In November, a team of neuroscientists made meaningful contact with a patient previously believed to be in a vegetative state. Unable to communicate for over a decade, he was able to tell them that he wasn’t in pain using the power of thought alone. We talk to ‘the mind reader’, Professor Adrian Owen, to find out how patients’ brain activity is translating into action.
In 1999, Scott Routley was driving through London, Ontario when he pulled out in front of a police car. Following the collision, he suffered severe brain damage and was diagnosed as being in a vegetative state. The prognosis was bleak: such patients cannot speak or react to stimuli, and even when awake they are presumed to be entirely unconscious.
Over the next 12 years, Routley’s parents refused to give up hope. Intuiting that their son was still with them, they claimed he sometimes used his eyes or thumbs to signal ‘yes’ or ‘no’. To others, though, this seemed like wishful thinking: at no stage had his neurologist picked up on any signs of responsiveness.
This limbo could have carried on indefinitely were it not for a strike of luck. At the nearby Brain and Mind Institute of Ontario, a team of researchers was using a $10 million grant to investigate cases of this type. Led by the British neuroscientist Professor Adrian Owen, they had performed fMRI scans on seemingly vegetative patients, and had already shown that a sizeable minority were in fact aware.
In November 2012, scanning Routley, they took their research to a whole new level. Not only were they able to detect consciousness, but through monitoring his neural blood flow they were able to broach a critical topic. “Is a banana yellow?” they asked him, by way of a safety check. Routley answered, “Yes”. Then came the pivotal question: “Are you in pain?” Using the power of thought alone, Routley answered: “No.”
A ray of hope
Medical breakthroughs are hardly an everyday phenomenon; still less medical breakthroughs that happen to be captured on camera. In Scott Routley’s case, the incident was featured in a British television documentary, The Mind Reader: Unlocking My Voice.
“The BBC were very diligent,” says Professor Owen, the ‘mind reader’ in question. “I did tell them it would never happen because these things tend to occur on the spur of the moment. But they followed me around for nearly two years to try and get that footage.”
Owen is now based in western Ontario, having relocated from Cambridge, UK in 2011. Even before the BBC documentary, his work attracted substantial media attention – he was listed in the The Times‘ Eureka 100, a list of the UK’s top scientists; profiled in a cover story for international science journal Nature; and inspired CBC News’ most-read health story of 2011. “There is as yet no therapy that has been proven to work in vegetative states,” he points out, wary of overhyping his findings, “but there are positive ways in which my research might offer hope.”
His first real breakthrough came in 1997, when Owen used positron emission tomography (PET) on a patient diagnosed as vegetative. Under the scan, it became apparent that she could recognise faces, and thus began her successful rehabilitation. Owen moved on to auditory tests, determining that some of his subjects retained the ability for sound perception and even speech comprehension.
Then, in 2006, he made headlines with functional magnetic resonance imaging (fMRI). He had asked his subject to imagine walking through the rooms of her house, and then playing tennis. In conscious volunteers, the task will activate distinctive regions of the brain – the parahippocampal gyrus for the rooms; the premotor cortex for tennis. To the surprise of all concerned, this notionally unconscious patient responded like a healthy participant. It wasn’t long before the findings were taken further still.
It struck Owen that the house-walking/tennis scenarios might open a window into locked-in patients’ worlds; through picturing one scenario for a ‘yes’ and the other for a ‘no’, they would have a means to answer yes/no questions.
“We asked quite dull questions that we could verify later, like do you have any brothers or sisters, are you married, are your parents both still alive?” explains Owen. “We could check the answers afterwards to make sure we were getting reliable responses.”
Sure enough, this task proved within the grasp of around one in five of his subjects. One man, Steven Graham, acknowledged the presence of a niece born after his accident, demonstrating not just that he was conscious but that he could lay down memories too. Thus when Scott Routley came to the fMRI scanner, the stage was set for a more challenging sort of exchange.
“We moved beyond addressing questions that could be externally verified, into relying solely on the fMRI to decode the answers,” says Owen. “This opens the door to using the technology in a more routine way to address issues that are fundamentally important to clinical care.”
A bridge to the outside world
The implication here is clear: brain scans may one day provide an interface between individuals like Routley and the outside world. After all, locked-in patients have long used ingenious methods of communication: the stroke victim Jean-Dominique Bauby was able to dictate a book purely through blinking his left eye. Owen’s research has uncovered a whole new subset of patients initially diagnosed as vegetative, who have the capacity to make contact using their thoughts.
To some, this scenario may seem far-fetched, and certainly the research has attracted its fair share of sceptics. Many have hinged their arguments on what Owen is actually assessing: after all, consciousness is not an either-or phenomenon, and no fMRI scan can precisely clarify a subject’s state of mind. Might patients react automatically, without awareness? Or could they be semi-conscious, like someone vacillating on the brink of sleep?
