“Surely, if we are going to make judgments about whether people should be kept or alive or allowed to die after serious brain injury, it’s better if the people themselves are involved in that decision-making process, rather than others – doctors, relatives, etc. – being entirely responsible for making that decision for them.”
Breakthroughs in cognitive neuroscience: Highlighting influential research from the past 20 years
This series explores influential papers in cognitive neuroscience, as measured by the number of times they are cited each year. The papers featured are a sampling of many important works in the field over the past 20 years. This is the fifth, and last, in the series. Read the first, second, third and fourth stories.
In 2006, a one-page paper in Science made big headlines around the world: Scientists had detected awareness in a patient who appeared to be in a vegetative state. Led by Adrian Owen, then at University of Cambridge, researchers asked a 23-year-old woman in a coma to imagine playing tennis and walking through the rooms of her house. They then recorded her brain activity with fMRI. They found that the same part of the brain that activates in healthy conscious adults asked to imagine the same scenarios – the parahippocampal gyrus – lit up in the woman who had been unresponsive for five months following an accident.
In the 7 years since that paper, researchers have made big strides in detecting such awareness in other patients and in communicating with them using new technologies. CNS talked with Owen, who is now at the University of Western Ontario, about his landmark paper, developments since then, how he views consciousness, and the future for communicating with patients in comas.
CNS: How and why did you become interested in cognitive neuroscience and specifically in consciousness?
Owen: My first degree was in Experimental Psychology at UCL, in London and the two things that really interested me during the course of my studies were neuropsychology (the study of the effects of damage to specific regions of the brain) and computing; this was in the very earliest days of personal computers and long before email, the web, etc. When brain imaging came along – first PET and then later fMRI – it felt like a perfect marriage between those two things. I could investigate brain function using some of the most sophisticated computer systems available. And that is still very true today. This joint interest in brain function and computing also fueled my curiosity about consciousness and the idea that I have had for many years that some patients who appear to be entirely unresponsive may have residual abilities that we simply don’t know about. But it really wasn’t until the right technology came along that I began to feel that we could actually tackle this problem.
CNS: Your 2006 Science paper was only a page but had a big impact. Did you anticipate the reception it received? Can you give an example of a memorable or unexpected reaction you received?
Owen: That’s a hard question to answer. When I first saw that data, showing that one of our patients who appeared to be entirely unresponsive and clinically vegetative was actually producing responses in the scanner, I knew that it was a tremendously important result. It was one that we had been working towards for almost 10 years at that point. Although it was only one patient, what struck me as most important about it was that it was the very first patient we had tried this particular technique with and that had to mean that there were many more out there. It simply couldn’t be that we had stumbled upon the only covertly conscious patient with our very first attempt. In fact, it made me believe that this must actually be quite common. The very first time I presented that data, Chris Frith was in the audience and was exceedingly enthusiastic about it. I think that also made me realize that the reception was likely to be very good. Chris also encouraged me to send it to Science and the rest is, well history as they say….
CNS: What have been some of the biggest developments in the field that stemmed from that paper?
Owen: Well, I think the first biggest development was to take this from the point that we were simply detecting hidden consciousness to the point that we were actually able to communicate with someone using their brain activity alone. This occurred in 2010, with a follow up study in which one patient, who had appeared to be vegetative for 5 years, was actually able to convey “yes” and “no” responses by simply changing his pattern of brain activity in the fMRI scanner.
For me personally, this result was most important because it immediately ended any further discussion about whether our technique really could detect consciousness or not – the fact that we had managed to decode answers that we did not know in advance to questions about this man’s life, based solely on his brain activity, could only be explained by the fact that he was conscious and actively trying to convey those answers to us by changing his brain activity; there’s simply no other explanation. That was a tremendous endorsement of the techniques that we had developed thus far. But that study was also important because it showed that the patient in the Science paper four years earlier was neither unique, nor particularly rare. In that later study, published in the New England Journal of Medicine, 4 out of 23 of the vegetative patients were shown to be covertly conscious.
A second crucial development in this field was to take the result out of the fMRI scanner, which is expensive and non-portable and so is not available to all patients in this situation. In 2011, we showed in a paper published in The Lancet that we could achieve the same feat with EEG, a cheaper and more portable technique. By visiting patients in their homes, nursing homes and hospitals, my team was again able to show that almost 20% of patients who clinically appear to be vegetative were in fact conscious – but this time, using cheaper and more portable technology that could be widely deployed.
CNS: Are we yet at the phase where an average person whose loved one is in a coma can use the technique you have helped developed to talk to their loved one?
Owen: No, unfortunately we are not. First and most importantly, for most patients in this situation, the technique will not be applicable because in both group studies to date, less than 20% of patients have been responsive. So for 80% of these patients, we have to assume for now that they are not covertly conscious.
For the responsive 20%, we have made enormous progress but we are not yet to the point that routine communication is possible. For the most part, the problem is a technological one. With fMRI, the technique is getting fairly reliable, but communication is only possible when the patient is in the scanner which is obviously not a day-to-day occurrence. With EEG, we are still at an earlier stage of development and it remains less sensitive than fMRI – for this reason, the technology is not yet ready to be used by non-experts in a non-scientific environment.
