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DURHAM, N.C. -- Monkeys that learn to use their brain
signals to control a robotic arm are not just learning to
manipulate an external device, Duke University Medical Center
neurobiologists have found. Rather, their brain structures are
adapting to treat the arm as if it were their own
appendage.

The finding has profound implications both for understanding
the extraordinary adaptability of the primate brain and for the
potential clinical success of brain-operated devices to give
the handicapped the ability to control their environment, said
the researchers.

Led by neurobiologist Miguel Nicolelis of Duke's Center for
Neuroengineering, the researchers published their findings in
the May 11, 2005, issue of the Journal of Neuroscience. Lead
author on the paper was Mikhail Lebedev in Nicolelis's
laboratory. Other coauthors were Jose Carmena, Joseph
O'Doherty, Miriam Zacksenhouse, Craig Henriquez and Jose
Principe. The work was supported by the Defense Advanced
Research Projects Agency, the James S. McDonnel Foundation, the
National Institutes of Health, the National Science Foundation
and the Christopher Reeve Paralysis Foundation.

In the study, Lebedev performed detailed analysis of the
mass of neural data that emerged from experiments reported in
2003, in which the researchers discovered for the first time
that monkeys were able to control a robot arm with only their
brain signals.

In those experiments, the researchers first implanted an
array of microelectrodes -- each thinner than a human hair --
into the frontal and parietal lobes of the brains of two female
rhesus macaque monkeys. The faint signals from the electrode
arrays were detected and analyzed by the computer system the
researchers developed to recognize patterns of signals that
represented particular movements by an animal's arm.

In the initial behavioral experiments, the researchers
recorded and analyzed the output signals from the monkeys'
brains as the animals were taught to use a joystick to both
position a cursor over a target on a video screen and to grasp
the joystick with a specified force.

After the animals' initial training, however, the
researchers made the cursor more than a simple display. They
incorporated into its movement the dynamics, such as inertia
and momentum, of a robot arm functioning in another room. While
the animals' performance initially declined when the robot arm
was included in the feedback loop, they quickly learned to
allow for these dynamics and became proficient in manipulating
the robot-reflecting cursor, found the scientists.

The scientists next removed the joystick, after which the
monkeys continued to move their arms in mid-air to manipulate
and "grab" the cursor, thus controlling the robot arm. However,
after a few days, the monkeys realized that they did not need
to move their own arms. Their arm muscles went completely
quiet, they kept the arm at their side, and they controlled the
robot using only their brain and visual feedback.

"After these experiments, a major question remained about
how the animals' brains adapted to the transition between
joystick and brain control," said Nicolelis. "Thus, drawing on
the extensive data from these experiments Mikhail analyzed very
carefully what happens functionally to the brain cells and the
brain cell ensembles in multiple brain areas during this
transition.

"And basically we were able to show clearly that a large
percentage of the neurons become more 'entrained' -- that is,
their firing becomes more correlated to the operation of the
robot arm than to the animal's own arm."

According to Nicolelis, the analysis revealed that, while
the animals were still able to use their own arms, some brain
cells formerly used for that control shifted to control of the
robotic arm.

"Mikhail's analysis of the brain signals associated with use
of the robotic and animals' actual arms revealed that the
animal was simultaneously doing one thing with its own arm and
something else with the robotic arm," he said. "So, our
hypothesis is that the adaptation of brain structures allows
the expansion of capability to use an artificial appendage with
no loss of function, because the animal can flip back and forth
between using the two. Depending on the goal, the animal could
use its own arm or the robotic arm, and in some cases both.

"This finding supports our theory that the brain has
extraordinary abilities to adapt to incorporate artificial
tools, whether directly controlled by the brain or through the
appendages" said Nicolelis. "Our brain representations of the
body are adaptable enough to incorporate any tools that we
create to interact with the environment. This may include a
robot appendage, but it may also include using a computer
keyboard or a tennis racket. In any such case, the properties
of this tool become incorporated into our neuronal 'space'," he
said. According to Nicolelis, such a theory of brain
adaptability has been controversial.

"Few researchers have been willing to go as far as
postulating such extraordinary adaptability for the brain and
how important this adaptability of brain circuitry is in
enabling us to learn to use tools," he said. "It has long been
appreciated that adaptability is a key capability of the
prefrontal cortex that is a hallmark of the human brain. It
gives us the ability to design, create, and use tools to do
everything from lift massive weights to make microscopic
manipulations.

"What Mikhail, I and our colleagues are suggesting is that a
fundamental trait of higher primates, in particular apes and
humans, is the ability to incorporate these tools into the very
structure of the brain. In fact, we're saying that it's not
only the brain that is adaptable; it's the whole concept of
self. And this concept of self extends to our tools. Everything
from cars to clothing that we use in our lives becomes
incorporated into our sense of self. So, our species is capable
of 'evolving' the perception of what we are.

"From a philosophical point of view, we're saying that the
sense of self is not limited to our capability for
introspection, our sense of our body limits, and to the
experiences we've accumulated," Nicolelis said. "It really
incorporates every external device that we use to deal with the
environment." The findings also have important clinical
significance, said Nicolelis.

"The experiments we have conducted not only represent a
proof of concept that such an external device can be directly
controlled in a clinical setting," he said. "This latest
analysis shows that the device is incorporated very intimately
as a natural extension of the brain. This is a fundamentally
important property if brain-machine interface technology is to
have any clinical future. If the brain was essentially static,
then paralyzed people would never be able to adapt to operate
external devices with enough dexterity to make them really
useful."

Importantly, said Nicolelis, truly useful "neuroprosthetic"
devices will have to be dexterous enough to give patients a
full range of mobility in robot arms, hands or other
appendages. "Our studies show that it will not be enough to
implant a few electrodes, measure a few signals and attain
sufficient capability for useful devices," he said. "The
ability to merely move a cursor on a screen or open or close an
artificial hand is not enough to justify the use of such
systems." Rather, he said, the objective in his laboratory is
to develop devices that offer paralyzed people fully functional
artificial appendages.

For example, he said, new experiments in his laboratory seek
to enable the brain to perceive a feedback sensation from
neuroprosthetic devices. Such feedback might be in the form of
visual information on the effects of moving a robotic arm. Or,
it might be tactile feedback fed as signals into electrodes
implanted in the brain.

Such feedback would greatly enhance people's ability to
learn and use the devices, said Nicolelis. Also, such feedback
would expand use of neuroprosthetics to amputees, because the
devices would include all the features -- including feedback --
of real appendages.

"In our new experiments, the idea is that by using vision
and touch, we're actually going to create inside the brains of
these animal a vivid perceptual image of what it is to have a
third arm," he said.