How the magic of cinema unlocked one man’s coma-bound world

Image from NIH. Click for source.An Alfred Hitchcock film helped to prove one patient had been conscious while in a coma-like state for 16 years. The discovery shows that neuroscience may still have lots to learn from the ancient art of storytelling, says Tom Stafford.

If brain injury steals your consciousness then you are in a coma: we all know that. What is less well known is that there exist neighbouring states to the coma, in which victims keep their eyes open, but show no signs of consciousness. The vegetative state, or ‘unresponsive wakefulness syndrome’, is one in which the patient may appear to be awake, and even goes to sleep at times, but otherwise shows no reaction to the world. Patients who do inconsistently respond, such as by flinching when their name is called, or following a bright object with their eyes, are classified as in a ‘minimally conscious state’. Both categories of patients show no signs of deliberate actions, or sustained reaction to the environment, and until recently there was no way for anyone to discern their true, inner, level of consciousness.

The fear is that, like the ‘locked-in syndrome’ that can occur after strokes, these patients may be conscious, but are just unable to show it. The opposite possibility is that these patients are as unconscious as someone in the deepest coma, with only circuitry peripheral to consciousness keeping their eyes open and producing minimal responses automatically.

In the last 10 years, research spearheaded by cognitive neuroscientist Adrian Owen has transformed our understanding of these shadowlands of consciousness. There is now evidence, obtained using brain scans, that some patients (around one in five) in these ‘wakeful coma’ states have conscious awareness. If asked to imagine playing tennis, the brain areas specifically controlling movement become active. If asked to imagine finding their way around their house, the brain regions involved in navigation become active. Using these signals a small minority of patients have even communicated with the outside world, with the brain scanner helping observers to mind-read their answers to questions.

The practical and ethical implications of these findings are huge, not least for the treatment of the hundreds of thousands of people who are in hospitals around the world in these conditions right now.

But the meaning of the research is still hotly debated. One issue is that the mind reading uses neural responses to questions or commands, and careful controls are needed to ensure that their patients’ brains aren’t just responding automatically without any actual conscious involvement. A second issue, and one that cannot be controlled away, is that the method used may tell us that these patients are capable of responding, but it doesn’t tell us much about the quality of conscious experience they are having. How alert, aware and focused they are is hard to discern.

In a relatively new study, a post-doctoral fellow at Owen’s lab, Lorina Naci, has used cinema to show just how sophisticated conscious awareness can be in a ‘minimally conscious’ patient.

The trick they used involved an 8 minute edit of “Bang! You’re dead”, a 1961 episode of “Alfred Hitchcock Presents”. In the film, a young boy with a toy gun obsession wanders around aiming and firing at people. Unbeknownst to him, and the adults he aims at, on this day he has found a real gun and it has a live bullet in the chamber.

The film works because of this hidden knowledge we, the viewers, have. Knowing about the bullet, a small boy’s mundane antics become high drama, as he unwittingly involves unsuspecting people in round after deadly round of Russian roulette.

Naci showed the film to healthy participants. To a separate group she showed a scrambled version involving rearranged one-second segments. This ‘control’ version was important because it contained many of the same features as the original; the same visual patterns, the same objects, the same actions. But it lacked the crucial narrative coherence – the knowledge of the bullet – which generated the suspense.

Using brain scanning, and the comparison of the two versions of the film, Naci and colleagues were able to show that the unscrambled, suspenseful version activated nearly every part of the cortex. Everything from primary sensory areas, to motor areas, to areas involved in memory and anticipation were engaged (as you might hope from a film from one of the masters of storytelling). The researchers were particularly interested in a network of activity that rose and fell in synchrony across ‘executive’ areas of the brain – those known to be involved in planning, anticipation, and integrating information from different sources. This network, they found, responded to the moments of highest suspense in the film; the moments when the boy was about to fire, for example. These were the moments you could only find so dramatic if you were following the plot.

Next the researchers showed the film to two patients in wakeful comas. In one, the auditory cortex became activated, but nothing beyond this primary sensory region. Their brain was responding to sounds, perhaps automatically, but there was no evidence of more complex processing. But in a second patient, who had been hospitalised and non-responsive for 16 years, his brain response matched those of the healthy controls who’d seen the film. Like them, activity across the cortex rose and fell with the action of the film, indicating an inner consciousness rich enough to follow the plot.

The astounding result should make us think carefully about how we treat such patients and marks an advance on the arsenal of techniques we can use to connect to the inner lives of non-responsive patients. It also shows how cognitive neuroscience can benefit from the use of more complex stimuli, such as movies, rather than the typically boring visual patterns and simple button-press responses that scientists usually use to probe the mysteries of the brain.

