The Brain That Misplaced Its Body

Though paralyzed on one side, Mrs. M. claimed she wasn't--at least until she had cold water poured in her ear. Then, for a while, her brain could again perceive her body. And a neuroscientist could glimpse a secret about how we construct reality.

By James Shreeve|Monday, May 01, 1995
RELATED TAGS: SENSES
Mrs. M. is adamant. People are saying her left side is paralyzed, and she knows they are wrong. Several days ago the 76-year-old Californian suffered a stroke. She now sits in a wheelchair while a doctor in a crisp cream-colored suit bends over her, asking questions. She answers them with perfect coherence. Does she know where she is? Yes, she is in a hospital, brought here by her daughter. Does she know what day of the week it is? Of course. It is Tuesday afternoon.

Then the doctor starts in again about her hands. Can she use her right hand? Yes. Her left? Yes, of course. He asks her to use her right hand to point to a student who is taking notes, and she obliges. He asks her to point to the student with her left hand instead. This time she doesn’t move.

Mrs. M., why didn’t you point? asks the doctor. For the first time, she hesitates.

Because I didn’t want to, she answers.

In fact, fibers in the motor cortex on the right side of her brain, which controls movement on her left side, have been irreparably damaged by the stroke, and she will never use her left arm again. But Mrs. M. is not a stubborn old woman refusing to admit a difficult truth. A few minutes later Mrs. M. looks at her left hand, resting inertly in her lap.

Doctor, she asks, whose hand is this?

Whose hand do you think it is?

Well, it certainly isn’t mine!

Then whose is it?

It is my son’s hand, Doctor.

Mrs. M.’s claim would be peculiar enough if her son were in the room, but he is miles away, unaware that in his mother’s mind his hand has become attached to her arm. Mrs. M. is suffering from a condition called anosognosia, which sometimes appears when a stroke has cut off blood being supplied to the brain through the middle cerebral artery. The stroke damages regions in the brain’s right hemisphere that include a territory called the right parietal cortex, a patch of neurons about two-thirds of the way back along the brain. The two parietal cortices (there is one in the left hemisphere also) are known to be involved in directing the brain’s attention to movements, objects, and sensations on the opposite side of the body, as well as in the perception of that entire side of the body in space.

While otherwise clearheaded, patients with damage to the right parietal cortex are unable--not just unwilling--to acknowledge the radical change that has overcome the left side of their body. (The term anosognosia derives from nosos and gnosis, the Greek words for disease and knowledge.) One of the best-known victims of the condition was Supreme Court justice William O. Douglas, who suffered a right-hemisphere stroke in 1974 that paralyzed his left side and eventually forced his retirement. He initially dismissed the paralysis as a myth, and weeks later he was still inviting reporters to go on hiking expeditions with him. When one visitor asked about his left leg, he claimed that he had recently been kicking 40- yard field goals with it in the exercise room and soon planned to try out for the Washington Redskins.

Mrs. M.’s form of anosognosia is even more extreme: she not only flatly denies she is paralyzed, she refuses to admit that the limp limb on the left has anything at all to do with her. One such anosognosiac became so incensed that somebody else’s leg was cluttering up his hospital bed that he heaved the thing out and was subsequently amazed to find himself on the floor. Another claimed that the arm on the left belonged to his daughter, who was trying to seduce him.

We are used to thinking of our bodies as our selves, says Vilayanur Ramachandran--the inquisitive doctor in the cream-colored suit. Something has gone wrong here that calls that fundamental truth into question.

Anosognosia is a fleeting condition, in most cases fading away within two weeks of the stroke that caused it. In the interim, however, patients like Mrs. M. may provide a window through which we can glimpse how we all perceive reality, how our minds organize and cope with the cognitive blitz of everyday life. While most of us have no trouble fessing up to ownership of our various body parts, we all are sometimes willfully ignorant of signals our bodies send to our brains--there might, for example, be a tiny twinge of ankle pain that we’d rather not notice just before that weekend tennis game. In a new theory, Ramachandran claims that anosognosia can help explain why, how, and even where in the brain such everyday denials take place and how we combine them into a representation of the world around us. If he is right, this theory may also shed light on the function of dreams, and even on the mechanisms of memory itself.

