Into the Gray Zone: A Neuroscientist Explores the Border Between Life and Death

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INTO the GRAY ZONE

The model of how pop science involving sensational subjects should be done.

—The Globe and Mail (Toronto)

Fascinating . . . With remarkable clarity, Owen punctuates his findings with concise dispatches on the human condition and the disparities between what is considered quality of life and what some consider an inhumane, dysfunctional existence. . . . A striking scientific journey that draws hopeful attention to how the brain reacts, restores, and perseveres despite grave injury.

—Kirkus Reviews

"[A] fascinating memoir . . . The Gray Zone reads like a thriller as [Owen] recounts his and his teams’ efforts to explore [the] ‘gray zone.’ . . . Owen’s enthusiasm for his science crackles from the pages. His determination to fight for the scores of voiceless gray-zone patients he encounters, to prove they’re ‘thinking, feeling people,’ is hugely thought-provoking and deeply moving."

—Mail on Sunday (UK)

Meshing memoir with scientific explication, Owen reveals how functional magnetic resonance imaging can probe the deep space of trapped minds. It’s a riveting read, from the march of technology and tests for neural responses—such as imagining playing a game of tennis—to extraordinary personal accounts of the ‘gray zone’ by partially recovered patients.

—Nature

"Into the Gray Zone weaves a fascinating tale using medical data, heart-wrenching case studies, and [Owen’s] own personal experiences."

—Good Housekeeping

Groundbreaking . . . a fascinating and accessible account of cutting-edge science, and of those whose lives have been altered in an instant. . . . Owen’s enthusiasm for his subject is infectious. . . . This book will be required reading for anyone sitting by a loved one’s bedside, caregivers, doctors, ethicists, lawyers, and philosophers.

—The Sunday Times (London)

Vivid, emotional, and thought-provoking . . . Owen’s story of horror and hope will long haunt readers.

—Publishers Weekly

"Into the Gray Zone is required reading for anyone who wants to explore the outer limits of consciousness, and the human spirit. Neuroscientist Adrian Owen takes us on a gripping, often harrowing journey into the most mysterious realm of human experience: the twilight zone between life and death."

—Joshua Horwitz, author of War of the Whales: A True Story, winner of the 2015 PEN/E. O. Wilson Literary Science Writing Award

A fascinating and highly readable book, written with evangelical fervor . . . gripping and moving.

—New Statesman (UK)

[A] remarkable book . . . Through examinations of human brains damaged by trauma, tumors, infections, and vascular accidents, [Owen] attempts to explore the nature of consciousness. . . . [His] experiments have allowed vegetative-state patients with residual consciousness to connect with the external world.

—Literary Review (UK)

"Although he has written hundreds of research papers about his work, Into the Gray Zone is Owen’s first book pulling it all together in fast-paced prose. Readers should prepare to be educated, yes. But more satisfyingly, they should prepare to be fascinated, astonished, and, at times, moved to tears."

—Winnipeg Free Press

"Into the Gray Zone is both a crystal-clear description of cutting-edge neuroscience from one of the pioneers in the field, and a set of intensely personal stories about patients in the twilight of consciousness. . . . One of the most moving and gripping science books you’re ever likely to read."

—Daniel Bor, author of The Ravenous Brain: How the New Science of Consciousness Explains Our Insatiable Search for Meaning

This is a great book—immensely moving, profound, and engaging, with a zest for life and science that bubbles off the page. . . . Adrian Owen has lived the dream of a neuroscientific discovery that changes thinking about a terrifying medical condition and how patients and their families can be given the answers they crave. Reading how this happened will make you alternately laugh, gasp, and cry.

—John Duncan, author of How Intelligence Happens

An unforgettable book. Owen weaves together stories of human resilience in the face of extraordinary adversity with an account of his own groundbreaking research, and in so doing takes us on a deeply moving journey to the very frontiers of consciousness. I couldn’t put it down.

—Tim Bayne, author of The Unity of Consciousness

An amazing book that challenges basic assumptions about what it means to be a person! What’s on display here is a curious branch of brain research that is both fascinating and, frankly, terrifying. . . . It should be required reading for anyone interested in the brain, and especially for all those who care for patients thought to be in a vegetative state.

—Katrina Firlik, author of Another Day in the Frontal Lobe: A Brain Surgeon Exposes Life on the Inside

Provides fascinating insight into cutting-edge neuroscience and the power of the human psyche. . . . Time and again, we are taken to the edge of our seats, reflecting on what it means to be alive and how hope can triumph in the most tragic of circumstances.

