VOLUME 29 , NUMBER 6 -June 1998


Why canít this man feel whether or not heís standing up?

One manís loss of sensation allows researchers a window into basic questions about touch and movement.

By Beth Azar

Until Ian Waterman was 19, he, like most every one else, thought little about his ability to sense the position and movement of his body. What 19th-century neuroanatomist Sir Charles Bell called the 'sixth sense' and what psychophysicists call proprioception and now consider a part of the haptic, or touch system, is so unconscious that few people realize itís there.

Watermanís obliviousness to that sense ended when a viral infection destroyed the nerves that control his sixth sense as well as those for feeling light touch. Heís lost all feeling below the neck and is unable to tell without looking how his body is positioned.

That was 1972 and even Watermanís doctors had a hard time understanding the extent of his disability.

Through trial and error over three years, Waterman, who lives in Hampshire, England, taught himself how to move again by consciously controlling and visually monitoring every action. To this day, if the lights go out unannounced, he crumples to the floor, unable to budge until they come back on. Itís almost impossible for most people to imagine his condition, he admits.

'How can one explain a total loss of proprioception?" a sense most people donít even know they have?' he is quoted as saying in 'Pride and a Daily Marathon' (MIT Press, 1995), the book neurophysiologist Jonathan Cole, MD, wrote about his condition.

Cole, of Poole Hospital, Poole England and Southampton University, met Waterman in 1986 and was the first physician to take a true interest in the case and Watermanís plight. 'Before I met Jonathan, I often thought I might be mad,' says Waterman. 'No one understood what was wrong or why life was such a struggle.'

Now, many researchers, including psychologists, are fascinated not only by Watermanís physical disorder but also by his ability to compensate for his loss. His case brings to life the critical importance of the sense of proprioception and touch, says psychologist Michael Turvey, PhD, who studies touch at the University of Connecticut (see article page 19). 'The haptic senses underlie almost everything we do that involves movement,' he says. 'At the same time, Waterman is able to do more than many theories of touch and movement would predict.'

The case represents a unique opportunity to test theories of touch; proprioception and movement that would be impossible otherwise, say researchers. They are able to examine how a total lack of feedback from the outside world affects how a person moves about in and interacts with the environment.

A remarkable recovery

Cases like Watermanís are remarkable in the precision of the damage: Waterman lost none of the nerves that control muscle movement and he is still able to feel temperature, pain, deep pressure and muscle fatigue (see chart on page 20). He has lost all of the cutaneous nerves that provide the skin with the sense of touch and all of the nerves attached to muscles and tendons that provide a sense of joint and limb position.

His recovery is equally unique. Although his movements can look mechanical, itís often hard to tell thereís anything wrong unless something unexpected happens and heís thrown off balance, say those who have met him.

Two other cases, a man in Pittsburgh and Ginette Lizotte in Quebec, have recovered different amounts of function: The man suffered his loss late in life and has limited movement. And Lizotte whose lack of touch begins just below the nose - made a conscious choice to stay in a wheelchair and not try to learn to walk again.

'We choose our own paths,' says Waterman. 'Lizotte chose the path to stay in a wheelchair. Was what I chose better? I donít know. Sometimes I wonder. Itís been a huge mental drain on me and still takes an awful lot of cognitive energy to maintain my movements.'

For researchers, the fact that Waterman and the others are able to move and interact with their environments is remarkable. Theories of movement wouldnít have predicted it, says Chantal Bard, PhD, who studies Lizotte and has collaborated with Cole. The patients represent a window into whatís possible without proprioception and touch.

One of the biggest surprises for Cole and Bard is that Waterman and Lizotte can accurately estimate the weight of objects they lift. Several psychophysical theories indicate that people judge properties such as weight and length by using feedback from the stretch of their tendons and muscles. To compensate for the loss of this type of feedback, Waterman and Lizotte use vision to watch how their bodies react to a set movement when they pick an object up: The faster and higher they move, the lighter the object must be.

Theyíve become so sensitive visually to how their bodies react, they can detect differences of as little as 10 percent of the weight of an object (a 90-gram object from a 100-gram object), find Cole and Bard. However, with their eyes shut, they can only tell dramatic differences in weight, 200-gram object from a 400-gram object, for example. This work is published in Brain (Vol. 118, p. 1149?1156).

By studying Waterman and the others, researchers are able to tease apart the actions that require feedback from the outside world and those that donít.

'Weíre able to look at the brainís motor signals, uncontaminated by feedback,' says Bard, a professor in the department of social and preventative medicine at the Universitť Laval in Quťbec, who collaborates with Normand Teasdale, Michelle Fleury and Lizotte's physician, neuroscience researcher Yves Lamarre.

A striking example of this came when Bard and her colleagues tested Lizotte's ability to perform the 'mirror drawing taskí, she had to draw a star while looking in a mirror rather than at the paper. Normally, it takes people more than seven tries to draw a decent star.

But Lizotte had no problem on her first try, says University of Marsailles researcher Jacques Paillard, PhD, who worked with Bard on the study, which is published in Neurology (Vol. 42, p. 1104?1106).

People normally have trouble with the task because 'we see what we are doing but behind [the visual cues] is a signal from the muscular senses that gets in our way,' says Paillard. For Lizotte that distraction is missing.

Moving without feedback

Lizotte and Waterman have learned to rely on vision for all of their controlled movements. Vision is their only source of feedback so when they are not looking at their bodies, they donít move much, unlike the rest of us who tend to unconsciously fidget and move all the time, says Paillard.

Cole and his colleagues have preliminary data from a brain-imaging study of Waterman. As expected, they find that the frontal cortex, which controls visual attention, is active when heís both making and seeing a simple finger movement. This area isnít active in normal people because the movement is automatic, says Cole.

