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Authors: V. S. Ramachandran,Sandra Blakeslee

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magician.

I wasn't sure I could help Philip with his request, but I realized that this was probably the first example in medical history of a successful "amputation" of a phantom limb! The experiment suggests that when Philip's right parietal lobe was presented with conflicting signals—visual feedback telling him that his arm is moving again while his muscles are

telling him the arm is not there—his mind resorted to a form of denial. The only way his beleaguered brain could deal with this bizarre sensory conflict was to say, "To hell with it, there is no arm!" And as a huge bonus, Philip lost the associated pain in his phantom elbow as well, for it may be impossible to experience a disembodied pain in a nonexistent phantom. It's not clear why his fingers didn't disappear, but one reason might be that they are overrepresented—like the huge lips on the Pen−field map—in the somatosensory cortex and may be more difficult to deny.

Movements and paralysis of phantom limbs are hard enough to explain, but even more puzzling is the agonizing pain that many patients experience in the phantom soon after amputation, and Philip had brought me face to face with this problem. What confluence of biological circumstances could cause pain to erupt in a nonexistent limb? There are several possibilities.

The pain could be caused by scar tissue or neuromas—little curled−up clusters or clumps of nerve tissue in the stump. Irritation of these clumps and frayed nerve endings could be interpreted by the brain as pain in the missing limb. When neuromas are removed surgically, phantom pain sometimes vanishes, at least temporarily, but then insidiously it often returns.

The pain could also result in part from remapping. Keep in mind that remapping is ordinarily modality−specific: That simply means that the sense of touch follows touch pathways, and the feeling of warmth follows warmth pathways, and so on. (As we noted, when I lightly stroke Tom's face with a Q−tip, he feels me touching his phantom. When I dribble ice water on his cheek, he feels cold on his phantom hand and when I warm up the water he feels heat in the phantom as well as on his face.) This probably means that remapping doesn't happen randomly. The fibers concerned with each sense must "know" where to go to find their appropriate targets. Thus in most people, including you, me and amputees, one does not get cross−wiring.

But imagine what might happen if a slight error were to occur during the remapping process—a tiny glitch in the blueprint—so that some of the touch input is hooked up accidentally to pain centers. The patient might experience severe pain every time regions around his face or upper arm (rather than neuromas) were brushed, even lightly. Such trivial

touches could generate excruciating pain, all because a few fibers are in the wrong place, doing the wrong thing.

Abnormal remapping could also cause pain two other ways. When we experience pain, special pathways are activated simultaneously both to carry the sensation and to amplify it or dampen it down as needed. Such

"volume control" (sometimes called gate control) is what allows us to modulate our responses to pain effectively in response to changing demands (which might explain why acupuncture works or why women in some cultures don't experience pain during labor). Among amputees, it's entirely possible that these volume control mechanisms have gone awry as a result of remapping—resulting in an echolike "wha wha"

reverberation and amplification of pain. Second, remapping is inherently a pathological or abnormal process, at least when it occurs on a large scale, as after the loss of a limb. It's possible that the touch synapses are not quite correctly rewired and their activity could be chaotic. Higher brain centers would then interpret the abnormal pattern of input as junk, which is perceived as pain. In truth, we really don't know how the brain 41

translates patterns of nerve activity into conscious experience, be it pain, pleasure or color.

Finally, some patients say that the pain they felt in their limbs immediately prior to amputation persists as a kind of pain memory. For example, soldiers who have grenades blow up in their hands often report that their phantom hand is in a fixed position, clenching the grenade, ready to toss it. The pain in the hand is excruciating—the same they felt the instant the grenade exploded, seared permanently in their brains. In London I once met a woman who told me she had experienced chilblains—a frostbitelike pain due to cold weather—in her thumb for several months in her childhood. The thumb later became gangrenous and was amputated. She now has a vivid phantom thumb and experiences chilblains in it every time the weather turns cold. Another woman described arthritic pain in her phantom joints. She'd had the problem before her arm was amputated but it has continued in the absence of real joints, with the pain being worse when it gets damp and cold just as it had in the real joints before amputation.

