A study of artists who paint with their feet shows that these individuals have finely tuned "toe maps" in their brains, where each toe can be linked with an area of brain activity visualized via fMRI. Although humans have well-defined hand maps, this is the first time that similarly robust toe maps have been identified in people. The findings appear September 10 in the journal Cell Reports and raise questions about how the limbs we use every day come to be represented in the brain.
Researchers in the brain plasticity laboratory of Tamar Makin at the Institute of Cognitive Neuroscience, University College London, regularly work with a network of amputee or congenital limbless support groups, limbless musicians, and participants in the Cybathlon (the world's Olympics for robotic prosthetics) to study how the brain adapts to limblessness or changes in limb function. While the group tends to focus mostly on the hand, this research focused on two foot artists who paint with their feet due to being born without arms, to learn more about the mysteries of human toe maps. The artists, Tom Yendell and Peter Longstaff, are two of only three foot artists in United Kingdom. They were born without upper extremities and have developed extreme dexterity with their feet because they use them to perform most daily activities.
"We are interested in the brain area known as the somatosensory cortex because it has incredible organization," says first author Harriett Dempsey-Jones. "Within this brain region, each part of the body is laid out in an organization that roughly approximates what it looks like in the actual human body to form a body map." However, recent research and the availability of high-resolution fMRI has made it clear that the body map is not as organized as previously thought in all body areas.
The researchers knew that handed people do not have toe maps, but non-human primates do. Wondering why humans appear to lack this brain organization, they performed a series of fMRI studies on Yendell and Longstaff and on nine limbed, male volunteers.
While the limbed volunteers were in an fMRI machine, the researchers touched one finger or toe at a time to see what area of the brain was activated. As expected, the fingers of the hand show individual spots of activity right next to each other. But when researchers examined the toes of handed individuals via fMRI using the same methods, they did not show identifiable toe maps. "It turns out that even though we have individual digits on our feet - toes - when we touch each toe in order we do not see a nice organized pattern," says Dempsey-Jones.
The artists, in contrast, both have individualized areas for each of the toes next to each other as they are in the body--that is, they have toe maps. And the maps in the artists are in the same area of the brain and oriented in the same direction as those in non-human primates.
"This was a fun experiment, but it has bigger implications," says study co-author Daan Wesselink (@DaanWess). "It's not important whether it's a hand or a foot but more that we saw what has been thought of as a disorganized area become organized, which opens up questions about organizational principles of the whole body system."
This research suggests many unanswered questions about brain plasticity and why these individuals with extreme toe dexterity have toe maps while others do not. The team points to two different possibilities. Perhaps all primates are born with organized toe maps but they are lost in humans because we do not use our toes or because feet are usually enclosed in shoes. Or perhaps humans are born without toe maps but develop them if we use our bodies in particularly dexterous ways.
"We know there is a critical period of plasticity early in life when the brain seems particularly capable of change," says Wesselink. "It could be that our artists were learning to use their toes when they were children during this time of maximal brain plasticity. We know the adult brain is more fixed once the critical period of plasticity closes. It may be that once that happens you can't really change the brain in a major way, such as this."
The researchers also emphasize that the artists were born without hands. "Perhaps they have a very different brain plasticity history when they were growing up," Wesselink says. "There could be some aspects related to brain changes that dramatically shift because they are born without upper limbs and hands."
Looking ahead, the team will use this information to see if they can incorporate different non-body like technology, such as a robotic prosthesis, into an adult individual's body map. "Whether it's the hand or toe, or any body part, we want to understand more about how the brain copes with these different types of changes," says Dempsey-Jones. "Mapping out finger and toe activity in the brain can help advance brain-machine interface technology where the brain learns how to control each digit of a prosthetic."
This work was supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society, an ERC Starting Grant, and funding by the UK-Israel Science Lectureship Scheme.
Cell Reports, Dempsey-Jones, et al.: "Organized toe maps in extreme foot users." https://www.cell.com/cell-reports/fulltext/S2211-1247(19)31061-7
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