The twilight zone

COVER STORY

Altered states

TESSAR LO

Consciousness is a strange beast. Most of the time you’re either awake or asleep, yet these are far from the only states our minds can enter. Over the next 10 pages we explore some of these journeys of the mind, from hypnosis to sleep paralysis. Some of them may seem scary and exotic, but most of us experience at least one at some point in our lives. All reveal the malleability of the human mind and the fragility of that sense of me, here, now. Enjoy the trip.

30 | NewScientist | 10 October 2009

You think you’re awake, yet part of your brain is sleeping. It could be happening to you right now, says Laura Spinney

The twilight zone E

ARLIER this year, a puzzling report appeared in the journal Sleep Medicine. It described two Italian people who never truly slept. They might lie down and close their eyes, but read-outs of brain activity showed none of the normal patterns associated with sleep. Their behaviour was pretty odd, too. Though largely unaware of their surroundings during these rest periods, they would walk around, yell, tremble violently and their hearts would race. The remainder of the time they were conscious and aware but prone to powerful, dream-like hallucinations. Both had been diagnosed with a neurodegenerative disorder called multiple system atrophy. According to the report’s authors, Roberto Vetrugno and colleagues from the University of Bologna, Italy, the disease had damaged the pair’s brains to such an extent that they had entered status dissociatus, a kind of twilight zone in which the boundaries between sleep and wakefulness completely break down (Sleep Medicine, vol 10, p 247). That this can happen contradicts the way we usually think about sleep, but it came as no surprise to Mark Mahowald, medical director of the Minnesota Regional Sleep Disorders Center in Minneapolis, who has long contested the dogma that sleep and wakefulness are discrete and distinct states. “There is now overwhelming evidence that the primary states of being are not mutually exclusive,” he says. The blurring of sleep and wakefulness is > 10 October 2009 | NewScientist | 31

WHEN A CRIME IS NOT A CRIME In 1988, a 23-year-old Canadian man named Kenneth Parks went on trial for the murder and attempted murder of his parents-in-law. One night in the previous year, he drove 23 kilometres across town to their home and attacked them with a tyre iron and a knife. He was acquitted on all counts, on the grounds that he was sleepwalking at the time. Since then, numerous defendants have pleaded “parasomnias” – an oldfashioned term for disorders involving partial arousal during sleep that is now mostly used in law. Mark Pressman, at the Lankenau Hospital in Wynnewood, Pennsylvania, estimates that they are used as a defence in between five and 10 cases worldwide each year. This raises tough issues about criminal responsibility and has been a source of

ongoing dispute among lawyers. One of the most contentious areas concerns men charged with sexual assault who claim sleep-related sexual behaviour, or sexsomnia, as a defence (New Scientist, 28 October 2006, p 40). Sexsomnia is a variation on sleepwalking and a recognised condition. The controversy arises when these men claim – sometimes successfully – that heavy alcohol consumption provoked their sexsomnia. “My colleagues and I have been actively opposing this defence on the grounds there is no scientific evidence that severe intoxication causes sleepwalking,” Pressman says. But he admits that it is a fiendishly difficult area of law, not least because no sleep study can shed light on what happened in a single individual’s brain on a single night in the past.

very clear in status dissociatus, but he which they had to subtract numbers, they believes it can happen to us all. If he is right, could do an average of 90 sums in 3 minutes we will have to rethink our understanding with few errors. After 52 hours deprived of of what sleep is and what it is for. Maybe sleep, their performance fell to around wakefulness is not the all-or-nothing 70 subtractions, with not many more errors. phenomenon we thought it was either. However, after they had slept for 2 hours the Received wisdom has it that at any given change was dramatic. “When we woke them time, healthy people are in one of three states up abruptly, and they rated themselves as alert of vigilance: awake, in rapid eye movement and ready to go, they couldn’t do even one (REM) sleep or in non-REM (NREM) sleep. Each subtraction,” says Dinges. People even seemed state is distinct and can be recognised by a to be dreaming as they attempted the task. characteristic pattern of brain activity, as measured by an electroencephalogram (EEG) (see chart, right). Wakefulness is easy to detect. ”It is no coincidence that Apart from the fact that a person’s eyes are alien abductions tend to open and they are responsive, their EEG shows occur in the transition from a pattern of high-frequency, low-amplitude waves. NREM sleep is divided into four stages, wakefulness to sleep” each of which has its own distinctive EEG pattern. REM is trickier to spot because in EEG terms it closely resembles stage 1 NREM sleep. One subject mused: “What if people ran faster So to be sure it really is REM, researchers also than normal people run home,” in the middle look for the telltale rapid eye movements and of a string of incorrect responses. a slackening in the muscles of the chin and jaw. Known as sleep inertia, a less extreme Mahowald is not the only person to have version of such disorientation is now generally questioned these neat distinctions. David recognised as the cause of the grogginess some Dinges, a psychiatrist at the University of people get after their alarm clock goes off. It is Pennsylvania, Philadelphia, has probably as if they are socially awake but functionally deprived more people of sleep in the name of asleep; as if the brain circuits underlying science than anyone else. In one such study in responsiveness are up and running, but those the late 1980s, Dinges and his team revealed mediating working memory are still offline. how easily the different states of vigilance can Mahowald is convinced that it is just one of become intermingled. When volunteers were many disorders that can be explained as a subjected to tests of working memory in breakdown in the boundaries between sleep 32 | NewScientist | 10 October 2009

