression (summarised in Table 1). Lifestyle Medicine involves the application of environmental, behavioural, and psychological principles to enhance physical and mental wellbeing, adding a therapeutic and potentially preventative approach to illness [3]. This may involve modification of: diet; physical activity and exercise; relaxation and sleep-wake cycles; recreation and work-rest balance; and minimisation/avoidance of smoking, alcohol or illicit substances, in addition to the use of mindfulness-based meditation techniques [2]. Although the evidence base remains in its infancy, environmental issues are also considerations, such as reducing exposure to pollution (air, water, noise, and chemicals) and increasing time spent in nature, and are areas of current investigation. Activity scheduling such as encouraging engagement in meaningful activities and adequate social contact [1] is additionally of value. Further, Lifestyle Medicine may involve the application of clinical psychological techniques, insofar as motivational and behavioural factors are intrinsic to people trying to embrace lifestyle changes [3].

Table 1 Lifestyle Medicine for Depression

Lifestyle element................Evidence level....................Cost
Diet............................................CS, LO.................Moderate expense 
PA/Exercise..........................CS*, LO*, CTs ...............Inexpensive 
Recreation.................................OB, CTs..................Variable expense 
Relaxation/Meditation.................CTs..........................Inexpensive
Sleep......................................CS, LO, CTs...................No expense 
Environment..........................CS, LO, CTs...........Potentially not adjustable 
Socialization..............................CS, LO.........................No expense 
Animal/Pet therapy....................CS, CTs.....................Moderate expense 
Vices (smoking/alcohol)............CS, LO.................Potential to save money

CS = Cross-sectional, OB = Observational Study, LO = Longitudinal, CTs - Clinical Trials, NAT = Nature-Assisted Therapy, PA = Physical Activity. 
*Data assessing the relationship between exercise and depression has revealed mixed outcomes.

Comments on each Lifestyle Element:

Diet - Relationship found between dietary quality and depression; RCTs now required to validate
PA/Exercise - Strong evidence of efficacy for improving mood
Recreation - No studies exploring recreational activities for depression (aside from music therapy)
Relaxation & Meditation - Evidence supports relaxation techniques (especially with a mindfulness component) in improving mood
Sleep - Strong causal link between sleep amount and quality, and depression risk
Environment - Association between reduction of pollution and mood; CTs showing NAT improves mood
Socialization - Strong association between social support/networks and mental health
Animal/Pet therapy - Studies support the psychological benefits of animals and pets
Vices (smoking, alcohol) - Association between smoking and alcohol, and depressed mood

While lifestyle modification has been recognised by practitioners for centuries as a means by which to improve health outcomes, the field of “Lifestyle Medicine,” particularly in the context of mental health, is a relatively new field. While papers have discussed its broader application on health and in particular prevention of chronic disease and cardiovascular/metabolic conditions, little attention has been given to its application for mental health, and in particular depression, which is predicted to be the predominant cause of disability in the developed world [4], and is being argued as one of the prevalent noncommunicable disorders [5]. Some studies show that patients with sub-threshold depression rate lifestyle or psychosocial approaches as strategies that are most helpful in improving their mood [6], while patients with clinical depression have rated exercise as the most effective intervention [7].

There is a heuristic theoretical framework explaining why the modern lifestyle may be impacting mental health. Obesity [8], poor diet [9], poor/decreased sleep [10], exposure to chemicals and pollutants [11], and high stress levels [12], may potentially disrupt the hypothalamic pituitary adrenal axis, increase cortisol and increase low-grade systemic inflammation and oxidative stress. Both neuroendocrine disruption and inflammation have been linked to the aetiology of depression [13,14]. Specifically, increased levels of proinflammatory cytokines, interferon gamma and neopterin, reactive oxygen and nitrogen species and damage by oxidative and nitrosative stress, in combination with lowered levels of antioxidants, may potentially damage mitochondria and mitochondrial DNA; this may result in neurodegeneration and reduced neurogenesis [14].

This opinion paper aims to provide a context for Lifestyle Medicine by providing an overview of the lifestyle factors that are linked with depression risk before exploring the evidence and clinical application of modifying these elements. The paper firstly explores data for which there is sound evidentiary support (diet, physical activity and exercise, mindfulness meditation, management of recreational substance misuse, sleep, and social interaction), and then touches on lifestyle and environmental elements that have nascent data and are subject to confirmatory investigation (greenspace and pollutant exposure, hobbies and relaxation, and animal/pet therapy).

Read the whole article.

Sleep Science with Penny Lewis (Brain Science Podcast 107)

 

In this recent episode of the Brain Science Podcast, Dr. Ginger Campbell speaks with Dr. Penny Lewis about her new book, The Secret World of Sleep: The Surprising Science of the Mind at Rest (2013).

Sleep Science with Penny Lewis (BSP 107)

March 18, 2014 / Ginger Campbell, MD


Penny Lewis

In The Secret World of Sleep: The Surprising Science of the Mind at Rest Dr. Penelope A. Lewis provides a highly readable account of the fascinating world of sleep research. Fascinating research is being carried out with animals as varied as fruit flies and rats, as well as with humans. I was surprised to learn that most people actually find it fairly easy to fall asleep in an fMRI scanner.

