An adventure of life and science

A few years ago I was shopping in Sainsbury's, and as I bagged up the groceries, the rather cheerful check-out assistant asked what I did for a living. After my ten second tutorial on cognitive neuroscience, he replied, 'Ah yes – I saw all about this on TV – the guy who uses a brain scanner to see if a patient in a coma is still really there.' Into the Grey Zone is Adrian Owen's account of the 20 years he has spent using brain imaging to show how some patients, apparently in deep coma, are aware of their surroundings, can understand what is said, can answer questions and enjoy the plot of an Alfred Hitchcock movie. It is a page-turning story of the research that has made him a household (or at least check-out) name.

In part, Into the Grey Zone is a personal story of the adventure of life and science, told with a zest that bubbles off the page. The scientific story begins with experiments in the late 1990s, scanning apparently vegetative patients to find that their brains still 'recognised' the faces of loved ones, or the meaning of words. Could it be that, at least in some cases, patients were still fully conscious, aware of their surroundings, understanding conversations, and simply unable to move or communicate in any way? To answer the question, the experiments moved on to using brain imaging for actual communication. The patient might be told: 'We will ask you some questions. If the answer is yes, imagine you are playing tennis. If the answer is no, imagine you are walking around your house.' Brain imaging can tell the difference between what happens when a person imagines playing tennis versus imagining walking round the home… might apparently vegetative patients be able to use this method to answer questions put to them?

Incredibly, sometimes, it worked… using brain imaging, the group had found a way to unlock the trap of a conscious mind in an uncontrollable body. Over two decades, many nuances have emerged. Consciousness and ability to communicate are certainly not present in all patients – probably, indeed, in a minority. For this minority, however, the importance of the findings is staggering. The methods have been developed to show that a patient can follow the plot of a movie, showing a normal, complex response to moments of suspense. They can be used to ask the deepest questions, sometimes showing that a trapped patient can still say that they are happy.  They can also sometimes predict who it is that will finally come out of their coma and return to their families and friends.

This is a deeply moving book, told through the stories of the real patients, their families, their histories, their successes and failures. It is also a personal story of a young (at first!) scientist developing a fascinating new strand of research, the collaborators ('a gangly Indian neurointensivist with impeccable manners'), the Cambridge lifestyle ('Waiting patiently for outcomes left plenty of time for speculation and croquet'), the academic disputes, the early girlfriend who herself became vegetative and perhaps launched the entire research programme. It is a book to be read at a single sitting, mixing tragedies with hope. In the words of the first ever patient, Kate – one of those who finally came back from the grey zone: 'I was unresponsive and looked hopeless, but the scans showed people I was in there.  It was like magic. It found me.'

- Professor John Duncan is at the MRC Cognition and Brain Sciences Unit, University of Cambridge.

Into the Grey Zone: A Neuroscientist Explores the Border Between Life and Death by Adrian Owen is published by Guardian Faber (£16.99)

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Image above by Ana Rosa Louis.

Read our interview with Adrian, and find out more about him and his work in our archive.

What follows is an exclusive extract, courtesy of Guardian Faber.

Tennis, anyone?

We were ready to test our new fMRI task … After years of preparation, the thrill of knowing that we could do it – at least in principle – combined with the uncertainty of knowing how long we'd have to wait for the right patient to come along, was spellbinding.

What happened next is the stuff of scientific fairy tales. Carol, a married twenty-three-year-old, was referred to us by her doctor from a town near Cambridge. In July of 2005, Carol had been hit by two cars while crossing a busy road. She suffered a traumatic brain injury and was admitted to a nearby hospital. A CT scan revealed brain swelling and substantial damage to her frontal lobes. …

When I first met Carol, I was shocked by her condition. It's never easy meeting victims of a traumatic brain injury, but Carol's accident was still relatively recent and she looked awful. The decompressive craniectomy she had required, lifesaving as it may be, is also visually arresting. Patients such as Carol look as if part of their head has sunken in; a shallow well of thin skin rests lightly on the surface of the brain. I have had to prepare many students for this sight before they met their first trauma victim, and I suspect many of them never fully recover from it. It was hard not to feel immensely sad for Carol. Whatever happened, even if she made a complete recovery, her life would never again be the same. In a single, deadly instant, two cars and a moment's distraction had redefined the rest of her life. She was a shocking reminder of how vulnerable we are and how quickly our lives can change.

Carol had lain in a hospital bed for months without responding or showing the slightest sign of inner awareness. Compared to the patients we were now seeing regularly, she was unremarkable. She had repeatedly been tested by experienced neurologists and diagnosed as vegetative. We didn't select her for any reason other than that she was the next in a line of patients who fulfilled all the requirements to go in the fMRI scanner.

We were starting to get some recognition for what we were doing – the publicity surrounding Kate's case had helped to generate interest from around the UK, and the scientific papers that we had published describing Kate, Debbie, and Kevin had attracted the attention of several other hospitals, which referred a regular flow of patients, sometimes one or two a month, who would travel to Cambridge by ambulance to be scanned by our team. But we were finally ready for something completely different. We were going to ask Carol to dosomething. This required that we give her instructions – tell her what we would like her to do and when. Until that point, we had simply done things to patients; showed them faces, played them words or whole sentences. All they had to do was just lie there and (we hoped) absorb what we were trying to convey. But we wanted Carol to follow a command, to activate her brain in certain ways in response to our instructions.

