Touching the Phantom

Amputees can feel missing hands grab a cup of coffee, missing feet itch, and missing legs ache. Behind these ghostly sensations lies the secret of touch.

By James Shreeve|Tuesday, June 01, 1993
RELATED TAGS: SENSES
Ten years ago, Fred Aryee almost lost his life in a storm at sea. When an enormous swell hit the tuna boat on which he served as engineer, a falling beam crushed his right arm. The boat was five days from land. His crew mates managed to stem the loss of blood and keep him alive until they reached shore, but it was too late to save the limb.

A decade later Aryee sits in a chair, stripped to the waist. The physical flesh of his right arm below the elbow has long since ceased to exist. The physical flesh of Aryee’s brain, however, has yet to be convinced of that fact.

See if you can reach out and grab this cup in your right hand, says neuroscientist Vilayanur Ramachandran, head of the Brain and Perception Laboratory at the University of California at San Diego. Aryee gestures with his stump toward a cup on a table, a couple of feet away.

What are you feeling now? asks Ramachandran.

I feel my fingers clasping the cup, says Aryee.

Okay, try it again, says Ramachandran. This time, as Aryee begins his motion, Ramachandran quickly moves the cup farther away, to see if Aryee’s imagined arm has the limitation of real flesh or can stretch out as long as needed to complete a task. The result astonishes him.

Ouch! says his patient, grimacing in pain. Why did you do that?

Do what?

It felt like you ripped the cup out of my fingers.

Fred Aryee’s eerily stubborn grip on that cup is a compelling example of phantom limb, the perception of vivid feeling arising from the airy appendages of amputees and the nerve-dead limbs of accident victims. A legless veteran complains of an irrepressible itch on an instep floating in space. A double arm amputee reports phantom arms that swing normally with his stride as he walks. Aryee, an avid tennis player, has managed to switch his game to his left hand, but he has trouble with his serving motion when his ghostly right arm insists on holding the racket, too. Another of Ramachandran’s patients, a young woman missing both arms since birth, feels her arms gesticulate in tempo with the points she is making in a heated discussion. Virtually all amputees experience such sensations.

More disconcerting is the pain. Patients complain of burning or prickling, horrible muscle cramps, or the feeling that their fingers are being twisted out of shape or pushed through their palms. Sometimes a tender bunion or a splinter that afflicted a real foot will harass the phantom too, in precisely the same spot. Arm amputees have said that they sometimes feel as if their fingernails are being pulled off.

The other night, it hurt so bad I was literally screaming, says 80-year-old Brian Sheehan, who has lost the lower portion of both of his legs as a result of diabetes. You just learn to live with it.

Some patients apparently do not, taking their own lives to escape from torments felt in purely phantom flesh.

Opiates and other drugs that address the pain system are useless, because that’s not what’s causing the pain anymore, says neurobiologist Jon Kaas of Vanderbilt University. It’s some other system, inadvertently signaling pain.

Since phantom limb pain was first described in the nineteenth century, researchers have been trying to figure out where in the tactile system the mysterious sensations originate. When a limb is removed, the severed nerves in the remaining stump--nerves that formerly carried messages of touch, temperature, and pain from the skin--form nodules called neuromas on their cut ends. The classic explanation for phantom limb pain is that these truncated nerve endings continue to send impulses up the spinal cord to the brain. Cutting the nerves just above the neuromas or where they enter the spinal cord does seem to bring some relief, but only temporarily. Applying the scalpel inside the spinal cord works no better. Within a few months or years the affliction of the ghost limb returns, painful proof that the true seat of the sensation must lie even farther up the touch pathway, within the brain itself.

While chasing the phantom, neurobiologists have thus been led to a solid revelation: the sense of touch, and the physical world it ushers into existence, has much more to do with what is going on in our heads than at our fingertips. The illusory sensations may even be on the verge of revealing one of the brain’s most powerfully guarded secrets. If neuroscientists like Ramachandran and Kaas are correct, the exotic phenomenon of phantom limb offers one keenly magnified perspective on what routinely happens in the brain as we engage the world around us and learn from the experience.

We’re looking at a new route to the Holy Grail of neurobiology, says Ramachandran. An understanding of the physical basis of learning and memory.