and wakefulness. He lists a whole raft of such conditions in the same issue of Sleep Medicine as Vetrugno’s description of people with status dissociatus (vol 10, p 159). One is REM behavioural disorder (RBD), in which people in REM sleep act out their dreams because the temporary paralysis, or cataplexy, that normally accompanies this state is replaced by the full mobility of wakefulness. In sleep paralysis the opposite is true. Here, cataplexy intrudes into wakefulness, and a person wakes to find him or herself unable to move. It is estimated that up to 40 per cent of people have experienced this disturbing phenomenon. Also surprisingly common are hypnagogic hallucinations – sensory illusions that occur on the cusp of sleep when the dreaming component of REM intrudes into wakefulness. Mahowald’s list also includes sleepwalking, night terrors and narcolepsy, which is an inherent instability in vigilance state boundaries characterised by rapid cycling between states and the tendency to fall asleep mid-sentence. Controversially, the list also includes near-death experiences and alien abductions. It is no coincidence, he says, that alien abductions almost always occur in the recumbent position, in the transition from wakefulness to sleep. Sleep is a highly complex phenomenon in which changes in sensory, muscular, hormonal and neural systems must be coordinated to create a particular state of vigilance. “When you think about it, there are billions of people in the world who are shifting between wakefulness, REM and non-REM multiple times every 24 hours,” says Mahowald. “It’s amazing that the switching is as accurate as it is.” This accuracy suggests that there is a strong adaptive drive to be fully in one state or another. But he also thinks that state dissociation – the presence of more than one vigilance state concurrently – is more common than anyone previously suspected. The boundaries between sleep and wakefulness are particularly blurred when we are sleep-deprived. Around a decade ago, Dinges realised that although his sleep-deprived volunteers seemed to be awake, they were in fact experiencing momentary lapses, or microsleeps. Since then, he has discovered that these fleeting naps last between half a second and 2 seconds, and become increasingly frequent the longer we are deprived of sleep, until finally we cannot recover and nod off. Dinges sees them as the outward sign of a tug-of-war between neural systems that are trying to initiate sleep, and others that

States of vigilance

The traditional way of distinguishing wakefulness from non-REM and REM sleep is to look for characteristic patterns of brain activity using an EEG, which measures electrical activity in the outer few millimetres of the cortex

Awake ALPHA ACTIVITY (RELAXED)

Non-REM sleep

0

1

Seconds 2 3 4

BETA ACTIVITY (ALERT)

5

Stage 1 sleep THETA ACTIVITY (DROWSINESS)

K COMPLEX (BRIEF AROUSAL)

Stage 2 sleep SPINDLE (BLOCKING AROUSAL)

DELTA ACTIVITY

REM sleep THETA ACTIVITY

BETA ACTIVITY

GROUND CONTROL TO MAJOR TOM Every so often, commercial pilots and other professionals whose jobs require them to be highly vigilant have to take something called the maintenance of wakefulness test. They must sit in a comfy chair in a dimly lit room and stay awake for 40 minutes, a procedure that is repeated four times over the course of 8 hours. If they should drop off, this is detected by EEG, eye movement and jaw slackness. However, these are fairly crude measures, and anyway people whose job is on the line tend to be highly motivated to stay awake. Sleep scientists acknowledge that a more sensitive test is required, and David

Dinges at the University of Pennsylvania, Philadelphia, believes he has one. His is a test of reaction time in which subjects have to repeatedly press a button in response to a light going on. This psychomotor vigilance test is “unbelievably sensitive” to instability in the boundaries between wakefulness and sleep, Dinges claims. A shortened version went up to the International Space Station in July, so that the astronauts could put it through its paces. If it accurately reflects their ability to do their job, it may soon be routinely applied to pilots, nuclear power station operators and others in life-or-death jobs.