I have just posted an interview with Dr. Lewis (BSP 107) that includes a discussion of the role of sleep in memory as well as interesting findings about how synapses in the brain actually change during sleep. We still don't know exactly what sleep (and dreaming) are essential, but research in this field is growing. Dr. Lewis is excited about emerging research that suggests improving slow wave sleep may significantly improve learning and memory.

Listen:

Ginger Campbell, MD
BSP 107 Sleep Science with Penny Lewis
69:55

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References:

The Secret World of Sleep: The Surprising Science of the Mind at Rest by Penelope A. Lewis
Dreamland: Adventures in the Strange Science of Sleep by David K. Randall (audible link)
Dreaming: A Very Short Introduction by J. Allan Hobson

• Xie L, Kang H, Xu Q, et.al. 2013. Sleep Drives Metabolite Clearance from the Adult Brain. Science 342: 373-377. DOI: 10.1126/science.1241224 
• G. Tononi and C. Cirelli, “Sleep and Synaptic Homeostatis: A Hypothesis,” Brain Res. Bull. 62 (2003): 143-150. 
• Bushey D, Tononi G, Cirelli C. Sleep and synaptic homeostasis: structural evidence in Drosophila. Science, 332(6037):1576-1581, 2011. [DOI: 10.1126/science.1202839]. 

See episode transcript for additional links and references.

Announcements:

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4 Ways to Make Your Brain Work Better - Chris Mooney at Mother Jones

Maria Konnikova is the author of Mastermind: How to Think Like Sherlock Holmes (2013) and her writing has appeared in The New Yorker, The Atlantic, The New York Times, Slate, The Paris Review, The Wall Street Journal, The New Republic, The Boston Globe, The Observer, Scientific American MIND, and Scientific American, among numerous other publications.

She is the guest for this episode of the Inquiring Minds Podcast with Chris Mooney and Indre Viskontas (via Mother Jones).

4 Ways to Make Your Brain Work Better

The New Yorker's Maria Konnikova explains the science behind why we need to sleep more, waste less time on the internet, and stop multitasking.

—By Chris Mooney
Friday, Feb. 7, 2014

michaeljung/Shutterstock

You're a busy person. Keeping up with your job, plus your life, has you constantly racing. It doesn't help that when working, you're distracted not only by your mobile devices, but also by your computer. You average 10 tabs open in your browser at any one time, and you compulsively click amongst them. One's your email, which never stops flowing in. At the end of the day, you sleep less than you know you should, but as you tell yourself, there's just never enough time.

If this is how you live, then Maria Konnikova has a simple message for you: Pause, step back, and recognize the actual costs of your habits. A psychology Ph.D. and popular writer for The New Yorker, Konnikova circles back, again and again, to a common theme: how we thwart our own happiness, and even sometimes harm our brains, in our quest for a simply unattainable level of productivity. "The way that we've evolved, the way our minds work, the way we work at our most optimal selves, is really not the way we have to operate today," Konnikova explained on this week's Inquiring Minds podcast. "I feel like I'm fighting a losing battle, but I hope that if there are enough voices out there, someone will finally hear that, 'Hey, this attempt at hyperproductivity is making us much less productive.'"



Based on Konnikova's writings, here are four ways that we can change our lifestyles so as to also improve our brains and how they function:

Maria Konnikova (Margaret Singer and Max Freedman.)

Sleep more. Science still has a lot to learn about how sleep deprivation affects us. But the research is starting to look pretty grave, especially in light of new studies (Konnikova has written about them here) suggesting that a crucial function of sleep is to purge the brain of biochemical waste products that are the result of conscious brain activity. This means that not sleeping enough could be contributing to the buildup of harmful proteins like beta-amyloids, which could in turn predispose us to neurodegenerative diseases like Alzheimer's.

So how do you fix your bad sleep habits? Not easily: It requires nothing less than a major lifestyle change. "You can't just think that, 'Well, I'm not ever going to get enough sleep, but on the weekends I'll sleep in and I'll be okay,'" says Konnikova. "It doesn't work that way." Recovering from one night with too little sleep is easy, but recovering from chronic sleep deprivation requires nothing less than chronic sleep, er, restoration.

How much sleep? People vary, but the National Sleep Foundation says adults need seven to nine hours per night.

Stop being an internet junkie. You've probably wondered what the internet is doing to your brain. And especially if you can actually remember the era before the internet's existence, you've probably noticed how the widespread availability of things like email has changed you. It might even have made you into a kind of addict, habituated to constant switching from task, to task, to task: Facebooking, tweeting, emailing, reading…and whatever else arises.

Using the internet in this frenetic way is just bad for us, says Konnikova. "Where the problem comes in is when we start to do it all simultaneously, when we start to multitask and really very quickly switch our attention from an article, to a tweet, to a Facebook post, and we're just all over the place," she explains. "Because that's very cognitively demanding, and that makes us less able to engage with what we're reading and what we're doing, and it also just makes us exhausted and worse at the tasks that we do have to accomplish."