One of my medical school professors told me a story that he swore was true, the tale of another physician, an eminent cardiologist, who developed a pulsating cramp in his leg caused by Buerger's disease—a malady that produces constriction of arteries and intense, pulsing pain in the calf muscles.

Despite many attempts at treatment, nothing eased the pain. Out of sheer despair, the physician decided to have his leg amputated. He simply couldn't live with the pain any longer. He consulted a surgeon colleague and scheduled the operation, but to the surgeon's astonishment, he said he had a special request: "After you amputate my leg, could you please pickle it in a jar of formaldehyde and give it to me?" This was eccentric, to say the least, but the surgeon agreed, amputated the leg, put it in a jar of preservative and gave it to the physician, who then put it in his office and said, "Hah, at last, I can look at this leg and laugh at it and say, T

finally got rid of you!' "

But the leg had the last laugh. The pulsatile pains returned with a vengeance in the phantom leg. The good doctor stared at his floating limb in disbelief while it stared back at him, as if to mock all his efforts to rid himself of it.

There are many such stories in circulation, illustrating the astonishing specificity of pain memories and their tendency to surface when a limb is amputated. If this is the case, one can imagine being able to reduce the incidence of pain after amputation simply by injecting the limb with a local anesthetic before surgery. (This has been tried with some success.)

Pain is one of the most poorly understood of all sensory experiences. It is a source of great frustration to patient and physician alike and can emerge in many different guises. One especially enigmatic complaint frequently heard from patients is that every now and then the phantom hand becomes curled into a tight, white−knuckled fist, fingers digging into palm with all the fury of a prizefighter ready to deliver a knockout blow.

Robert Townsend is an intelligent, fifty−five−year−old engineer whose cancer caused him to lose his left arm six inches above the elbow. When I saw him seven months after the amputation, he was experiencing a vivid phantom limb that would often go into an involuntary clenching spasm. "It's like my nails are digging into my phantom hand," said Robert. "The pain is unbearable." Even if he concentrated all his attention on it, he could not open his invisible hand to relieve the spasm.

We wondered whether using the mirror box could help Robert eliminate his spasms. Like Philip, Robert looked into the box, positioned his good hand to superimpose its reflection over his phantom hand and, after making a fist with the normal hand, tried to unclench both hands simultaneously. The first time he did this, Robert exclaimed that he could

42

feel the phantom fist open along with his good fist, simply as a result of the visual feedback. Better yet, the pain disappeared. The phantom then remained unclenched for several hours until a new spasm occurred spontaneously. Without the mirror, his phantom would throb in pain for forty minutes or more. Robert took the box home and tried the same trick each time that the clenching spasm recurred. If he did not use the box, he could not unclench his fist despite trying with all his might. If he used the mirror, the hand opened instantly.

We have tried this treatment in over a dozen patients and it works for half of them. They take the mirrored box home and whenever a spasm occurs, they put their good hand into the box and open it and the spasm is eliminated. But is it a cure? It's difficult to know. Pain is notoriously susceptible to the placebo effect (the power of suggestion). Perhaps the elaborate laboratory setting or the mere presence of a charismatic expert on phantom limbs is all you need in order to eliminate the pain and it has nothing to do with mirrors. We tested this possibility on one patient by giving him a harmless battery pack that generates an electric current.

Whenever the spasms and abnormal postures occurred, he was asked to rotate the dial on the unit of his

"transcutaneous electrical simulator" until he began to feel a tingling in his left arm (which was his good arm).

We told him that this would immediately restore voluntary movements in the phantom and provide relief from the spasms. We also told him that the procedure had worked on other patients in his predicament.

He said, "Really? Wow, I can't wait to try it."

Two days later he was back, obviously annoyed. "It's useless," he exclaimed. "I tried it five times and it just doesn't work. I turned it up to full strength even though you told me not to."