—Richard Wiseman, bestselling author of The Luck Factor and 59 Seconds: Think a Little, Change a Lot

Truly moving and inspirational . . . an uplifting testament to the power of scientific curiosity and the extraordinary resilience of the human spirit. This book delivers an eloquent message: even in the most desperate circumstances, there can be hope.

—Roger Highfield, former editor of New Scientist and coauthor of SuperCooperators and The Arrow of Time

"Simply unputdownable . . . Taking my evening bath while dipping into the opening pages of Into the Gray Zone, I finished three hours later, with the water cold. What kept me in the bathtub is Owen’s account of communicating with the most impaired neurological patients—those unfortunate individuals whose damaged bodies and brains often put them at a greater distance from us than an astronaut lost in space."

—Christof Koch, PhD, president and chief scientific officer, Allen Institute for Brain Science

What an amazing read! . . . The book is a real page-turner, both because it unpacks the complexities of modern neuroscience in an accessible way and because it directly confronts profound ethical questions.

—Melvyn Goodale, PhD, coauthor of Sight Unseen: An Exploration of Conscious and Unconscious Vision

Captivating . . . In this book, which will bring new hope to many, we see Owen explore new realms of consciousness—ones experienced by patients who are devastated by brain injury yet surprisingly endowed with thought, feeling, and memory.

—Kevin Nelson, author of The Spiritual Doorway in the Brain: A Neurologist’s Search for the God Experience

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CONTENTS

For Jackson

In case I’m not here to tell you the story myself

That you may see the meaning of within

It is being

It is being

—John Lennon and Paul McCartney

PROLOGUE

I’d been watching Amy for almost an hour when she finally moved. She had been sleeping when I arrived at her bedside in a small Canadian hospital a few miles from Niagara Falls. It seemed unnecessary, even a little rude, to wake her. I knew there was little point in trying to assess vegetative-state patients when they are half-asleep.

It wasn’t much of a movement. Amy’s eyes flicked open; her head came up off the pillow. She stayed that way, rigid and unblinking, her eyes roving around the ceiling. Her thick dark hair was cropped short, but perfectly styled, as though someone had been working on it only moments earlier. Was this sudden movement simply the result of automatic firing of the neural circuitry in her brain?

I peered into Amy’s eyes. All I saw was emptiness. That same deep well of emptiness that I had seen countless times before in people who, like Amy, were thought to be awake but unaware. Amy gave nothing back. She yawned. A big openmouthed yawn, followed by an almost mournful sigh as her head collapsed back onto the pillow.

Seven months after her accident, it was hard to imagine the person Amy must once have been—a smart college-varsity basketball player with everything to live for. She’d left a bar late one night with a group of friends. The boyfriend she’d walked out on earlier that evening was waiting. He shoved her and she toppled, slamming her head on a concrete curb. Another person might have walked away with a few stitches or a concussion, but Amy was not so lucky. Her brain hit the inside of her skull. It pulled from its moorings. Axons stretched and blood vessels tore as ripples of shock waves lacerated and bruised critical regions far from the point of impact. Now Amy had a feeding tube surgically inserted into her stomach that supplied her with essential fluids and nutrients. A catheter drained her urine. She had no control over her bowels, and she was in diapers.

Two male doctors breezed into the room. What do you think? said the more senior of the two, looking straight at me.

I won’t know unless we do the scans, I replied.

Well, I’m not a betting man, but I’d say she’s in a vegetative state! He was upbeat, almost jovial.

I didn’t respond.

The two doctors turned to Amy’s parents, Bill and Agnes, who’d been patiently sitting while I observed her. A good-looking couple in their late forties, they were clearly exhausted. Agnes gripped Bill’s hand as the doctors explained that Amy didn’t understand speech or have memories, thoughts, or feelings, and that she couldn’t feel pleasure or pain. They gently reminded Bill and Agnes that she would require round-the-clock care for as long as she lived. In the absence of an advanced directive stating otherwise, shouldn’t they consider taking Amy off life support and allowing her to die? After all, isn’t that what she would have wanted?

Amy’s parents weren’t ready to take that step and signed a consent form to allow me to put her in an fMRI scanner and search for signs that some part of the Amy they loved was still there. An ambulance shuttled Amy to Western University in London, Ontario, where I run a lab that specializes in the assessment of patients who have sustained acute brain injuries or suffer from the ravages of neurodegenerative diseases such as Alzheimer’s and Parkinson’s. Through incredible new scanning technology, we connect with these brains, visualizing their function and mapping their inner universe. In return, they reveal to us how we think and feel, the scaffolding of our consciousness, and the architecture of our sense of self—they illuminate the essence of what it means to be alive and human.