So how do you use the internet better? Set rules for yourself, advises Konnikova: a half-hour of email, followed by a half-hour of Twitter, and so on. You can force yourself to have this kind of discipline, or, you can use a tool to help you with it. To get writing done, Konnikova herself uses an app that blocks you from using the internet for a set period of time, forcing you to work and focus.

ollyy/Shutterstock

Put a check on your multitasking. Our problems with using the internet productively are just a subset of a broader problem: multitasking. We have a culture that encourages it, even though it forces us to use our brains suboptimally (at best). "How many job descriptions have you seen where it says, 'Good at multitasking,' or, 'We need someone who's a good multitasker'?" asks Konnikova. "It's just this mindset that this is a very very good thing."

It isn't. Konnikova wrote recently about how open offices, which are widespread, distract us and leave us stressed out and less productive. It's because they thwart our ability to focus; the space itself is structured for multitasking and a lot of distractions and interruptions. And yet, being able to focus is closely related to happiness. "There's really interesting work showing that when you're focused on what you're doing, you become happier, even if what you're doing is incredibly boring," says Konnikova. "And even if you're doing something very fun, it will be less fun for you if you're not paying attention to it."

So how do you stop multitasking? First, try to make a habit of noticing how much you do it, Konnikova says. And instead, as with the internet, try to discipline yourself, so that you do only one thing at a time.

Practice mindfulness. But there's also a broader solution. It's called mindfulness, and it's outlined in detail in Konnikova's bestselling book Mastermind: How to Think Like Sherlock Holmes.

The most striking thing about Arthur Conan Doyle's character is his supreme attentiveness, his ability to perceive the details that everybody else misses. And yet Konnikova notes that Holmes solves his crimes, in significant part, through inactivity. "He often just sits in his armchair and does a lot of nothing," says Konnikova. "He has his eyes closed, or is playing the violin, but often just does nothing at all." It is this rest, this calm, that enables Holmes to be such a hyperfocused and attentive detective when he's actually on the case.

So how do you think like Sherlock Holmes? Konnikova says you need to mimic the detective in his armchair: Take 10 to 15 minutes each day, set them aside, and designate them as your time for not doing anything. "All you really need to do, for instance, is sit in your chair in your office, and close your eyes for 10 minutes, and focus on your breath, just on the ins and outs of your breath," says Konnikova. "And that's it."

Research shows that such mindfulness exercises help improve your attention, your focus. "It's like a muscle, it starts growing stronger, bigger," says Konnikova. "You start being able to focus much more easily, and for longer stretches of time."

But, you might be thinking, making these changes would be so hard! Yet that very way of thinking is itself the problem. "It's this mindset that this is the way we need to operate, but it's really counterproductive," says Konnikova. "And what we don't realize is that it's making us less creative, it's making us unhappy, and it's not using humans to the best of their capacity on both a mental and physical level."

You can listen to the full interview with Maria Konnikova here:



This episode of Inquiring Minds, a podcast hosted by neuroscientist and musician Indre Viskontas and best-selling author Chris Mooney, also features a report by Climate Desk's Tim McDonnell on how climate change is threatening winter sports, and a special guest appearance by science communicator Dr. Kiki Sanford, who helps us break down what happened in the widely watched Bill Nye vs. Ken Ham creationism debate earlier this week.

To catch future shows right when they are released, subscribe to Inquiring Minds via iTunes or RSS. We are also available on Stitcher and on Swell. You can follow the show on Twitter at @inquiringshow and like us on Facebook. Inquiring Minds was also recently singled out as one of the "Best of 2013" shows on iTunes—you can learn more here.

From the open-access Frontiers in Psychology: Consciousness Research, researchers from the Max Planck Institute of Psychiatry in Munich looked at the reflective (volitional) aspects of consciousness across three different states - waking, dreaming, lucid dreaming (becoming conscious of the dream while in the dream).

From the abstract:

Overall, experienced volition was comparable for lucid dreaming and wakefulness, and rated significantly higher for both states compared to non-lucid dreaming. However, three subscales showed specific differences across states of consciousness: planning ability was most pronounced during wakefulness, intention enactment most pronounced during lucid dreaming, and self-determination most pronounced during both wakefulness and lucid dreaming. Our data confirm the multifaceted nature of consciousness: different higher-order aspects of consciousness are differentially expressed across different conscious states.

In essence, lucid dreaming is clearly a higher order state of consciousness. Nice research that will hopefully be replicated by others so that lucid dreaming becomes a more widely accepted phenomena.


