Phantoms in the Brain: Probing the Mysteries of the Human Mind (10 page)

So here we have a paradox. Mirabelle never had arms in her entire life, yet she can move her phantoms. Irene had just lost her arm a year earlier and yet she cannot generate a flicker of movement. What's going on here?

To answer this question we need to take a closer look at the anatomy and physiology of the motor and sensory systems in the human brain. Consider what happens when you or I close our eyes and gesticulate. We have a vivid sense of our body and of the position of our limbs and their movements. Two eminent English neurologists, Lord Russell Brain and Henry Head (yes, these are their real names), coined the phrase "body image" for this vibrant, internally constructed ensemble of experiences— the internal image and memory of one's body in space and time. To create and maintain this body image at any given instant, your parietal lobes combine information from many sources: the muscles, joints, eyes and motor command centers.

When you decide to move your hand, the chain of events leading to its movements originates in the frontal lobes—especially in the vertical strip of cortical tissue called the motor cortex. This strip lies just in front of the furrow that separates the frontal lobe from the parietal lobe. Like the sensory homunculus that occupies the region just behind this furrow, the motor cortex contains an upside−down "map" of the whole body—

except that it is concerned with sending signals to the muscles rather than receiving signals from the skin.

Experiments show that the primary motor cortex is concerned mainly with simple movements like wiggling your finger or smacking your lips. An area immediately in front of it, called the supplementary motor area, appears to be in charge of more complex skills such as waving good−bye and grabbing a banister. This supplementary motor area acts like a kind of master of ceremonies, passing specific instructions about the proper sequence of required movements to the motor cortex. Nerve impulses that will then direct these movements travel from the motor cortex down the spinal cord to the muscles on the opposite side of the body, allowing you to wave good−bye or put on lipstick.

Every time a "command" is sent from the supplementary motor area to the motor cortex, it goes to the muscles and they move.2 At the same

time, identical copies of the command signal are sent to two other major "processing" areas—the cerebellum and the parietal lobes—informing them of the intended action.

Once these command signals are sent to the muscles, a feedback loop is set in motion. Having received a command to move, the muscles execute the movement. In turn, signals from the muscle spindles and joints are sent back up to the brain, via the spinal cord, informing the cerebellum and parietal lobes that "yes, the command is being performed correctly." These two structures help you compare your intention with your actual performance, behaving like a thermostat in a servo−loop, and modifying the motor commands as needed (applying brakes if they are too fast and increasing the motor outflow if it's too slow). Thus intentions are transformed into smoothly coordinated movements.

Now let's return to our patients to see how all this relates to the phantom experience. When John decides to move his phantom arm, the front part of his brain still sends out a command message, since this particular part of John's brain doesn't "know" that his arm is missing— even though John "the person" is unquestionably aware of the fact. The commands continue to be monitored by the parietal lobe and are felt as movements. But they are phantom movements carried out by a phantom arm.

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Thus the phantom limb experience seems to depend on signals from at least two sources. The first is remapping; recall that sensory input from the face and upper arm activates brain areas that correspond to the

"hand." Second, each time the motor command center sends signals to the missing arm, information about the commands is also sent to the parietal lobe containing our body image. The convergence of information from these two sources results in a dynamic, vibrant image of the phantom arm at any given instant—an image that is continuously updated as the arm "moves."

In the case of an actual arm there is a third source of information, namely, the impulses from the joints, ligaments and muscle spindles of that arm. The phantom arm of course lacks these tissues and their signals, but oddly enough this fact does not seem to prevent the brain from being fooled into thinking that the limb is moving—at least for the first few months or years after amputation.

This takes us back to an earlier question. How can a phantom limb be paralyzed? Why does it remain "frozen"

after amputation? One possibility is that when the actual limb is paralyzed, lying in a sling or brace, the brain sends its usual commands—move that arm, shake that leg.

The command is monitored by the parietal lobe, but this time it does not receive the proper visual feedback.