Owen has looked into this quandary closely. Diagnostically speaking, ‘vegetative state’ is one step below ‘minimal consciousness’, a state in which uncommunicative patients do retain residual cognition. He has spent some time probing the grey area between fully vegetative and fully aware.
By way of example, he cites an fMRI study completed in 2009. “We showed that around 40% of these patients, vegetative and minimally conscious, will respond to speech when it’s played in a scanner,” he points out. “Now, you might think that maybe that means 40% are actually conscious, but we also know that when you anaesthetise a healthy person, their brain still lights up to speech. That tells us that speech perception per se is not something that depends on consciousness. We’ve reported on the whole spectrum of patients.”
As the shades on this spectrum become clearer, Owen’s findings strike right to the heart of what is meant by ‘vegetative state’. When the present diagnostic criteria were laid down in the early 2000s, fMRI communications had yet to become a reality. But following the advance of brain imaging, many patients’ diagnoses no longer seem so apposite.
“We absolutely have to revisit this issue,” affirms Owen. “While Scott fits the bill for a vegetative state patient, he is clearly not in a vegetative state because he is awake and aware. If a patient could consistently squeeze the left hand for a yes and the right hand for a no, we would call them functionally communicative. Scott is doing the same thing with his fMRI, so I think we should find a term that adequately describes what he is.”
Ultimately, though, this is a matter for specially designated medical bodies: Owen himself is not intent on determining a threshold of consciousness or creating a taxonomy of mental states. He takes a pragmatic approach, with a view to surpassing the practical hurdles faced by his team.
Electroencephalography and the ‘EEGeep’
So far, their primary problem has been the fMRI technology itself: not only are scanners costly and cumbersome, but they require the subject to stay stock-still. Because vegetative patients are prone to wriggling, scanning is not always a viable option. Still further, many of them have metal implants in their heads, rendering magnetic resonance imaging impossible.
He and his team have therefore been investigating another type of brain scan, electroencephalography (EEG). While EEG lacks fMRI’s precision and cannot peer as deeply into the brain, it is far cheaper, far smaller, and unaffected by patient movement or metal plates. Most importantly, it can be used at the bedside. In a twist best suited to a sci-fi film, Owen’s team have invested in a jeep fully configured with EEG equipment. Proudly naming it the ‘EEGeep’, they drive it all over Canada assessing patients for signs of consciousness.
The technology is in its nascent stage. As yet, nobody has managed to communicate with a patient using EEG, and – as evinced by a null response in some healthy patients – it does not seem altogether infallible as a gauge of awareness. That said, Owen’s team are investing a huge amount of time and resources into fine-honing their techniques.
“Technically, it’s a relatively small step to using that technology to say: switch the light off, switch TV channels or turn on the radio,” says Owen. “But they’re things that could be tremendously important to a patient who’s had everything decided by their carers for many years. While we’re never going to live in a world where patients have an fMRI scanner at home, I can imagine a world where they have an EEG kit.”
In this notional world, EEG will give locked-in patients a voice. It will allow them to exert some control over their environment – selecting their own entertainment, for instance, and making their wishes known. And in the meantime, there is a more tangible means by which brain scans can improve patients’ lives.
“We can definitely help in targeting attempts to rehabilitate,” says Owen. “With the fMRI we are able to identify cognitive faculties that may be more intact than others – for example, if a patient’s vision wasn’t particularly good but their sense of hearing was intact, we could clearly determine that, and would focus on auditory stimuli rather than visual stimuli during rehabilitation.”
Owen doesn’t dwell too long on the knottier ethical dilemmas opened up by his research, although he acknowledges the issues at stake are profound. Each year, there are several high-profile court cases concerning the withdrawal of nutrition and hydration from vegetative patients. And while the distinction between ‘vegetative’ and ‘minimally conscious’ may seem small, it could have life-or-death ramifications – patients are typically not allowed to die should they show residual awareness. This highlights the need for diagnoses to be as accurate as they possibly can be.
For now, considering the possibilities ahead, Owen is ebullient. “If we’re going to chronologically go through the series of breakthroughs, we showed that you could detect consciousness in a patient assumed to be vegetative,” he says. “We went on to show that you could use fMRI to communicate with that patient and ask mundane but nevertheless important questions.
“We’ve come on to show that we can even ask therapeutically relevant questions with fMRI about pain. We can even imagine asking questions about what people’s expectations or wishes are for the future. And if we could get a patient communicating routinely with a portable cost-effective system like EEG, then I think we would have profoundly affected someone’s life. Then we will really have done something remarkable.”
Soon, it will be possible to ascertain whether patients like Scott Routley agree.
Professor Adrian Owen
Professor Adrian Owen is the Canada Excellence Research Chair (CERC) in Cognition and Neuroimaging at the University of Western Ontario, Canada. His work combines structural and functional neuroimaging with neuropsychological studies of brain-injured patients. Since 1990, Dr Owen has published over 200 articles and chapters in scientific journals and books.
This is the cover story for the February 2013 issue of Medical Imaging Technology