Full Citation: 
Dresler M, Eibl L, Fischer CFJ, Wehrle R, Spoormaker VI, Steiger A, Czisch M and Pawlowski M. (2014, Jan 2). Volitional components of consciousness vary across wakefulness, dreaming, and lucid dreaming. Frontiers in Psychology: Consciousness Research; 4:987. doi: 10.3389/fpsyg.2013.00987

Volitional components of consciousness vary across wakefulness, dreaming, and lucid dreaming

Martin Dresler, Leandra Eibl, Christian F. J. Fischer, Renate Wehrle, Victor I. Spoormaker, Axel Steiger, Michael Czisch, and Marcel Pawlowski

Max Planck Institute of Psychiatry, Munich, Germany

Abstract 

Consciousness is a multifaceted concept; its different aspects vary across species, vigilance states, or health conditions. While basal aspects of consciousness like perceptions and emotions are present in many states and species, higher-order aspects like reflective or volitional capabilities seem to be most pronounced in awake humans. Here we assess the experience of volition across different states of consciousness: 10 frequent lucid dreamers rated different aspects of volition according to the Volitional Components Questionnaire for phases of normal dreaming, lucid dreaming, and wakefulness. Overall, experienced volition was comparable for lucid dreaming and wakefulness, and rated significantly higher for both states compared to non-lucid dreaming. However, three subscales showed specific differences across states of consciousness: planning ability was most pronounced during wakefulness, intention enactment most pronounced during lucid dreaming, and self-determination most pronounced during both wakefulness and lucid dreaming. Our data confirm the multifaceted nature of consciousness: different higher-order aspects of consciousness are differentially expressed across different conscious states.

Introduction

The ability to engage in volitional behavior has traditionally been closely associated with human consciousness: to freely act implies to make conscious decisions (Dijksterhuis and Aarts, 2010). However, consciousness is not an all-or-nothing phenomenon; its multiple facets differ across species, vigilance states, or health conditions. A striking variation in consciousness is experienced every day during the sleep–wake cycle: during wakefulness, human subjects are normally alert, aware of external and internal stimuli, able to reflect on their perceptions, emotions and thoughts, and capable to volitionally act according to their intentions. While most of these properties of waking consciousness fade during the process of falling asleep, many basal features of consciousness reappear during dreaming. Dream mentation may occur in all sleep stages, but is most intense and vivid during rapid eye movement (REM) sleep (Hobson et al., 2000). The dreamer perceives and interacts with a hallucinated dream environment and often experiences strong emotions (Hobson and Pace-Schott, 2002). However, typical dreaming is deficient of many higher-order aspects of consciousness: the dreaming subject experiences highly impoverished self-reflective capabilities and therefore does not recognize that he is dreaming. Instead of volitionally and systematically acting according to his intentions, the dreamer is a rather passive subject in the chaotic flow of the dream narrative. In contrast, the rare state of lucid dreaming is characterized by full-blown consciousness including all higher-order aspects: the dreamer regains metacognitive abilities and memory, becomes fully aware of his current state of consciousness, and experiences volition and fully realized agency (Metzinger, 2003; Windt and Metzinger, 2007). As phrased by Van Eeden (1913), who coined the term lucid dreaming: “the sleeper remembers his day-life and his own condition, reaches a state of perfect awareness, and is able to direct his attention, and to attempt different acts of free volition.”

On a closer look, however, the situation is less clear: on the one hand, during alert wakefulness, the experience of volitional capabilities may be strikingly impaired as seen, e.g., in pathological cases such as delusions of alien control in schizophrenic patients (Lafargue and Franck, 2009) or in alien hand syndrome (Biran and Chatterjee, 2004). On the other hand, during altered states of consciousness such as hypnosis (Oakley and Halligan, 2013) or even non-lucid REM sleep (Takahara et al., 2006), volitional behavior can be observed. Moreover, lucid dreaming is not an all-or-nothing phenomenon, but might occur in different degrees from pre-lucid reflections to full-blown lucid control dreams (Tyson et al., 1984; Barrett, 1992; Kahan and LaBerge, 1994). Descriptions of higher-order aspects of consciousness in lucid dreaming, including volitional capacities, rely mainly on anecdotal evidence, but have rarely been studied systematically. Two recent exceptions are the Metacognitive, Affective, Cognitive Experience questionnaire (MACE; Kahan and Sullivan, 2012) and the Lucidity and Consciousness in Dreams scale (LuCiD; Voss et al., 2013) which have been used to assess metacognition during different states of consciousness including lucid dreaming.

Here, we assessed different aspects of volition during normal dreaming, lucid dreaming, and wakefulness with an adapted version of the Volitional Components Questionnaire (VCQ; Kuhl and Fuhrmann, 1998) in lucid dreamers. We hypothesized that experienced volition would be generally higher in both wakefulness and lucid dreaming compared to non-lucid dreaming. We exploratively tested if the subscales of the VCQ would differentially vary between the three states of consciousness.

Materials and Methods

Ten healthy subjects (mean age 28.1 ± 9.8 years, age range 19–47 years, five female) recruited at the University of Munich or from a volunteer database of the Max Planck Institute of Psychiatry participated in this study. They all were experienced lucid dreamers with a reported mean frequency of 1.9 ± 0.7 lucid dreams per week. Lucid dreaming ability was verified in five of the subjects in a sleep laboratory with full polysomnographic recordings, exploiting the classical eye signaling technique (LaBerge et al., 1981). For the other five subjects, lucid dreaming ability was assessed by self-report.