The visual system says, "nope, this arm is not moving." The command is sent out again—arm, move. The visual feedback returns, informing the brain repeatedly that the arm isn't moving. Eventually the brain learns that the arm does not move and a kind of "learned paralysis" is stamped onto the brain's circuitry. Exactly where this occurs is not known, but it may lie partly in motor centers and partly in parietal regions concerned with body image. Whatever the physiological explanation turns out to be, when the arm is later amputated, the person is stuck with that revised body image: a paralyzed phantom.

If you can learn paralysis, is it possible that you can unlearn it? What if Irene were to send a "move now"

message to her phantom arm, and every time she did so she got back a visual signal that it was moving; that, yes, it was obeying her command? But how can she get visual feedback when she doesn't have an arm? Can we trick her eyes into actually seeing a phantom?

I thought about virtual reality. Maybe we could create the visual illusion that the arm was restored and was obeying her commands. But that technology, costing over half a million dollars, would exhaust my entire research budget with one purchase. Fortunately, I thought of a way to do the experiment with an ordinary mirror purchased from a five−and−dime store.

To enable patients like Irene to perceive real movement in their nonexistent arms, we constructed a virtual reality box. The box is made by placing a vertical mirror inside a cardboard box with its lid removed. The front of the box has two holes in it, through which the patient inserts her "good hand" (say, the right one) and her phantom hand (the left one). Since the mirror is in the middle of the box, the right hand is now on the right side of the mirror and the phantom is on the left side. The patient is then asked to view the reflection of her normal hand in the mirror and to move it around slightly until the reflection appears to be superimposed on the felt position of her phantom hand. She has thus created the illusion of observing two hands, when in fact she is only seeing the mirror reflection of her intact hand. If she now sends motor commands to both arms to make mirror symmetric movements, as if she were conducting an orchestra or clapping, she of course "sees"

her phantom moving as well. Her brain receives confirming visual feedback that the phantom hand is moving correctly in response to her command. Will this help restore voluntary control over her paralyzed phantom?

The first person to explore this new world was Philip Martinez. In 1984 Philip was hurled off his motorcycle, going at forty−five miles an hour down the San Diego freeway. He skidded across the median, landed at the foot of a concrete bridge and, getting up in a daze, he had the presence of mind to check himself for injuries.

A helmet and leather jacket prevented the worst, but Philip's left arm had been severely torn near his shoulder.

Like Dr. Pons's monkeys, he had a brachial avulsion— the nerves supplying his arm had been yanked off the 38

spinal column. His left arm was completely paralyzed and lay lifeless in a sling for one year. Finally, doctors advised amputation. The arm was just getting in the way and would never regain function.

Ten years later, Philip walked into my office. Now in his midthirties, he collects a disability benefit and has made a rather impressive reputation for himself as a pool player, known among his friends as the "one−armed bandit."

Philip had heard about my experiments with phantom limbs in local press reports. He was desperate. "Dr.

Ramachandran," he said, "I'm hoping you can help me." He glanced down at his missing arm. "I lost it ten years ago. But ever since I've had a terrible pain in my phantom elbow, wrist and fingers." Interviewing him further, I discovered that during the decade, Philip had never been able to move his phantom arm. It was always fixed in an awkward position. Was Philip suffering from learned paralysis? If so, could we use our virtual reality box to resurrect the phantom visually and restore movements?

I asked Philip to place his right hand on the right side of the mirror in the box and imagine that his left hand (the phantom) was on the left side. "I want you to move your right and left arms simultaneously," I instructed.

"Oh, I can't do that," said Philip. "I can move my right arm but my left arm is frozen. Every morning when I get up, I try to move my phantom because it's in this funny position and I feel that moving it might help relieve the pain. But," he said, looking down at his invisible arm, "I have never been able to generate a flicker of movement in it."

"Okay, Philip, but try anyway."