The genius of this research is that to test for the rich consciousness of the patient who appears unresponsive you need to use rich stimuli. The Hitchcock film was perfect because of its ability to create drama by what we believe and expect not because of what we merely see.

My BBC Future column from last week. The original is here. The original paper is: Naci, L., Cusack, R., Anello, M., Owen, A. M. A common neural code for similar conscious experiences in different individuals. PNAS. 2014;111(39):14277–82.

Twelve minutes of consciousness

The Economist has an excellent video on consciousness, what it is, why and how it evolved.

The science section of The Economist has long had some of the best science reporting in the mainstream press and this video is a fantastic introduction to the science of consciousness.

It’s 12 minutes long and it’s worth every second of your time.

Intuitions about free will and the brain

Libet’s classifc experiment on the neuroscience of free will tells us more about our intuition than about our actual freedom

It is perhaps the most famous experiment in neuroscience. In 1983, Benjamin Libet sparked controversy with his demonstration that our sense of free will may be an illusion, a controversy that has only increased ever since.

Libet’s experiment has three vital components: a choice, a measure of brain activity and a clock.

The choice is to move either your left or right arm. In the original version of the experiment this is by flicking your wrist; in some versions of the experiment it is to raise your left or right finger. Libet’s participants were instructed to “let the urge [to move] appear on its own at any time without any pre-planning or concentration on when to act”. The precise time at which you move is recorded from the muscles of your arm.

The measure of brain activity is taken via electrodes on the scalp. When the electrodes are placed over the motor cortex (roughly along the middle of the head), a different electrical signal appears between right and left as you plan and execute a movement on either the left or right.

The clock is specially designed to allow participants to discern sub-second changes. This clock has a single dot, which travels around the face of the clock every 2.56 seconds. This means that by reporting position you are reporting time. If we assume you can report position accurately to 5 degree angle, that means you can use this clock to report time to within 36 milliseconds – that’s 36 thousandths of a second.

Putting these ingredients together, Libet took one extra vital measurement. He asked participants to report, using the clock, exactly the point when they made the decision to move.

Physiologists had known for decades that a fraction of a second before you actually move the electrical signals in your brain change. So it was in Libet’s experiment, a fraction of a second before participants moved, a reliable change could be recorded using the electrodes. But the explosive result was when participants reported deciding to move. This occurred in between the electric change in the brain and the actual movement. This means, as sure as cause follows effect, that the feeling of deciding couldn’t be a timely report of whatever was causing the movement. The electrode recording showed that the decision had – in some sense – already been made before the participants were aware of having taken action. The brain signals were changing before the subjective experience of taking a decision occurred.

Had participants’ brains already made the decision? Was the feeling of choosing just an illusion? Controversy has raged ever since. There is far more to the discussion about neuroscience and free will than this one experiment, but its simplicity has allowed it to capture the imagination of many who think our status as biological creatures limits our free will, as well as those who argue that free will survives the challenge of our minds being firmly grounded in our biological brains.

Part of the appeal of the Libet experiment is due to two pervasive intuitions we have about the mind. Without these intuitions the experiment doesn’t seem so surprising.

The first intuition is the feeling that our minds are a separate thing from our physical selves – a natural dualism that pushes us to believe that the mind is a pure, abstract place, free from biological constraints. A moment’s thought about the last time you were grumpy because you were hungry shatters this illusion, but I’d argue that it is still a persistent theme in our thinking. Why else would we be the least surprised that it is possible to find neural correlates of mental events? If we really believed, in our heart of hearts, that the mind is based in the brain, then we would know that every mental change must have a corresponding change in the brain.

The second pervasive intuition, which makes us surprised by the Libet experiment, is the belief that we know our own minds. This is the belief that our subjective experience of making decisions is an accurate report of how that decision is made. The mind is like a machine – as long as it runs right, we are happily ignorant of how it works. It is only when mistakes or contradictions arise that we’re drawn to look under the hood: Why didn’t I notice that exit? How could I forget that person’s name? Why does the feeling of deciding come after the brain changes associated with decision making?

There’s no reason to think that we are reliable reporters of every aspect of our minds. Psychology, in fact, gives us lots of examples of where we often get things wrong. The feeling of deciding in the Libet experiment may be a complete illusion – maybe the real decision really is made ‘by our brains’ somehow – or maybe it is just that the feeling of deciding is delayed from our actual deciding. Just because we erroneously report the timing of the decision, doesn’t mean we weren’t intimately involved in it, in whatever meaningful sense that can be.