To measure volition in different states of consciousness, we adapted the German short version of the VCQ (Selbststeuerungs-Inventar, SSI-K3; Kuhl and Alsleben, 2012). The VCQ is an instrument to measure different aspects of volitional competence; it specifically aims at assessing the subjective experience of volitional components supporting central coordination of goal-maintenance and self-maintenance (Kuhl and Fuhrmann, 1998). The short form includes 13 subscales consisting of four items each. The test subjects have to rate the extent to which the item applies to themselves on a four-point Likert scale from 1 (not at all) to 4 (wholly). The validity of both the long and short versions has been repeatedly demonstrated (Forstmeier and Rüddel, 2008). Since several of the 13 subscales are not meaningfully applicable to the dreaming state, as they, e.g., ask to evaluate time frames of several weeks, we chose to restrict the study to six subscales: self-determination, planning ability, intention enactment, powers of concentration, self-access, and integration. As a measure for the general experience of volitional capacity, an overall score consisting of the mean of all six subscales was calculated. Where necessary, questions were adapted to be applicable to the dreaming state, e.g., the integration subfactor item “On many days I feel the opposite of what I felt before” was changed to “I often feel the opposite of what I felt before.” The sequential order of questions was adopted from the original questionnaire.

Subjects were asked to complete the questionnaire at least once for each of the three states of consciousness: in the morning after awakening from a non-lucid dream, in the morning after awakening from a lucid dream, and after a normal day of wakefulness, i.e., before going to bed in the evening. Specifically, subjects were instructed to rate their general experience during the respective state, using the preceding dream or day as an anchor or reminder thereof. For those individuals who completed the questionnaire more than once for one of the three states of consciousness, we used the mean score of the given state for further analysis. For wakefulness, four subjects contributed multiple questionnaires adding up to a total of 15; for non-lucid dreaming, five subjects contributed multiple questionnaires adding up to a total of 20; for lucid dreaming, four subjects contributed multiple questionnaires adding up to a total of 14.

For statistical analysis of the VCQ overall score, we performed a repeated measures ANOVA with the three factor levels non-lucid dreaming, lucid dreaming, and wakefulness. For specific comparisons between the three states of consciousness, we performed post hoc two-sided paired t-tests. For statistical analysis of the six subscales, we first performed a repeated measures MANOVA with the three factor levels non-lucid dreaming, lucid dreaming, and wakefulness. For further analysis of the subscales that revealed significant results in the following ANOVAs, we subsequently performed two-sided paired t-tests to analyze specific differences between the states of consciousness. All significance levels were set at p = 0.05.

Results

The ANOVA for the VCQ overall score revealed a significant effect of the state of consciousness (F2,18 = 4.4, p = 0.027, η2 = 0.33). Subsequent t-tests demonstrated that both wakefulness (t9 = 2.7, p = 0.026, r = 0.66) and lucid dreaming (t9 = 2.3, p = 0.044, r = 0.61) differed from non-lucid dreaming, however not from each other (t = 0.5, p = 0.618, r = 0.17). Hence, volition was strongly experienced during wakefulness and lucid dreaming, but considerably less so during non-lucid dreaming. For comparisons of the overall results, see Table 1.

TABLE 1

TABLE 1. Experienced volition during wakefulness, lucid dreaming and non-lucid dreaming according to theVolitional Components Questionnaire (VCQ) overall and subscale results.

The MANOVA for the subscales of the VCQ revealed a significant effect of the state of consciousness (F12,26 = 8.9, p < 0.001, η2 = 0.80), which turned out to be significant for the subscales self-determination (F2,18 = 15.4, p < 0.001, η2 = 0.63), planning ability (F2,18 = 31.2, p < 0.001, η2 = 0.78), and intention enactment (F2,18 = 7.3, p = 0.007, η2 = 0.45), but not for powers of concentration (F2,18 = 0.1, p = 0.942, η2 = 0.01), self-access (F2,18 = 0.6, p = 0.573, η2 = 0.06), or integration (F2,18 = 0.7, p = 0.503, η2 = 0.07). Subsequent t-tests demonstrated that self-determination was significantly more pronounced during both wakefulness (t9 = 5.6, p < 0.001, r = 0.88) and lucid dreaming (t9 = 5.2, p < 0.001, r = 0.87) compared to non-lucid dreaming, however did not differ between the two former states of consciousness (t9 = 0.9, p = 0.461, r = 0.28). Planning ability was most pronounced during wakefulness compared to both lucid (t9 = 6.5, p < 0.001, r = 0.91) and non-lucid dreaming (t9 = 5.7, p < 0.001, r = 0.88), but did not differ between the latter two states (t9 = 0.8, p = 0.407, r = 0.25). Intention enactment turned out to be most pronounced during lucid dreaming compared to both wakefulness (t9 = 3.9, p = 0.004, r = 0.79) and non-lucid dreaming (t9 = 3.2, p = 0.011, r = 0.73), while the latter two states did not differ from each other (t9 = 0.2, p = 0.862, r = 0.06). For subscale comparisons, see Table 1.

Discussion

Comparing the experience of volition as assessed by the VCQ during three different states of consciousness, we found volition to be generally most pronounced during both wakefulness and lucid dreaming as compared to non-lucid dreaming. A more differential picture appeared when the subscales of the VCQ were analyzed separately.

