Lynne Malcolm: Hi, it's All in the Mind on RN, I'm Lynne Malcolm. Today, detecting consciousness in those assumed to be in a vegetative state.

Martin Pistorious: My awareness was something that happened gradually, so it wasn't like one moment I was asleep and the next moment I was awake. It is quite difficult to describe, but I often say that it is sort of like looking at a grainy, completely out of focus image, and then gradually the colours start to flow back and the image becomes clearer and clearer, until it is crystal clear and in vibrant colour.

As my awareness returned, it took me a while to fully comprehend that I was trapped inside my body. Of course as the reality dawned on me that not only was I trapped in my body but that I was probably going to spend the rest of my life in this state was something I really struggled with.

The feeling of complete and utter powerlessness is probably the worst feeling I have ever experienced, and if I can help it I never want to experience again. It is like you don't exist and every single thing in your life is decided by someone else.

Obviously there were a lot of conversations and even arguments about me. I was also an invisible observer, and people can do the funniest things when they think nobody is watching, they will pick their nose or fart really loudly. Some will sing or talk to themselves in front of the mirror. I remember one lady prancing around imagining she was a model.

Lynne Malcolm: That's Martin Pistorious speaking to me with his computer assisted voice about his ten-year ordeal, locked inside his body. You may have heard his remarkable story in the previous episode of All in the Mind. Martin can now see a light hearted side, but overall, I think you'd agree, being fully conscious and aware, yet not being able to communicate is everyone's worst nightmare.

Adrian Owen is Professor of Neuroscience at the University of Western Ontario and has focussed his research on defining and measuring levels of consciousness, particularly in people who are in a coma-like state. He was inspired to study this, almost 20 years ago, by one of his patients.

Adrian Owen: Yes, it's a very interesting story. It's a story about serendipity really. I trained in neuroimaging and neuropsychology. And then in 1997 I was working at the University of Cambridge and I was introduced to a patient whose name is Kate Bainbridge who was in a vegetative state, and I really was the right person in the right place at the right time because I had the imaging expertise, and she was a patient who is in a vegetative state and we put two and two together and thought, well, wouldn't it be interesting to put this person into the scanner. And back then very few vegetative patients had gone into brain scanners because people just assumed you would see nothing, there would be nothing going on in their brain.

And Kate was an amazing case because we scanned her, and while she was in the PET scanner we showed her pictures of faces of her friends and relatives, and the part of her brain that we know is involved in processing faces lit up just as it would in a healthy participant. So there was a response in her brain to familiar faces. And at the time this was very amazing, it was completely unexpected and very, very exciting and it was the first time I think that imaging had been used to show that some vegetative patients have some residual cognitive activity in their brains, and that really started the whole thing rolling.

Lynne Malcolm: So what did you do with that information? How did you start testing whether patients are able to comprehend what they are hearing or seeing if they are in a vegetative state?

Adrian Owen: Well, it was really a whole series of experiments that we conducted after that one first patient. Because knowing that a patient in a vegetative state could respond to faces, our immediate response was, well, what else can patients like that do? Kate, fortunately for her, went on to recover. So she wasn't somebody that we were particularly interested in scanning subsequently. But a couple of years later we came across another patient, and she was quite similar to Kate and we put her into the scanner and we played her short sentences. We were able to deduce that her brain responded to those sentences, again as if your brain or my brain would respond. She had a perfectly normal brain response to listening to speech. So this immediately begged the question, well, is her brain understanding that speech or is it a sort of fuzzy type of listening to speech, the sort of experience you might have if you were listening to a foreign language, for example.

So then we started to do another series of experiments where we changed the type of speech that she was listening to, and we had other patients start to come along, and we gradually started to work out that some of these patients could not only perceive speech, their brains would not only respond to the sounds of speech, but they could comprehend it as well. There was something else going on in their brain that suggested that they were actually processing that speech in a way that made us believe they were actually understanding what they were hearing.

Lynne Malcolm: Professor Adrian Owen. He explains how scanning a patient's brain can give researchers information about what the person is aware of.

Adrian Owen: In general the process is that we know a fair bit about which parts of the brain are responsible for certain things, like for example listening to speech. When your brain hears speech, certain parts of it will activate in a different way than if your brain was to listen to a lawnmower, for example, because the brain has specific modules that are specialised for detecting speech as speech. Similarly, there are parts of the brain that are involved in comprehending or understanding speech, and those are different areas of the brain and they will only light up or blood flow will only change in those areas of the brain if the person is understanding speech. So essentially we are sort of mapping what's the patient's brain can and can't do based on which areas are activating in response to different types of external stimulation.

