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.
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
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.
A small boy’s mundane antics become high drama, as he unwittingly involves unsuspecting people in round after deadly round of Russian roulette
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.
Even though the second patient had been lying in a coma for 16 years, his brain response matched the reactions of healthy people who’d seen the film
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.
Update: This article has been edited to more accurately reflect Lorina Naci's status.
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