At the edges of awareness

Imagine this. Following a brain injury you lie in a hospital bed and from the outside you appear to be totally unconscious. You don’t respond to anything the doctors or your family say, you make no voluntary movements, and although you still go to sleep and wake up there seems to be nobody at home. But your ‘inner universe’ of conscious awareness still remains, perhaps flickering and inconsistent, but definitely there. How could anyone else ever know, and how could you ever communicate with your loved ones again?

Two new radio dramas, The Sky is Wider and Real Worlds, engage with these critical questions by drawing on the cutting edge of the neurology and neuroscience. Recent advances have enabled researchers to not only diagnose ‘residual’ awareness following severe brain injuries, but also to open new channels of communication with behaviourally unresponsive patients. The key medical challenge is to distinguish between the so-called ‘vegetative state’ in which there truly is no conscious awareness, from ‘minimally conscious’ or ‘locked-in’ conditions where some degree of consciousness persists (even normal consciousness, in the locked-in state), even though there are no outward signs.

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Brain activity during mental imagery, in a behaviourally unresponsive patient and in a  control subject.  Source: MRC via The Guardian

Linda Marshall Griffith’s drama The Sky is Wider takes inspiration from an ‘active approach’ in which the neurologist asks questions of the patient and monitors their brain activity for signs of response. In a classic study from about 10 years ago, Adrian Owen and his team asked behaviourally unresponsive patients to imagine either walking around their house or playing tennis, while their brains were scanned using functional MRI (which measures regional metabolic activity in the brain). These questions were chosen because imagining these different behaviours activates different parts of the brain, and so if we see these selective activations in a patient, we know that they have understood and are voluntarily following the instructions. If they can do this, they must be conscious. It turns out that between 10-20% of patients behaviourally diagnosed as being in the vegetative state can pass this test. Equally important, this same method can be used to establish simple communication by (for example) asking a patient to imagine playing ‘tennis’ to answer ‘yes’ and walking around a house to answer ‘no’.

These developments represent a revolution in clinical neurology. Current research is increasing the efficiency of active approaches by using the more portable electroencephalography (EEG) instead of bulky and expensive MRI. ‘Passive’ techniques in which residual consciousness can be inferred without requiring patients to perform any task are also rapidly improving. These methods are important because active approaches may underestimate the incidence of residual awareness since not all conscious patients may understand or be able to follow verbal instructions.

Alongside these scientific developments we encounter pressing ethical questions. How should we treat patients in these liminal states of awareness? And given a means of communication, what kinds of questions should we ask? The Sky is Wider explores these challenging ethical issues in a compelling narrative which gives dramatic voice to the mysterious conditions of the vegetative and minimally conscious states.


 

In Real Worlds, Jane Rogers takes us several years into the future. Communication with behaviourally unresponsive patients is now far advanced and is based on amazing developments in ‘virtual reality’. The clinical context for this drama is the ‘locked-in syndrome’ where a patient may have more-or-less normal conscious experiences but completely lack the ability to move. In Real Worlds, a locked-in patient transcends these limitations by controlling a virtual reality avatar directly using brain signals. These avatars inhabit virtual worlds in which the avatars of different people can interact, while the ‘real’ person behind each may remain hidden and unknown.

This drama deliberately inhabits the realm of science fiction, but there is solid science behind it too. The development of so-called ‘brain computer interfaces’ (BCI) is moving fast. These interfaces combine brain imaging methods (like EEG or fMRI, or sometimes more ‘invasive’ methods’ in which electrodes are inserted directly into the brain) with advanced machine learning methods to perform a kind of ‘brain-reading’. The idea is to infer, from brain activity alone, intended movements, perceptions, and perhaps even thoughts. These decoded ‘thoughts’ can then be used to control robotic devices, or virtual avatars. In some cases, a person’s own body might be controlled via direct stimulation of muscles. Progress in this area has been remarkably rapid. In a landmark but rather showy example, the Brazilian neuroscientist Miguel Nicolelis used a BCI to allow a paralysed person to ‘kick’ the first ball of the 2014 football world cup, through brain-control of a robotic avatar. More recently, brain-reading methods have allowed a paralysed man to play Guitar Hero for the first time since his injury.