Research on how people like Waterman move when they canít see their bodies provides researchers with a view of how the brain controls movement with no feedback at all, says Bard. A couple of years ago, she and her co-workers and Cole tested Watermanís and Lizotteís ability to point at a target flashed on the wall, without being able to see their arms.

The task was to rest an arm on a tabletop and sweep it left or right to point at the target. Even with no feedback about whether or where they moved their arms, they accomplished the task reasonably well.

However, if unbeknownst to Waterman or Lizotte, the researchers blocked an arm movement to the left from straight ahead, and the next target flashed straight ahead, Waterman and Lizotte would inappropriately move their arms to the right.

This finding disputes theories that the brain plans movements around an equilibrium point that represents the actual position of the arm. Instead, it supports the theory that the brain calculates an angle of movement and moves that far from wherever the limb is, says Bard. She and her colleagues published their findings in Experimental Brain Research (Vol. 109, p. 473?482).

Automatic gestures

The University of Chicagoís David McNeill worked with Waterman and Cole recently to test one of his theories about gestures, the hand movements that accompany speech. He contends that gestures are a part of speech and are therefore controlled by a different mechanism than more intentional movements.

McNeill sought to study Waterman because he seems to control his gestures more smoothly than his other movements. A video of Waterman shows that his gestures appear completely normal, even in slow motion. In contrast, when Waterman makes an intentional movement, such as putting a hand on a chairís arm, he performs the task in several calculated steps that he controls cognitively using visual feedback.

In a series of experiments to test whether Watermanís gestures can be controlled via the meanings of his speech, McNeill and his colleagues asked him to narrate a story using gestures, once while looking at his hands and again without being able to see his hands. Although the gestures were smaller when he couldnít see his hands, they were almost as frequent and as well synchronized with his words as when he could see his hands, the researchers found.

In another experiment, McNeill and the others asked Waterman to describe the route he took to reach the laboratory. This time they tracked his eye movements and found that he often made gestures when his gaze prohibited him from viewing his hands except with extreme peripheral vision. This time, the gestures were no smaller than in the story condition when he watched his hands.

At some level, the gestures are conscious. Waterman can decide whether or not to use them, and he says he consciously learned to synchronize speech with gesture and still has to think about it. But the evidence from McNeillís lab indicates that at another level, Watermanís gestures are produced as an integral part of the process of speaking. This enables him to perform gestures normally, says McNeill.

'Waterman says that he wills his gestures, but I donít believe that he can consciously synchronize his gesture strokes with speech in the precise and completely normal way that he does, 'says McNeill, who, with Cole and others, plans to present his findings at a meeting in France this winter.

Instead, McNeill believes that Waterman likely decides to present an idea in the form of both a word and a gesture, then the brain takes over and synchronizes the two.

The brainís back-up system?

The research on Waterman and others demonstrate how resilient the human body is, says Cole. While the cases highlight how critical touch and proprioception are to normal movement, they also demonstrate the brainís remarkable ability to utilize back-up systems.

'Ian has allowed us to look at motor programming in a way we couldnít do otherwise,' says Cole.

He and Waterman are in high demand by researchers interested in studying touch and proprioception. Even NASA has been interested in how Waterman uses his fingers because his solutions to dexterity problems are similar to the ones they use to develop and program robotic limbs.

He also may provide insight in why some astronauts have short-term problems of stability and movement on their return to Earth from space. Next January, Waterman will take a ride on NASA's 'vomit comet' zero-gravity flight trainer to see how his body reacts to microgravity.

'I have no idea how I will react,' says Waterman. 'It will be another interesting challenge for me and the researchers.'

Research participant and collaborator?

Since his first job as a butcherís apprentice in the early 1970s, Ian Waterman has taken work very seriously, always striving to do the best he could.

After he was struck down with a viral infection that destroyed his ability to feel anything below the neck (see main article), he could barely move, let alone return to butchering. But, as neurologist Jonathan Cole, MD, describes in his book on Waterman, 'Pride and a Daily Marathon' (MIT Press, 1995), Watermanís pride in his work never waned. He poured his diligence into teaching himself how to move without feedback from the outside world.

After recovering his ability to move about, Waterman worked for years in a health statistics office, insisting on pulling his own weight without special treatment for his disability. He also met Cole, who has engaged him as a subject of scientific research. He tries to limit the research work to about two weeks a year.

'It doesnít pay the bills, you know,' says Waterman, who most recently began consulting for companies wanting to comply with the British version of the Americans with Disabilities Act. He has a contract with a hotel chain and several cinemas to evaluate how they can better serve people with disabilities.

He isnít much interested in the science of his disability, but works hard when in the lab. He tries to forewarn researchers if he notices problems with their experimental design. Certain 'tricks' that heís learned to compensate for his disability may get in the way of the best-planned study, heís found.

For example, in one experiment, Cole and his colleagues were testing how well Waterman could point his arm toward a moving visual target. They immobilized his head so he could only use his eyes to track the target; they blocked his view of his arm; and they placed his arm on a smooth tabletop, forcing him to move it in a two-dimensional arc. Ian took one look at the setup and knew heíd best wear long sleeves and gloves because heís learned to use temperature as a way to tell heís moved a limb.

'I could work out how far I had moved my arm by how long the table felt cool,' he explains. The same went for the sound of his arm moving across the table, so Waterman had to wear headphones. 'I consider Ian a true collaborator,' says Cole. 'We canít always tell him the premise of an experiment before we do it because he might figure out a trick for accomplishing the task. But once weíve conducted a test, I always talk to him and get his perspective on what was happening.'

?Beth Azar

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