More is written about the Libet experiment every year. It has spawned an academic industry investigating the neuroscience of free will. There are many criticisms and rebuttals, with debate raging about how and if the experiment is relevant to the freedom of our everyday choices. Even supporters of Libet have to admit that the situation used in the experiment may be too artificial to be a direct model of real everyday choices. But the basic experiment continues to inspire discussion and provoke new thoughts about the way our freedom is rooted in our brains. And that, I’d argue, is due to the way it helps us confront our intuitions about the way the mind works, and to see that things are more complex than we instinctively imagine.

This is my latest column for BBC Future. The original is here. You may also enjoy this recent post on Critical strategies for free will experiments

Critical strategies for free will experiments

waveBenjamin Libet’s experiment on the neuroscience of free will needs little introduction. (If you do need an introduction, it’s the topic of my latest column for BBC Future). His reports that the subjective feeling of making a choice only come after the brain signals indicating a choice has been made are famous, and have produced controversy ever since they were published in the 1980s.

For a simple experiment, Libet’s paradigm admits to a large number of interpretations, which I think is an important lesson. Here are some common, and less common, critiques of the experiment:

The Disconnect Criticism

The choice required from Libet’s participants was trivial and inconsequential. Moreover, they were specifically told to make the choice without any reason (“let the urge [to move] appear on its own at any time without any pre-planning or concentration on when to act”). A common criticism is that this kind of choice has little to tell us about everyday choices which are considered, consequential or which are actively trying to involve ourselves in.

The timing criticism(s)

Dennett discusses how the original interpretation of the experiment assumes that the choosing self exists at a particular point and at particular time – so, for example, maybe in some central ‘Cartesian Theatre’ in which information from motor cortex and visual cortex come together, but crucially, does not have direct report of (say) the information about timing gathered by the visual cortex. Even in a freely choosing self, there will be timing delays as information on the clock time is ‘connected up’ with information on when the movement decision was made. These, Dennett argues, could produce the result Libet saw without indicating a fatal compromise for free choice.

My spin on this is that the Libet result shows, minimally, that we don’t accurately know the timing of our decisions, but inaccurate judgements about the timing of decisions doesn’t mean that we don’t actually make the decisions themselves that are consequential.

Spontaneous activity

Aaron Schurger and colleagues have a nice paper in which they argue that Libet’s results can be explained by variations in spontaneous activity before actions are taken. They argue that the movement system is constantly experiencing sub-threshold variation in activity, so that at any particular point in time you are more or less close to performing any particular act. Participants in the Libet paradigm, asked to make a spontaneous act, take advantage of this variability – effectively lowering their threshold for action and waiting until the covert fluctuations are large enough to trigger a movement. Importantly, this reading weakens the link between the ‘onset’ of movements and the delayed subjective experience of making a movement. If the movement is triggered by random fluctuations (observable in the rise of the electrode signal) then there isn’t a distinct ‘decision to act’ in the motor system, so we can’t say that the subjective decision to act reliably comes afterwards.

The ‘only deterministic on average’ criticism

The specific electrode signal which is used to time the decision to move in the brain is called the readiness potential (RP). Electrode readings are highly variable, so the onset of the RP is a statistical artefact, produced by averaging over many trials (40 in Libet’s case). This means we lose the ability to detect, trial-by-trial, the relation between the brain activity related to movement and the subjective experience. Libet reports this in his original paper [1] (‘only the average RP for the whole series could be meaningfully recorded’, p634). On occasion the subjective decision time (which Libet calls W) comes before the time of even the average RP, not after (p635: “instances in which individual W time preceded onset time of averaged RP numbered zero in 26 series [out of 36] – which means that 28% of series saw at least one instance of W occurring before the RP).

The experiment showed strong reliability, but not complete reliability (the difference is described by Libet as ‘generally’ occurring and as being ‘fairly consistent’, p636). What happened next to Libet’s result is a common trick of psychologists. A statistical pattern is discovered and then reality is described as if the pattern is the complete description: “The brain change occurs before the choice”.

Although such generalities are very useful, they are misleading if we forget that they are only averagely true, not always true. I don’t think Libet’s experiment would have the imaginative hold if the result was summarised as “The brain change usually occurs before the choice”.

A consistent, but not universal, pattern in the brain before a choice has the flavour of a prediction, rather than a compulsion. Sure, before we make a choice there are antecedents in the brain – it would be weird if there weren’t – but since these don’t have any necessary consequence for what we choose, so what?