The other technology highlighted in Real Worlds is virtual reality (VR), which – thanks to its enormous consumer potential – is developing even more rapidly. All the major technology and AI companies are getting in on the act, and VR headsets are finally becoming cheap enough, comfortable enough, and powerful enough to define a new technological landscape. Here at the Sackler Centre for Consciousness Science at the University of Sussex, we are exploring how VR can help shed light on our normal conscious experience. In one example, we use a method called ‘augmented reality’ (AR) to project a ‘virtual’ body into the real world as seen through a camera mounted on the front of a VR headset. This experiment revealed how our perception of what is (and what is not) our own body can be easily manipulated, indicating that our experience of ‘body ownership’, which is so easy to take for granted, is in fact continuously and actively generated by the brain. In a second example, we developed a method called ‘substitutional reality’ in which a VR headset is coupled with panoramic video and audio taken from a real environment, manipulated in various ways. The resulting experiences are much more immersive than current computer-generated virtual environments and in some cases people cannot distinguish them from actually ‘real’ environments.

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A ‘virtual reality’ hand, part of a Sackler Centre study to explore the mechanisms underlying experiences of body ownership.  VR programming by Dr. Keisuke Suzuki.

Just as in the first drama, ethical questions risk outpacing the science and technology. As VR becomes increasingly immersive and pervasive, its potential to impact our real lives is ever more powerful. While benefits are easy to imagine – for instance in bringing distant relatives together or enabling remote experiences of inaccessible places – there are also legitimate concerns. High on the list would be what happens if people become increasingly unable to distinguish the real world from the virtual, whether in the moment or (more plausibly) in their memories. And what if they progressively withdrew from ‘reality’ if the available virtual worlds became more appealing places to be? Of course, simple dichotomies are unhelpful since VR technologies are part of our real worlds, just like mobile phones and laptop computers. Jane Rogers’ Real Worlds explores these complex ethical issues by imagining VR as a future treatment – perhaps ‘prosthesis’ would be a better word – for the disorders of consciousness like those encountered in The Sky is Wider.

Together, these dramas explore the human and societal consequences of existing and near-future clinical technologies. With artistic license they ask important questions that scientists and clinicians are not yet equipped to address. Ultimately, I think they convey an optimistic message, that we can understand and treat – if not cure – severely debilitating conditions that may otherwise have remained undiagnosed let alone treated. But they also lead us to consider, not just what we could do, but what we should do.


The Sky is Wider (written by Linda Marshall Griffiths) and Real Worlds (written by Jane Rogers) were produced by Nadia Molinari for BBC Radio 4. I acted as the scientific consultant. The original ideas were formulated during a 2014 Wellcome Trust ‘Experimental Stories’ workshop in a conversation between myself, Nadia, and Linda.

The science of selfhood

lorna-zoe-wanamaker-by-johan-persson2-1200x800.jpgZoë Wanamaker as Lorna in Nick Payne’s Elegy.

“The brain is wider than the sky,
For, put them side by side,
The one the other would contain,
With ease, and you besides”

Emily Dickinson, Complete Poems, 1924

What does it mean to be a self? And what happens to the social fabric of life, to our ethics and morality, when the nature of selfhood is called into question?

In neuroscience and psychology, the experience of ‘being a self’ has long been a central concern. One of the most important lessons, from decades of research, is that there is no single thing that is the self. Rather, the self is better thought of as an integrated network of processes that distinguish self from non-self at many different levels. There is the bodily self – the experience of identifying with and owning a particular body, which at a more fundamental level involves the amorphous experience of being a self-sustaining organism. There is the perspectival self, the experience of perceiving the world from a particular first-person point-of-view. The volitional self involves experiences of intention of agency, of urges to do this-or-that (or, perhaps more importantly, to refrain from doing this-or-that) and of being the cause of things that happen.

At higher levels we encounter narrative and social selves. The narrative self is where the ‘I’ comes in, as the experience of being a continuous and distinctive person over time. This narrative self – the story we tell ourselves about who we are – is built from a rich set of autobiographical memories that are associated with a particular subject. Finally, the social self is that aspect of my self-experience and personal identity that depends on my social milieu, on how others perceive and behave towards me, and on how I perceive myself through their eyes and minds.

In daily life, it can be hard to differentiate these dimensions of selfhood. We move through the world as seemingly unified wholes, our experience of bodily self seamlessly integrated with our memories from the past, and with our experiences of volition and agency. But introspection can be a poor guide. Many experiments and neuropsychological case studies tell a rather different story, one in which the brain actively and continuously generates and coordinates these diverse aspects of self-experience.

