Antonio Meno Ortega (R) is cared for by his parents Juana (L) and Antonio (C) in November 2010. He has been in a persistent vegetative state since a botched nose operation in 1989. Photo: Getty Images
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Reading the minds of those trapped in their own bodies, unable to ask for help

Thousands remain trapped between life and death. Three scientists are working to free them. Roger Highfield reports.

“Imagine you wake up, locked inside a box,” says Adrian Owen. “It’s only just big enough to hold your body but sufficiently small that you can’t move.

“It’s a perfect fit, down to every last one of your fingers and toes. It’s a strange box because you can listen to absolutely everything going on around you, yet your voice cannot be heard. In fact, the box fits so tightly around your face and lips that you can’t speak, or make a noise. Although you can see everything going on around the box, the world outside is oblivious to what’s going on inside.

“Inside, there’s plenty of time to think. At first, this feels like a game, even one that is strangely amusing. Then, reality sets in. You’re trapped. You see and hear your family lamenting your fate. Over the years, the carers forget to turn on the TV. You’re too cold. Then you’re too hot. You’re always thirsty. The visits of your friends and family dwindle. Your partner moves on. And there’s nothing you can do about it.”

Owen and I are talking on Skype. I’m sitting in London, UK, and he’s in another London three-and-a-half thousand miles away at the University of Western Ontario, Canada. Owen’s reddish hair and close-cropped beard loom large on my screen as he becomes animated describing the torment of those with no voice: his patients.

People in a ‘vegetative state’ are awake yet unaware. Their eyes can open and sometimes wander. They can smile, grasp another’s hand, cry, groan or grunt. But they are indifferent to a hand clap, unable to see or to understand speech. Their motions are not purposeful but reflexive. They appear to have shed their memories, emotions and intentions, those qualities that make each one of us an individual. Their minds remain firmly shut. Still, when their eyelids flutter open, you are always left wondering if there’s a glimmer of consciousness.

A decade ago, the answer would have been a bleak and emphatic no. Not any longer. Using brain scanners, Owen has found that some may be trapped inside their bodies yet able to think and feel to varying extents. The number of patients with disorders of consciousness has soared in recent decades, ironically, because of the rise and success of intensive care and medical technologies. Doctors have steadily got better at saving patients with catastrophic injuries, though it remains much easier to restart a heart than restore a brain. Today, trapped, damaged and diminished minds inhabit clinics and nursing homes worldwide - in Europe alone the number of new coma cases is estimated to be around 230,000 annually, of which some 30,000 will languish in a persistent vegetative state. They are some of the most tragic and expensive artefacts of modern intensive care.

Owen knows this only too well. In 1997, a close friend set off on her usual cycle to work. Anne* had a weak spot on a blood vessel in her head, known as a brain aneurysm. Five minutes into her trip, the aneurysm burst and she crashed into a tree. She never regained consciousness.

The tragedy left Owen numb, yet Anne’s accident would shape the rest of his life. Owen began to wonder if there was a way to determine which of these patients were in an unconscious coma, which were conscious and which were somewhere in between?

That year, he had moved to the Medical Research Council’s Cognition and Brain Sciences Unit in Cambridge, where researchers used various scanning techniques. One, positron emission tomography (PET), highlights different metabolic processes in the brain, such as oxygen and sugar use. Another, known as functional magnetic resonance imaging (fMRI), can reveal active centres in the brain by detecting the tiny surges in blood flow that take place as a mind whirrs. Owen wondered whether he could use these technologies to reach out to patients, like his friend, stuck between sensibility and oblivion. At the core was a deceptively simple question: how do we know that another person is conscious?

Half a century ago, if your heart stopped beating you could be pronounced dead even though you may have been entirely conscious as the doctor sent you to the morgue. This, in all likelihood, accounts for notorious accounts through history of those who ‘came back from the dead’. As a corollary, those who were fearful of being buried alive were spurred on to develop ‘safety coffins’ equipped with feeding tubes and bells. As recently as 2011, a council in the Malatya province of central Turkey announced it had built a morgue with a warning system and refrigerator doors that could be opened from the inside.

What do we mean by ‘dead’? And who should declare when an individual is dead? A priest? A lawyer? A doctor? A machine? Owen discussed these issues at a symposium in Brazil with the Dalai Lama and says he was surprised to find that they both agreed strongly on one point: we need to create an ethical framework for science that is based on secular, rather than religious, views; science alone should define what we mean by death.

The problem is that the scientific definition of ‘death’ remains as unresolved as the definition of ‘consciousness’. Much confusion is sowed by the term ‘clinical death’, the cessation of blood circulation and breathing. Even though this is reversible, the term is often used by mind-body dualists who cling to the belief that a soul (or self) can persist separately from the body. Today, however, being alive is no longer linked to having a beating heart, explains Owen. If I have an artificial heart, am I dead? If you are on a life-support machine, are you dead? Is a failure to sustain independent life a reasonable definition of death? No, otherwise we would all be ‘dead’ in the nine months before birth.

The issue becomes murkier when we consider those trapped in the twilight worlds between normal life and death - from those who slip in and out of awareness, who are trapped in a ‘minimally conscious state’, to those who are severely impaired in a vegetative state or a coma. These patients first appeared in the wake of the development of the artificial respirator during the 1950s in Denmark, an invention that redefined the end of life in terms of the idea of brain death and created the specialty of intensive care, in which unresponsive and comatose patients who seemed unable to wake up again were written off as ‘vegetables’ or ‘jellyfish’. As is always the case when treating patients, definitions are critical: understanding the chances of recovery, the benefits of treatments and so on all depend on a precise diagnosis.

Pioneering work to understand and categorise disorders of consciousness was carried out in the 1960s by neurologist Fred Plum in New York and neurosurgeon Bryan Jennett in Glasgow. They were the odd couple. Jennett - or ‘BJ’, as he was known to colleagues - was reserved and gentlemanly, with an unusually penetrating and analytical mind. Plum was larger than life, commanding and an inspiring teacher who was famous for his idiosyncratic ways of diagnosing neurological conditions. ‘Fred Plum stories’ abound: he would diagnose hemispatial neglect (where damage in one cerebral hemisphere makes a person behave as if their opposite side does not exist) by seeing if the patient could tell if his glasses were askew and one arm pulled out of a sleeve of his coat.

Plum coined the term ‘locked-in syndrome’, in which a patient is aware and awake but cannot move or talk. With Plum, Jennett devised the Glasgow Coma Scale to rate the depth of coma, from a minimum of 3 to a maximum of 15, and Jennett followed up with the Glasgow Outcome Scale to weigh up the extent of recovery, from death to mild disability. Together they adopted the term ‘persistent vegetative state’ for patients who, they wrote, “have periods of wakefulness when their eyes are open and move; their responsiveness is limited to primitive postural and reflex movements of the limbs, and they never speak”. In 2002, Jennett was among a group of neurologists who chose the phrase ‘minimally conscious’ to describe those who are sometimes awake and partly aware, who show erratic signs of consciousness so that at one time they might be able to follow a simple instruction and another they might not. In this way, Plum’s yin and Jennett’s yang launched the field of coma science. Even today, however, we’re still arguing over who is conscious and who isn’t.

§

Adrian Owen has a well-honed routine he uses at public events. A confident performer - helped no doubt by spending 14 years as the lead singer of a band called You Jump First - he asks the audience to raise their left arms. They obey. After a pause, he asks them to raise their right arms. Once again, they comply. “I know you’re conscious because you’ve all got your hands up,” he declares.

The same sort of test features in countless medical dramas, when the doctor clasps the hand of a seemingly unconscious patient and says, “Squeeze if you can hear me”. A tightening grip would represent an act of will. That basic interaction between two conscious minds is the only real signature of being both aware and awake, says Owen. But what if the patient does not squeeze? What is a doctor supposed to think then?

The public perception of coma (from the Greek koma, meaning ‘deep sleep’) is of a patient lying peacefully, eyes shut, without a glimmer of arousal or consciousness, eventually awakening to make a full recovery. The images of films such as Hable con Ella (Talk to Her) and While You Were Sleeping are a long way from the intubations, double incontinence and uncertainty of the reality: a person cannot be awakened, does not respond to pain, light or sound, and does not undergo a normal cycle of sleep and wakefulness.

