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.”

Put to the test

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.

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 US 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%. Schiff, who weighs up the extent of misdiagnosis a different way, goes further. Based on recent studies, he says around 40% 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.

In 2009, Laurey’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 Liege 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.”

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.

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.”

Mind limitations

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.

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. 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). And 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.

Then there is 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.”