Looking at patients like Mrs. M. can be spooky at first, says Ramachandran, a neuroscientist and physician at the University of California at San Diego, and the Salk Institute nearby. But then you realize you’re really looking at yourself, in amplified form.

Ramachandran has made a career out of using spooky phenomena to reveal the workings of the brain. With optical illusions, he has explored the neural circuitry of vision. More recently he helped track down the neural basis for phantom limb, the sensation that most amputees have that their lost arms or legs are still attached to their bodies. His findings helped illuminate how the brain restructures itself during learning. From patients who feel phantom arms in the empty space beyond their shoulders, it was a logical step to look next at patients who denied arms that were indisputably real.

Ramachandran was unsatisfied by the two conventional explanations for the rending of body image demonstrated by anosognosiacs. The first is Freudian: to protect the ego against the appalling truth that one side of the body has been rendered permanently senseless, the mind simply refuses to admit to the facts at hand. But patients with paralysis caused by stroke in the left parietal cortex rarely deny their condition. Why should only people with right-brain stroke need to protect their egos from the truth?

The second explanation is more neurological and less psychoanalytic: anosognosia is a special case of a more general syndrome that textbooks refer to as unilateral neglect. Some stroke patients with damage to the right parietal cortex fail to recognize anything in the left side of their perceptual domain. If they are asked to follow an examiner’s finger as he moves it across their visual field from right to left, their eyes track the finger up to the midpoint, then stop. Patients with unilateral neglect may eat food from only the right-hand side of a plate, or shave only the right side of the face. Anosognosiacs like Mrs. M. often exhibit such behavior, too. Perhaps they are simply neglecting their paralysis in the same way they disregard everything else on the left side.

Clearly the two phenomena seem related. Yet Ramachandran thinks this explanation, too, leaves much unaccounted for. Patients with neglect will ignore an object in the left side of the visual sphere, but they will readily acknowledge the object if their attention is drawn to it--if, for example, an examiner wiggles his finger in the neglected side of their visual domain and says, Now do you see it? Anosognosiacs, on the other hand, do not passively ignore their paralysis; they actively deny it, in spite of their complete inability to move. If pressed to account for such a conflicting state of affairs, they remain silent or try to explain it away, often concocting elaborate stories or chillingly surreal rationalizations. Neuroscientist Edoardo Bisiach at the University of Milan in Italy reported one 74-year-old stroke patient who repeatedly claimed that his left hand belonged to the doctor examining him. The doctor finally grasped the paralyzed hand between his own two and held it up to the patient’s face.

Whose hands are these? he asked.

Your hands, the patient replied.

How many of them?

Three.

Ever seen a man with three hands? the doctor asked.

A hand is the extremity of an arm, said the patient. Since you have three arms, it follows that you must have three hands.

There is more going on here than simply an indifference to or neglect of the left side of the body, says Ramachandran. And that’s what’s crying out for an explanation.

One explanation might be that anosognosiacs only appear to be ignorant of their paralysis while in fact they are fully aware of what has happened but for some reason do not wish to express it. To test this hypothesis, Ramachandran devised a devilish experiment. He presented Mrs. M. and two other elderly stroke victims with a simple choice. They could win themselves a small box of candy or some other trivial reward by completing a task requiring one hand, such as fastening a large nut onto a bolt mounted on a heavy base or stacking some blocks. Alternatively, they could earn a much larger box of candy by successfully finishing an easy activity requiring two hands, such as tying a bow or cutting a circle out of paper with scissors. All three subjects exhibited neglect and denied the paralysis on their left side, but they were otherwise alert and aware of their physical condition. (One even responded to the choice by chiding, I am diabetic, Doctor. I don’t eat candy. You should know that!) For control subjects Ramachandran chose two stroke patients who were also recently paralyzed on the left side by stroke and showed clear signs of neglect but no trace of anosognosia.

As might be expected, the controls unhesitatingly chose to obtain the small box of candy by performing the task requiring only one hand, expressing surprise that anyone would even present them with such a choice since the two-handed tasks were obviously beyond their ability. But in 15 out of 16 trials, the anosognosiacs opted to try to win the large box of candy. After fumbling feebly with the laces or scissors, they would remain silent or offer some excuse for their failure. (I guess my arthritis is acting up. Oh, I’ve never been very ambidextrous.) Curiously, they never seemed to learn from their previous botched attempts or even remember them from one trial to the next.