For both lucid dreaming and wakefulness, self-determination was rated higher than for non-lucid dreaming. This subscale is probably the most prototypical volitional component, asking to what degree the subject experiences being able to act freely according to his will. The fact that the result of this subscale is in line with the overall score confirms the hypothesis that volition is generally more pronounced during both wakefulness and lucid dreaming compared to non-lucid dreaming.

For wakefulness, planning ability was rated higher than for both lucid and non-lucid dreaming. This subscale asks for how well organized the subject pursues his plans and intentions. The fact that this subfactor is most pronounced during wakefulness compared to both dreaming states might be interpreted as a sign for a more spontaneous execution of intentions during dreaming.

For lucid dreaming, intention enactment was rated higher than for both wakefulness and non-lucid dreaming. This factor asks for how promptly and determined intentions are executed. On first sight, this seems to be a surprising finding, demonstrating that a component of volition is more strongly experienced during a state of sleep than during wakefulness. However, on second sight a strong feeling of being able to enact one’s intentions during lucid dreaming seems reasonable, as the dreamer is aware that in contrast to the constraints of waking life, during dreams all potential obstacles are not real and hence can easily be overcome. This interpretation would also be in line with the former finding of a comparably low level of experienced planning ability during lucid dreaming: organized planning might be possible during lucid dreaming in principle, however is rarely actually performed since intention execution is possible without such effort.

Neither powers of concentration, nor self-access, nor integration differed between the three states of consciousness. The first of these subfactors asks for how easily the subject gets distracted from his current line of intentional thought. The failure to find any difference between the three states of consciousness is rather surprising, since concentration and goal-directed thinking are generally thought to be strongly impaired during non-lucid dreaming (Hobson and Pace-Schott, 2002; Metzinger, 2003). The subfactor self-access asks for the quality of access to one’s intentions and feelings in stressful situations. It might be speculated that in such situations, also during wakefulness and lucid-dreaming, self-reflection might be impaired, thereby leveling potential differences of self-access that would occur in non-stressed situations. The subfactor integration asks for the occurrence of seemingly contradictory behaviors and emotions. It is rather surprising that non-lucid dreaming does not differ from the other two states, since incongruities and inconsistencies are generally associated most strongly with the dreaming state (Mamelak and Hobson, 1989). However, such inconsistencies are typically attributed to the dream plot rather than to the dreamer, whose mental complexity is narrow and “single-minded” compared to a much broader repertoire of behaviors and thoughts experienced during wakefulness or lucid dreaming (Rechtschaffen, 1978). Hence, compared to a bizarre and highly incongruent dream plot, the single-mindedness of dream cognition might be experienced as relatively straightforward.

In the following, we will try to embed the topic of volition in a broader discussion of the multiple facets and neural correlates of human consciousness.

Basal Vs. Higher-Order Aspects of Consciousness

The enquiry into consciousness has long been the domain of philosophy, however recent years witnessed a growing interest also among neuroscientists in the problems surrounding consciousness. While there is still little agreement on a specific characterization or definition, it seems clear that consciousness is a multifaceted concept, with its different aspects varying dramatically between species, vigilance states, or health conditions. A common categorization differentiates between basal and higher-order aspects of consciousness: the concept of basal (or primary) consciousness comprises perceptions and emotions, whereas higher-order (or secondary) consciousness is proposed to constitute reflections on these (for a review cf. Morin, 2006). As phrased by Edelman (2003, p. 5521):“Higher-order consciousness allows its possessors to go beyond the limits of the remembered present of primary consciousness. An individual’s past history, future plans, and consciousness of being conscious all become accessible.”

A striking variation in consciousness is experienced every day during the sleep–wake cycle: awake human subjects are normally alert, aware of external and internal stimuli, and able to reflect on their perceptions and emotions and to volitionally act according to their intentions. These experiences and capabilities fade during the process of falling asleep, however the progress through the sleep cycle is associated with a reinstatement of essential features of consciousness: REM sleep evokes the most vivid and intense dreams, in which the sleeper perceives a hallucinated environment and often experiences strong emotions.

However, the dreaming state instantiates only basal aspects of consciousness, being deficient in reflective thought, metacognition and volitional capabilities: the internally generated perceptions and emotions experienced during dreaming typically show many cognitive abnormalities, with a bizarre dream plot full of gaps, delusional thought, and a complete lack of insight into the current condition (Hobson and Pace-Schott, 2002; Metzinger, 2003). Rechtschaffen (1978) called this persistence of a single train of related thoughts and images without disruption from other simultaneous thoughts or reflections the “single-mindedness” of dreams. He pointed out that without reflectiveness, there could hardly be volitional control. Nevertheless, some rudimentary processes of reflection and volition have been reported to occur during dreaming (Kahan et al., 1997; Wolman and Kozmová, 2007), even though less often than for waking episodes (Kahan et al., 1997; Voss et al., 2013). Our results confirm these findings, suggesting a generally weaker experience of volition during non-lucid dreaming compared to wakefulness, however with some components being similarly expressed during wakefulness and dreaming.

