Brain immediately recognizes transplanted hand

When David Savage was 19 years old, his right hand was crushed in a metal-stamping machine and subsequently amputated at the wrist by doctors. Afterwards, Savage was fitted with a mechanical cable-hook prosthesis, which he wore until December, 2006, when he became the third American recipient of a hand transplant from a cadaver donor (above).

Amputation of a limb leads to significant reorganization of the primary somatosensory cortex, that part of the brain which processes touch- and pain-related information. The cortical region normally devoted to the amputated body part is suddenly deprived of sensory inputs, but because the adult brain is plastic, it does not lay dormant - the area assumes other functions, and begins to process sensory information from other parts of the body.

One consequence of this functional reorganization is phantom limb syndrome, which Savage experienced for a short time following removal of his hand. This is thought to occur because although the deprived somatosensory cortical region takes on another function, it somehow retains a representation of the amputated limb. As a result, the amputee will occasionally experience sensations, sometimes painful ones, which are perceived to be in the missing body part.

In Savage's case, it was thought that these changes may be irreversible, because his brain had been deprived of inputs from the right hand for some 35 years. But a team of neuroscientists led by Scott Frey of the University of Oregon now show that this is not the case. In a functional neuroimaging study published today in Current Biology, they report that Savage's somatosensory cortex has been restored to something like its pre-amputation state, with the transplanted hand "recapturing" the cortical area which represented his own right hand.

The vast majority of the somatosensory cortex is devoted to processing information from the face and hands, because these are the most sensitive parts of the body. The face is represented by a large strip of cortex located behind the ears; immediately above this is another large area which represents the hand. Following amputation of a hand, the deprived somatosensory cortical area often adopts the function of the adjacent area and begins to process sensory information from the face. In someone whose hand has been amputated, stimulation of a part of the face may sometimes lead to a phantom sensation.

The researchers therefore expected that the cortical representation of the face in Savage's brain would encroach significantly upon the hand area. Surprisingly though, the fMRI results showed otherwise. When the palm of Savage's transplanted rigth hand was mechanically stimulated by stroking with a coarse sponge, a robust response was observed in the hand area of the left somatosensory cortex (above left). This response was comparable to that observed in four male non-amputee controls (above right). Stimulation of Savage's right check, however, evoked no response in the hand area. 

This study shows that the reorganizational changes which occur following amputation are reversible. 35 years after Savage lost his hand, the organization of his somatosensory cortex returned to a state that is indistinguishable from what would have been expected in before the amputation, even though the functional reorganization would have increased with time. Furthermore, the re-reorganization observed by Frey's team happened remarkably quickly - the functional neuroimaging was performed only 4 months after the hand transplant procedure.

When the tests were carried out, Savage had only regained partial sensitivity in his transplanted hand, at the base of the thumb. This suggests that the recapture of the somatosensory hand region by the grafted hand occurs before increased sensitivity in the grafted hand. The study did not determine the extent to which individual digits of Savage's new hand were represented. Studies in adult monkeys suggest that hand transplantation disrupts digit representation, because the topography of the median nerve, which innervates the hand and branches just after the elbow, is lost during transection and repair. Thus the researchers are now testing their prediction that the cortical representation of digits in Savage's somatosensory cortex remain disordered.

Because the researchers did not test Savage before his hand transplant, they cannot rule out the possibility that the representation of the face did not intrude upon the area devoted to the amputated hand. They note that somatosensory reorganization seems to be mroe pronounced in amputees who experience significant phantom pain, and that Savage suffered from this only a little. Nonetheless, the findings should help provide a better understanding of the brain's response to amputation, and could be of benefit to those developing advanced prosthetic limbs.

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Frey, S. et al (2008). Chronically deafferented sensory cortex recovers a grossly typical organization after allogenic hand transplantation Curr. Biol. 18: 1530-1534. DOI: 10.1016/j.cub.2008.08.051