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New hand, same brain map

Neural activity of a hand-transplant recipient shows how the brain may reverse its own amputation-related changes

10:53am, October 9, 2008
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David Savage probably never expected to look down and see someone else’s hand attached to his right arm. Neither did he anticipate using the strange appendage to illuminate how the brain works. But that’s precisely what the 56-year-old hand-transplant patient has done.

Four months after his December 2006 transplant, Savage’s partial sense of touch in the new hand activated the same brain area that would have controlled his original right hand 35 years earlier, say neuroscientist Scott Frey of the University of Oregon in Eugene and colleagues.

At the age of 19, a machine-press accident led to the amputation of Savage’s right hand.

When Savage had both hands, part of his right brain responded to his left hand, and a corresponding part of his left brain responded to his right hand. After the amputation, that same part of his left brain would have been sensory-deprived and thus ready to adopt duties of adjacent sensory areas, such as those for the right arm and possibly his face.

Much animal and human research has documented that such neural reorganization begins within hours of limb loss or debilitation.

Yet decades later, with a new hand in place, the former “hand area” of Savage’s brain has reclaimed its old territory, Frey’s team reports in the Oct. 14 Current Biology. “The capacity of the brain to reverse reorganizational changes is all the more striking in light of the fact that his brain was fully mature when the amputation occurred,” Frey says.

Although the researchers have no data about Savage’s brain from just before or just after the amputation, sensory areas responsible for his missing right hand must have assumed new duties, remarks neuroscientist Jon Kaas of VanderbiltUniversity in Nashville. At a minimum, the neural map for Savage’s right hand would have begun to respond to stimulation of parts of his right arm, Kaas suggests.

Kaas has studied the lifelong ability of monkeys’ brains to reorganize sensory areas following the loss of sight, hearing or limb sensation.

“It’s remarkable that an original neural pathway for the hand can be reinstated after years and years,” Kaas says.

No consensus exists on how the brain rapidly reorganizes sensory maps following hand amputation and then reverses course after surgical attachment of a new hand, comments neurologist Carine Neugroschl of H´pital Erasme in Brussels, Belgium. In a 2005 brain-imaging study of a hand-transplant patient before and after surgery, Neugroschl’s team reported reactivation of the corresponding neural hand map as early as ten days after the operation.

In the new investigation, functional MRI recorded Savage’s brain activity while each of his of his hands, along with each of his cheeks, was stroked with a coarse sponge.. The same experiment was carried out on four healthy men who had never experienced an amputation. Savage reported full left-hand and full facial sensation, as well as sensation in his right palm near the thumb. During right-hand testing, Savage displayed much the same left-brain activation that the other men did.

Savage’s recovery so far is limited to major nerves in the right hand, not to peripheral nerve connections for individual fingers, Frey says. It’s unclear how the neural map of the right hand will adapt as Savage’s finger nerves regenerate and finger sensation develops.

Stroking of Savage’s cheeks yielded no signs that neural areas responsive to his transplanted hand also responded to facial stimulation. That is further evidence that his brain responded to the new hand as it had to the old one, Frey says.

Unlike some amputees, Savage suffered few pains at the site of his missing hand. Pain from a phantom limb typically accompanies major neural reorganization after amputation, notes neuroscientist Thomas Elbert of the University of Konstanz in Germany. “Neural reorganization in this patient before the hand transplant might have been quite small,” Elbert says.

Frey’s team speculates that the right-brain map for Savage’s intact left hand responded to his amputation by increasing communication with left-brain sensory tissue. Stroking of Savage’s left hand activated not only corresponding right-brain tissue but also left-brain sensory areas largely outside the region associated with his right hand.

Men in the comparison group displayed minimal left-brain responses to stimulation of the left hand.

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