Kate Bainbridge, a 26-year-old schoolteacher, lapsed into a coma three days after she came down with a flu-like illness. Her brain became inflamed, including the primitive region atop the spinal cord, the brain stem, which rules the sleep cycle. A few weeks after her infection had cleared, Kate awoke from the coma but was diagnosed as being in a vegetative state. Luckily, the intensive care doctor responsible for her, David Menon, was also a Principal Investigator at the newly opened Wolfson Brain Imaging Centre in Cambridge, where one Adrian Owen then worked.

Menon wondered if elements of cognitive processing might be retained in patients in a vegetative state and discussed with Owen how to use a brain scanner to detect them. In 1997, four months after she had been diagnosed as vegetative, Kate became the first patient in a vegetative state to be studied by the Cambridge group. The results, published in 1998, were unexpected and extraordinary. Not only did Kate react to faces: her brain responses were indistinguishable from those of healthy volunteers. Her scans revealed a splash of red, marking brain activity at the back of her brain, in a part called the fusiform gyrus, which helps recognise faces. Kate became the first such patient in whom sophisticated brain imaging (in this case PET) revealed ‘covert cognition’. Of course, whether that response was a reflex or a signal of consciousness was, at the time, a matter of debate.

The results were of huge significance for science but also for Kate and her parents. “The existence of preserved cognitive processing removed the nihilism that pervaded the management of such patients in general, and supported a decision to continue to treat Kate aggressively,” recalls Menon.

Kate eventually surfaced from her ordeal, six months after the initial diagnosis. She described how she was indeed sometimes aware of herself and her surroundings. Each day she woke up, she fell asleep, but like all such patients she could not respond to people’s questions. Worse, she had a raging thirst that was never slaked.

“They said I could not feel pain,” she says. “They were so wrong.” Sometimes she’d cry out, but the nurses thought it was just a reflex. She felt abandoned and helpless. Hospital staff had no idea how much she suffered in their care. Kate found physiotherapy scary: nurses never explained what they were doing to her. She was terrified when they removed mucus from her lungs. “I can’t tell you how frightening it was, especially suction through the mouth,” she has written. At one point, her pain and despair became so much that she tried to snuff out her life by holding her breath. “I could not stop my nose from breathing, so it did not work. My body did not seem to want to die.”

Kate says her recovery was not so much like turning a light on but a gradual awakening. It took her five months before she could smile. By then she had lost her job, her sense of smell and taste, and much of what might have been a normal future. Now back with her parents, Kate is still very disabled and needs a wheelchair. Twelve years after her illness, she started to talk again and, though still angry about the way she was treated when she was at her most vulnerable, she remains grateful to those who helped her mind to escape.

She sent Owen a note.

Dear Adrian,
Please use my case to show people how important the scans are. I want more people to know about them. I am a big fan of them now. I was unresponsive and looked hopeless, but the scan showed people I was in there.
It was like magic, it found me. 

§

When you are awake, your brain has to make sense of a flood of information from your senses. To make the most of its limited data-processing resources, our ancestors evolved a brain that can focus on that approaching spear or lurking lion rather than a broad sweep of savannah landscape. One can think of it as a spotlight of attention that illuminates key sensory information in the brain, which then enters into conscious awareness. This is the mind’s spotlight on the outside world, with awareness at its focus and the degree of wakefulness tuning its intensity.

Steven Laureys, who leads the Coma Science Group at the University of Liège in Belgium, is one of those seeking the source of this illumination. He sits before me clutching a little plastic brain. There are islands of blue on the surface, one at the front and one at the back. He divides it in two, revealing a further blue dot deep inside. This is the thalamus, a two-sided structure that sits atop the brain stem and acts as a relay station for incoming sensory information. “There is no such thing as a ‘consciousness region’ in the brain,” he explains. But subtract the fMRI scans of vegetative patients who are awake and unaware from the scans of those who are awake and fully aware and you find the difference boils down to an ‘awareness network’, the areas marked in blue on his plastic brain.  

Laureys describes a thought experiment. “If I use a scalpel to remove the blue regions you would still be awake, breathe and move but you would not be aware.” Similar networks exist in other mammals to varying extents, he explains, and the traditional idea that we alone are conscious while all other animals are automata is unlikely to be true. “Given our studies of vegetative patients, we have tended to underestimate consciousness in the past,” he says.

This idea of an awareness network chimes with various theories of consciousness, such as the ‘global workspace’ first proposed by Amsterdam-born neurobiologist Bernard Baars. In essence, it suggests that awareness emerges from neurons distributed throughout the cortex in a network that blends sensory information and filters out contradictory or unnecessary information to create a unified picture of reality.

This view complements the work of Nicholas Schiff at Weill Cornell Medical College in New York. A neurologist, he started out as a disciple of Fred Plum’s school. Schiff’s working life is a balancing act between putting the interests of his patients and their families first and keeping true to the science as he wrestles with disorders of consciousness. “There’s a lot we don’t know,” he admits. “Frankly, I am wrong a lot of the time.”

Schiff started to piece together this neural circuitry, building on pioneering experiments conducted on cats in the 1940s. These showed how the animals could be revived from anaesthesia by stimulating the thalamus, which plays a crucial part in the brain’s complex orchestra. Studies suggest that a key population of nerve cells (intralaminar thalamic neurons), radiating from this hub to the outer rind (the cortex) and every corner of the brain, have a central role in arousal and waking up. By the same token, they have a central role in coma too: they are more vulnerable than other nerve cells to harm, such as oxygen starvation, which helps to explain why brain damage can lead to unconsciousness.

Schiff is interested in how the relay post that is the thalamus links with a surrounding structure called the striatum and with the frontal cortex. And among these deeper brain regions is an area dubbed the posterior medial complex, a network whose activity is impaired in vegetative brains.

Illustration: Bret Syfert/Wellcome Images (CC-BY)

The thalamus and frontal lobe are also more active in conscious and locked-in patients. Together, Schiff and Laureys have identified three broad brain circuits - those in the thalamus, the frontal lobe and the posterior medial complex - that are key to consciousness. 

At scientific meetings, Schiff has outlined a more detailed version of this neural structure, called the ‘mesocircuit’, which actually consists of two circuits linking the thalamus to the cortex. Some of the connections involved in the mesocircuit stimulate nerve activity, others reduce or prevent it. Overall, higher-level consciousness emerges as a dynamic coalition of these two parallel interactive brain networks. This theory, which he and Laureys are putting to the test, also reveals a way in which one might jump-start a stalled brain. Over the years, a remarkable series of experiments have shown how a mind might be coaxed back into awareness.

§

In 1995, Schiff studied an 81-year-old woman with a disordered consciousness. As a result of an acute stroke, she had suffered hemispatial neglect. She was unable to identify her right hand as her own. Ice-cold water was squirted into her ear, as a standard test to see the extent to which her responses were lopsided. To Schiff’s amazement, the water reversed almost all her symptoms: “That’s my hand!” she cried out. Schiff believed that the chill had stimulated her inner ear, which controls the sense of balance through the vestibular system, and, in turn, her thalamus, knitting together the networks that had been disrupted by the stroke. Four minutes later, when the water had warmed, she lost her hand once again.

The case helped him work up the basic neuroscience of how to increase awareness in a brain stalled in limbo by stimulating the thalamus. Armed with this understanding, Schiff has provided insight into the paradoxical discovery that some patients in vegetative states can be awoken with a sedative, zolpidem. One of the best-known cases is the South African Louis Viljoen, who had been left vegetative by a road accident. One day in 1999, Wally Nel, a GP working near Johannesburg, gave Louis the drug to ease the way that he clawed at his mattress. Instead of being relaxed, Viljoen sat bolt upright, smiled, and said: “Hello Mum. Am I in hospital?” Schiff believes that the drug dampens down so-called ‘medium spiny neurons’ in the part of the mesocircuit that links the striatum, the globus pallidus and the thalamus. Because these neurons inhibit the thalamus, quelling their activity can actually boost awareness. Just as a little alcohol can initially stimulate a buzz, so zolpidem can help “turn the brain on rather than off”, says Schiff.

