Inside a comatose mind

On Dec. 20, 1999, Scott Routley, 26, was leaving his grandfather’s house in Sarnia, Ont. His girlfriend was with him. Just a few blocks away, according to his mother, Anne, Routley’s car collided with a police cruiser. The police officer and Routley’s companion were taken to hospital with minor injuries. As for him, “he only had one injury,” she says. “The bump on his head.” That injury would prove devastating. Routley, who’d studied honours physics at the University of Waterloo and had a promising career in robotics, was diagnosed as being in what doctors term a persistent vegetative state: awake, but completely unaware of himself and his surroundings.

Anne Routley, who worked as a lab technologist, retired “the day of the accident,” she says. Her husband, Jim, a former banker and trucker, retired, too. They relocated to a one-storey bungalow outside London, Ont., where Scott could stay part-time. (He spent most days in a long-term care facility.) Despite his diagnosis, Jim and Anne believed that their son, who loved listening to music from The Phantom of the Opera and Les Misérables, was responding to them. “His face is expressive,” said Anne in early September. “He blinks. He does thumbs-up for positives.”

Twelve years after the accident, Adrian Owen, a British neuroscientist who holds the Canada Excellence Research Chair in Cognitive Neuroscience and Imaging, arrived at the University of Western Ontario, and heard about Scott Routley. “A clinician said he’s been seen by a neurologist every year and always comes up vegetative, but the parents are convinced he’s communicating,” Owen recalls. “I said, fine. Let’s scan him.” In February 2012, Routley was scanned using functional magnetic resonance imaging (fMRI), which measures brain activity by detecting changes in blood flow and oxygenation. By activating certain parts of his brain for a “yes” or a “no” reply, he was able to answer questions, identifying his name, the name of his personal support worker and the date. When asked if he was in physical pain—the first time any PVS patient had been been able to answer—he replied “no.”

“Scott looks exactly the same as a vegetative-state patient and he fulfills all the clinical criteria,” says Owen. “But the reality of the situation is that [cognitively], he’s perfectly fine.” Scott Routley has become the most famous scientific case of his kind in the world. And Owen’s groundbreaking research, which raises the unsettling possibility that some vegetative patients are, in fact, aware, is redefining human consciousness.

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The implications for end-of-life care are potentially huge. When a patient’s vegetative state is considered permanent, and families feel their loved ones wouldn’t want to live this way, doctors can remove any feeding tubes and end artificial hydration. (Laws governing the process vary slightly between provinces.) “The ultimate problem is that you can’t talk to the patient and find out what his values and beliefs are,” says Toronto lawyer Mark Handelman, an expert in end-of-life decisions, “or when the patient thinks, ‘Enough is enough.’ ” If Owen is correct, it may one day be possible to ask some of these patients to weigh in on their own treatment—and even, perhaps, whether they wish to live as they are.

Owen’s discovery that Routley was, in fact, aware didn’t come as news to his family. “It was vindication,” says Jim. “We weren’t surprised at all,” adds Anne. “It was just, ‘Well, now somebody believes us.’ ”

It’s long been assumed that vegetative patients are not conscious, although that doesn’t form part of the official diagnosis. A vegetative state results from brain injury caused by any number of things, such as a heart attack, a near-drowning, or—as in Routley’s case—a car accident. But they aren’t lying in a coma, nor do they suffer from locked-in syndrome, a rare condition in which patients are aware, yet paralyzed from head to toe. (French editor Jean-Dominique Bauby, locked-in after a stroke in 1995, dictated his memoir, The Diving Bell and the Butterfly, through blinks from his left eyelid.) Vegetative patients wake up and fall asleep; their basic reflexes are intact; they may grind their teeth or grimace, and their eyes rove about the room, although they don’t fixate on anything.

Owen says he didn’t know much about vegetative patients until 1996, when he came across Kate Bainbridge, a young woman who’d slipped into a coma after acquiring a viral infection. She eventually emerged into a vegetative state. Owen, who was setting up a brain imaging facility at the University of Cambridge, decided to scan her brain. He showed her pictures of her family, “and bingo! Her brain lit up,” he says. “It was very unexpected.” Her responses looked like what he’d seen in healthy subjects, although she’d been non-responsive and seemingly unaware.

Bainbridge slowly regained consciousness. “I don’t like the term ‘wake up,’ ” she wrote in an email to Maclean’s. “That implies it all comes back quickly, [and] for me, it took months.” Now 43, she lives in Cambridge with a full-time caregiver. She can’t walk or sit up on her own; for 12 years, she couldn’t speak, but now she can, although “not well,” she writes. The infection, which attacked her brainstem, has had a lifelong impact. “I can’t say how lucky I was to have the scan,” Bainbridge writes, adding that it gave her parents hope to carry on, too. “[It] really scares me to think what would have happened if I hadn’t had it.”

