I love fools' experiments. I am always making them.
-CHARLES DARW I N
A
s A M E D I C A L S T U D E N T I E X A M I N E D A PA T I E N T N A M E D M I K H E Yduring my neurology rotation. Routine clinical testing required me to poke her neck with a sharp needle. It should have been mildly painful, but with each poke she laughed out loud, saying it was ticklish. This, I realized, was the ultimate paradox: laughter in the face of pain, a microcosm of the human condition itself. I was never able to investigate Mikhey's case as I would have liked.
Soon after this episode, I decided to study human vision and percep
tion, a decision largely influenced by Richard Gregory's excellent book Eye and Brain. I spent several years doing research on neurophysiology and visual perception, first at the University of Cambridge's Trinity Col
lege, and then in collaboration with Jack Pettigrew at Caltech.
But I never forgot the patients like Mikhey whom I had encountered during my neurology rotation as a medical student. In neurology, it seemed, there were so many questions left unresolved. Why did Mikhey laugh when poked ? Why does the big toe go up when you stroke the outer border of the foot of a stroke patient ? Why do patients with tem
poral lobe seizures believe they experience God and exhibit hypergraphia (incessant, uncontrollable writing) ? Why do otherwise intelligent, per
fectly lucid patients with damage to the right parietal lobe deny that their left arm belongs to them ? Why does an emaciated anorexic with perfectly normal eyesight look in a mirror and claim she looks obese ? And so, after years of specializing in vision, I returned to my first love:
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neurology. I surveyed the many unanswered questions of the field and decided to focus on a specific problem : phantom limbs. Little did I know that my research would yield unprecedented evidence of the amazing plasticity and adaptability of the human brain.
It had been known for over a century that when a patient loses an arm to amputation, she may continue to feel vividly the presence of that arm-as though the arm's ghost were still lingering, haunting its former stump. There had been various attempts to explain this baffling phe
nomenon, ranging from flaky Freudian scenarios involving wish fulfill
ment to invocations of an immaterial soul. Not being satisfied with any of these explanations, I decided to tackle it from a neuroscience perspective.
I remember a patient named Victor on whom I conducted nearly a month of frenzied experiments. He came to see me because his left arm had been amputated below the elbow about three weeks prior to his visit.
I first verified that there was nothing wrong with him neurologically:
His brain was intact, his mind was normal. Based on a hunch I blind
folded him and started touching various parts of his body with a Q-tip, asking him to report what he felt, and where. His answers were all nor
mal and correct until I started touching the left side of his face. Then something very odd happened.
He said, "Doctor, I feel that on my phantom hand. You're touching my thumb."
I used my knee hammer to stroke the lower part of his jaw. "How about now ? " I asked.
"I feel a sharp object moving across the pinky to the palm," he said.
By repeating this procedure I discovered that there was an entire map of the missing hand on his face. The map was surprisingly precise and consistent, with fingers clearly delineated (Figure 1 . 1 ) . On one occasion I pressed a damp Q-tip against his cheek and sent a bead of water trick
ling down his face like a tear. He felt the water move down his cheek in the normal fashion, but claimed he could also feel the droplet trickling down the length of his phantom arm. Using his right index finger, he even traced the meandering path of the trickle through the empty air in front of his stump. Out of curiosity I asked him to elevate his stump and point the phantom upward toward the ceiling. To his astonishment he felt the next drop of water flowing up along the phantom, defying the law of gravity.
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F I G U R E I . I A patient with a phantom left arm. Touching different parts of his face evoked sensations in different parts of the phantom : P, pinky; T, thumb; B, ball of thumb; I, index finger.
Victor said he had never discovered this virtual hand on his face before, but as soon as he knew about it he found a way to put it to good use: Whenever his phantom palm itches-a frequent occurrence that used to drive him crazy-he says he can now relieve it by scratching the corresponding location on his face.
Why does all this happen ? The answer, I realized, lies in the brain's anatomy. The entire skin surface of the left side of the body is mapped onto a strip of cortex called the postcentral gyrus (see Figure lnt.2 in the Introduction) running down the right side of the brain. This map is often illustrated with a cartoon of a man draped on the brain sur
face (Figure 1 .2). Even though the map is accurate for the most part, some portions of it are scrambled with respect to the body's actual layout.
Notice how the map of the face is located next to the map of the hand instead of being near the neck where it "should " be. This provided the clue I was looking for.
Think of what happens when an arm is amputated. There is no lon
ger an arm, but there is still a map of the arm in the brain. The job of this map, its raison d 'etre, is to represent its arm. The arm may be gone
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Lowtr lip
Teeth. gums, dnd Ja w
Tongue
Toes Gemtals
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F I G U R E r . 2 The Penfield map of the skin surface on the postcentral gyrus (see Figure lnt.2). The d rawing shows a coronal section (roughly, a cross section) going through the middle of the brain at the level of the postcentral gyrus. The artist's whimsical depiction of a person d raped on the brain surface shows the exaggerated representations of certain body parts (face and hand) and the fact that the hand map is above the face map.
but the brain map, having nothing better to do, soldiers on. It keeps rep
resenting the arm, second by second, day after day. This map persistence explains the basic phantom limb phenomenon-why the felt presence of the limb persists long after the flesh-and-blood limb has been severed.