Lynne Malcolm: So does that mean that we could develop ways of communicating with people in a vegetative state?

Adrian Owen: Well, you know, it's interesting question because in 2006 we really reached a bit of a brick wall because we discovered many of these patients could respond in this way or at least their brains could respond. But we still didn't know whether they were actually conscious, whether they were actually aware. And that's where we really conducted our classic experiment, if you like, where we really worked out how to determine that a patient is aware, and that has really been the way that we have been able to go on and communicate with some of these patients.

And what we did on that occasion was we asked ourselves, well, what sort of brain activity would we have to show for us to be convinced that a patient was aware? And the idea came from thinking about the way that we test awareness, for example, by the roadside when a patient has had an accident. I'm sure everybody listening to this has seen a TV drama where a doctor takes a patient's hand and says, 'Squeeze my hand if you can hear me.' Well, that's how we know that the patient is aware and is listening and can understand, because if you get a squeeze back you know they've understood.

So our reasoning went, well, could we get a patient to activate their brain when asked to do so? And the way we did it was by getting a patient to imagine that she was playing a game of tennis. And we literally said, 'When you hear the word tennis please imagine that you're playing a game of tennis.' And the reason why we did this is because there's a part of the brain known as the premotor cortex which is particularly involved in imagining moving your arms around. It's the part of the brain that sends messages to the mortar cortex to actually move. So even if you don't actually move your arms around as if you are waving a tennis racket in the air, your premotor cortex will still activate if you imagine it because it's almost as though it's about to produce an action, it's about to activate the motor cortex.

So we had a patient who was in a vegetative state, she had been involved in a road traffic accident. She was no different to any other patients that we had seen thus far, and we put her into the scanner and we said, 'Please imagine playing tennis now.' And amazingly the premotor cortex lit up. And then we said 30 seconds later, 'Well, stop playing tennis now,' and activation disappeared. And then we said, 'Do it again, imagine playing tennis,' and the activation came back. And it was exactly as though we were saying to her, 'Squeeze my hand if you can hear me,' but we were saying, 'Activate your premotor cortex if you can hear me.'

And this was our first absolutely concrete evidence that a patient who clinically appeared to be in a vegetative state might actually be in a condition that we have no name for, sort of a complete locked-in situation. The patient was absolutely conscious and aware of everything going on around her but nevertheless entirely unable to move or respond in any physical way at all.

What we then did is we took that basic method, and this again was another patient, a patient we saw a few years later, and we said, well, let's get this guy to imagine playing tennis to say yes and to do something else to say no and let's see whether we can communicate with him. So we had two different tasks here. We told him upfront…again, he was in a vegetative state, he'd been like that for five years. We had no idea whether he was in there at all. We said, 'If you can hear us, if you can understand us, we want you to imagine playing tennis if the answer to a question is yes, and we want you to imagine moving from room to room in your house if the answer is a no.' And that's because if you imagine moving around your house, parts of your brain that are involved in what psychologists called spatial navigation light up. The parts of your brain that help us get from place to place and know exactly where we are in an open space.

We started to ask this guy questions, and these were questions that we didn't know the answer to. It was, again, an amazing situation. We'd been given potential questions by the family, and we said things like, 'Is your father's name Alexander?' And amazingly his premotor cortex would light up, as though he were playing tennis because he was conveying a yes by imagining playing tennis to say yes. And then we said, 'Is your father's name Oscar?' And other areas of the brain, an area known as the parahippocampal gyrus, which is involved in navigating from place to place would light up, indicating that he was thinking about moving around his house in order to tell us a no. And in this way, just by imagining these two scenarios, he was able to convey a series of yes and no responses to us and answer various questions to communicate with us while he was in the scanner.

Lynne Malcolm: So you were using these particular situations for them to imagine, because there's no way of imagining no or imagining yes.