It’s very strange, says Ramachandran. No matter how often they failed, they never showed any sense of surprise or frustration.

The inextinguishable faith in their two-handed abilities seemed to indicate that if the anosognosiacs knew they were paralyzed, that knowledge lay deep, buried well below the level where it could be freely accessed by their conscious mind. Yet certain things they said hinted at tacit knowledge of their condition, meaning that the information had been recorded in some part of the brain, whether or not it was immediately available. After failing repeatedly at the bimanual task of tying a shoelace, Mrs. R., a former journalist who was now in her seventies, later told a student that the nice Indian doctor asked me to tie a lace, and I did it, with both hands.

Normal, unparalyzed people don’t feel the need to draw attention to the fact that they can use both hands; they just do it, says Ramachandran. As Shakespeare said, ‘The lady doth protest too much.’

To probe the depth of that tacit knowledge, Ramachandran made use of an experiment performed earlier by Bisiach and his colleagues. They had temporarily reduced the symptoms of an anosognosiac by the simple means of pouring a small amount of cold water in her ear. The treatment wasn’t as far-fetched as it might sound. In addition to hearing, our ears function as our gyroscopes. They house fluid-filled canals lined with microscopic hairs that sense acceleration; this information is transmitted through nerves known as the vestibular system to different parts of the brain. Some of these parts direct our bodies to make the adjustments needed to maintain our balance. Other parts, like the parietal cortices, are responsible for letting our eyes steadily track moving objects. To do so, they need to have information about how our bodies are moving in space--thus the connection between the vestibular system and the parietal cortices, and the basis for Bisiach’s seemingly bizarre treatment.

Bisiach’s patient, a right-brain stroke victim in her eighties, claimed that her arm belonged to her mother, who had apparently left it behind in the bed when she was discharged from the hospital. When Bisiach poured cold water in the woman’s left ear, her overstimulated vestibular system began to send confused signals to her brain, which concluded that her head was turning, and after a few minutes she involuntarily began moving her eyes rapidly back and forth to compensate--a process known as nystagmus. The patient was asked again whom the arm belonged to, and this time she admitted that it was her own. Bisiach ran a series of cold-water trials and found that it took anywhere from 15 seconds to two hours for the effect of the cold water to wear off. But once it did, the woman would invariably lapse back into the eerily unconcerned delusion that her arm was her mother’s.

Look, it’s queer, but that’s how it is, she said.

Ramachandran decided to try Bisiach’s experiment on Mrs. M. Working with fellow San Diego neuroscientists Leah Levi and Lance Stone, he poured cold water into her left ear and waited until the rapid eye movement of nystagmus appeared. Asked to identify the owner of the arm lying in her lap, she stated that it was hers, of course. She also acknowledged that the arm was paralyzed. When Ramachandran asked her how long she had been in that condition, she accurately replied that she had been unable to move her arm for several days. Remarkably, it seemed that all the time Mrs. M. had been denying her paralysis, the knowledge of it was nevertheless being recorded in her brain. Yet when the effect of the cold water wore off several hours later, she not only reverted to denying the paralysis, she had no recollection of ever having come out of that state of denial. It was as if there were two completely separate Mrs. M.’s: an anosognosiac version who was convinced that she was perfectly able to move her arm, and a cold- water version who acknowledged her paralysis but expressed total ignorance that she had ever denied it.

The curious effect of the cold water on Mrs. M. fit neatly into a hypothesis brewing in Ramachandran’s own mind. At any given moment in our waking lives, our brains are flooded with information pouring in from various senses, all of which has to be fitted coherently into a perspective that’s based on what our stored memories already tell us is true about the world. In order to act, the brain must have some way of selecting from this superabundance of detail and ordering it into a consistent belief system, a story that makes sense of the available evidence.

But what happens when the information arriving from some source conflicts with the existing plot? If the conflicting information is only mildly important, one easy response might be to just ignore it. The twinge of pain in the ankle of that weekend tennis player, for instance, does not jibe with the reports received from other joints and muscles, much less with his senses’ appreciation of the glorious sunny day and his memory of last week’s exciting game. To keep the story consistent and intact, his brain edits out the information coming from pain receptors in the ankle. He might deny to himself that the pain exists, or he could rationalize it to fit with the prevailing belief system, perhaps by telling himself it will go away as soon as he loosens up.