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Now, how to explain the bizarre tendency to attribute touch sensa
tions arising from the face to the phantom hand ? The orphaned brain map continues to represent the missing arm and hand in absentia, but it is not receiving any actual touch inputs. It is listening to a dead chan
nel, so to speak, and is hungry for sensory signals. There are two pos
sible explanations for what happens next. The first is that the sensory input flowing from the facial skin to the face map in the brain begins to actively invade the vacated territory corresponding the missing hand.
The nerve fibers from the facial skin that normally project to the face cortex sprout thousands of neural tendrils that creep over into the arm map and establish strong, new synapses. As a result of this cross-wiring, touch signals applied to the face not only activate the face map, as they normally do, but also activate the hand map in the cortex, which shouts
"hand ! " to higher brain areas. The net result is that the patient feels that his phantom hand is being touched every time his face is touched.
A second possibility is that even prior to amputation, the sensory input from the face not only gets sent to the face area but partially encroaches into the hand region, almost as if they are reserve troops ready to be called into action. But these abnormal connections are ordinarily silent; perhaps they are continuously inhibited or damped down by the normal baseline activity from the hand itself. Amputation would then unmask these ordi
narily silent synapses so that touching the face activates cells in the hand area of the brain. That in turn causes the patient to experience the sensa
tions as arising from the missing hand.
Independent of which of these two theories-sprouting or unmask
ing-is correct, there is an important take-home message. Generations of medical students were told that the brain's trillions of neural connections are laid down in the fetus and during early infancy and that adult brains lose their ability to form new connections. This lack of plasticity-this lack of ability to be reshaped or molded-was often used as an excuse to tell patients why they could expect to recover very little function after a stroke or traumatic brain injury. Our observations flatly contradicted this dogma by showing, for the first time, that even the basic sensory maps in the adult human brain can change over distances of several centimeters.
We were then able to use brain-imaging techniques to show directly that our theory was correct: Victor's brain maps had indeed changed as pre
dicted (Figure 1 .3).
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F I G U R E 1 . 3 A MEG (magnetoencephalograph) map of the body surface in a right-arm amputee. Hatched area, hand; black areas, face; white areas, upper arm. Notice that the region corresponding to the right hand (hatched area) is missing from the left hemisphere, but this region gets activated by touching the face or upper arm.
Soon after we published, evidence confirming and extending these findings started to come in from many groups. Two Italian research
ers, Giovanni Berlucchi and Salvatore Aglioti, found that after ampu
tation of a finger there was a "map" of a single finger draped neatly across the face as expected. In another patient the trigeminal nerve (the sensory nerve supplying the face) was severed and soon a map of the face appeared on the palm : the exact converse of what we had seen.
Finally, after amputation of the foot of another patient, sensations from the penis were felt in the phantom foot. (Indeed, the patient claimed that his orgasm spread into his foot and was therefore "much big
ger than it used to be.") This occurs because of another of these odd
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discontinuities i n the brain's map of the body: The map of the genitals is right next to the map of the foot.
M Y S E C O N D E X P E R I M E N T on phantom limbs was even simpler. In a nutshell, I created a simple setup using ordinary mirrors to mobilize par
alyzed phantom limbs and reduce phantom pain. To understand how this works, I first need to explain why some patients are able to "move"
their phantoms but others are not.
Many patients with phantoms have a vivid sense of being able to move their missing limbs. They say things like "It's waving goodbye" or "It's reaching out to answer the phone." Of course, they know perfectly well that their hands aren't really doing these things-they aren't delusional, just armless-but subjectively they have a realistic sensation that they are moving the phantom. Where do these feelings come from ?
I conjectured that they were coming from the motor command cen
ters in the front of the brain. You might recall from the Introduction how the cerebellum fine-tunes our actions through a servo-loop process. What I didn't mention is that the parietal lobes also participate in this servo-loop process through essentially the same mechanism. Again briefly: Motor out
put signals to the muscles are (in effect) cc'ed to the parietal lobes, where they are compared to sensory feedback signals from the muscles, skin, joints, and eyes. If the parietal lobes detect any mismatches between the intended movements and the hand's actual movements, they make corrective adjust
ments to the next round of motor signals. You use this servo-guided system all the time. This is what allows you, for instance, to maneuver a heavy juice pitcher into a vacant spot on the breakfast table without spilling or knocking over the surrounding tableware. Now imagine what happens if the arm is amputated. The motor command centers in the front of the brain don't "know" the arm is gone-they are on autopilot-so they con
tinue to send motor command signals to the missing arm. By the same token, they continue to cc these signals to the parietal lobes. These signals flow into the orphaned, input-hungry hand region of your body-image center in the parietal lobe. These cc'ed signals from motor commands are misinterpreted by the brain as actual movements of the phantom.