Adrian Owen: Exactly. That's a great question and it's one that many people wonder. The problem is we are pretty good at understanding how the brain works, and our brain scanning techniques are getting better and better all the time. But I can't decode you thinking a word. If you think the word 'no', I can't tell the difference between that in the brain and you thinking the word 'yes'. If I could, this process would be a whole lot easier. But that's why we have to resort to these proxy tasks, tasks that we do know the that we can detect in the brain but that are indicative of a yes or a no once we've given the patient the relevant instructions.

Lynne Malcolm: So it's really raising that question of what is consciousness, and whether consciousness is a complete on or off state or whether there are gradients of consciousness.

Adrian Owen: Yes, that's also a very good question, and it's something that we are looking at right now. And there's a condition that's referred to as the minimally conscious state that people will hear more and more about in the coming years. And that's a condition that is very like the vegetative state. The patients seem very similar, except essentially they can respond some of the time to indicate that they have some level of awareness. So it might be that the patient might squeeze your hand when asked to do so more often than would be expected by chance, but not all of the time.

And we are doing a lot of work at the moment to try and understand what is this like, to be in a minimally conscious state? Is it like being fully conscious some of the time and fully unconscious the rest of the time, or is it like being in sort of a dream state where you are almost there but not quite, you are sort of drifting in an out of a fully conscious state? We really have no idea. And I suspect the answer is that it's going to be different for different patients.

Lynne Malcolm: And one of the things you've investigated is humour, by telling jokes to people and seeing their response in the brain.

Adrian Owen: Yes, I'm often quite embarrassed to discuss this study because I think people are quite alarmed when I say that I tell jokes to patients who are in a vegetative state while they are in the scanner, because it sounds like some kind of wacky science. But actually there are very good scientific principles behind it. And basically it's that we are trying to detect a response, whatever that response may be. An emotion is a very powerful driver in the brain, it's something that if you get a really good emotional response it's something that is pretty easy to detect in the brain.

The problem is, something like fear is a great emotional response but really I wouldn't want to deal with the ethical repercussions of scaring patients who are in a vegetative state, it's not something I'm particularly interested in doing and I'm sure my local ethics committee wouldn't be either. So we picked a positive emotion, and happiness is a positive emotion. But the way the scanning works, you really have to get a happy response, but sort of triggered by an event in time. You can't just look at the brain and know that a person is happy based on what's going on in the brain. You have to kind of make them happy at a particular point in time, and that's basically what a joke is. It has a punchline and it gives you a laugh at a particular moment in time.

So it turns out to be a great way of us determining whether the patients are responsive, whether they have any emotional responses, but also it tells us a lot more than that. It tells us that they understand language because you can't get a joke unless you understood it. And they understand language at a very high level because the sorts of puns that we use in our joke study were extremely sophisticated and they required a pretty good knowledge of the English language to really process them and understand them. So even though it sounds a little bit wacky, telling vegetative state patience jokes in the scanner was actually a very important thing for us to have done.

Lynne Malcolm: So how did you tell by the scan if they found the joke funny?

Adrian Owen: Well, there are parts of the brain that we know are particularly responsive to humour. So the point that we appreciate a joke or have a humorous response to a joke we see activity in particular parts of the frontal lobe of the brain. We also know that there are particular parts of the brain that are responsible for processing, comprehending or understanding language. And our jokes were of the sort where a lot of them were a play on words where you really had to understand that, you know, a tank was something that fish could live in or it was an armoured vehicle.

One of our great jokes was there were two fish in a tank, one says to the other, 'Do you know how to drive this thing?' That's one of my favourite jokes. And to understand that joke you have to understand that the word 'tank' can refer both to an armoured vehicle and to the physical glass object that holds fish. It's a little bit surreal, the fact that two fish might be driving an armoured vehicle, it's quite a surreal idea, and it also inject some humour into it. But for the brain to respond to a joke like that, it really has to be…and I'm going to put it quite bluntly…it really has to be pretty intact. A brain that has been very badly damaged and is perhaps minimally conscious or vegetative is not going to have that level of ability or residual processing available to it to be able to comprehend the fact that it's a funny idea that fish might be driving an armoured vehicle, and you are led to believe they're in a fish tank but at the end of the joke you find out about actually in an armoured vehicle. These are the sorts of things that are only processed by brains that are pretty intact. And when we see the areas of the brain activated that we see in healthy participants, we know that this is a good sign, this means these patients are actually in a good place right now, at least in so far as what is going on inside their brains.

Lynne Malcolm: So do you have any idea of what percentage of people that are in vegetative states may have the consciousness enough to respond to these sorts of techniques?