A study by Schiff and Laureys shows how slow waves of nerve activity, of the kind seen in sleep or anaesthesia, wash over the brain before the drug is given, but afterwards sluggish synchronicity gives way to the crackle of high-frequency brain waves typically seen in conscious patients. PET images tell the same story, revealing how the drug ramps up brain metabolism. Similar effects are caused by another compound, the anti-Parkinson’s drug amantadine. Laureys’s team in Liège finds that about half of patients in a minimally conscious state show mild improvement in awareness as a result of receiving the drug.

The awareness network can be electrically roused. Laureys and his colleagues recently tested transcranial direct-current stimulation (tDCS), in which scalp electrodes are used to pass a weak direct current through the skull to alter the excitability of underlying brain tissue. The Liège team applied tDCS for 20 minutes to part of the mesocircuits of 55 people who were in a minimally conscious or vegetative state. They found that 15 showed glimmers of consciousness as a result. Some showed responses to commands, even though it was several years after they had been declared minimally conscious. Most dramatic, for two patients who had been declared minimally conscious a few months earlier, tDCS enabled them to nod or move their eyes in response to six questions.

The method offers a powerful way to probe which circuits have to be manipulated to awaken a silent brain. “In theory, at least, tDCS offers another way to reactivate circuits to help a damaged brain to recover some functionality, even several years after suffering severe damage,” Laureys explains. However, the results are not as remarkable as those seen in a case where the thalamus was stimulated directly.

In 2005, Schiff applied his emerging understanding of the circuits of consciousness to Jim*, a 38-year-old man who had been beaten and robbed and was left minimally conscious. Jim’s eyes had mostly remained shut. He showed no sign of awareness that his family could detect. His plight seemed hopeless. Eventually, Jim’s mother gave a ‘do not resuscitate’ order to doctors. Schiff thought different.

Schiff had earlier scanned Jim with fMRI, in 2001. His team had played subjects, including Jim, an audiotape in which a relative or loved one reminisced. Jim showed near-normal patterns in the language-processing areas of his brain and this told Schiff that some of Jim’s neural networks were still working. In detailed fMRI scans, Jim had shown that, despite having a very underactive brain, he had strongly preserved large-scale language networks. When he heard a story that meant something to him, his brain lit up. This encouraged Schiff to revive the idea he had mulled over for a decade. What if they activated Jim’s thalamus by deep brain stimulation?

A brain pacemaker was implanted into Jim. Thanks to the regular pulses of electricity it delivered to his thalamus, he was able to use words and gestures, respond reliably to requests, eat normally, drink from a cup, and carry out simple tasks such as brushing his hair. Schiff believes that once a brain re-engages with the world, it accelerates processes of repair. For the next six years, before Jim died of unrelated causes, he kept his mind above the minimally conscious state. “He could converse in short sentences reliably and consistently and make his wishes known,” says Schiff. “He could chew and swallow and eat ice cream and hang out. His family told us that they had him back.” The case made the front page of the New York Times. “I prayed for a miracle,” his mother told me at the time he was brought back. “The most important part is that he can say ‘Mummy and Pop, I love you’. God bless those wonderful doctors. I still cry every time I see my son, but it is tears of joy.”  

In a forested campus south of Liège, Steven Laureys studies vegetative patients in research that dates back decades. Working there as part of the Cyclotron Research Centre in the 1990s, he was surprised when PET brain scans revealed that the patients could respond to a mention of their own name: meaningful sounds produced a change in blood flow within the auditory primary cortices. Meanwhile, on the other side of the Atlantic, Nicholas Schiff was finding that within catastrophically injured brains lay partially working regions, clusters of remnant neural activity. What did it all mean?

At that time, doctors thought they already knew the answers: no patient in a persistent vegetative state was conscious. Never mind that staring at images made the brain light up, they carped: you can do that in a sedated monkey. Based on previous experience, a brain starved of oxygen as a result of a heart attack or a stroke was unlikely to recover if it didn’t in the first few months. These patients had suffered a fate that many people regarded as worse than death itself: they were functionally brainless. Undead. Doctors, with the best intentions, thought it was perfectly acceptable to end the life of a vegetative patient by starvation and the withdrawal of water. This was the age of what Laureys calls “therapeutic nihilism”.

What Owen, Laureys and Schiff were proposing was a rethink of some of the patients who were considered vegetative. A few of them could even be classed as being fully conscious and locked-in. The establishment was doggedly opposed. “You cannot imagine the environment in the late 1990s,” says Schiff. “The hostility we encountered went well beyond simple scepticism.” Looking back, Laureys pauses and smiles thinly: “Medical doctors do not like to be told they are wrong.” Schiff, Laureys and Owen cut lonely and isolated figures at academic conferences, desperately trying to explain their findings to their peers, who remained unconvinced, even antagonistic. The trio’s ideas were condemned as a waste of time.

Then came 2006. Owen and Laureys were trying to find a reliable way to communicate with patients in a vegetative state, including Gillian*. In July 2005, this 23-year-old had been crossing a road, chatting on her mobile phone. She was struck by two cars. Yet, though she had been diagnosed as vegetative, there was something about her that caught the attention of Martin Coleman of the University of Cambridge Impaired Consciousness Research Group, who submitted her for study by Owen.

Five months later, a strange stroke of serendipity allowed Gillian to unlock her box. The key arose from a systematic study Owen started with Laureys in 2005. They had asked healthy volunteers to imagine doing different things, such as singing songs or conjuring up the face of their mother. Then Owen had another idea. “I just had a hunch,” he says. “I asked a healthy control to imagine playing tennis. Then I asked her to imagine walking through the rooms of her house.” Imagining tennis activates part of the cortex, called the supplementary motor area, involved in the mental simulation of movements. But imagining walking around the house activates the parahippocampal gyrus in the core of the brain, the posterior parietal lobe, and the lateral premotor cortex. The two patterns of activity were as distinct as a ‘yes’ and a ‘no’. So, if people were asked to imagine tennis for ‘yes’ and walking around the house for ‘no’, they could answer questions via fMRI.

Gazing into Gillian’s ‘vegetative’ brain with the brain scanner, he asked her to imagine the same things - and saw strikingly similar activation patterns to the healthy volunteers. It was an electric moment. Owen could read her mind.

Gillian’s case, published in the journal Science in 2006, made front-page headlines around the world. The result provoked wonder and, of course, disbelief. “Broadly speaking, I received two types of email from my peers,” says Owen. “They either said ‘This is amazing - well done!’ or ‘How could you possibly say this woman is conscious?’”

As the old saw goes, extraordinary claims require extraordinary evidence. The sceptics countered that it was wrong to make these ‘radical inferences’ when there could be a more straightforward interpretation. Daniel Greenberg, a psychologist at the University of California, Los Angeles, suggested that “the brain activity was unconsciously triggered by the last word of the instructions, which always referred to the item to be imagined”. 

Parashkev Nachev, a neurologist now at University College London, says he objected to Owen’s 2006 paper not on grounds of implausibility or a flawed statistical analysis but because of “errors of inference”. Although a conscious brain, when imagining tennis, triggers a certain pattern of activation, it does not necessarily mean that the same pattern of activation signifies consciousness. The same brain area can be activated in many circumstances, Nachev says, with or without any conscious correlate. Moreover, he argues that Gillian was not really offered a true choice to think about playing tennis. Just as a lack of response could be because of an inability to respond or a decision not to cooperate, a direct response to a simple instruction could be a conscious decision or a reflex. Nachev says that he is weary of stating, as he has time and again to the media, that profound conceptual issues with the techniques used to redefine this penumbra of consciousness remain unresolved.

What is needed is less philosophising and more data, says Owen. A follow-up study published in 2010 by Owen, Laureys and colleagues tested 54 patients with a clinical diagnosis of being in a vegetative state or a minimally conscious state; five responded in the same way as Gillian. Four of them were supposedly in a vegetative state at admission. Owen, Schiff and Laureys have explored alternative explanations of what they observed and, for example, acknowledge that the brain areas they study when they interrogate patients can be activated in other ways. But the 2010 paper ruled out such automatic behaviours as an explanation, they say: the activations persist too long to signify anything other than intent. Owen is grateful to his critics. They spurred him on, for instance to develop a method for asking patients questions that only they would know how to answer. “You cannot communicate unconsciously - it is just not possible,” he says. “We have won that argument.” 