Now you may wonder why, if this is true, you don't experience the same sort of vivid phantom movement when you imagine moving your
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hand while deliberately holding it still. Here is the explanation I pro
posed several years ago, which has been since confirmed by brain-imag
ing studies. When your arm is intact, the sensory feedback from the skin, muscles, and joint sensors in your arm, as well as the visual feed
back from your eyes, are all testifying in unison that your arm is not in fact moving. Even though your motor cortex is sending "move" signals to your parietal lobe, the countervailing testimony of the sensory feedback acts as a powerful veto. As a result, you don't experience the imagined movement as though it were real. If the arm is gone, however, your mus
cles, skin, joints, and eyes cannot provide this potent reality check. With
out the feedback veto, the strongest signal entering your parietal lobe is the motor command to the hand. As a result, you experience actual movement sensations.
Moving phantom limbs is bizarre enough, but it gets even stranger.
Many patients with phantom limbs report the exact opposite: Their phantoms are paralyzed. "It's frozen, Doctor." "It's in a block of cement."
For some of these patients the phantom is twisted into an awkward, extremely painful position. "If only I could move it," a patient once told me, "it might help alleviate the pain."
When I first saw this, I was baffled. It made no sense. They had lost their limbs, but the sensory-motor connections in their brains were pre
sumably the same as they had been before their amputations. Puzzled, I started examining some of these patients' charts and quickly found the clue I was looking for. Prior to amputation, many of these patients had had real paralysis of their arm caused by a peripheral nerve injury: the nerve that used to innervate the arm had been ripped out of the spinal cord, like a phone cord being yanked out of its wall jack, by some vio
lent accident. So the arm had lain intact but paralyzed for many months prior to amputation. I started to wonder if perhaps this period of real paralysis could lead to a state of learned paralysis, which I conjectured could come about in the following way.
During the preamputation period, every time the motor cortex sent a movement command to the arm, the sensory cortex in the parietal lobe would receive negative feedback from the muscles, skin, joints, and eyes.
The entire feedback loop had gone dead. Now, it is well established that experience modifies the brain by strengthening or weakening the syn
apses that link neurons together. This modification process is known
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as learning. When patterns are constantly reinforced-when the brain sees that event B invariably follows event A, for instance-the synapses between the neurons that represent A and the neurons that represent B are strengthened. On the other hand, if A and B stop having any appar
ent relationship to each other, the neurons that represent A and B will shut down their mutual connections to reflect this new reality.
So here we have a situation where the motor cortex was continually sending out movement commands to the arm, which the parietal lobe continually saw as having absolutely zero muscular or sensory effect.
The synapses that used to support the strong correlations between motor commands and the sensory feedback they should generate were shown to be liars. Every new, impotent motor signal reinforced this trend, so the synapses grew weaker and weaker and eventually became moribund.
In other words, the paralysis was learned by the brain, stamped into the circuitry where the patient's body image was constructed. Later, when the arm was amputated, the learned paralysis got carried over into the phantom so the phantom felt paralyzed.
How could one test such an outlandish theory ? I hit on the idea of constructing a mirror box (Figure 1 .4). I placed an upright mirror in the center of a cardboard box whose top and front had been removed. If you stood in front of the box, held your hands on either side of the mirror and looked down at them from an angle, you would see the reflection of one hand precisely superimposed on the felt location of your other hand.
In other words, you would get the vivid but false impression that you were looking at both of your hands; in fact, you would only be looking at one actual hand and one reflection of a hand.
If you have two normal, intact hands, it can be entertaining to play around with this illusion in the mirror box. For example, you can move your hands synchronously and symmetrically for a few moments-pre
tending to conduct an orchestra works well-and then suddenly move them in different ways. Even though you know it's an illusion, a jolt of mild surprise invariably shoots through your mind when you do this.
The surprise comes from the sudden mismatch between two streams of feedback: The skin-and-muscle feedback you get from the hand behind the mirror says one thing, but the visual feedback you get from the reflected hand-which your parietal lobe had become convinced is the hidden hand itself--reports some other movement.
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F I G U R E I · 4 The m irror arrangement for animating the phantom limb. The patient "puts" his paralyzed and painful phantom left arm behind the mi rror and his intact right hand in front of the mi rror. If he then views the mi rror reflection of the right hand by looking into the right side of the mirror, he gets the illusion that the phantom has been resurrected . Moving the real hand causes the phantom to appear to move, and it then feels like it is moving-sometimes for the first time in years. In many patients this exercise relieves the phantom cramp and associated pain. In clinical trials, mirror visual feedback has also been shown to be more effec
tive than conventional treatments for chronic regional pain syndrome and paralysis resulting from stroke.
Now let's look at what this mirror-box setup does for a person with a
Now let's look at what this mirror-box setup does for a person with a