Brain immediately recognizes transplanted hand

david_savage_hand_transplant.jpg

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.

david_savage_fMRI.bmp


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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ResearchBlogging.org

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

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The title of this topic appears on the main scienceblogs site as: "Brain immediately recognizes transplanted hand, 35 years after amputation "
I was looking forward to reading how they managed to keep his amputated hand alive for 35 years!

Why would cortical changes following amputation be assumed to be irreversible? Is it simply because amputation itself is typically irreversible? Previous amputations would have shown a one-way change in the brain because the amputation was one-way. I would have expected that the cortical reorganization following amputation to be evidence in favor of reversible plasticity! After all, if it can change once, why should it be unable to change twice? Could you give us the rationale for the assumption?

Anon - I think the functional changes were thought to be irreversible because they increase with time, and Savage had his transplant so long after his hand was amputated. Also, limb transplantation has not been possible in the vast majority of amputees, so this is the first such study.

I agree it's no big surprise that the changes are reversible. What I do find remarkable, however, is how quickly the reversal occurred.

Awesome! So I take it that he stopped suffering phantom limb after the original amputation? Also, were they able to get any movement?

Yes, he suffered from phantom limb only minimally. The NPR story (first link) has a photograph of Savage lifting a weight, so I suppose that means his new hand is somewhat functional, although there's no mention of it in the paper.

Mo, i could cut off my hand and have it replaced?

That is pretty impressive. I wonder if it would work on somebody who never developed the necessary brain features (born without a hand, say, then had one transplanted later in life)?

On a slightly different topic, how does this relate to the various new-hotness nerve-connected mechanical prosthetics also being worked on? Would the anti-rejection regimen for a donor hand be nasty and/or ineffective enough to make mechanical stuff worth refining, or would transplants be decisively superior?

Please pardon a very unscientific: Wow! This is just amazing. We are still obviously a very long way from understanding the full capability of the human brain.

Fascinating. I wonder how much of a part conscious awareness of the fact he once again had a hand played, if any. After all they mention the brain area recovered before he even had sensation in the new hand...

I second Karyn's Wow! This just is so fantastic and amazing... didn't I just read of someone getting a full arm?

KAS

phisrow - I heard somewhere (can't remeber where) that a hand transplant reduces life expectancy by about 10 years, so mechanical prosthesis will still be a viable option. If I was in that position, I think I would prefer the prosthesis.

Also, the supply of useable used hands is probably less than the demand.

By Militant Agnostic (not verified) on 21 Oct 2008 #permalink

I'm a newcomer to neurophilosophy--can you say a quick word or two about digit representation? I can't seem to find anything about it, though I may just be searching in all the wrong places.

If you never had a hand, you have no effective phantom (phantom pains are just one sign of a phantom) for it, and so you have no use for a prosthesis, any more than any human being could learn to use a prosthetic prehensile tail.

This is well illustrated by the people who grew up without legs or arms due to their mothers having taken thalidomide: prostheses for them are rarely or never functional.

Actually, children born without limbs can experience phantom pain, suggesting that the higher order mental representation of the body (the "body image") is hard wired.