Since Owen’s 2006 Science paper, studies in Belgium, the UK, the USA and Canada suggest that a significant proportion of patients who were classified as vegetative in recent years have been misdiagnosed - Owen estimates perhaps as many as 20 per cent. Schiff, who weighs up the extent of misdiagnosis a different way, goes further. Based on recent studies, he says around 40 per cent of patients thought to be vegetative are, when examined more closely, partly aware. Among this group of supposedly vegetative patients are those who are revealed by scanners to be able to communicate and should be diagnosed as locked-in, if they are fully conscious, or minimally conscious, if their abilities wax and wane. But Schiff believes the remainder will have to be defined another way altogether, since being aware does not necessarily mean being able to use mental imagery. Nor does being aware enough to follow a command mean possessing the ability to communicate.

In 2009, Laureys’s team asked one of the original group of 54 patients that he and Owen had studied - patient 23 - a series of yes-or-no questions. It was the usual drill: imagine playing tennis for yes, navigating the house for no. The Liège patient, who had been in a vegetative state for five years, was able to answer five of six questions about his earlier life - and all of those were correct. Had he been on holiday to a certain place prior to his injury? Was such-and-such his father’s name? It was an exciting moment, said Laureys. “We were stunned,” adds Owen, who helped independently score the tests. “By showing us that he was conscious and aware, patient 23 moved himself from the ‘do not resuscitate’ category to the ‘not allowed to die’ category. Did we save his life? No. He saved his own life.”

§

“This is your big chance. Just do your best.” Owen gazed down at 39-year-old Scott Routley, lying on a gurney. Scott had studied physics at the University of Waterloo, Ontario, but his promising career in robotics came to an end when, aged 26, he collided with a police vehicle. Since that accident, on 20 December 1999, Scott had been diagnosed as being in a vegetative state by a well-seasoned neurologist, Bryan Young, and in 2012 his diagnosis was confirmed by Owen’s team, again using traditional methods.

As Owen talked to him, Scott’s mouth remained wide open, apparently unaware, the same way that he’d been in the 12 years since the accident. This encounter was filmed by a crew from the BBC. Reporter Fergus Walsh was there to witness the moment that Owen attempted to reach inside Scott’s mind. Owen admits now that he was sceptical that the scans would reveal anything at all.

The team scanned Scott several times. To their surprise, the pattern of brain activity showed Scott knew exactly who he was, where he was and that he was actively choosing to answer the team’s questions. “My heart stopped when we asked if, after 12 years, Scott was in pain,’’ Owen recalls. “Thankfully, the answer was no.”

Although Owen’s colleague, Lorina Naci, recounts how the experience of telling the Routley family the news was “quite emotional”, the BBC crew were surprised at their relative lack of celebrations. Not Owen. Scott’s parents, Jim and Anne, and his brother, Ritch, had always been convinced that he was conscious. They insisted he could lift a thumb or move his eyes to indicate as much, even though standard tests had always reached the same gloomy conclusion: Scott was unresponsive.

Scott had the same neurologist - Young - for more than a decade and had appeared vegetative in every assessment, including more than a dozen separate assessments by Owen’s own team. Perhaps the family discerned subtle signs of consciousness that were almost undetectable, even to the trained eye. Or perhaps they had deceived themselves, as many families do for comfort. “Either way, it was the word of the family against that of my team, and their word against an army of specialists over many years,” says Owen. Where the family saw a sign of cognition, the doctors saw only wishful thinking. “The scans showed that they were right, perhaps for the wrong reasons - we will never know - but Scott’s story teaches us the value of objective measures. And the need for a little humility.” 

There’s anecdotal evidence that when contact is re-established with the occupant of a living box they are understandably morose, even suicidal. They have been ground down by frustration at their utter powerlessness, over the months, even years, it can take to recognise their plight. Yet the human spirit is resilient, so much so that they can become accustomed to life in this twilight state. In a survey of patients with locked-in syndrome, Laureys has found that when a line of communication is set up, the majority become acclimatised to their situation, even content (again, these insights took some time to be accepted by the medical and scientific establishment - and even to be published in a scientific journal - reflecting the prevailing unease about the implications for hospitals and care homes).

The important question is detecting the extent to which such patients are conscious. Studies of large numbers of patients with brain injuries, and how they fare over the years, show that it makes a huge difference to the chance of recovery if a patient is minimally conscious rather than vegetative. The former have fragmentary understanding and awareness and may recover enough to return to work within a year or two. Yet there are still surprises, such as the case of New York fireman Don Herbert, who awoke after a decade from a minimally conscious state caused by a severe brain injury suffered while fighting a fire in 1995. In the past year, Schiff has recommended withdrawing care from a man who had lain in a coma for eight weeks after a cardiac arrest. “I was wrong,” he says. “This man is now back at work.” Schiff has used a technique called diffusion tensor imaging to show how a brain can rewire itself even decades after an injury.

It is important too not to lose sight of the impact on the families. Take Jamel, a 41-year-old construction worker left unconscious after a cardiac arrest. His family became convinced he had a glimmer of awareness and, fighting against the doctor’s stark diagnosis, spent almost 14,000 euros transporting him to Liège and Steven Laureys’s team for a detailed diagnosis. Sadly, their scans revealed no signs of consciousness. The family took the news badly. His sister Leila insists that Jamel can hear what they are saying. He was tired out by travel and surgery before he had his scan, she explains. The family has vowed to gather video evidence to show Laureys.A patient’s story

Parashkev Nachev has not changed his view since he first criticised Owen’s work and has spelt out the basis of his unease in a more detailed paper published in 2010. “For every relative of a living PVS [persistent vegetative state] patient given (probably false) hope, another is burdened with the guilt of having acquiesced in the withdrawal of treatment from someone who - he has been led to believe - may have been more alive than it seemed,” he says. “There are moral costs to false positives as well as to false negatives.” 

“I find the whole media circus surrounding the issue rather distasteful,” he told me. “The relatives of these patients are distressed enough as it is.”

Laureys, Owen and Schiff spend a great deal of time with the families and understand these sensitivities only too well. Owen counters that, from his years of experience dealing with the families, they are grateful that doctors and scientists take an interest and are doing everything that they can. “These patients have been shortchanged over the years,” he insists. A recent study showed that many people would grant more ‘moral rights’ to a corpse than to someone in a vegetative state. This surprising finding emerged when a team from the University of Maryland and Harvard University asked 201 people to read accounts of a car accident in which the protagonist lived, died or sank into a persistent vegetative state. The latter was regarded as worse than death.

Owen is adamant that doctors have a moral duty to provide a correct diagnosis, even if the results do cause guilt, unease or distress. “We must give every patient the best chance of an accurate diagnosis, so we can give them the appropriate care that goes along with that diagnosis.”

Under the umbrella classification of ‘vegetative’ lies a vast array of different brain injuries and, as a result, even some of the most vocal critics accept that some vegetative patients are not as diminished as traditional measures suggest. Lynne Turner-Stokes chairs a group for the Royal College of Physicians that is revising UK guidelines on ‘Prolonged Disorders of Consciousness’. She remains unconvinced that the exceptional cases identified by Owen, Laureys and Schiff are particularly common or that enough has been done to establish brain scanners as a standard tool for routine diagnosis, particularly when the cost and convenience of these methods are taken into account. When it comes to extending these tests to all patients in a vegetative states as standard practice, “the evidence is just not there yet,” she says.

Despite all the hard work done since the pioneering research of Plum and Jennett, there’s still a need for basic spadework to harmonise standards, tools and timescales of assessment for these patients, says Turner-Stokes. More has to be done to ensure that a vegetative patient in, say, the UK is assessed in the same way as one in the USA, and to close gaps in understanding of this very complex group of patients, notably how their brains can change and heal over time. But she stresses that she is simply being cautious, not sceptical, describing the work of Owen, Laureys and Schiff as “important and exciting”.

“We are only just beginning to scratch the surface,” she says. “But I have no doubt [these techniques] will have a place, eventually, in the evaluation of patients.” 