Owen continued to examine vegetative patients. The question of “consciousness” nagged at him. If the brain lights up in a scanner, it doesn’t necessarily indicate awareness of what’s going on: Our brains respond automatically to certain stimuli, including words and sounds. “That’s when the ‘imagine playing tennis’ idea came up,” Owen says, which he calls his “home run.” In a 2006 Science paper, he asked a 23-year-old vegetative patient either to imagine playing tennis, or moving around her home, activating two different parts of the brain. She showed activation in patterns that were “indistinguishable” from healthy volunteers. “It was obvious she was conscious,” he says. By asking her to turn on one part of her brain, then the other, “we’d done the functional equivalent of saying, ‘Raise your left arm, now your right arm, 10 times’—and she did it 10 times.” In a 2010 paper in The New England Journal of Medicine, Owen took this further, using his technique to elicit “yes” or “no” answers. One patient who’d been vegetative for five years communicated information, such as his father’s name, in response to questions.

But the fMRI isn’t ideal for examining patients, at least not on a regular basis. Scanners aren’t readily available and subjects have to be brought to a special facility, which can be stressful and challenging. Electroencephalography (EEG), which uses electrodes to detect the brain’s electrical activity, is relatively cheap and portable. Owen’s team began using EEG to look for signs of consciousness at patients’ bedsides, asking them to imagine squeezing the right hand, or wiggling their toes. (EEG doesn’t look deep enough into the brain to replicate the tennis study.) In 2010, Owen was recruited to Canada. In his first work published here, in 2011, he found that three of 16 vegetative patients were able to follow commands with EEG.

Scott Routley has been examined with fMRI and EEG. In one study, published in August in the Journal of the American Medical Association for Neurology, Routley (in the fMRI) heard a series of numbers with “yes” and “no” mixed in: “YES-1-2-6-7-YES-2-0-4-NO-5-6-NO-2-7-4,” Owen demonstrates. Routley was instructed to attend to either the “yes” or the “no.” “It’s pretty complicated, which is why it’s so amazing Scott could do it. Even the young undergraduates we have in to scan sometimes get confused.”

Owen’s work has stirred up controversy. Consciousness exists on a continuum that’s different for each patient, says Parashkev Nachev, a neurologist at University College London. “The brain is so tightly connected to the body and the outside world,” he continues. “The likelihood that there will be many cases where the only problem is the output is going to be small.” After reanalyzing data from Owen’s 2011 EEG study, a team led by Weill Cornell Medical College called into question its results in The Lancet, concluding it was impossible to know if patients were aware during testing. This is partly because EEG signals could have been muddied by electrical signals from the muscles. Owen, who published a response in the same journal, calls this a difference of “statistical opinion, rather than scientific fact.”

The biggest objection to the work has been that it may be giving people false hope. It’s not unusual for families of vegetative patients to see what they believe to be glimmers of consciousness, even when their loved ones are no longer measurably there. “There’s nothing in our experience to help us cope with this circumstance,” Nachev says. “It’s very hard to accept the idea that, if somebody in front of us is breathing, he’s blinking, his heart is beating, his eyes are open, he’s actually dead.”

Yet it’s increasingly clear that at least some vegetative patients are conscious, if only minimally so. “We are misdiagnosing a subpopulation of patients as vegetative,” says neurologist Dr. Nicholas Schiff of Cornell, co-author of the analysis that questioned Owen’s EEG results. “This will be obvious to everyone in five or 10 years.” Despite Routley’s unchanging diagnosis, “he’s not vegetative,” Dr. Bryan Young, neurologist and professor emeritus at Western University, who has treated him, said in early September. “He’s cognitively aware.”

The stark ethical and legal implications of this are already apparent. In December, the Supreme Court of Canada heard the case of Hassan Rasouli, an Iranian-born Toronto man who acquired a brain infection after surgery to remove a tumour, and was pronounced vegetative. Doctors at Sunnybrook Health Sciences Centre wanted to take Rasouli off life support. His wife and children refused. Whether the Supreme Court rules on behalf of the doctors or the patient’s family, it will affect countless people. (Owen has since assessed Rasouli and diagnosed him as minimally conscious.) It costs an estimated $1 million per year to keep Rasouli in his bed at Sunnybrook’s intensive care unit.

Owen believes that as many as one in five vegetative patients might be aware and conscious, but unable to communicate outside of the fMRI or EEG. (There is no official name for this condition as of yet. Owen calls them “locked-in plus.” They’re locked in, as Bauby was, but unable even to communicate through eyelid blinks.) He wonders if that number might be low. “It’s not even been 10 years since we first discovered anybody like this.”

As the technology and our methods improve, he hopes his research will improve the lives of people like Scott Routley and Kate Bainbridge. For the rare vegetative patient who does recover, “the biggest complaint, typically, is not ‘I missed seeing my grandson grow up,’ ” Owen says. “It’s frustration of not controlling the little things,” such as turning the lights on and off, or having a well-meaning family member leave hockey on the TV 12 hours a day. In the future, Owen imagines that scientists will design a brain-computer interface to allow patients to communicate, giving them a chance to participate more fully in their lives—and treatment.

Scott Routley died on Sept. 27, 2013. Speaking with Maclean’s earlier that month, his parents recognized that any major advances likely would not arrive in time to help their son. “Scott’s the type of person who’d be very happy to be helping someone else down the road,” his mother said. Routley may have been silent for 14 years, but he never stopped communicating.