We asked Carol to imagine playing tennis; we asked her to think about swinging her arm back and forth, a volley here, a drop shot there, and perhaps an occasional smash. We repeated these instructions five times. We wanted her to imagine that she was playing tennis as if her life depended on it. As though she were playing match point, centre court, in the finals at Wimbledon!

As the instructions were read to her one last time over the intercom, the atmosphere in the control room was tense. Did this make any sense? In one way it felt like total madness. We were asking a vegetative-state patient to imagine that she was playing a game of tennis! But inside the scanner, something amazing was happening. Whenever we asked Carol to imagine playing tennis, she would activate her premotor cortex just like healthy volunteers! When we asked her to stop – to just relax and "empty her mind" – the activity in the premotor cortex disappeared. Incredible, to say the least!

We then asked Carol to imagine walking around her home. Again, we asked her to do this five times. We wanted her to take herself back to that place where she had spent every day of her life before the accident. We wanted her to think about the layout of the house, to move from room to room, visualising the furniture, pictures, doors, and walls.

We knew we were asking a lot, but Carol was obviously up for the task. When we told her to walk from room to room, her pattern of brain activity was identical to that of healthy volunteers. When we told her to let her mind go blank, she did that, right on cue. It reminded me of cheesy medical dramas when doctors ask patients, "Squeeze my hand if you can hear me." But we weren't asking Carol to squeeze our hand. We were asking her to activate her brain. And she was doing it! Kate's words echoed through my head: Keep up the brain scanning. It was like magic, it found me. This time, it really was like magic. We had found Carol. She wasn't vegetative at all. She was responding to us, doing everything we asked.

I was ecstatic. Carol was conscious and we knew it!

This thrilling "eureka" moment came after years of experi­menting, refining, tweaking, and thinking, tunneling down and down, chipping away at the problem, hoping that the answer lay around every next corner. And we were there! We'd found the mother lode.

It may seem odd that we didn't then just go blazing ahead, scanning Carol day in, day out to find out what her world was like and, perhaps, improve her quality of life. Unfortunately, that's not how science works. Our only way to push the science forward was to stick to the strict protocols that we had established beforehand with our ethics committee – protocols that would be scrutinised and approved by the wider scientific community when Carol's story was eventually published in a scientific journal. With Carol, our stated goal had been to detect consciousness, not to haphazardly engage her in a tête-à-tête. We had invested an enormous amount of money and energy, scientific capital if you will, to get to this point and move the field forward. We were playing a long game – Carol and our other early patients were the first pioneers who would make contact with people in her situation possible, not to mention cast a new bright light on the nature of consciousness itself.

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It is, perhaps, ironic that Carol's family were never explicitly told that we had detected a conscious mind in her. We wanted to tell the family, but we simply weren't prepared. When we'd applied to the ethics committee to do this research, we hadn't even considered the possibility that we'd find a conscious person and, if so, what we'd do about it. Even small changes to the protocol, such as the number of scans that you intend to do on each patient, need to be cleared with the ethics committee in advance. Here we had much more than a change of protocol – it was a whole new reality! The principle at the heart of this rule – that every research study is scrutinised in advance by an impartial ethics committee – is good, as frustrating as it was for me at the time. Imagine, for example, that we had told Carol's mother that her daughter was conscious and locked inside her own body, and Carol's mother was so distressed by this news that she killed herself. Imagine it made Carol's husband so angry that he murdered the driver of one of the vehicles that had run Carol down five months earlier. These are dramatic and unlikely outcomes for sure, but were they to happen, who would be responsible? A more likely scenario was that the family's attitude to Carol would change, and the consequences of this also needed to be thought through carefully in advance. Would they understand that being conscious did not necessarily mean that her likelihood of recovery was greater? Would we be giving them false hope? Would they realise that, although we had made contact and established that Carol was conscious, right now that was all we could do? There was no cure, no solution, and no way to communicate with Carol on a regular basis. We hadn't thought through any of this because we didn't know that we were ever going to find an entirely nonresponsive patient who was conscious.

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In the end it wasn't my decision. I was just the guy who asked the scientific questions and then devised the methods to answer them. Our ethics protocol permitted the scans, but made no mention of what we would tell the family if we found a patient such as Carol. Carol's future care was a clinical matter, and I had no authority to interfere with that. If her family was going to be told, then it would have to come from the attending physician, who in this case decided that telling the family would not be clinically beneficial for Carol. I suppose he felt that the burden of knowing that Carol was in there, conscious and aware with no way of expressing herself, was worse than the burden of just not knowing, or assuming that Carol had no inner life at all. Or perhaps he felt that the ethical can of worms that cases such as Carol's opened up was not something worth addressing – less urgent perhaps than ensuring that her medical condition remained stable. I disagreed. I remembered Kate and Debbie, both of whom had experienced some improvement in their conditions after their families learned of their positive scans, and I couldn't help but wonder whether the same might be true for Carol and her family. But that wasn't enough to convince the attending physician. It was heartbreaking.

Nevertheless, Carol sparked my interest in the ethical complexities and legal issues in doing science with this unique group. I resolved to tackle some of the questions that her case had presented by engaging with philosophers and ethicists who understood the complexities of these issues. It was all I could do to make sure that this situation never occurred again. Carol was returned to her home town, and I never saw her again. There was no point – we had found her, but at the time we could do nothing further about it. She died in 2011 of long-term complications arising from her injury.