§

The art of mind reading is constantly being refined. Owen and Lorina Naci have come up with a more reliable way to communicate with patients by getting them to focus their attention while in the scanner. First, a yes/no question is asked, and then a recording is played of the word ‘yes’ repeated several times interspersed with distracting, random numbers, and a similar recording with ‘no’. The participant has to count how many of the correct answer they hear and ignore the incorrect answer. This mental effort (‘selective auditory attention’) shows up distinctively when Naci and Owen examine the brain scans, so they can decode the responses correctly based on activity changes within the attention network of the brain.

In follow-up studies using this method, Scott Routley showed he knew his own name, as distinct from another, and that he was in a hospital rather than elsewhere, indicating he possessed a higher level of self-awareness. “This not only further corroborated that he was, indeed, consciously aware but also revealed that he had far richer cognitive reserves than could be assumed based on his diagnosis as being vegetative,” says Owen. “He had autobiographical knowledge and awareness of his location in time and space.” 

Yet there are many issues left to resolve. After the initial diagnosis, relatively little effort is made to systematically explore brain function in these patients, says Schiff. There are also minimally conscious patients who may not be able to imagine tennis and so on, when a few exceptional vegetative patients can. Schiff’s team has encountered a patient who had remained vegetative, or in a very low-level minimally conscious state, for more than one year, who had not responded to fMRI, but later regained the ability to make conversation (though, of course, whether they had truly been vegetative is another question). And a 2014 study by Laureys’s group suggests that PET could be better than fMRI at predicting the likelihood that a patient may wake up. It also estimates that the standard diagnostic procedure misses signs of responsiveness in around a third of patients classed as minimally conscious - which Owen notes is consistent with his and Schiff’s findings.

Indeed, other limitations are caused by the use of medication during trials or the huge diversity of the patients that are usually collapsed into groups (to spare doctors from carrying out the same procedures on the same patient again and again). When it comes to younger patients, there is a limit to the number of PET scans they can have in a given period because a radioactive tracer has to be injected into the body. fMRI is also hindered by the fact that huge, multimillion-dollar imaging machines - confining and magnetic - are unsuitable for patients whose bodies are affected by spasticity or have been rebuilt with screws, plates, pins and other metal.

But more convenient alternatives are in development. Laureys is studying pupil dilation, which is linked with thought (the wider the pupil, the higher a patient’s emotional arousal, while more subtle dilations have been linked to mental functions such as decision making). Another method implants fine electrodes in the hand of a patient to measure ‘sub-threshold’ muscle activity triggered when they are asked to move. 

Perhaps the most promising alternative is electroencephalography (EEG), which detects crackles of electrical activity in the brain through electrodes attached to the scalp. This is cheap, relatively portable and fast (with milliseconds of lag, compared with 8 seconds for fMRI), meaning that a research team can ask up to 200 questions in 30 minutes. This method can also cope with patients who twitch and move, or who have been reconstructed with implants. “This is a vulnerable patient population, and moving them is never easy,” says Owen, whose team have equipped a jeep. “We pack our gear in our ‘EEJeep’ and visit them instead.”

A bedside EEG consciousness detector has been tested in Addenbrooke’s Hospital, Cambridge, and in the University Hospital of Liège. It looks promising but doubts remain, even among the believers, with Schiff’s team sceptical whether one particular EEG methodology used with the detector really works. “One has to be careful of the dead salmon effect,” admits Laureys, referring to an apparently frivolous study of a deceased fish that made a serious point about the limitations of fMRI. The methodology struggled to distinguish real brain activity from background ‘noise’, suggesting that the dead Atlantic salmon that had been put in the scanner was actually thinking. “We don’t want to get excited about dead fish,” says Laureys, “but, on other hand, we do not want to be so conservative and demanding of statistics that we miss things.” The dispute has caused some tensions - though united against their critics, the groups are still competitive - but Schiff stresses that it is all for the greater good: “We are all funded on [a] multinational grant to cross-validate and share methods and agree that they work. That is why we pushed our criticisms hard and in the end it was better for everybody.”

§

Today it is normal to think of the transition between life and death as a question of ‘how the brain is’ rather than ‘how the heart is’. A patient in a persistent vegetative state still has a functioning brain stem and can breathe unaided. They may possess some degree of consciousness and have a slim chance of recovering. By comparison, a PET scan of a brain-dead person reveals a black void within the skull, a barren neural landscape with no chance of sparking back into activity again: their body cannot survive without artificial help.

Though they are becoming rarer, there are still chilling stories that apparently blur the boundaries between life and death. In October 2009, Colleen Burns was admitted to St Joseph’s Hospital Health Center in New York after a drug overdose. Doctors pronounced the 39-year-old dead while she was in a drug-induced coma. Fortunately for Burns, she woke minutes before the first incision was to be made to harvest her organs. “Remember that not a single patient who showed clinical criteria of brain death has ever recovered consciousness,” says Laureys. “Whenever a brain-dead patient does manage this feat, it turns out they were not properly examined and the criteria for brain death not properly applied.”

Schiff believes that a combination of devices, drugs and cell therapies, laying the foundations for a new generation of diagnostics and treatments, will illuminate the penumbra between conscious and unconscious. “We’re not quite there yet,” he stresses. Much of the work to date has demonstrated the value of brain scans on populations of patients but, ultimately, they need dependable methods that will work on a patient-by-patient basis, which means precise definitions and standards. They need ways to deal with false positives and false negatives, and to make sense of the impact of a bewildering array of brain injuries, from oxygen starvation to blows and bullet wounds. “We are going to have to do some amazing small-scale studies to show what is possible in one or two subjects before everyone gets simple things done that can help them today,” Schiff says. Eventually, he believes there will be a “cultural shift”. Laureys thinks we may need to start with the language used to describe these patients - he wants replace the loaded term ‘vegetative’ with the neutral ‘unresponsive wakefulness’.

Despite the scepticism, the difficulties in dealing with such diverse groups of patients, and the challenges of standardising diagnosis, the research is moving forward. It is already making a difference, enabling a few patients to tell their doctors whether they need pain relief. 

Back on Skype, Owen smiles, considering whether to tell me what he is planning next. Owen’s partner, Jessica Grahn, also a neuroscientist, became pregnant at the start of 2013. What happens when consciousness winks on in the developing brain?

He emails me a video of their unborn child, a montage of fMRI slices through their baby’s head, as it twists and turns in Jessica’s womb. “My colleagues have been doing fMRI on my wife’s tummy every week for a few weeks now to see if we can activate the fetus’s brain,” he writes. “It is AMAZING.”  

Scott Routley died in September 2013 with his family by his side.

Adrian Owen’s friend Anne remains in a vegetative state.

Adrian Owen and Jessica Grahn’s baby boy, Jackson, was born on 9 October 2013.

* Some names have been changed to protect identities.

This article was commissioned by Mosaic, a new digital publication from the Wellcome Trust dedicated to exploring all strands of the science of life. It is reproduced under a Creative Commons Attribution 4.0 International Licence.

MILES COLE FOR NEW STATESMAN
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Is it Ruth Davidson's destiny to save the Union?

Ruth Davidson is a Christian, gay, kick-boxing army reservist who made a passionate case for the EU and has transformed the fortunes of the Tories in Scotland.

In the end it made no difference, but during the EU referendum campaign Ruth Davidson achieved something that nobody else did: she made the case for Remain sound thrillingly righteous. In a live, televised BBC debate at Wembley Arena in London, she denounced the “lies” of the Leave campaign, turning to the crowd to declare, twice: “You deserve the truth!” Funny, fervent and pugnacious, Davidson pounced on the bluff assertions of Boris Johnson with gusto, a terrier savaging a shaggy dog. As she departed the podium, flashing a light-bulb grin, she left a question hanging in the air: how far can Ruth Davidson go?

On the face of it, it was a risk for the ­Remain campaign to send the leader of the Scottish Conservatives to Wembley, when most of its persuadable voters lived in England. Yet, according to Andrew Cooper, David Cameron’s pollster and an influential Remain strategist, “Ruth’s name was inked in from the beginning.” After the debate, nobody called this confidence misplaced. Davidson was acclaimed as the star of the night. English observers began to appraise her as a major player in national politics, even as a possible future prime minister.