As an analogy, think of a military general in a war room, planning for a battle, says Ramachandran. He would ordinarily collect evidence from a large number of scouts, add it all up, and arrive at a decision on what to do next. Let’s say the information from his scouts led him to call for an attack the next morning. But just before the scheduled attack, imagine one more scout arrives and tells him that he has underestimated the enemy’s strength by a quarter. Even though that new information contradicts everything else he has been told, the general cannot afford to rethink the whole decision. Instead, he simply ignores the report from the new scout or tells him to get in line with what everybody else is thinking. He may even tell him to lie in order to preserve troop morale.

Ramachandran describes this metaphoric general--who roughly corresponds to Freud’s concept of the ego--as a die-hard conservative coping with reality by promoting the status quo and denying or rationalizing away any information that threatens it, in the interest of preserving stability. Such everyday defense mechanisms are not really maladaptive: they keep the brain from being hounded into directionless indecision by the sheer number of possible stories that might be written from the material available from the senses. Frequently, however, new, conflicting reports arrive that are too critical to ignore. If a scout presents a general with last-minute news that the enemy possesses nuclear weapons, it would be disastrous for the commander to carry on according to the existing plan. Likewise, the weekend tennis player can deny knowledge of his sensitive ankle without penalty, up to a point. If the pain receptors in his ankle are commanding attention whenever he puts weight on the leg, to ignore them would defeat the purpose of having pain receptors in the first place. Instead, the tennis player abandons the prevailing story--Tennis anyone?--and constructs a completely new one in line with the undeniable truth shooting up his leg from his ankle: Better rest up this week.

To balance the conservative, maintain-the-status-quo strategy of the general, there must therefore be another decision maker, an anomaly detector, as Ramachandran calls it. The anomaly detector’s job is to constantly evaluate the general’s official story, decide when the conflict between the old belief system and new information passes a certain threshold, and then intervene, destroying the official story and working with the general to write a new one.

Mrs. M.’s anomaly detector has fallen asleep at the post. Her brain endeavors to construct a plausible story about her body image according to the evidence received from various sensory systems, just like a normal brain. But then a radically conflicting report arrives, one that a normal brain would quickly perceive as too anomalous to fit into preexisting beliefs. (I am telling my hand to move, and it is not responding!) Since the anomaly detector is not doing its job, however, the incongruous information is swallowed into the existing story, and Mrs. M.’s brain fails to recognize its incompatibility. The general is free to file away the tragic news of her paralysis, maintaining the status quo with a blanket of denials, rationalizations, and confabulations that can accommodate even the most bizarre conflict because there is nothing holding it up to scrutiny.

Since we know which part of the brain is disabled in anosognosia, the curious delusions of a damaged mind may thus provide the means to anchor the airy abstractions of Freudian psychology in the physical flesh of the brain. In Ramachandran’s scenario, the story-building of the conservative general--Freud’s ego--largely involves the left side of the brain, where the language centers called Broca’s area and Wernicke’s area are also located. Challenging the general’s story, on the other hand, can take place only in a healthy right hemisphere. So according to his theory, when Ramachandran poured cold water into Mrs. M.’s left ear, and by means of the vestibular system stimulated brain areas in her right hemisphere, he reawakened the anomaly detector, which promptly saw that the general’s story had been clearly outrageous for several days. She was then able to grasp the reality of her condition until the cold-water stimulation faded and the anomaly detector went back to sleep.

Does that mean the anomaly detector actually resides in the right parietal cortex--an area known to be damaged in anosognosiacs like Mrs. M.? It would be unreasonable to suggest that such a complex cognitive function exists in some precise location in the brain, Ramachandran says. But given the breakdown in anomaly detection shown in anosognosia, it would seem that the parietal cortex and associated areas damaged by the stroke are somehow involved.