When I gave him the mirror to try that same afternoon, he was able to open his phantom hand instantly. The spasms were eliminated and so too was the "digging sensation" of nails biting into his palm. This is a mind−boggling observation if you think about it. Here is a man with no hand and no fingernails. How does one get nonexistent nails digging into a nonexistent palm, resulting in severe pain? Why would a mirror eliminate the phantom spasm?

Consider what happens in your brain when motor commands are sent from the premotor and motor cortex to make a fist. Once your hand is clenched, feedback signals from muscles and joints of your hand are sent back through the spinal cord to your brain saying, Slow down, enough. Any more pressure and it could hurt. This propriocep−

tive feedback applies brakes, automatically, with astonishing speed and precision.

If the limb is missing, however, this damping feedback is not possible. The brain therefore keeps sending the message, Clench more, clench more. Motor output is amplified even further (to a level that far exceeds anything you or I would ever experience) and the overflow or "sense of effort" may itself be experienced as pain. The mirror may work by providing visual feedback to unclench the hand, so that the clenching spasm is abolished.

But why the sensation of digging fingernails? Just think of the numerous occasions when you actually clenched your fist and felt your nails biting in your palm. These occasions must have created a memory link in your brain (psychologists call it a Hebbian link) between the motor command to clench and the unmistakable sensation of "nails digging," so you can readily summon up this image in your mind. Yet even though you can imagine the image quite vividly, you don't actually feel the sensation and say, "Ouch, that hurts." Why not?

The reason, I believe, is that you have a real palm and the skin on the palm says there is no pain. You can imagine it but you don't feel it because you have a normal hand sending real feedback and in the clash between reality and illusion, reality usually wins.

43

But the amputee doesn't have a palm. There are no countermanding signals from the palm to forbid the emergence of these stored pain memories. When Robert imagines that his nails are digging into his hand, he doesn't get contradictory signals from his skin surface saying, "Robert, you fool, there's no pain down here."

Indeed, if the motor commands themselves are linked to the sense of nail digging, it's conceivable that the amplification of these commands leads to a corresponding amplification of the associated pain signals. This might explain why the pain is so brutal.

The implications are radical. Even fleeting sensory associations such as the one between clenching our hands and digging our fingernails into our palms are laid down as permanent traces in the brain and are only unmasked under certain circumstances—experienced in this case as phantom limb pain. Moreover, these ideas imply that pain is an
opinion
on the organism's state of health rather than a mere reflexive response to an injury. There is no direct hotline from pain receptors to "pain centers" in the brain. On the contrary, there is so much interaction between different brain centers, like those concerned with vision and touch, that even the mere visual appearance of an opening fist can actually feed all

the way back into the patient's motor and touch pathways, allowing him to feel the fist opening, thereby killing an illusory pain in a nonexistent hand.

If pain is an illusion, how much influence do senses like vision have over our subjective experiences? To find out, I tried a somewhat diabolical experiment on two of my patients. When Mary came into the lab, I asked her to place her phantom right hand, palm down, into the mirror box. I then asked her to put a gray glove on her good left hand and place it in the other side of the box, in a mirror image position. After making sure she was comfortable I instructed one of my graduate students to hide under the curtained table and put his gloved left hand into the same side of the box where Mary's good hand rested, above hers on a false platform. When Mary looked into the box she could see not only the student's gloved left hand (which looked exactly like her own left hand) but also its reflection in the mirror, as if she were looking at her own phantom right hand wearing a glove. When the student now made a fist or used his index finger pad to touch the ball of his thumb, Mary felt her phantom moving vividly. As in our previous two patients, vision was enough to trick her brain into experiencing movements in her phantom limb.

What would happen if we fooled Mary into thinking that her fingers were occupying anatomically impossible positions? The box permitted this illusion. Again, Mary put her phantom right hand, palm down, in the box.

BOOK: Phantoms in the Brain: Probing the Mysteries of the Human Mind
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