When nerve endings in the skin, known as receptors, receive a stimulus--a brush of silk or the prick of a needle, an icy stream of water or the grip of a warm hand--the bioelectrical impulse generated by the receptors travels through the spinal cord to connections called synapses in the brain stem. Further synapses send the signal to a critical relay station in the brain called the thalamus. From there the impulses are routed up to the somatosensory cortex. This projection screen for sensation is as neatly laid out as a French garden. Nerve impulses originating in the thumb stimulate a region of the cortex devoted only to the thumb, a region that lies immediately adjacent to one responding to nerves from the index finger, and so on down the digits. Arm cortex lies next to shoulder cortex, shoulder next to trunk, with just a few topographically necessary odd pairings. (The toes, for instance, plunk their signals down next to impulses zinging in from the genitals.) The more receptors active in an area of skin, the bigger its allotment of sensory cortex. (In us humans, nearly a quarter of the skin cortex is dedicated to our highly sensitive hands.) It is as if there exists a tiny, orderly, though distorted version of oneself--a homunculus--outlined on the pleated surface of the brain.

In their search to find the source of phantom limb, researchers came up against this fastidiously arranged little person. It was waving a fundamental credo of neuroscience in their faces. Since the early 1960s, neuroscientists have generally accepted the notion that except for a critical period of flexible growth in infancy, the brain’s neuronal circuitry is hardwired, its connections as fixed in place as the electrical system of a house. The critical-period theory derived largely from experiments such as those of David Hubel and Torsten Wiesel, who shared a Nobel Prize in 1981. Hubel and Wiesel found that a patch placed over one eye of a kitten during its critical period of neural growth would lead to permanent blindness in that eye. While the eye was patched, inputs arriving from the functioning eye would take over the deprived eye’s allotment of visual cortex. The blind eye was unable to recover once the patch was removed because it was too late for the inputs to be redirected-- they had become fixed in place. Other studies on eye, ear, and touch reception supported the idea that the adult brain was rigidly organized.

The sensory homunculus in the cortex is, of course, a part of that hardwired brain. How then can it possibly be the source of phantom limb? What is dead in a hardwired system is simply dead; once nerve impulses from an amputated or paralyzed limb are no longer received by the cortex, the portion of its map allotted to the limb should forever after be as silent as a telephone whose line has been cut. Thus, after chasing phantom limb up into the brain itself, most clinical neurobiologists have lost sight of it in a fog of semi-explanations and begged questions. As two researchers recently concluded in the Canadian Medical Association Journal, the feelings are probably psychic, the evidence suggesting some form of obsession neurosis having to do with the ghastly trauma of losing a piece of one’s body.

We suggest that general measures of a psychotherapeutic nature are likely to be of benefit, they wrote. Headshrinking, in other words.

A possible tunnel through this impasse--with perhaps a glimpse of the Holy Grail shining in its recesses--was first approached in the mid- 1980s by Michael Merzenich of the University of California at San Francisco, working with Jon Kaas of Vanderbilt, among others. Merzenich and his colleagues wanted to see what would happen to the skin map in the cortex when it was deprived of normal input. In one experiment, they amputated a finger of an adult monkey, waited a few weeks, and then took recordings of signals reaching the associated part of the monkey’s cortical map. According to the critical-period theory, this region of cortex, lacking input from touch receptors, would be as lifeless as an office building abandoned by its tenants. Instead, the researchers discovered, neurons within the region fired whenever the two fingers adjacent to the missing one were touched. Apparently nerve impulses from neighboring sections were being remapped into the vacated zone--suggesting that the adult brain was a much more flexible commodity than most scientists thought.

There had always been a countercurrent to the mainstream that suspected the brain could make such adjustments, says Merzenich. We witnessed them happening.

Nevertheless, the amount of remapping Merzenich and his colleagues had seen might still be explained with no threat to the dogma of a hardwired brain. The nerve impulses from the neighboring regions of the monkey’s sensory cortex had encroached only one or two millimeters. This just happens to be the length of an individual nerve axon, the business end of nerve cells, which makes connections with other nerves running from the thalamus to the sensory cortex. When Merzenich and his colleagues amputated two of the monkey’s fingers, the cortical remapping was not as extensive. The most likely explanation, therefore, was that existing, unused branches of the axons were already in contact across the borders of the cortical regions. When normal input from one amputated finger ceased, these dormant connections were unmasked, and new impulses were sent into the vacated region--but only so far as an individual axon could reach. In other words, you could teach an old brain new tricks, as long as you used preexisting hardwired circuits to do the learning.