The EU debate was, for Davidson and for Scots, the least energetically contested of four recent contests, following the Scottish independence referendum in 2014, the general election in 2015 and the Scottish Parliament elections in May 2016. In the last one, Davidson led her party to second place, overtaking Labour, and the Conservatives became the main opposition to Nicola Sturgeon’s Scottish Nationalists. It was their best result in nearly 60 years and evidence of an astonishing turnaround.

When Davidson was elected leader in 2011, it was like being declared the mayor of a ghost town. Her party’s core voters had long fled, first to Labour and then to the SNP. Margaret Thatcher and successive national Tory leaders had made it almost impossible for Scots to admit to voting Conservative, or even to being friends with anyone who did. It wasn’t just that the Tories were poisonous to the touch; they were on the verge of irrelevance. They held 15 out of the 129 seats at Holyrood. They barely mattered.

They matter now. The stigma of voting Tory has not been entirely erased, but the Conservative brand has been saved, or perhaps subsumed by its Scottish leader’s personal brand. On the ballot paper in May, voters were invited to put a cross next to the slogan “Ruth Davidson for a strong opposition”; party activists knocking on doors introduced themselves as being from “Team Ruth”. A recent poll found that Davidson was the most popular politician in Scotland, surpassing Sturgeon.

Ruth Davidson has been a politician for just five years. If you need reminding of how hard it is, even if you are clever and able, to become a high-level political performer on half a decade’s experience, recall the defining moments of a few Labour MPs of the 2010 generation: Liz Kendall’s flameout, Chuka Umunna’s failure to launch, Owen Smith’s bellyflop. David Cameron’s rise might seem to have been comparably quick, but he had been working in Westminster politics, on and off, for 13 years before he ­became an MP. Three years before being elected leader of the Scottish Tories, Davidson hadn’t even joined a political party.

Davidson may be the most gifted politician in Britain. “She’s a natural, and they are very rare in politics,” Cooper told me. The question for her is whether she will ever convert talent into power.

 

*****

In August, I went to see Davidson speak in Belfast at an event organised by Amnesty International on behalf of the campaign for gay marriage in Northern Ireland. She made a case for equal marriage that was also a case for the institution of marriage. “More than 40 years married and my parents still love each other – and I look at what they have and I want that, too, and I want it to be recognised in the same way,” she said.

She paused to note that the passage was taken from an address that she made at Holyrood during the first reading of Scotland’s equal marriage bill in 2013: “I’ll be honest. I was absolutely bricking it.”

Davidson met her partner, Jen Wilson, in 2014. The couple got engaged this year on holiday in Paris, just after the May election campaign. Wilson, who is 34 and from County Wexford, Ireland, works in the charity sector. In 2015, she appeared with Davidson in a party political broadcast, which showed the couple strolling along Elie Harbour, Fife, and taking selfies with Davidson’s parents. It wasn’t a big deal and yet, at the same time, it felt significant. As Davidson noted in her speech, homosexuality was still a prosecutable offence in Scotland in the year she was born (it was not decriminalised north of the border until 1980).

After the event, I met her for a drink with members of her team at the bar of her hotel. She had returned to Edinburgh from a holiday in Spain in the early hours of that morning, shortly before boarding a plane to Belfast for a full day of engagements. Yet she bristled with energy, giving the illusion of movement even when she was sitting still, her attention distributed between emails on her phone, the conversation at the table and the level of everyone’s drinks. She had enjoyed the event, she said, although she had been hoping for more argument.

In September, we met again for a longer conversation in her small office at Holyrood. In person, she is friendly in a businesslike way, mentally fast (often starting her response before the question is finished) and generous with her answers. As she talks, her eyes fix you in your seat. “Ruth is a brilliant reader of people, including our opponents, and spots weaknesses very early,” her colleague Adam Tomkins told me. “She can see through me. I would hate to play poker with her.”

Before our meeting, I watched First Minister’s Questions, the first after the summer recess. The atmosphere in the chamber at Holyrood is very different from that in the Commons: quieter, less theatrical. The leaders of the main parties are not cheered to their seat. Sturgeon, dressed in black, walked to her desk at the front of the hall, unacknowledged by her colleagues, as a cabinet secretary answered a question on national parks. Davidson entered shortly afterwards, in a violently pink jacket that contrasted vividly with the muted tones preferred by most MSPs.

In the chamber, Davidson often holds her own against the First Minister. The two have contrasting styles: Sturgeon poised and coolly effective, Davidson a study in controlled fury. “Ruth has a real aggression to her,” says the journalist Kenny Farquharson, a columnist for the Times in Scotland. “She’s always looking for the next fight.”

 

*****

Ruth Elizabeth Davidson was born at the Simpson Memorial Maternity Pavilion in Edinburgh in 1978, the second of two daughters to Douglas and Elizabeth Davidson. Her family lived in Selkirk, where her father worked at the wool mill. This was Douglas’s second career: his first had been as a professional footballer, for Partick Thistle and Selkirk FC. The Davidsons moved to Fife when Ruth was a child, after the mill closed. Her parents were Tory voters, without being especially political.

When Ruth Davidson was five years old, she was run over by a truck near her home and nearly killed. The accident shattered her leg, fractured her pelvis and severed her femoral artery, leading to a huge loss of blood. In interviews, she makes quick work of what other politicians might be tempted to craft into a narrative turning point. “My legs are still a bit squint . . . but it has never really stopped me from doing anything,” she told the Scotsman in 2012.

Her family was Presbyterian, in the Church of Scotland, a more austere and morally fiery tradition than Anglicanism. (A Scottish journalist remarked to me, “To us, Anglicanism is Christianity with all the fibre removed.”) Davidson is a practising Christian. Her piety does not extend to abstention from alcohol or profanity – she is a world-class swearer – but it is manifest in her moral muscularity, preacher-like cadences and horror of malingering.

In Fife, Davidson attended Buckhaven High School, a large comprehensive with a working-class intake. She is often referred to as working class, which isn’t quite right. Her mother and father were working-class Glaswegians. Her mother left school at 15, her father at 16. Douglas grew up on an estate in Castlemilk, a district then infamous for its deprivation and crime. He was one of the few Protestants in a solidly Catholic community, during a time of deep divisions.

The Davidsons, however, were upwardly mobile. Douglas had been a manager at the mill in Selkirk and then ran a whisky distillery on the Isle of Arran. The children had the importance of effort and self-improvement drummed into them. Ruth has recalled getting a school report that gave her a 1 for results in science – the best possible mark – and a 2 for effort. “I got a mini-bollocking for that. My mum would have been much happier if it had been the other way round.” Both children attended university (Ruth’s sister is now a doctor).

Davidson did well at school and excelled at sport. She played squash for her county and tennis to a level at which she can teach it. In adulthood, she took up kick-boxing, condemning herself to be forever tagged as a “kick-boxing lesbian” in the British press. Sport has been central in her life, not so much a leisure activity as a method of striving for new goals.

After graduating from Edinburgh University, where she studied English literature and took part in debating competitions, ­Davidson moved to Glasgow and started a career in journalism. In 2002 she joined BBC Scotland, becoming a radio presenter on a drive-time show, reporting on gifted pets one minute and traffic disasters the next. By all accounts, she was excellent: fluent, well prepared, interested in whomever she was talking to. Her producer Pat Stevenson remembers her as “a fantastic interviewer, incisive and forensic, able to spot bullshit a mile off. And she was fun.” Her abiding image of Davidson at the microphone is of a head thrown back in laughter.

Stevenson recalls being vaguely aware that Davidson held right-of-centre views, though these were less of a talking point with her BBC colleagues than her Christianity, or, even more so, her weekends spent deep in a forest, being shouted at while trying to read a map. Davidson served as a signaller in the Territorial Army for three years from 2003 and trained to be an officer. “It was very tough,” says Steve Bargeton, who oversaw the officers’ course. “Most fail or drop out, but Ruth flew through. She had tremendous character.” Davidson won a place at Sandhurst but broke her back during a training exercise, forcing her to end her military career.