SOURCE: JIM HORNE, LOUGHBOROUGH UNIVERSITY

DELTA ACTIVITY (DEEP SLEEP)

Stages 3 & 4 slow-wave sleep

are trying to maintain wakefulness. This chimes with the ideas of James Krueger of Washington State University in Pullman, who has argued that the individual processing units in the brain – known as cortical columns – fall asleep independently when they become tired. In his view, shifts between wakefulness and sleep occur when enough columns are in one state or the other (Nature Reviews Neuroscience, vol 9, p 910). Krueger believes this mosaic pattern of sleep explains sleep inertia and sleepwalking. Some people are more prone to microsleeps than others. In a 2007 study, Dinges and his colleagues showed that there are enormous differences in people’s ability to resist the lure of sleep when tired. Among a group of healthy, non-sleep-deprived adults, the differences in alertness are small. “But as soon as we provoke the system with some sleep deprivation, those differences get larger and larger,” he says (Journal of Sleep Research, vol 16, p 170). This has implications for all of us, especially those in professions where staying awake is a life-or-death matter (see “Ground control to Major Tom”). “If you’re doing 100 kilometres per hour on a highway and you have a lapse, your fingers go lax on the steering wheel and you drift off the road at a 4-degree angle,” says Dinges. “Two seconds is all it takes to be completely out of your lane.” Up to 20 per cent of traffic accidents are fatigue-related. Brain imaging has recently revealed a mental back-up system in people who remain alert when sleep-deprived (Journal of Neuroscience, vol 29, p 7948). While other people have reduced brain activity when tired, sleep-resistant individuals manage to maintain their brain activity levels. More interestingly, they also recruit new areas to help compensate for having been awake for so long. These people were selected for the study because they had a gene variant found in around 40 per cent of people that is thought to be associated with resistance to sleep deprivation. It seems likely that such people are also less prone to state dissociation, although this has not yet been tested. Another group who appear to be more vigilant than most are people who suffer from primary insomnia – insomnia not associated with any other condition. There is evidence to suggest they are in a constant state of hyperarousal, with relatively high metabolic rates and high levels of the stress hormone cortisol. “It’s as though somebody just cranked up their alertness over 24 hours, so they are more alert at night, but they are also more alert in the day,” says Mahowald. > 10 October 2009 | NewScientist | 33

ALTERED STATES As the blur between sleep and wakefulness becomes more widely accepted, researchers are devising techniques for capturing the brain’s fleeting lapses and vacillations. For example, neuroscientist Giulio Tononi of the University of Wisconsin, Madison, is eavesdropping on sleeping brains using EEGs with 256 electrodes rather than the more usual 32, to improve spatial resolution and help him catch the brain in the act of mosaic napping. Microsleeps are just the tip of the iceberg, Tononi says. He is particularly concerned by the possibility that parts of our brain might be going offline without us even realising it. “In many respects, it would be like having a temporary mental disorder without anybody, including yourself, being aware of it,” he says. Forgetfulness and daydreaming

”It is like having a temporary mental disorder without anyone, including yourself, being aware of it” could be examples of this, but so could more bizarre and even criminal behaviours (see “When a crime is not a crime”, page 32). Meanwhile, Pierre Maquet at the University of Liège in Belgium has started to use fMRI to chart the patterns of brain activity associated with different sleep states. His team is already finding that the distinctions between sleep and wakefulness look quite different when you compare patterns of activity across the whole brain, including deep structures, as opposed to using EEG, which measures activity in just the outer few millimetres of the cortex. Lurking in the background is the hope that these approaches will shed light on the vexed issue of what sleep is for. A leading theory is that it is important for memory consolidation. Yet one of the puzzling aspects of the two Italians with status dissociatus is that, despite complete disruption of both their REM and NREM sleep, they showed no memory deficit. Does this add grist to the mill of those who believe that sleep has no other purpose than to save energy and keep us safe (New Scientist, 15 March 2008, p 30)? Or does it mean, as Mahowald believes, that the two individuals were in fact experiencing some sort of mosaic sleep? Armed with a less black-and-white definition of sleep and wakefulness, and more sensitive tools for measuring them, that question might finally be resolved. ■ Laura Spinney is a writer in Lausanne, Switzerland 34 | NewScientist | 10 October 2009

The mind unshackled