To my mind the demonstration that you can use fMRI to reproduce the Libet effect but with brain signals changing up to 10 seconds before the movement (and an above chance accuracy at predicting the movement made), only reinforces this point. We all believe that the mind has something to do with the brain, so finding patterns in the brain at one point which predict actions in the mind at a later point isn’t surprising. The fMRI result, and perhaps Libet’s experiment, rely as much on our false intuition about dualism as conclusively demonstrating anything new about freewill.

Link: my column Why do we intuitively believe we have free will?

Never mind the neuromarketing

CC Licensed Photo by Flickr user SMI Eye Tracking. Click for source.I’ve got an article in The Observer about the state of neuromarketing – where companies pay millions of wasted dollars to apply brain science to marketing.

The piece looks at the three forms of neuromarketing – advertising fluff, serious research, and applied neuroscience. The first is clearly bollocks, the second a solid but currently abstract science, and the third a triumph of selling style over substance.

Finally, there is the murky but profitably grey area of applied neuromarketing, which is done by commercial companies for big-name clients. Here, the pop-culture hype that allows brain-based nonsense in consumer adverts meets the abstract and difficult-to-apply results from neuromarketing science. The result is an intoxicating but largely ineffective mix that makes sharp but non-specialist executives pay millions in the hope of maximising their return on branding and advertising.

The piece also looks at what turns out to be the most powerful innovation in marketing taken from cognitive science, but which doesn’t make the headlines like neuromarketing.

Full article at the link below.

Link to article in The Observer.

She’s giving me hallucinations

Last year I did a talk in London on auditory hallucinations, The Beach Boys and the psychology and neuroscience of hallucinated voices, and I’ve just discovered the audio is available online.

It was part of the Pint of Science festival where they got scientists to talk about their area of research in the pub, which is exactly what I did.

The audio is hosted on SoundCloud which gives you an online stream but there’s no mp3 download facility. However, if you type the page URL into the AnythingToMP3 service it’ll present you with you an mp3 to download.

It was a fun talk, so do enjoy listening.

UPDATE: The nice folks at Pint of Science have made the mp3 downloadable directly from the SoundCloud page so no second website trickery needed.

Link to audio of Vaughan’s talk on hallucinated voices.

How is the brain relevant in mental disorder?

The Psychologist has a fascinating article on how neuroscience fits in to our understanding of mental illness and what practical benefit brain science has – in lieu of the fact that it currently doesn’t really help us a great deal in the clinic.

It is full of useful ways of thinking about how neuroscience fits into our view of mental distress.

The following is a really crucial section, that talks about the difference between proximal (closer) and distal (more distant) causes.

In essence, rather than talking about causes we’re probably better off talking about causal pathways – chains of events that can lead to a problem – which can include common elements but different people can arrive at the same difficulty in different ways.

A useful notion is to consider different types of causes of symptoms lying on a spectrum, the extremes of which I will term ‘proximal’ and ‘distal’. Proximal causes are directly related to the mechanisms driving symptoms, and are useful targets for treatment; they are often identified through basic science research. For example, lung cancer is (proximally) caused by malfunction in the machinery that regulates cell division. Traditional lung cancer treatments tackle this cause by removing the malfunctioning cells (surgery) or killing them (standard chemotherapy and radiotherapy)…

By contrast, distal causes are indirectly related to the mechanisms driving symptoms, and are useful targets for prevention; they are often identified through epidemiology research. Again, take the example of lung cancer, which is (distally) caused by cigarette smoking in the majority of cases, though it must be caused by other factors in people who have never smoked. These could be genetic (lung cancer is heritable), other types of environmental trigger (e.g. radon gas exposure) or some interaction between the two. Given the overwhelming evidence that lung cancer is (distally) caused by smoking, efforts at prevention rightly focus on reducing its incidence. However, after a tumour has developed an oncologist must focus on the proximal cause when proposing a course of treatment…

The majority of studies of depression have focused on distal causes (which psychologists might consider ‘underlying’). These include: heritability and genetics; hormonal and immune factors; upbringing and early life experience; and personality. More proximal causes include: various forms of stress, particularly social; high-level psychological constructs derived from cognitive theories (e.g. dysfunctional negative schemata); low-level constructs such as negative information processing biases (also important in anxiety); and disrupted transmission in neurotransmitter systems such as serotonin.

It’s not a light read, but it is well worth diving into it for a more in-depth treatment of the brain and mental illness.

Link to Psychologist article neuroscience and mental health.