At birth, an infant has only the sketchiest notion of its own body. Only from moving its arms and legs and sensing the effects on skin, muscle and joints does a baby learn what belongs to itself and what to the external world. By the age of 9, a child's body image is more sophisticated, consisting of a set of visual snapshots that are no longer tied to actions and that allow self-recognition, say in profile on a closed-circuit TV screen.
As we get older, the brain's image of the body becomes totally detached from the physical constraints of the world -- a symbolic representation that allows us to incorporate tools or appendages such as a prosthetic leg.
It's that mature body image that allows Lleyton Hewitt to become skillful with a tennis racket -- he is just a little better than the rest of us at incorporating that racket into his body image, at treating it as an extension of his arm and, hence, at sending the ball exactly where he wants it to go. Similarly, the difference between an expert user of chopsticks and a novice is that the expert's brain treats them as an extension of his arm.
Without this "silent sense" humans would be unable to function in the world. Every time you make a movement, get on and off a bus, climb stairs, this sense is monitoring your movements -- and feeding into the sensory system.
Imagine if you couldn't identify your own hand. If it's not yours, how can you use it? You couldn't type, like I am now, you couldn't scratch your head, open a door or reliably use that hand at all. The loss of this silent sense gives rise to the amputee's sensation of carrying round a phantom limb or the case described by neurologist Oliver Sacks, in which a man complained that his own leg was that of a corpse some prankster had put in his bed.
It's the ability to recognize self even when the body is dramatically altered -- by the loss of a limb, say, or the addition of a false one, that scientists believe formed the foundation of abstract reasoning and language.
The ability is considered to be unique to humans. So when cognitive neurobiologist Atsushi Iriki of Tokyo Medical and Dental University reported otherwise, at the annual meeting of the Organization for Human Brain Mapping in Sendai in June, his claims caused quite a stir. Iriki's latest findings suggest that monkeys can recognize themselves on a video screen and become dexterous users of tools.
Iriki and colleagues trained macaques to manipulate a hand-held rake to retrieve pieces of fruit that were placed just out of their reach. During the two weeks that it took the monkeys to become skillful rakers, the researchers used electrodes to record the electrical activity of cells in their parietal cortex toward the back of the brain.
They found that parietal neurons respond to both visual and touch input, and Iriki suggests that they integrate the two types of information into a coherent body image. Over the course of the training period, the visual receptive fields of these cells -- i.e. the area of external space in which a visual stimulus elicited a response from them -- gradually extended along the length of the rake until they incorporated the entire implement. In other words, the neurons learned to fire in response to the sight of the rake in the same way that they would to the monkey's own hand.
However, the fact that a monkey can learn to manipulate a rake does not by itself imply that it has a sense of self, says neuropsychologist Michael Graziano of Princeton University, New Jersey. The animal could just be learning a simple association between a certain action and a desired response.
Yet Iriki believes he has strong evidence that monkeys do in fact have a body image that they can dissociate from their physical beings, mentally rotate and still recognize as self, i.e. incorporate the rake into a mental body image. When he prevented his rake-wielding monkeys from seeing their own hand and showed them instead a video image of the hand, rake and the fruit reward, he found that they were able to use the rake just as skillfully. What's more, simultaneous recordings from the parietal neurons showed that their receptive fields were now responsive to that part of visual space filled by the video image.
Using a novel technique that he describes as "a sort of biopsy," Iriki has now analyzed the brain chemicals responsible for the plasticity of the receptive field.
The technique involves inserting a needle through the skull of an anesthetized animal and, using a vacuum pump, extracting a couple of cubic millimeters of neurons. The monkeys' health is affected only mildly: Although the tissue is not replaced and the monkeys may initially display some behavioral impairments, they recover almost completely in a matter of weeks.
Iriki found increases in the brain-derived neurotrophic factor (BDNF), which promotes neuronal growth, but only during the monkey's training period, not once it had acquired the skill. The new body image, explained Iriki, with the tool as extension of the arm, is constructed when the trophic factor is secreted. This drives changes in the neural connections between vision-related brain areas and the parietal cortex.
According to Iriki, who's latest work is as yet unpublished, the macaque's body image matches that of a 9-year-old child and can teach us much about how body image develops in humans. But it might also throw light on those bizarre cases of body image gone wrong, according to Salvatore Aglioti, a neuropsychologist at the Universities of Rome and Verona, Italy.
"The entire set of studies carried out by Iriki et al. may help to get close to the mystery of delusional beliefs, like supernumerary limbs and feeling of non-belonging, in brain-damaged patients," says Aglioti.
In 1996, Aglioti and colleagues reported the case of a woman who has since become famous in the neurological literature.
Following injury to the right side of her brain (including the parietal cortex), the woman denied ownership of the rings on her left hand . . . as well as the hand itself.
"Since Iriki found that learning induced the expression of BDNF," said Aglioti, "one important implication for human studies is the theoretical possibility of learning about the substances that can help recovery following neural damage."