She soon set herself a new goal: to be elected to parliament by the time she was 40. In 2009, she left the BBC and joined the Tory party. Davidson has attributed her career change to David Cameron’s call, after the MPs’ expenses scandal, for people who had never been political to get involved, but it is likely she had already decided that politics was the next hill to climb. Either way, she quickly acquired influential sponsors in Edinburgh and London. By the 2010 election, she was head of the private office of Annabel Goldie, the then leader of the Scottish Tories. She stood for an unwinnable Commons seat in Glasgow, twice, both times winning barely 5 per cent of the vote.

Even as the elections to Holyrood came around in May 2011, she was not expected to make it to parliament. She was second on Glasgow’s regional list, which all but ruled her out. A couple of months before the vote, however, the candidate at the top of the list was removed following allegations of past financial problems. The Conservative Party chairman promptly promoted Davidson, who was elected to Holyrood (she won a constituency seat of her own this year in Edinburgh, where she now lives).

In the 2011 election, the SNP, under Alex Salmond, won an unprecedented overall majority in Holyrood. This success transformed the politics of Scotland, and thus that of the UK. Labour’s grip on the votes of working-class Scots was broken. The Conservative Party, already a corpse, failed to twitch. It at once became clear that Salmond had won a mandate for a referendum on independence and that this would be the defining question of Scottish politics until it was resolved.

On the Monday after the election, Annabel Goldie announced that she was resigning. Four days after her election to the Scottish Parliament, Davidson began to consider a run at the leadership of her party. She was encouraged by senior figures, including David Mundell (then a Scotland Office minister, now the Scottish party’s sole MP in Westminster) and David Cameron. In her way stood the Scottish Tories’ deputy leader, Murdo Fraser, an Edinburgh-based lawyer who had been a Conservative activist for a quarter of a century. It was, by common consent, his turn.

Fraser, sensing a threat, committed to an act of excessive radicalism that proved to be his undoing: he proposed that the party ditch the name “Conservative” and break entirely from its southern counterpart. He argued that this measure (Alex Massie, writing in the Spectator, called it the euthanasia option) was the only way to move on from the past and compete with the SNP as a truly Scottish party. He did not recommend a new name; mooted alternatives included the Scottish Reform Party, the Caledonians and Scotland First.

Fraser’s gambit propelled Davidson into the race. She felt that his proposal would unmoor the Scottish Conservatives from their purpose, and also that it was politically naive, as there was little chance that voters would not realise that this was the same party in different clothes. In tactical terms, Fraser had opened up space for a candidate to run on preserving the status quo, rarely an unpopular position among Tories. For his challenger, it was a ripe alignment of conviction and opportunity, a ball bouncing into the perfect position for a killer forehand. Davidson declared on 4 September 2011 and won the final round against Fraser, 55 per cent to 45 per cent. She was 32.

 

****

It is easy to underestimate how much politics, in opposition, is simply about getting noticed. When Davidson became leader, Scottish politics was a (rather one-sided) battle between the SNP and Labour. She needed to fight her way to centre stage and into the calculations of voters – there wasn’t much point repositioning the Tory brand if nobody was watching. As Andrew Cooper put it to me, “You didn’t get to the toxic problem until you dealt with the irrelevant problem.”

Davidson excels at getting noticed. She has – even if she would not appreciate the comparison – a Donald Trump-like understanding of how to get and keep attention. She is at home on social media, something that is true of all the Scottish party leaders, though Davidson’s tweets are the most fearless and funny. She is also an artist of the photo opportunity: here she is in a pink scarf, bestriding the gun of a tank, a Union flag fluttering in the background; playing the bagpipes, or being played by them, eyes popping out of her head; smashing a football into the back of the net.

Such photos do more than get attention. They reinforce the sense of a person unintimidated by the rules of political protocol; indeed, of someone who scorns limitations. There is something almost cartoonish about Davidson’s public profile: the big eyes, the flashing grin, the unstoppable, barrelling walk. In debates, as she winds up to a clinching point, you can, if you half close your eyes, see her swinging her arm through a hundred revolutions before extending it across the stage to smack an opponent. She is one of us, and not like us at all. Flattened by a truck, she gets up and walks away.

Davidson’s willingness to play the fool wouldn’t work if she was not able to convey seriousness at the same time. The leadership race set the template for her political profile as an untraditional traditionalist. Davidson doesn’t look or talk like a typical Tory, but her ideological touchstones are profoundly Conservative. She is a British patriot, a churchgoer, a passionate supporter of the armed forces, an advocate for marriage, a believer in self-reliance. On becoming leader, she set about reviving a type of blue-collar Conservatism not seen since the 1980s. The former Scottish Tory MP Sir Teddy Taylor coined the expression “tenement Tories”: working-class voters with conservative instincts, sceptical of high taxes, patriotic but not nationalist. Davidson, the daughter of tenement Tories, is able to pitch herself as one of them.

To do so has required performing a balancing act with respect to her party in Westminster. She admired Cameron and, politically speaking, was in his debt. Her leadership is staked on the unity of the Scottish and English branches of the party. Yet she has managed, somehow, to position herself against the party’s privileged English elite – the “private-school boys”. Her evident animus against Boris Johnson is both strategic and personal. During the EU campaign, as the polls tightened, she asked Downing Street if it wanted her to go on a “suicide mission” against Johnson, a senior aide to the former prime minister says.

 

****

In Ruth Davidson’s first year as leader, her inexperience showed. She made a prolonged and embarrassing climbdown from a foolhardy promise, made during the leadership campaign, to draw a “line in the sand” against further devolution. Meanwhile, Alex Salmond, a skilled and pitiless debater, successfully patronised her every week at First Minister’s Questions. An impression that she had been promoted prematurely was discreetly given credence by members of her own party (most Scottish Tory MSPs had voted for Fraser).

Davidson was learning not only how to be a leader in public, but how to manage an organisation, a skill for which journalism had not prepared her. A rule change that came into effect when she took over gave her far-reaching powers over the party. As she says, she suddenly found herself responsible for MSPs, staff and activists, but with “no idea how to manage”. She fell back on her training in the Territorial Army. “I had to apply what I learned about leadership in the British army. The toolkit I used was from officer training: how to identify problems, make decisions, bring people with you.”

At Wembley this summer, debating national security, Davidson remarked icily, “I think I’m the only one on this panel who’s ever worn the Queen’s uniform.” Her TA training provides her with a rhetorical trump card and legitimises photo opportunities on tanks, but it does more for her than that. Military metaphors pervade her thinking and fire her imagination. One of her favourite books is Defeat into Victory, an account of the Allied forces campaign in Burma in the Second World War, by William Slim, a British field marshal. “It is the best examination of leadership you’ll ever find,” she told me, and then related, excitedly, an encounter she once had with a Second World War veteran who had witnessed Slim addressing his troops.

After getting heard, Davidson’s most urgent task as leader was to overhaul a demoralised and moribund institution. She focused on candidate recruitment – looking for better signallers. “I wanted to rebuild around the message carriers,” Davidson told me. After their run of bad elections, the Tories had stopped trying to pick winners: “They were asking good, hard-working foot soldiers to stand, just to get a name on the ballot.” Long-standing members would be asked to put their name down and reassured that they wouldn’t have to do anything, and so, by and large, they didn’t.

Davidson put together a new candidates’ board: a former human resources director for Royal Mail, a QC who had been a world champion debater, an expert in corporate leadership. She designed a series of tests based on the officer assessment test that she underwent before Sandhurst (“minus the assault course and press-ups”).

Applicants were asked to sit around a ­table with three others, each with a piece of paper in front of them. When they turned it over, they discovered who they were and what they needed to solve. A new policy was about to affect voters in four neighbouring constituencies, but in different ways: it would be detrimental to those in the first constituency, neutral for those in the second and third and advantageous for those in the fourth. Each candidate represented a different constituency. How would they agree a position?

“It was about making people interact in a way they hadn’t before,” Davidson said. “I made every sitting MSP go through it, including myself.” Her aim was to assemble a team of experts, from business, law, the armed forces and the third sector.