In 1991 neuroscientist Timothy Pons of the National Institute of Mental Health announced new evidence that both supported Merzenich’s observations and utterly confounded any such tidy explanation for them. Pons’s study made serendipitous use of the infamous Silver Spring monkeys, a group of macaques that, in an unrelated experiment 12 years earlier, had had the sensory nerves from one arm cut where they entered the spinal cord. The monkeys had become the focal point of a celebrated animal rights trial (see Discover, January 1992). While the ethical issue raged in the courts, the monkeys languished in limbo, off-limits to research but deteriorating to the extent that the courts agreed four of them would be better off put to sleep. Before they were killed, however, Pons was permitted to plant electrodes in their cortex to see what 12 years of dormancy had done to the portion of brain map once devoted to impulses from the unplugged limbs. He expected to find confirmation of Merzenich’s results: a couple of millimeters of encroachment from the two adjacent sensory regions--in this case, from the face and the trunk. Certainly the encroachment should be no more than the length an individual nerve axon could reach.

We were astounded, says Pons. Instead of a little bit of trespassing from both sides, we discovered that the face region had completely invaded the neighboring cortex. In each of the four animals, the entire hand and arm zone responded when we stimulated the face.

In effect, fully a third of the entire touch map--over half an inch of cortex--had switched its allegiance. With no orders coming in from the numbed limb, it had married its fortunes to those of the face instead. This is neural reorganization on a massive scale, unimaginable in a hardwired brain. Input from dormant branches of neighboring axons could not be the answer, since they are not nearly long enough to make connections over such a vast swath of gray matter.

It’s really a mystery how this can occur, says Pons. We don’t have the mechanism yet to explain it.

Given that years had elapsed since the monkeys’ nerves had been severed, one possible explanation was that new connections between neurons had actually sprouted up, forging links from the facial cortex right across the whole vacated zone. Such fecund growth of tissue in the cortex seems unlikely, however, given that adult brains have never been known to grow any new neuronal connections--they only lose them. On the other hand, experiments on monkeys have shown that new axons can sprout from already existing cells in the spinal cord. Pons speculates that the enormous changes witnessed in the monkeys’ skin maps might be the consequence of relatively modest growth occurring in more constricted places farther down the touch pathway, before the nerve impulses ever reach the cortex itself.

One obvious point of constriction is the thalamus. Within this relay station, nerve impulses traveling from the face to the cortex must pass through the region that is simultaneously receiving input from the hand and arm. Normally the facial pathway crosses through the hand-and-arm portion of thalamus without making any connections, like a road crossing a highway without an interchange. Over time, however, even a little local sprouting where these facial nerves pass through the limb’s portion of thalamus could create new synapses--and throw the whole facial input up onto the hand and arm region of the cortical map. Pons prefers the analogy of hooking up your telephone line to the neighbors’ house. At this constricted, local level, it doesn’t take much wire to send your calls spinning out over their entire long-distance network.

Whatever its ultimate explanation, the flagrant remapping Pons had witnessed in the Silver Spring monkeys sent a surge of excitement through the growing coterie of neuroscientists who believe in brain plasticity. Among the inspired was Ramachandran. For several years he had been probing the mystery of blind spots in the visual system. Everyone has a small natural blind area on each retina, about 15 degrees off center. None of us walks around with a corresponding black hole in our visual field, however, because the brain fills in the missing portion with information from the surrounding background. Victims of stroke or head wounds may have much larger blind spots--yet in most circumstances, they too automatically fill in the gap with details from the background. Ramachandran and others strongly suspected that this neural sleight of hand is achieved by the remapping of impulses normally delivered to adjacent parts of the visual cortex.

When Ramachandran saw Pons’s paper, he began to wonder whether much the same sort of filling in was taking place in the tactile system of phantom limb sufferers. He recruited some amputees to help test his hypothesis. One volunteer was a teenager named Victor Quinterro, who had lost his left arm in an auto accident only four weeks earlier. As Victor sat blindfolded in a chair, Ramachandran gently touched his face with a Q- tip.

Where do you feel that? he asked.

You are touching my face, said the teenager. But I also feel my left thumb tingling.

And here? asked Ramachandran, stroking the skin above Victor’s upper lip.

You are touching my index finger.

Now? The Q-tip moved to Victor’s chin.

My pinkie.

Ramachandran continued his probing, touching his patient’s chest, abdomen, and various points on his good arm, without any reaction from the phantom. Only when he touched the cotton-tipped wand to an area just above Victor’s stump did the magic return.