CNS: Can you give an example of a memorable moment working with with families of patients in comas?
Owen: There are many, both good and bad. It’s always very difficult to report back to families when we have found no evidence that their loved one is conscious, but I am always surprised by how positive most families appear to be. In many cases, even when the news is bad, there seems to be some relief in the fact that they have tried absolutely everything, including some of our new scientific approaches that are still not widely available. Of course, it’s more pleasant when we have good news to report.
I recall one occasion in particular, here in Canada, where we were scanning a young man who had been entirely non-responsive for several years following a car accident and his parents were in the scanning room with us because the event was being filmed for a BBC documentary. We were all very tense and the cameras were rolling. As we started to detect his conscious responses, it became extremely difficult to remain composed. Even though many of us have experienced this on quite a number of occasions, it still blows my mind every time it happens.
CNS: Why do you think this work continues to be so controversial?
Owen: I don’t really think what we do is “controversial,” but I am keen to explore what you mean by that. In the early days, immediately after the Science paper came out, people would sometimes refer to our paper as “controversial,” which would irritate me because I felt that it implied somehow that our result was possibly untrue – in the same way that brain training is often described as “controversial” because some studies suggest that it might work, but others suggest that it does not. To my knowledge, no one provided any evidence at all that a non-responsive patient, like our patient, could generate predefined patterns of brain activity at exactly the time that we asked her to, if that patient was not conscious. Of course, some people did not believe the result, but that is a different thing altogether. …
Any irritation I felt did subside with the 2010 paper, where we communicated with such a patient using “yes” and “no” questions, because there really was no other explanation than that the patient was conscious. Unsurprisingly perhaps, people stopped referring to the work as “controversial,” at least in the scientific sense.
But there is another sense in which our work is sometimes described as “controversial” and that is because it has very clear ethical implications. If things proceed as they are now, I think it’s exceedingly likely that these methods might be used, at some point, to tackle some really difficult ethical questions, such as asking a patient whether they would like to live or die. But honestly, I don’t think that is “controversial” either, at least not in the sense that it produces any new ethical dilemmas. Surely, if we are going to make judgments about whether people should be kept or alive or allowed to die after serious brain injury, it’s better if the people themselves are involved in that decision-making process, rather than others – doctors, relatives, etc. – being entirely responsible for making that decision for them. And ultimately, that is all that we are seeking to do – to allow those who have been denied a voice, a chance to express an opinion about their destiny.
CNS: How do you define consciousness?
Owen: I am not going to do that here because many long books have been written on the subject and I can not do all that is known about consciousness justice in a few words. Briefly, I confine my musings about consciousness to that which is measurable, because I am a scientist and, as such, I am only interested in what I can measure. There are two components of consciousness that are measurable, arousal – wakefulness – and awareness. For example, think about what happens when you undergo a general anesthetic for major surgery – you close your eyes and you start to fall asleep, that is to say, you lose wakefulness, and you stop having any sense of the where you are, who you are, and the predicament that you are in, i.e., you lose awareness. The wakefulness component of consciousness is relatively easy to assess – if your eyes are open, then you are awake. But assessing the awareness component of consciousness is much more difficult and that is the component that we seek to measure with our fMRI and EEG techniques. As such, I think our research is less concerned with what consciousness is, than whether a given being is conscious or not.
CNS: What else are you working on now ?
Owen: I think I have mostly covered it. The success of our recent advances in fMRI and EEG techniques for detecting awareness, and even communicating, with some non-responsive patients paves the way for the development of true “brain-computer interfaces” – or simple, reliable communication devices – in this patient group and we are investing a lot of energy in that right now. We are also trying to find new, faster, cheaper ways of assessing consciousness with 100% accuracy that can be rolled out for general use to all patients, wherever they are. We are very proud of our EEJEEP – a fully equipped Jeep kitted it out with electrodes, amplifiers, and the most powerful laptops we can find, which we use to go out on the road visiting patients and families in their homes, care homes, and hospitals. We also have a very productive collaboration with a group of philosophers and bioethicists at the Rotman Institute of Philosophy here in Canada and that has pushed us in several new and interesting directions – specifically, we are trying to develop ethical frameworks for how one might use the sort of technologies we are developing to allow patients to take part in the decision-making processes that govern their care.
CNS: What are a couple of the most exciting lines of research for this area heading into the next 20 years? What is your ultimate goal?
Owen: An obvious answer is to say that we all want to be communicating by ‘thought alone’ 20 years from now, but I don’t think that’s very likely. We are only just starting to be able to decode human thoughts with any degree of accuracy using techniques like functional MRI and EEG, but it’s still enormously complicated, costly, time consuming, and immobile. It will take more than 20 years to overcome all of the scientific and logistic challenges required to prepare this technology for everyday use. But we’ll be a lot closer!
—
Media contact: Lisa M.P. Munoz, CNS Public Information Officer, cns.publicaffairs@gmail.com