Lucid Dreaming as Higher-Order Consciousness

In contrast to the restricted consciousness of normal dreaming, the rare state of lucid dreaming is characterized by full-blown consciousness including all higher-order aspects: the sleeping subject is no longer deluded by the dream narrative, but becomes fully aware of the true nature of his current state of consciousness (LaBerge et al., 1981). This wake-like intellectual clarity comprises a restored access to memory functions including increased availability of self-related information, and fully realized agency, enabling the dreamer to volitionally execute his intentions within the dream narrative (Metzinger, 2003; Windt and Metzinger, 2007). Lucid dreaming can be trained (LaBerge, 1980; Purcell et al., 1986), which makes this phenomenon a promising research topic despite its rarity in untrained subjects (Schredl and Erlacher, 2011).

In comparing lucid and non-lucid REM sleep, the distinction between basal and higher-order consciousness is of great value, since the contrast between lucid and non-lucid dreaming strikingly mirrors the conceptual contrast between basal and higher-order consciousness (Dresler et al., 2009; Hobson, 2009): while all basal features of consciousness like perceptions and emotions are present in normal dreaming, metacognitive reflections and the insight into the current state of consciousness is – by definition – bound to lucidity. Since also in non-lucid dream reports some reflective thoughts have been reported and since also during daydreaming and other phases of wakefulness active reflections are frequently absent, it has been argued that metacognitive activity differs only quantitatively and not qualitatively between dreaming and waking consciousness (Kahan et al., 1997; Kahan and LaBerge, 2011). However, this absence is only a “local,” not global feature of such phases: it is hardly imaginable, at least for non-pathological cases, that the day-dreaming subject misinterprets the daydream for reality once paying attention to his current state. For the dreaming state, in contrast, this is completely normal – unless the dreamer eventually achieves lucidity through these “prelucid” reflections (Tyson et al., 1984).

Lucid dreaming may even be critical to fully understanding the neural correlates of higher-order consciousness, because in contrast to, e.g., coma–wake, anesthesia–wake, or sleep–wake comparisons, there is no major shift in vigilance state as defined by formal neurophysiological criteria: lucid REM sleep still is REM sleep proper according to the classical Rechtschaffen and Kales (1968) or new AASM (Iber et al., 2007) sleep scoring criteria. When compared to wakefulness, pathological or pharmaceutically induced loss of consciousness also reduces the brain’s basal metabolism, as does deep sleep. Dreaming therefore provides the only phenomenon we know of, that can contrast basal consciousness with full-blown higher-order consciousness within the same vigilance level (Spoormaker et al., 2010), allowing for comparison of cerebral activity by means of EEG, PET, or fMRI without differences in the basal activity state.

Neural Correlates of Lucid Dreaming

On the phenomenological level, REM sleep is the sleep stage associated with the most vivid sleep mentation (Fosse et al., 2001). On the neurobiological level, it is associated with strong activation of visual association areas and limbic structures such as the amygdala, while the dorsolateral prefrontal cortex (DLPFC) and parietal areas are deactivated (Maquet et al., 1996; Braun et al., 1998). This activation pattern has been proposed to underlie the visual hallucinations, emotional intensifications, and metacognitive impairments experienced in most dreams (Hobson and Pace-Schott, 2002; Schwartz and Maquet, 2002). In particular diminished activity in the DLPFC during REM sleep has been related to cognitive aspects of dreaming such as impaired directed thought, volitional control, and a complete lack of insight into the current state of consciousness (Hobson and Pace-Schott, 2002; Schwartz and Maquet, 2002).

In contrast to normal dreaming, the regaining of wake-like metacognitive capabilities during lucid dreaming is related to increased EEG gamma-band activity over dorsolateral prefrontal areas (Voss et al., 2009). fMRI data have confirmed increased activation of the DLPFC during lucid dreaming, as well as of bilateral frontopolar and parietal areas (Dresler et al., 2012). These brain regions have been related to self-focused metacognitive evaluation (Stuss et al., 2001; Schmitz et al., 2004), supervisory modes (Burgess et al., 2007), and self-referential processing in general including the experience of agency (Cavanna and Trimble, 2006). Their activation during lucid dreaming is in line with the notion that lucidity consists in an increased availability of self-related information, leading to a much higher degree of coherence and stability of the phenomenal self during lucid dreaming (Metzinger, 2003). Our findings fit well into this literature, demonstrating that volition is similarly experienced during wakefulness and lucid dreaming as compared to non-lucid dreaming.

Neural Correlates of Volition

As is the case for consciousness, volition is a multifaceted concept, hence not traceable to one specific brain region. However, several cortical areas have repeatedly been demonstrated to be related to volitional processes. While most studies show motor areas to be involved in volitional action, this research mainly focuses on willed motor actions (Haggard, 2008), which seem to share similar neural substrates during wakefulness and dreaming (Erlacher and Schredl, 2008; Dresler et al., 2011). In contrast, more general or abstract intentions are thought to rely on the dorsolateral prefrontal cortex (Roskies, 2010). In addition, early stages of intentional action have been related to anterior prefrontal brain regions. Such processing of complex information, only broadly determined by specific task demands, is then thought to travel posteriorly to enter later stages of intentional action (Brass et al., 2013). The subjective experience of volitional agency has been associated with parietal brain regions (Roskies, 2010). Hence, in line with our findings, general aspects of volitional control and the subjective experience thereof rely on brain regions that are highly active during lucid compared to non-lucid dreaming.