Among her recruits was Adam Tomkins, a professor of public law at Glasgow University, now an MSP and one of Davidson’s closest allies. “By late 2011, it was clear the referendum was coming. I wasn’t involved in party politics but I was a strong believer in the Union and I knew I wanted to do something. I wasn’t a Tory, though. In fact, I had been pretty hostile to them.” He offered his expertise to Labour but came away from meetings with the party’s leaders depressed by their tribalism. Davidson was different: intellectually curious, open-minded, eager to take advice. In 2013, she formally asked him to help the Tories formulate a constitutional policy and he agreed. On New Year’s Day 2014, he joined the Conservatives.

The Scottish independence referendum was the making of Davidson as a national leader, as it was of Nicola Sturgeon, who escaped Salmond’s shadow to become a force in her own right. In TV debates during the campaign, Davidson was the most compelling defender of the Union, capable of winning sympathy for even its most unpopular ingredients. “Ruth emerged as someone who could defend Trident and get applause,” says the journalist David Torrance.

After the referendum in September 2014, she once again had to battle for attention. She needed to convince the media that the Conservatives might yet play a big role at Holyrood – that she was more than an amusing sideshow. The referendum had shown her how decayed Labour’s relationship was with its own voters, and this gave her renewed impetus. She also grasped that, far from enabling Scottish politics to move on from independence, the referendum was still having the opposite effect.

In September 2015 the new Scottish Labour leader, Kezia Dugdale, announced that Labour MSPs would have a free vote on independence in the event of another referendum. In April 2016, she committed to an increase in the top rate of income tax. Together, the two moves were an attempt to move past the issue of independence. “I want people who voted both Yes and No to see that the Labour Party is the vehicle for progressive change in this country,” she said. Yet Dugdale misjudged the relentlessly centrifugal dynamic of Scottish politics after the referendum. Every policy position – from tax rates to tuition fees – returned to the question of what it signalled about Scotland’s relationship with England.

Davidson understood that if Labour was softening its position on the Union, she need only harden and amplify hers. At this year’s Holyrood election, she presented herself not as an alternative first minister, but as the most forceful voice of opposition to Sturgeon. In the campaign debates, she demonstrated it. By doing so, she was able to convince enough pro-Union Labour voters to defect to achieve second place.

For someone who is still relatively new to politics, Davidson has well-tuned strategic instincts. When I asked Tomkins what she excels at, he said: “Her framework is politics, not policy as such. She is brilliant at tactics, messaging, strategy.”

Davidson seems to have developed a serious interest in politics only as an adult, and then only because she thought that it presented a worthy challenge for her abilities (by contrast, most of the leading Scottish Nationalists joined the SNP before they were 18). A little like David Cameron, she just thought that she would be good at it. When I asked her to name her political heroes, or politicians whom she particularly admired, she struggled to come up with any from real life, naming Thomas More in A Man for All Seasons, Shakespeare’s Henry V and Atticus Finch in To Kill a Mockingbird. She wasn’t being coy – it’s just that, like most people, she has never looked to politics for role models. With prompting, she eventually named Peter Mandelson, for his part in making the Labour Party electable again, and William Hague, for his work on women’s rights while foreign secretary.

This lack of political nerdery is part of what makes her able to connect so directly with voters, but it is also a limitation. A consistent criticism of Davidson, even among those who admire her, is that she is not interested in policy, or at least that she does not have a set of distinctive policy ideas. This isn’t quite fair – she has published a paper on education and successfully focused attention on the attainment gap between poor and middle-class students. But she has not yet committed to a detailed alternative (a school vouchers policy was raised and then quietly dropped). Other than “maintain the Union”, it is difficult to know what a Davidson-led government would do.

The word everyone uses about her is “authentic”; like Sturgeon, she projects comfort in her own skin. But in a sense Davidson is a lucky politician, as well as a precociously accomplished one. It is much easier to be yourself in politics when what you believe matches so neatly with what you need to do to win. Her decision to present herself in the Holyrood elections as an effective opponent, rather than an alternative first minister, was tactically smart, but it raised a larger question. As one observer put it to me, “We know what she’s against. But what is Ruth Davidson for?”

 

*****

On 12 July, the day after it became clear that Theresa May would be the new Conservative leader, Davidson spoke at a Press Gallery lunch in Westminster and delivered what was, in essence, a stand-up comedy set. Even by her standards, it was indiscreet. On the difference between the Tories’ truncated leadership contest and Labour’s lengthy deliberation, she remarked: “Labour’s still fumbling with its flies while the Tories are enjoying a post-coital cigarette after withdrawing our massive Johnson.”

It is difficult to say it without sounding like a stick in the mud, but to me this routine felt misjudged. Political leaders can be funny but not that funny – not without compromising our sense of their stability. Nor was it wise to be so rude. Johnson is in the same party as she is, after all, and may yet become leader (nobody, possibly least of all Davidson, is sure what she would have done had Johnson succeeded Cameron). Like many funny people, Davidson metabolises anger into humour and I suspect that, after Brexit, her anger was surging.

It wasn’t just that she thought the decision was profoundly wrong, or that she was contemptuous of Leave’s tactics. It was also that she was being forced to rethink her future. If Remain had won, the chance of another independence referendum may well have receded, allowing Scottish politics to normalise. The SNP would have found it harder to present itself as being simultaneously in office and opposition. Davidson could have embarked on the last stage of the Scottish Tory recovery: making it an alternative government. She might even have considered the option of taking a Westminster seat – after which, who knows?

The vote in favour of Brexit knocked all of this on the head. It put independence firmly back on the agenda. Instead of either disappearing or becoming imminent, the prospect of a second referendum will squat in the middle distance of Scottish politics for years to come. In a sense, this is convenient for Davidson, because she will remain the strongest voice on one side of the only real issue in town. She can make further inroads into the heartlands of a Labour Party that, at a UK-wide level, is strangling itself to death, while picking up SNP voters who lose patience with Sturgeon when she blames every problem with the National Health Service or schools on London.

Theresa May is not nearly so good a bogeyman for Sturgeon as Cameron was. Davidson gets on well with her despite some stylistic differences. Both are observant Christians and care about their duties to the Tory flock. When May came to Scotland to meet Sturgeon in the week after she became Prime Minister, she also attended a meeting of local Conservative members, which Davidson greatly appreciated (Cameron wouldn’t have done such a thing). Davidson has not, as May has, marinated for years in local Tory association meetings but she takes her responsibility to the membership seriously, in the manner of a general concerned with the troops’ morale.

Yet a referendum that is always two years away is one that she can never win or lose. It is hard for her to come up with distinctive ideas when there is little point devoting effort to envisioning a policy agenda that will be distorted through the prism of independence. Given the odds that she overcame to take her party to where it is now, nobody should dismiss the chance that she might one day become first minister. But Scottish politics is defined by long periods of single-party hegemony and the SNP under Sturgeon may well have just started its turn.

Then there is the option of running for a (Scottish) seat in Westminster. Davidson says that she has no interest in swapping Edinburgh for London, either politically or personally, and I believe her. Yet there may come a point at which she is forced to confront the possibility that this is the only way to escape a career in permanent opposition. She might also come to see it as the best way to defend the Union. Sturgeon has suggested that there is no longer any such thing as British politics. What a rebuke it could be to that idea to have one of Scotland’s most popular politicians in the cabinet at Westminster, or, indeed, in 10 Downing Street (a possibility hardly less plausible than Davidson’s elevation to first minister). On the other hand, Davidson may leave politics altogether. She was strikingly keen to emphasise, in our interview, that at some point she will seek an entirely new challenge.

We like to think that the best politicians will somehow find their way to power – that talent will rise to its appropriate level. But Davidson has only two paths to high office open to her: becoming first minister, or quitting Edinburgh for Westminster. Both are exceedingly steep. If she cannot or will not take either, in decades to come she may be remembered as we now recall her performance at Wembley: a firework show, lighting up the landscape without changing it.

Ian Leslie’s “Curious: the Desire to Know and Why Your Future Depends on It” is published by Quercus. Twitter: @mrianleslie

Ian Leslie is a writer, author of CURIOUS: The Desire to Know and Why Your Future Depends On It, and writer/presenter of BBC R4's Before They Were Famous.

This article first appeared in the 29 September 2016 issue of the New Statesman, May’s new Tories