The many ways of being a self can come apart in surprising and revealing situations. For example, it is remarkably easy to alter the experience of bodily selfhood. In the so-called ‘rubber hand illusion,’ I ask you to focus your attention on a fake hand while your real hand is kept out of sight. If I then simultaneously stroke your real hand and the fake hand with a soft paintbrush, you may develop the uncanny feeling that the fake hand is now, somehow, part of your body. A more dramatic disturbance of the experience of body ownership happens in somatoparaphrenia, a condition in which people experience that part of their body is no longer theirs, that it belongs to someone else – perhaps their doctor or family member. Both these examples involve changes in brain activity, in particular within the ‘temporo-parietal junction’, showing how even very basic aspects of personal identity are actively constructed by the brain.

Moving through levels of selfhood, autoscopic hallucinations involve seeing oneself from a different perspective, much like ‘out of body’ experiences. In akinetic mutism, people seem to lack any experiences of volition or intention (and do very little), while in schizophrenia or anarchic hand syndrome, people can experience their intentions or voluntary actions as having external causes. At the other end of the spectrum, disturbances of social self emerge in autism, where difficulties in perceiving others’ states of mind seems to be a core problem, though the exact nature of the autistic condition is still much debated.

When it comes to the ‘I’, memory is the key. Specifically, autobiographical memory: the recollection of personal experiences of people, objects, and places and other episodes from an individual’s life. While there are as many types of memory as there are varieties of self (for example, we have separate memory processes for facts, for the short term and the long term, and for skills that we learn), autobiographical memories are those most closely associated with our sense of personal identity. This is well illustrated by some classic medical cases in which, as a result of surgery or disease, the ability to lay down new memories is lost. In 1953 Henry Moliason (also known as the patient HM) had large parts of his medial temporal lobes removed in order to relieve severe epilepsy. From 1957 until his death in 2008, HM was studied closely by the neuropsychologist Brenda Milner, yet he was never able to remember meeting her. In 1985 the accomplished musician Clive Wearing suffered a severe viral brain disease that affected similar parts of his brain. Now 77, he frequently believes he has just awoken from a coma, spending each day in a constant state of re-awakening.

Surprisingly, both HM and Wearing remained able to learn new skills, forming new ‘procedural’ memories, despite never recalling the learning process itself. Wearing could still play the piano, and conduct his choir, though he would immediately forget having done so. The music appears to carry him along from moment to moment, restoring his sense of self in a way his memory no longer can. And his love for his wife Deborah seems undiminished, so that he expresses an enormous sense of joy on seeing her, even though he cannot tell whether their last meeting was years, or seconds, in the past. Love, it seems, persists when much else is gone.

For people like HM and Clive Wearing, memory loss has been unintended and unwanted. But as scientific understanding develops, could we be moving towards a world where specific memories and elements of our identity can be isolated or removed through medical intervention? And could the ability to lay down new memories ever be surgically restored? Some recent breakthroughs suggest these developments may not be all that far-fetched.

In 2013, Jason Chan and Jessica LaPaglia, from Iowa State University showed that specific human memories could indeed be deleted. They took advantage of the fact that when memories are explicitly recalled they become more vulnerable. By changing details about a memory, while it was being remembered, they induced a selective amnesia which lasted for at least 24 hours. Although an important advance, this experiment was limited by relying on ‘non-invasive’ methods – which means not using drugs or directly interfering with the brain.

More recent animal experiments have shown even more striking effects. In a ground-breaking 2014 study at the University of California, using genetically engineered mice, Sadegh Nabavi and colleagues managed to block and then re-activate a specific memory. They used a powerful (invasive) technique called optogenetics to activate (or inactivate) the biochemical processes determining how neurons change their connectivity. And elsewhere in California, Ted Berger is working on the first prototypes of so-called ‘hippocampal prostheses’ which replace a part of the brain essential for memory with a computer chip. Although these advances are still a long way from implementation in humans, they show an extraordinary potential for future medical interventions.

The German philosopher Thomas Metzinger believes that “no such things as selves exist in the world”. Modern neuroscience may be on his side, with memory being only one thread in the rich tapestry of processes shaping our sense of selfhood. At the same time, the world outside the laboratory is still full of people who experience themselves – and each other – as distinct, integrated wholes. How the new science of selfhood will change this everyday lived experience, and society with it, is a story that is yet to be told.

Originally commissioned for the Donmar Warehouse production of Elegy, with support from The Wellcome Trust.  Reprinted in the programme notes and in Nick Payne’s published script.