Philip rotated his body, shifting his shoulder, to "insert" his lifeless phantom into the box. Then he put his right hand on the other side of the mirror and attempted to make synchronous movements. As he gazed into the mirror, he gasped and then cried out, "Oh, my God! Oh, my God, doctor! This is unbelievable. It's mind−boggling!" He was jumping up and down like a kid. "My left arm is plugged in again. It's as if I'm in the past. All these memories from so many years ago are flooding back into my mind. I can move my arm again. I can feel my elbow moving, my wrist moving. It's all moving again."

After he calmed down a little I said, "Okay, Philip, now close your eyes."

"Oh, my," he said, clearly disappointed. "It's frozen again. I feel my right hand moving, but there's no movement in the phantom."

"Open your eyes."

"Oh, yes. Now it's moving again."

It was as though Philip had some temporary inhibition or block of the neural circuits that would ordinarily move the phantom and the visual feedback had overcome this block. More amazing still, these bodily sensations of the arm's movements were revived instandy,3 even though they had never been felt in the preceding ten years!

Though Philip's response was exciting and provided some support for my hypothesis about learned paralysis, I went home that night and asked myself, "So what? So we have this guy moving his phantom limb again. But it's a perfectly useless ability if you think about it—precisely the sort of arcane thing that many of us medical researchers are sometimes accused of working on." I wouldn't win a prize, I realized, for getting someone to move a phantom limb.

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But maybe learned paralysis is a more widespread phenomenon.4 It might happen to people with real limbs that are paralyzed, say, from a stroke. Why do people lose the use of an arm after a stroke? When a blood vessel supplying the brain gets clogged, the fibers that extend from the front part of the brain down to the spinal cord are deprived of oxygen and sustain damage, leaving the arm paralyzed. But in the early stages of a stroke, the brain swells, temporarily causing some nerves to die off but leaving others simply stunned and

"off−line," so to speak. During this time, when the arm is nonfunctional, the brain receives visual feedback:

"Nope, the arm is not moving." After the swelling subsides, it's possible that the patient's brain is stuck with a form of learned paralysis. Could the mirror contraption be used to overcome at least that component of the paralysis that is due to learning? (Obviously there is nothing one can do with mirrors to restore paralysis caused by actual destruction of fibers.)

But before we could implement this kind of novel therapy for stroke patients, we needed to ensure that the effect is more than a mere temporary illusion of movement in the phantom. (Recall that when Philip closed his eyes, the sense of movement in his phantom disappeared. )

What if the patient were to practice with the box in order to receive continuous visual feedback for several days? Is it conceivable that the brain would "unlearn" its perception of damage and that movements would be permanently restored?

I went back the next day and asked Philip, "Are you willing to take this device home and practice with it?"

"Sure," said Philip. "I'd love to take it home. I find it very exciting that I can move my arm again, even if only momentarily."

So Philip took the mirror home. A week later I telephoned him. "What's happening?"

"Oh, it's fun, doctor. I use it for ten minutes every day. I put my hand inside, wave it around and see how it feels. My girlfriend and I play with it. It's very enjoyable. But when I close my eyes, it still doesn't work. And if I don't use the mirror, it doesn't work. I know you want my phantom to start moving again, but without the mirror it doesn't."

Three more weeks passed until one day Philip called me, very excited and agitated. "Doctor," he exclaimed,

"it's gone!"

"What's gone?" (I thought maybe he had lost the mirror box.)

"My phantom is gone."

"What are you talking about?"

"You know, my phantom arm, which I had for ten years. It doesn't exist anymore. All I have is my phantom fingers and palm dangling from my shoulder!"

My immediate reaction was, Oh, no! I have apparently permanently altered a person's body image using a mirror. How would this affect his mental state and well−being? "Philip—does it bother you?"

"No no no no no no," he said. "On the contrary. You know the excruciating pain I always had in my elbow?

The pain that tortured me several times a week? Well, now I don't have an elbow and I don't have that pain anymore. But I still have my fingers dangling from my shoulder and they still hurt." He paused, apparently to let this sink in. "Unfortunately," he added, "your mirror box doesn't work anymore because my fingers are up too high. Can you change the design to eliminate my fingers?" Philip seemed to think I was some kind of 40