There, my thumb tingled again . . . now my index finger . . . the ball of my thumb . . .

In effect, Ramachandran’s Q-tip had ferreted out the physical, fleshly substance of Victor’s illusory hand. Neurologically speaking, at least, the hand was not missing at all--indeed, it was now a pair of left hands, one meticulously laid out across his lower face, the other wiggling its digits just below his shoulder. In the version of Victor mapped into his somatosensory cortex, these two regions happen to border the area that formerly received messages from the amputated arm. This suggests that much the same kind of complete, orderly takeover as Pons had witnessed in his monkeys was indeed occurring in phantom-limb patients too. In this case, however, the invasion was a flank attack from both adjacent regions, rather than from the face alone.

Ramachandran performed similar experiments on half a dozen other patients. All possessed at least one remapped edition of the lost piece of themselves, the transference achieved with uncanny orderliness and vivid clarity. Another patient, who had had both his right arm and part of his shoulder removed, was amazed to feel Ramachandran’s Q-tip tracing out his complete missing forequarter across his face--the shoulder tucked into the jaw joint, the elbow etched across the elbowlike bend of the lower jaw, the hand and fingers reaching toward his chin. Another version of the amputated region was mapped onto his torso, which was so sensitive that nudging a single body hair at one point keenly tickled his phantom elbow. Working with another patient, a man who had lost all feeling in his left arm when its nerves were yanked from his spinal cord in an auto accident, Ramachandran accidentally dribbled a little warm water from his Q-tip. It ran down the patient’s face and under his collar.

Hey, that was really weird, said the patient. It felt like you were literally pouring water down my arm.

Perhaps the most astonishing observation was the shortness of time it had apparently taken for the remapping to be completed--in Victor Quinterro’s case, only four weeks. To Ramachandran, such a rapid remapping of inputs makes Pons’s sprouting hypothesis unlikely, because there simply isn’t enough time for even a modest amount of new nerve tissue to grow. Instead, he believes, hidden circuits must already exist in the neural wiring that allow for the expansion of one cortical area into an adjacent one. As long as the normal, stronger inputs are being received from the touch receptors, these circuits lie dormant. But when the receptors suddenly shut down--for example, when a limb is amputated or paralyzed--the latent circuits are unmasked and the whole limb cortex begins to sing its neighbor’s tune.

It is as if there is a competition going on between different circuits, says Ramachandran, with the strongest one laying claim to the whole contested territory.

If he is right, the unmasking hypothesis might hold some therapeutic wisdom. Normally, stroke victims who have lost the use of a hand are encouraged to exercise their arms as much as possible to encourage feeling in the adjoining hand to return. But if unmasking is the secret to cortical remapping, then logically the arm should be immobilized instead, its input muted as much as possible to allow the hand’s weakened circuits a chance to reestablish their former hegemony over their parcel of cortex.

Pons insists, however, that there is no evidence for latent circuits capable of invading whole cortical regions, waiting to be unmasked. It’s like saying that when your electricity blacks out, your backup generator will kick in, he says. Only in this case, there isn’t any backup generator.

Like Pons, Ramachandran admits that at this point his favored explanation for how remapping occurs is little more than speculation. But he is confident nonetheless. We know now that the source of phantom limb is in the brain itself, he says. Far from being deadweight in the brain, the cortex associated with the lost limb is alive and well, passing messages further on up the system. The messages may not be originating in the limb anymore, but the rest of the brain doesn’t know that.

Is the rest of the brain, then, just an innocent dupe, taken in by a switch play of inputs in the cortex? What is happening in phantom limb further on up the system? The precise region where Tim Pons witnessed massive remapping in his monkeys--called the primary somatosensory cortex, or S1 for short--is in fact only the initial receiving station in a chain of a dozen or so increasingly complex skin maps in the cortex. Each presents an opportunity for shaping and refining the sensations arriving from farther down--and another opportunity for inputs to be remapped. This touch pathway runs parallel to another series of cortical maps--which respond to receptors in the muscles and joints--governing proprioception, the sense that allows you to know the position of your limbs and other body parts. Both the touch system and the body-position system communicate with cortical regions controlling muscle movements, and they jointly feed another area of the brain, in the parietal lobe, that is responsible for body image and recognition. A brain lesion in this region can lead to a condition called unilateral neglect--a sort of bizarre mirror image of phantom limb. Rather than feeling sensations from a nonexistent appendage, the sufferer denies that a perfectly functional part of his body belongs to him; he may stubbornly shave only one side of his face, or thrust away the stranger’s leg that is inexplicably attached to his own body.