Five days later I walked back into Amy’s room, where I found Bill and Agnes by her bedside. They looked up at me expectantly. I paused for a moment, took a deep breath, and then gave them the news that they hadn’t allowed themselves to hope for:

The scans have shown us that Amy is not in a vegetative state after all. In fact, she’s aware of everything.

After five days of intensive investigation we had found that Amy was more than just alive—she was entirely conscious. She had heard every conversation, recognized every visitor, and listened intently to every decision being made on her behalf. Yet she had been unable to move a muscle to tell the world, I’m still here. I’m not dead yet!

Into the Gray Zone is the story of how we figured out how to make contact with people such as Amy, and the profound effects for science, medicine, philosophy, and law of what has become a new and rapidly evolving field of inquiry. Perhaps most important, we have discovered that 15 to 20 percent of people in the vegetative state who are assumed to have no more awareness than a head of broccoli are fully conscious, although they never respond to any form of external stimulation. They may open their eyes, grunt and groan, occasionally utter isolated words. Like zombies, they appear to live entirely in their own world, devoid of thoughts or feelings. Many really are as oblivious and incapable of thought as their doctors believe. But a sizable number are experiencing something quite different: intact minds adrift deep within damaged bodies and brains.

The vegetative state is one realm in the shadowlands of the gray zone. Coma is another. Comatose people do not open their eyes and look completely unaware. In the Disney version of Sleeping Beauty (which most parents know all too well), Aurora’s condition resembles coma, akin to a bewitched slumber. In real life, the picture is far less romantic: disfiguring head injuries, contorted limbs, broken bones, and wasting illnesses are the norm.

Some people in the gray zone can signal that they’re aware. Referred to as minimally conscious, they occasionally respond to requests to move a finger or track an object with their eyes. They seem to fade in and out of awareness, occasionally emerging from some deep pool of oblivion, breaking the surface and signaling their presence before sinking back into the murky depths.

Locked-in syndrome is not technically a gray-zone state, but it is close enough to give us insight into what life might be like for some of the people we scan. Locked-in people are fully conscious and can typically blink or move their eyes. Jean-Dominique Bauby, French editor of Elle magazine, was a famous example of someone locked in. A massive stroke left him permanently paralyzed except for the ability to blink his left eye. With the help of an assistant and a writing board, he composed The Diving Bell and the Butterfly, a memoir, which took two hundred thousand blinks to complete.

Bauby vividly recounted his experience: My mind takes flight like a butterfly. There is so much to do. . . . You can visit the woman you love, slide down beside her and stroke her still-sleeping face. You can build castles in Spain, steal the Golden Fleece, discover Atlantis, realize your childhood dreams and adult ambitions. Of course, this is Bauby’s butterfly: the mind unbound, unconstrained by physicality or responsibility, free to flit here and there. But Bauby was also locked inside the diving bell, an iron chamber from which there is no escape and which sinks ever deeper into the abyss.

Back at Amy’s bedside a few days after her fMRI scans, I again sat watching her closely, desperately wanting to know what she was thinking and feeling. All of those convulsive movements and spasmodic gurgles. Was her experience like Bauby’s? Had she entered Bauby’s imaginative realm of freedom and possibility? Or was her inner world an excruciating prison from which there was no escape?

Following our scans, Amy’s life changed beyond recognition. Agnes would barely leave her bedside, reading to her more or less constantly. Bill popped in each morning, delivering the daily papers and updating Amy on the latest family gossip. A constant stream of friends and relatives visited. Amy went home on weekends, and parties were held on her birthdays. She was taken to the movies. The care staff always introduced themselves to her, explaining that they were going to wash or change her before approaching her bedside. Every intervention, every drug, every change of routine, was carefully explained. After seven months in the gray zone, Amy became a person again.

I didn’t delve into this new field of science with anything resembling a clear idea in mind of what I wanted to do. The beginning felt like a fluke, an offhand coincidence. Yet as I look back, it’s clear that what set this story in motion points to the inner fabric that binds all of us together in ways that are monstrously complex and impossible to anticipate. My explorations into the gray zone emerged out of something dark and strange that happened in a leafy, genteel suburb of south London on a warm July day twenty years ago. . . .

CHAPTER ONE

THE GHOST THAT HAUNTS ME

People don’t live or die, people just float

She went with the man in the long black coat

—Bob Dylan

The scientific process works in mysterious ways.