Consciousness in Humans and Non-Human Animals

Higher-order aspects of consciousness are traditionally thought to be most pronounced in humans (Edelman, 2001). In particular volitional capabilities have been proposed to be a distinctive human attribute (Dijksterhuis and Aarts, 2010; Frith, 2013). If the contrast between ordinary and lucid dreaming mirrors that between basal and higher-order consciousness, data on the neural correlates of dream lucidity might shed new light on this debate. Indeed it turns out that cerebral regions showing increased activity during lucid dreaming also show extensive volumetric expansion in humans as compared to non-human primates (Van Essen and Dierker, 2007; see Figure 1). Recently the hypothesis was proposed that only animals possessing higher-order aspects of consciousness may develop psychotic states – “in other words an animal needs to have a highly developed mind in order to go out of it” (Hobson and Voss, 2011, p. 993). Neuroimaging data on lucid dreaming support this claim: areas activated during lucid dreaming (Dresler et al., 2012) do not only mirror human vs. non-human primate brain differences (Van Essen and Dierker, 2007), but also show striking overlap with brain areas associated with insight deficits in psychosis (Dresler et al., in revision).

FIGURE 1 

FIGURE 1. Brain areas subserving the transition from basal to higher-order consciousness in REM sleep dreaming mirror those with strongest volumetric expansion in humans compared to non-human primates. Left: during lucid dreaming, the dorsolateral prefrontal and frontopolar cortices, parietal lobules, and inferior/middle temporal gyri among other cortical regions are strongly activated as compared with non-lucid REM sleep (republished with permission of the American Academy of Sleep Medicine, from Dresler et al. (2012); permission conveyed through Copyright Clearance Center, Inc.). Right: neuroanatomical differences between humans and non-human primates (Van Essen and Dierker, 2007; reprint with permission of Cell Press). Color-coded are regional volumetric expansions in the human relative to the macaque brain hot colors depict up to a 32-fold volumetric increase in humans. Right lateral view.

Limitations
A couple of limitations have to be kept in mind for the interpretation of our study’s results. First, we used an adapted version of VCQ that was not specifically validated for its use in different states of consciousness. This applies in particular to the overall score combining the six subscales. While the original version was created to evaluate time frames of several weeks, for our adapted version only items were chosen that are applicable to shorter episodes like dreams. Second, whereas the ratings for lucid and non-lucid dreaming were collected after awakening from the respective dream phase in the early morning, the ratings for wakefulness were collected after a full day of wakefulness in the evening. Thus, the length of the rated episodes differed, and it cannot be excluded that chronobiological influences affected the ratings. Third, the order of data collection was not randomized, but started for all subjects with the wakefulness ratings, followed by the non-lucid dreaming ratings, which were finally followed by the lucid dreaming ratings. Thus, order effects might have influenced the results. However, several subjects completed more than one questionnaire and did so after a complete round of ratings. Since the scores from these repeated ratings did not differ from the first ratings, it is rather unlikely that rating order affected the results. Fourth, gender differences for content and recall have been reported for non-lucid (Schredl et al., 2004) and lucid (Schredl and Erlacher, 2011) dreams, however our small sample size does not allow a reliable analysis of possible gender effects on state-dependent volition. An explorative analysis did not reveal gender effects (p > 0.2) or gender × state interactions (p > 0.4).

Conclusion and Future Directions

Our study confirmed the multifaceted nature of consciousness: volitional components of higher-order consciousness are differentially expressed among different conscious states. On a coarser level, the generally wake-like expression of volition during lucid dreaming is well in line with the neural activity pattern observed during this state. Up until 15 years ago, using lucid dreaming for the study of consciousness was not seen as experimentally advantageous (Crick and Koch, 1998). However, neuroimaging research into the neural correlates of lucid dreaming and its association with metacognitive and volitional processes has proven lucid dreaming to be a highly promising approach for the investigation of higher-order aspects of consciousness. Neural correlates of lucid dreaming show a remarkable overlap with areas and networks subserving self-reflective thought and volitional capabilities. In addition, these areas show the strongest differences between human and non-human primates, strengthening suggestions that higher-order aspects of consciousness are most pronounced in humans.

While research into lucid dreaming is currently hampered by the rarity of the phenomenon, systematic training (Stumbrys et al., 2012), and new technical approaches for its induction like transcranial direct current stimulation (tDCS; Noreika et al., 2010; Stumbrys et al., 2013) might lead to research programs beyond a collection of case studies. In such research programs, subjects might be asked to actively engage in metacognitive processes and volitional acts during lucid dreaming, thereby tracing higher-order consciousness from its state-dependent absence to the regaining of the ability to engage in higher-order conscious thought to its actual execution. Using neuroimaging methods in combination with refined measures of the degree of lucidity, e.g., by exploiting scales that assess several dimensions of volition and insight during dreams (Voss et al., 2013), the specific involvement of several brain regions in distinct higher-order aspects of consciousness may be disentangled. Such studies would further refine the neural correlates underlying the multiple facets of human consciousness.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References available at the Frontiers site