A key question to resolve is whether the extreme denials of anosognosiacs represent a breakdown in anomaly detection in general or are only an isolated aberration specific to how they perceive their bodies. One circumstantial hint that Ramachandran has tapped into a global process is a certain common pattern in stroke victims. Patients with right-brain stroke damage, even those who don’t exhibit anosognosia, often appear oddly oblivious to illness or other problems, carelessly shrugging off news that they have a malignant tumor or that a loved one has been in a serious accident. Since the right side of the brain is commonly thought of as the emotional hemisphere, such blasé responses have previously been considered a result of the stroke’s suppression of emotional circuits. Ramachandran’s model suggests instead that the affected circuits are involved with anomaly detection: the patients do not react to disturbing information, because their active left-brain circuits have filed it away as too threatening to the status quo, and no complementary critique of that action takes place in the right hemisphere of the brain.

Meanwhile, it is common for victims of stroke in the left side of the brain to suffer a contrary fate. Far from denying their illness and problems, they dwell on them, their obsession with all that is wrong spiraling down into deep depression. In the global model Ramachandran envisions, these people have no left-brain general operating to smooth over life’s difficulties by repressing information. Instead, they struggle to attend to every unpleasant detail.

Ramachandran plans several lines of research to test his hypothesis experimentally. One is already under way: he is studying the responses of anosognosiacs to a situation in which sensory information about their arm has been intentionally brought into conflict. The experiment makes use of a trick wooden chamber. The subject’s hand is placed in the box through a hole in the front, and the subject looks down on it through a hole in the top. Unbeknownst to her, however, the box contains another hole in the rear and a system of mirrors that enables a hidden accomplice of the examiner to extend a hand into the box from behind a partition. The mirrors substitute an image of the accomplice’s hand for the subject’s. (Both hands are gloved, to mask the deception.) The examiner can then tell the patient to move her hand or keep it still, at the same time giving a surreptitious cue to the accomplice to do just the opposite. The subject’s visual system thus receives one message while at the same time her sense of body position and movement is sending a completely conflicting one.

In a recent trial, an anosognosiac’s paralyzed left hand was placed in the box, and she was asked to watch her hand and move it to the beats of a metronome. The accomplice was given a cue, and the hand in the box began to move accordingly. On the first trial, the patient’s response left everyone utterly perplexed. Not only did she show no surprise at seeing her hand moving up and down, she denied seeing any hand at all. When Ramachandran repeatedly asked her what she saw, she admitted that the box was not empty. But there was definitely no hand inside. There was a wedding cake.

Though it is only guesswork, Ramachandran believes that in response to such a bizarre mix of signals, her brain simply canceled all inputs and substituted a hallucination in their place. In a later trial, a different patient reported that her left hand moved when she was asked to move it, a result that might be expected given her professed denial of her paralysis. But then Ramachandran asked her to place her good right hand in the box instead and move it. Once again she said she could see the hand moving--even though his accomplice was keeping her hand still. Thus the patient was patently denying an obvious truth that had little to do with the left-side paralysis itself--an indication, perhaps, that the functions damaged by the stroke involved more than the specific circuits concerned with the left side of the body.

The minute there was a discrepancy in the existing story, she tried to make it fit, because her anomaly detector wasn’t there to catch it, says Ramachandran.

To better test whether the anomaly detector is global or specific to body image--or whether it exists at all--Ramachandran plans a series of experiments using a brain scanning technique called functional magnetic resonance imaging, which can pinpoint areas of the brain activated by stimuli. It would be extremely suggestive, for instance, if part of the right parietal cortex implicated in anosognosia was activated when normal subjects detected the anomaly in an object quickly glimpsed, such as a flashed image of a red ace of spades.

Until Ramachandran has a chance to use this high-priced imaging equipment, though, he is the first to admit that his theory of the nature of mind is highly speculative. But he doesn’t mind speculating further. Much of his reasoning hangs on the mysteriously therapeutic effect of cold water poured into an anosognosiac’s ear. The most common explanation for this phenomenon follows from the view that anosognosia is a manifestation of unilateral neglect, wherein the stroke-damaged patient ignores all that is happening on the left side of the perceptual domain. It could be that the shock delivered to the vestibular system by the cold water jump-starts the right parietal cortex, enabling the patient to again pay attention to everything on her left side, including her paralysis.

Ramachandran finds this answer unsatisfying for the same reason he balks at attributing anosognosia to neglect in the first place: the patient isn’t simply ignoring her paralysis, she is adamantly denying it. He believes instead that the cold-water stimulation triggers circuits in the parietal cortex involved in anomaly detection, allowing a patient like Mrs. M. to perceive the glaring discrepancy between her belief that she can move and the sensory evidence that she patently cannot.