As a young neuropsychologist at the University of Cambridge, studying the relationship between behavior and the brain, I fell in love with Maureen, a Scottish woman who was also a neuropsychologist. We met in the fall of 1988 in Newcastle upon Tyne, an English city sixty miles from the Scottish border. I had been sent up to Newcastle University to solidify a collaborative relationship between my boss, Trevor Robbins, and Maureen’s boss, the improbably named Patrick Rabbitt, who was doing innovative work on how the brain ages. Maureen and I were thrust together. I was immediately charmed by her dry wit, amazing head of chestnut hair, and lovely eyes that would tightly close whenever she laughed, which she did all the time. I was soon returning to Newcastle upon Tyne for less academic reasons, driving six hours up and back through murderous weekend traffic in my ancient Ford Fiesta, a banged-up piece of junk that I’d picked up for £1,100 from my first paycheck.

Maureen introduced me to music. Not the bland early-eighties glam rockers in eyeliner, hair spray, and jumpsuits such as Adam and the Ants, Culture Club, and Simple Minds that I’d been infatuated with through my adolescence, but the music that I still carry with me. Passionate music that told stories about land and history mixed with relationships and burning desire. The driving, soulful Celtic-based music of the Waterboys, Christy Moore, and Dick Gaughan. Maureen’s brother Phil, who lived in St. Albans, about forty-five miles from Cambridge, quickly persuaded me that a future without a guitar in hand was no future at all and took me to buy my first axe—a Yamaha that I still own and always will.

After some months of commuting between Cambridge and Newcastle upon Tyne, I moved sixty miles south to London because that’s where the patients I was studying were being treated. I continued to work as a neuropsychologist, paid by my boss in Cambridge, and signed on for a PhD at the Institute of Psychiatry at the University of London, driving between the two cities several times a week to fulfill the obligations of both posts. It was a grueling schedule, but I loved the work. Maureen gave up her job in Newcastle, took a position in London, and we soon bought our own place—a small third-floor one-bedroom apartment that was a short walk from the Maudsley Hospital and the Institute of Psychiatry in South London, where we both were based.

As a building, or set of buildings, the institute is extremely disappointing—a sprawling jumble that lacks a physical presence to match its formidable academic reputation. My office was in a prefabricated building, or portacabin, as we call them in the UK. Freezing in winter, sweltering in summer, it shook each time the main door slammed. We were promised more permanent digs every year: the portacabins would be razed. But I would return decades later and discover, to my surprise and amusement, that there they were, probably still housing aspiring PhDs.

The initial flush of excitement and romance that Maureen and I felt about moving in together was soon replaced with the more humdrum business of driving to see patients all over southern England, sitting in endless lines of stationary London traffic, searching in vain for vacant parking spots within walking distance of our home, and jump-starting my Fiesta when it decided not to start in the morning—which was all the time.

Working at the institute and the Maudsley, it was impossible not to be moved by the patients: legions of depressives, schizophrenics, epileptics, and demented souls pacing the drafty corridors. Maureen, an empathic, caring person, was deeply affected by them. She soon decided to train as a psychiatric nurse. Despite the doubtless nobility of this calling, her decision struck me as an abnegation of what could have been a glittering academic career. She began spending long evenings out with her new colleagues while I stayed home, writing and rewriting my first scientific papers, describing the shifts in behavior of patients who had had pieces of their brains removed to alleviate epilepsy or eradicate aggressive tumors.

The histories and stories of what had happened to these patients once their brains had been tampered with fascinated me. One patient I worked with had minimal frontal-lobe damage but became wildly disinhibited as a result. Before his injury he was described as a shy and intelligent young man. Postinjury he abused strangers in the street and carried a canister of paint with him to deface any public or private surface he could get his hands on. His speech was littered with expletives. His wild behavior escalated: he persuaded a friend to hold his ankles while he hung from the window of a speeding train, a lunatic activity by any measure. His skull and most of the front part of his cortex were crushed when he crashed headlong into a bridge. By some circular twist of fate, his minor frontal-lobe injury led directly to major damage to the same part of his brain.

Perhaps the most bizarre case I encountered concerned a young man with automatisms—brief unconscious behaviors during which you are unaware of your actions. Automatisms are typically caused by epileptic seizures that start in the temporal or frontal lobes and then quickly spread—an escalating cascade of neuronal firing that engulfs the entire brain. During these episodes, patients hang in a kind of gray zone. Their eyes remain open, and they are strangely animate and seemingly purposeful in their actions. These usually include routine activities: cooking, showering, or driving a familiar route. Following the episode, the patient regains consciousness and often feels disoriented but has no memory of the event.