Adrian Owen: We do, we have a very good idea about this now. We've conducted two studies. We are about to publish a third. And it's just a little less than 20%. Close to one in five patients that we see who pass all of the clinical tests for being vegetative, when we put them in the scanner and we say 'imagine playing tennis', we will see activity. So it's not all vegetative patients, that's a very important point to take away from this. But it is a significant minority. It is one in five patients.

Lynne Malcolm: You're with All in the Mind on RN, I'm Lynne Malcolm. We're discussing the latest research on detecting levels of consciousness in patients who are often wrongly assumed to be in a vegetative state.

Professor Adrian Owen from the University of Western Ontario tells the story of one of his recent patients, which demonstrates how people's level of consciousness can often be underestimated.

Adrian Owen: This is a very interesting case that we had recently here in Ontario. A patient who came to us, we put him into the scanner and went through all of the usual processes, tested him. We have a number of new techniques now for detecting consciousness that I haven't described yet, but we tried to get him to imagine playing tennis and do all of the usual scans. We sent him home, and the results were mixed. Some of the activity looked like he could have some awareness but some of it didn't.

Nine months later we followed him up, we called his mother and we said, 'How is he doing?' And she said, 'Well, why don't you ask him?' And this patient came on the line and he was able to talk, he was able to converse very clearly. We immediately brought him into my lab because really over the 20 years or so we've been working in this area, he was the first patient who has made that level of recovery. I've had other patients that have got better but it's typically better by a few degrees. This guy was extremely well recovered and he was able to talk to us over the phone. He came in, he was clearly cognitively completely fine, he had returned to normal, he still had some physical difficulties with walking, but he is back at college, he takes himself on his wheelchair on the bus to school every day.

So that was interesting in and of itself, the fact that he had recovered. But what was then interesting is that he said, you know, 'I was very interested about the scanning that you did on me.' I said, 'What do you mean? And he said, 'Well, going into that fMRI scanner, that was kind of scary.' And it became apparent very quickly that he remembered absolutely every detail of the day nine months earlier when we scanned him.

And so we quickly pulled together a memory test. We had pictures of some of my students that he had met on that day and pictures of students he hadn't met and we showed him the pictures and we said, 'Do you remember any of these people?' And he said, 'Yes, that's Steve, your graduate student.' And I said, 'Can you tell me anything about Steve?' And he said, 'Yes, he's got a really deep voice.' This was a level of detail that even I didn't remember nine months later, but he remembered who it was, he said, 'Laura is your research coordinator.' We asked him what colour were the electrodes that we put on his head. He knew they were blue and not red.

Not only had he been entirely conscious, he had been taking mental note of absolutely every aspect of that day nine months earlier. And again, just to reiterate, at the time he appeared to be entirely vegetated. He made no responses, he gave us no information that would suggest he was anything but in a vegetative state. But nine months later he was able to tell us every last detail of that day that he came to visit us.

Lynne Malcolm: Incredible. So what are the implications for this research and the implications for I guess treatment and perhaps even diagnosis?

Adrian Owen: I'll take those in reverse order. The implications for diagnosis I think are pretty clear, that I think there is now no question that there are a reasonably large number of patients…and again, I'll say something like one in five, who appear to be entirely vegetative but are in fact absolutely conscious but just not able to respond. And that of course raises important ethical questions. I think it suggests that we do need to try and find these people, we have to improve the diagnosis, we have to put these patients into scanners and find out who they are and whether or not they really are in a vegetative state. So diagnosis is absolutely important.

There is a second issue which is about prognosis. Many people will be aware that reasonably frequently in most civilised countries there are legal cases surrounding the withdrawal of nutrition and hydration in some of these patients because they are very expensive to keep and sometimes they can survive for many years, decades even. So, fairly frequently there will be a case in any country, it happens in Australia I know, in Canada here it happens reasonably frequently that there will be a petition to have a patient's nutrition and hydration removed to allow them to die. And typically those cases turn on whether the patient has any chance of recovery and whether the patient has any level of consciousness. And of course we can answer that second question now with the imaging.