While the cold water’s effect on the vestibular system is no doubt implicated in Mrs. M.’s recovery of perception, what fascinates Ramachandran is the rapid eye movement that accompanies this sudden release from denial. What if her apprehension of the disturbing truth of paralysis was linked to another context in which rapid eye movement appears just as repressed information is allowed to well up to the surface? There is only one state in normal life where your eyes move back and forth and you pull up unpleasant memories and disturbing beliefs about yourself, he says, and that is the REM, or rapid eye movement, sleep that produces dreams.

According to Ramachandran, while we are awake the left-hemisphere general is working hectically--selecting, ordering, and repressing information to produce a coherent story for subsequent action. Our anomaly detector intervenes only at critical junctures, since the brain’s story has to be consolidated under the constant pressure to respond to new stimuli. As a result, some information may end up being repressed that might actually prove useful in the future. In REM sleep, the brain can review these buried perceptions and memories of the past and rehearse them on the risk-free stage of dreams--what Ramachandran calls nature’s own virtual reality. If the information still cannot be accommodated under existing beliefs, the material is repressed again, unless the dreamer happens to be awakened accidentally and temporarily glimpses the script in progress. But we remember very little of our dreaming. Most of it, Ramachandran suggests, is comfortably and invisibly integrated into the belief system supported by the conscious mind, which in the process becomes progressively more liberated from unnecessary defenses.

At the risk of pushing the metaphor too far, Ramachandran says, imagine the general during the day, in the heat of battle. He doesn’t have time to review the contrary reports from every scout who comes in, so he shoves them into file drawers marked Top Secret. When he has a chance to relax late at night, he takes some of these files out of the drawer and gives them a second look. The anomaly detector joins the general over drinks, as it were, and shows him where the files dangerously contradict the official story. In my view, this is what is happening each time you dream. You open your top-secret files and psychoanalyze yourself, deciding which memories to repress and which to uncover.

The link between the cold-water confessions of an anosognosiac and the normal function of dreams in REM sleep is still hypothetical. Curiously, however, the currently popular therapy called EMDR (Eye Movement Desensitization and Reprocessing) relies on the purported ability of the therapist to relieve the distress of repressed traumatic memories by focusing the patient’s eyes on a finger waved rapidly back and forth. Ramachandran does not actively support or plan to use the therapy on anosognosiacs, but he finds the coincidence with his own hypothesis intriguing. We’re not saying that putting cold water in somebody’s ear makes them dream, he says. But perhaps the stimulation mimics REM and some of the phenomena that happen during dreaming, one of which is this dredging up of unpleasant memories.

His plan to test this aspect of his theory is simple: he intends to awaken anosognosiacs from REM sleep and ask about their dreams. In contrast to Freud’s notion that dreams are wish fulfillments, Ramachandran’s idea predicts that anosognosiacs should dream that they are paralyzed, since during REM their anomaly detector should be reawakened. It may even be that dreams cure anosognosia. By reviving the anomaly detector night after night, an anosognosiac integrates the fact of paralysis into his or her belief system over several days.

Ramachandran plans to conduct the same low-tech experiment on victims of anterograde amnesia, in which brain trauma destroys the individual’s capacity to form long-term memories after the injury occurred. Anterograde amnesiacs are equally forgetful of emotionally neutral information, such as a list of words, and major circumstances in their lives, such as the identity of people whom they’ve met since their injury. Even attending physicians have to reintroduce themselves to anterograde amnesiacs every time they enter their presence--as if they had never met before. According to Ramachandran’s hypothesis, these amnesiacs may have lost the capacity to consolidate any information into a working story in the left side of their brains. Instead, their generals indiscriminately file all inputs into drawers marked TOP SECRET, where they cannot be accessed by the conscious mind. Since these are the drawers that are opened during REM sleep, an amnesiac awakened while dreaming might be able to recover memory of some recent events. In any case, it’s worth a try.

My colleagues would give this idea maybe a 10 percent chance of being right, Ramachandran says. I’d give it 30 to 40 percent. But even if I’m wrong about the entire theory, it does suggest some interesting directions, doesn’t it? Who would have thought to wake up amnesiacs and ask them about their dreams?
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