My patient was a lanky youth with wild hair whom I tested for memory impairments following surgery that he had received to combat seizures. He was also the defendant in a murder trial. The victim was his own mother, strangled while she was securely locked in the house with her son. Just the two of them. The case turned on his being a martial arts expert with a history of epileptic automatisms, and he could (although the evidence remained entirely circumstantial) have killed her through a series of routine martial arts maneuvers and remained entirely unaware of this dreadful act.

When I assessed his memory using what were then our state-of-the-art computerized tests, I sat near the door—a strategy I had seen in numerous TV crime dramas. I didn’t feel safe. I needed a weapon. All this now seems ludicrous, but there I was, sitting in a closed office with a man who was accused of killing his own mother with his bare hands without even knowing that he’d done it! If he had done it, could he be judged responsible? I wasn’t sure. The thinking then and now was that automatisms, rather than expressing subconscious impulses, are automatic programs firing in the brain, completely outside our control. If he had been a carpenter, he would have been sawing a piece of wood rather than karate-chopping his mom.

Could his brain make him kill again? That was the uppermost question in my mind. What could I use to defend myself? The office around me was stacked high with papers, books, and the paraphernalia of scientific investigation—not exactly an armory. Beside the desk I spied a squash racquet. I clutched it, mulling over some vague plan to parry the young man’s blows. Fortunately for both of us the session passed without incident. I have often thought what an odd sight it would have been: the patient attacking me like a ninja while I tried to swat him about the head with a squash racquet.

The work was enthralling, but all the while I was losing touch with Maureen. Within a year of buying our apartment, the relationship fell apart. We were going in different directions: me into a career in science and her into a job in psychiatric care. Something had changed between us. I couldn’t understand why she’d lost the sense of shared wonder about the brain and how it is affected by damage and disease. I couldn’t understand the appeal of what felt like simply caring for a problem rather than trying to solve it. I’d made the decision, some years earlier, not to pursue a traditional medical career. I’d never wanted to be a physician, listening to people’s ailments and dishing out medication according to standard protocols. I wanted to try to understand the mysteries of the way our minds work and perhaps discover new approaches to treatment and cures. That’s what neuroscientists do. I thought that I had my eye on the bigger picture, but I was probably just insufferably self-righteous, driven by the ambition and idealism of a young scientist. I thought we might be able to understand and then cure Parkinson’s and Alzheimer’s diseases.

I was also dazzled by what then impressed me in my naïveté as the glamour that a high-flying career in neuroscience might offer. My boss was sending me to exotic locales to give talks in his stead. At an academic conference in Phoenix, Arizona, I found myself in a hot tub in the desert with two other English neuroscientists. Can you imagine? The day before we had all been plodding through the perpetual precipitation and dreariness of England, and then there we were, luxuriating among the cacti.

I must have been a bit smug when I came home from these trips. Maureen and I had a running argument about the rights and wrongs of psychiatric care, science for science’s sake, and the innate tensions between scientific discovery and medical care.

It’s all very well studying these people, I remember Maureen saying. But helping them deal with their problems is a much better use of resources.

If we don’t do the science, these problems will persist! I countered.

"Science might help someone down the line, years from now. But it mostly comes to nothing. And it doesn’t help patients who donate their time to your research projects, naively assuming that you are going to make their lives better."

"I do tell them that my research is not going to help them personally."

"Wow. Aren’t you nice?"

Our running argument had undertones of England versus Scotland. Since the beginning of time, the Scots have felt exploited by the English, whom they see as cold, bloodless mercenaries while they are passionate, earthly, and honest. In retrospect, our care-versus-pure-science positions echoed this age-old conflict.

Eventually, I met someone else and I left Maureen, moving out in 1990 just as the UK economy and housing market collapsed. Our £60,000 apartment was suddenly worth £30,000. We had an enormous negative equity. The interest rate on our mortgage doubled, which was barely manageable while Maureen lived in the apartment. Things rapidly deteriorated when she also moved in with someone else. To make the mortgage payments we were forced to rent the apartment to Brazilian friends, but Maureen wanted nothing more to do with it. I collected rent, paid the mortgage, and took care of taxes and repairs. Maureen and I were no longer on speaking terms—just sending angry letters back and forth. I ended up sleeping on the floor of a friend’s apartment in