But we can also begin to answer the first question as well. And it turns out that if you do have responses in the scanner, there is a better chance of you recovering than if you don't. Very few of the patients that we see who aren't able to imagine playing tennis or who don't respond, very few of those people will actually go on to recover. But for those that can do these amazing tricks with their brain in the scanner, the chances of recovery are better. So again, this is useful information because it means that if we scan more of these patients we can begin to predict who has a chance of recovery, and therefore I guess by extension if we are going to put the limited resources that we have somewhere, where we should be putting them.

The question that is closest to my heart though that I think is raised by this is whether we can as often as possible give some autonomy back to the patient. The really heartbreaking thing about this group of patients is that decisions about their care and decisions about their future and often decisions about whether they live or die have to be made by close family members, and that is an awful situation. It's something that none of us want to do because we never really can get into the head of even the people that we love most. And I think if we can use this technology to return some of that decision-making capacity to the patient themselves, let the patient who is in this situation decide whether they have that new and dangerous treatment, or decide whether they live or die, then I think it's better than having other people decide for them, even if those other people are their nearest and dearest because honestly nobody wants to make those decisions on behalf of anybody else. And I think we will get into that situation very soon.

Lynne Malcolm: Adrian Owen and his team have not only used functional magnetic resonance imaging to detect consciousness, but have also used a technique known as electroencephalography. However, Adrian Owen emphasises the importance of combining the information gleaned from technology with human communication.

Adrian Owen: It's interesting in science how you have to tackle some of these issues, and the way we went about it is by actually communicating with some of these patients. We did the same thing with fMRI, back in 2006 I understood completely when people looked at these patterns of activity or blobs on the brain and said, 'How can you really know that that person is conscious?' For me, a neuroscientist with more than 20 years experience of imaging, I know that that blob couldn't have cropped up if the person hadn't been conscious. But I appreciate completely that somebody who doesn't have that expertise may not have that same level of faith in a picture of a blob on the brain.

That's really what pushed us to go on and start communicating with these patients because once you start to communicate with a patient and you ask them questions that you can't possibly know the answer to, there is no other possibility than that they are conscious. There's no way that I could know how a patient in 2010's father was Alexander and not Oscar, there's no way I could have known that the last place he went on vacation before his injury five years earlier was the United States of America. I only know it because he told me, and he could have only told me if he was conscious.

And the other example is the recent patient who recovered. Again, I'm sure this guy…most of us have never been into an MRI scanner, most of us have never been to an MRI scanning centre, the only time he did it was when he was supposedly in a vegetative state. So how could he have known this information if he actually hadn't been conscious at the time. So in a sense you can just use common sense to know that the methods are working without necessarily needing to resort to whether the statistics are correct or not.

Lynne Malcolm: And I think your work is considered by some as the first real example of demonstrating that fMRIs are really showing us something new.

Adrian Owen: Yes, it's interesting that you say that, and it's very gratifying. I get many, many letters now, 10 years on from that science paper, I get many letters from people that say they teach that paper in their courses around the world, which is satisfying, and the way they say they teach it is that yes, it was a demonstration of something that was truly useful with fMRI. I think that's probably giving it more credit than it deserves, but I think the point is that up until that point fMRI had been used for lots of what we used to call brain mapping, lots of working out which bits of the brain did what, which bit of the brain is involved in perceiving faces, which bit is involved in understanding speech.

And most of the work in the first few years of fMRI was confirmatory. We weren't finding new things out, we were checking what we thought we already knew and making sure that we were correct. We knew which part of the brain understands and processes speech long before fMRI came along, but fMRI helped us to confirm that and take it a little bit further. I think the interesting thing about our study is it was completely different. The idea that you could use fMRI to detect consciousness really sort of came out of nowhere because up until that point there was no way of detecting consciousness. There was no other method. We didn't know how to detect it. And suddenly we could do it and it turns out we could do it pretty reliably.

Lynne Malcolm: Professor Adrian Owen from the University of Western Ontario in Canada.

You'll find further information on the All in the Mind website, and from there, or on your ABC mobile app, you can also catch up on the story of Martin Pistorious and his reflection on ten years of being locked inside his body.

Martin Pistorious: I think that there is always hope, no matter how small. Treat people how you would want to be treated, with kindness, dignity, compassion and respect, whether you think they understand or not. Never underestimate the power of the mind, the importance of love and faith, and to never stop dreaming.

Lynne Malcolm: Thanks to producer Diane Dean and sound engineer Joe Wallace. I'm Lynne Malcolm. Great to have your company, until next time.