Ramachandran suspects that regions along this proprioceptive pathway must also remap for the phantom limb phenomenon to occur. But would this explain why Fred Aryee feels a shock of pain as a cup is wrenched out of a hand that exists only in his mind? According to the neuroscientist, Aryee’s discomfort might be explained by the involvement of motor command centers in the brain, which are sending a signal to the missing limb, telling it to grab the cup. In the absence of proprioceptive feedback from the hand itself, the motor command virtually swamps the pathway, barking its imperative--GRAB THE CUP!--much more forcefully than normal. The same phenomenon might explain why the young woman missing both arms since birth is hyper-aware of the animated gestures her arms make during an argument. Or maybe it doesn’t.

The surprising thing about her is that after 22 years of never receiving feedback from her arms, she still feels the phantom, says Ramachandran. We can’t explain everything yet.

Ronald Melzack, a neuropsychologist at McGill University in Montreal, believes that such an encompassing explanation will only come from the understanding of an extensive neuromatrix of circuits, extending beyond the sensory pathways and into the brain’s limbic system, which is critical to emotion and motivation. Remapping sits just fine with me, he says. But you can’t just focus on the primary somatosensory cortex alone, as if that’s the place where all the bells are ringing. It’s only part of the picture.

Nevertheless, from a research point of view, it is the part of burning interest. Talk about vast networks of interacting neurons is notoriously cheap; a glimpse of a piece of such a network physically reorganizing itself is a priceless novelty. The major question, of course, is why.

I doubt that it does anybody any good to have their missing arm mapped out across their face, or to suffer from extreme phantom pain, says Kaas. But these things demonstrate that the adult brain has far greater flexibility than we thought. They are a result of brain plasticity that works against the person.

In normal circumstances, Kaas believes, the ability of the brain to restructure itself may be what allows people to recover from head injuries that snap axons in the brain and sever critical connections. After a period of confusion, normal functioning returns--presumably because other, adjacent areas of the brain are able to take over the chores of the dead nerves. Neuronal loss is in fact a natural process that continues through adult life, whether you are clobbered on the head or not. Up to a certain age, perhaps our brains cope with their own steady deterioration by recommitting still-lively regions of the cortex to the tasks formerly handled by the defunct circuits. Much would depend on keeping the alternative circuits strong by using them. This may explain why people who remain mentally engaged as they grow older seem to hold on to their acuity longer.

There’s been folklore that says ‘Use it or lose it,’ says Kaas. This work gives a theoretical justification for that belief.

The boldest hope of all is that the understanding of brain plasticity will eventually solve the mystery of learning and memory. When a tennis player practices a new backhand or a pianist masters a sonata, something must physically change in their brains to allow them to perform effortlessly a task that was initially difficult. Remapping in and among higher levels of the brain may be that something. Recently, Merzenich and his colleagues trained monkeys to recognize different vibrations using their middle fingers. As the monkeys became more adept at discriminating different frequencies of vibration, neuronal connections within the cortical maps of their middle fingers grew stronger, and the map itself expanded into adjacent areas. Neurobiologist Alvaro Pasqual-Leone of the National Institutes of Health has shown that training blind people to read braille similarly swells the cortical maps devoted to their newly literate fingers.

The idea that training actually modifies the microstructure of the brain has terrific implications for the future, says brain researcher Vernon Mountcastle of Johns Hopkins. If structure can be modified at low- level ranges like these, why not at higher levels too? You might eventually be able to train for specific skills in better ways.

Much remains to be understood, however, before we can send our children to neurology labs to have their math aptitude puffed. The first step would be a resolution to the nagging mystery of the mechanism of remapping--is it the sprouting of new axons, as Pons suspects, or the unmasking of latent circuits, as Ramachandran believes? The two investigators may soon be collaborating on new experiments, testing amputees with a powerful new brain scanning technique called functional magnetic resonance imaging. With no harm to the patient, the technique produces snapshots of the brain clear enough to determine where in the touch pathway inputs from missing limbs first go astray. Knowing that could tip the balance toward one explanation or the other. At the outset, however, each scientist concedes that his own favorite hypothesis seems barely more possible than its rival.

That’s the real excitement of all this, says Pons. We are forced to consider the impossible.
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