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VOLUME 29 , NUMBER
6 -June 1998 Why can’t this man feel whether or not he’s
standing up?
One man’s 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 it’s there. Waterman’s
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. He’s
lost all feeling below the neck and is unable to tell without looking how his
body is positioned. That was 1972 and even Waterman’s
doctors had a hard time understanding the extent of his disability. Through trial and error
over three years, Waterman, who lives in 'How can one explain a
total loss of proprioception?" a sense most people don’t 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 Now, many researchers,
including psychologists, are fascinated not only by Waterman’s 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 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 Waterman’s
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, it’s often hard to tell there’s
anything wrong unless something unexpected happens and he’s thrown off
balance, say those who have met him. Two other cases, a man
in 'We choose our own
paths,' says Waterman. 'Lizotte chose the path to stay in a wheelchair. Was
what I chose better? I don’t know. Sometimes I wonder. It’s 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 wouldn’t have predicted it,
says Chantal Bard, PhD, who studies Lizotte and has collaborated with Cole.
The patients represent a window into what’s 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. They’ve 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 don’t. 'We’re able to look at
the brain’s motor signals, uncontaminated by feedback,' says Bard, a
professor in the department of social and preventative medicine at the
Université Laval in Québec, 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 task’, 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 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 don’t 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 he’s both making and seeing a simple finger movement. This area isn’t
active in normal people because the movement is automatic, says Cole. Research on how people
like Waterman move when they can’t 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 Waterman’s and Lizotte’s
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 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 chair’s arm, he performs
the task in several calculated steps that he controls cognitively using
visual feedback. In a series of
experiments to test whether Waterman’s 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 couldn’t
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 McNeill’s lab indicates that at
another level, Waterman’s 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 don’t 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 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 brain’s 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 brain’s remarkable ability to utilize
back-up systems. 'Ian has allowed us to
look at motor programming in a way we couldn’t 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 butcher’s 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), Waterman’s 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 doesn’t 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 isn’t 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 he’s learned to compensate for his
disability may get in the way of the best-planned study, he’s 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 he’d best wear
long sleeves and gloves because he’s learned to use temperature as a way to
tell he’s 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 can’t
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 we’ve conducted a
test, I always talk to him and get his perspective on what was happening.' ?Beth Azar |
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