The body imaginary

New research on tool-using monkeys has revealed that they have a surprising awareness of body image. Laura Spinney explores the implications for our understanding of how human consciousness evolved

Imagine flying a kite, walking on stilts, or eating with a knife and fork. Easy, isn't it? We can do that because the human brain is able to perform imaginary gymnastics with a mental image of the body. This so-called body image is sophisticated and malleable, and can be twisted and rotated in the three dimensions of space. We need it to do many of the things that we humans do, such as playing football, driving a car or eating with chopsticks.

But for a person to be really good at playing football or eating with chopsticks, the brain has to incorporate the ball or the chopsticks into its body image. The difference between a first-time user of chopsticks and an expert is that in the expert's mental self-representation, the chopsticks are treated as an extension of the arm.

The recent discovery that a female New Caledonian crow called Betty can both make and manipulate a simple tool made from garden wire to get at its food suggests that this idea of a mental body image may not be unique to humans. And it's not just Betty. Research on chimpanzees also suggests that the concept of body image may also exist to some extent among other animals.

Human consciousness is intimately linked with the idea of body image. Without this "silent sense" we would be unable to function. Yet, because it is always with us we don't really notice it until it disappears. This happens in weird and devastating impairments such as an amputee's sensation of a "phantom limb" – the feeling that the missing leg is still there. Or the case described by the neurologist Oliver Sacks in which a man complained that his own leg was the leg of a corpse that some prankster had put in his bed.

When it is working properly, the body image shows an extraordinary fluidity, adapting to the smallest physical demand while allowing the individual to continue to differentiate himself from the external world. "Even subtle changes, like an injury that weakens one muscle of the arm, will throw off the calibration and require the system to re-adjust," says Michael Graziano, a neuropsychologist at Princeton University in New Jersey. "Thus, the system retains a high degree of plasticity throughout life. In a sense, we have no problem using a club with spatial accuracy because the brain treats it like an altered arm," he says.

It is this ability to recognise self even under changing circumstances that scientists believe formed the foundation of symbolic thought, abstract reasoning and, ultimately, language – hence the interest in how and where it is encoded in the brain. And although chimps may possess certain fuzzy elements of it, it was generally regarded as the exclusive domain of humans.

So, when the cognitive neurobiologist Atsushi Iriki, of Tokyo Medical and Dental University in Japan, reported last year that monkeys can also recognise themselves on a video screen and become dextrous users of tools, he caused something of a stir. In a remarkable series of experiments, Iriki and colleagues trained macaques to manipulate a hand-held rake to retrieve pieces of fruit that were placed just out of reach. During the two weeks that it took them to become skilful swipers, the researchers recorded the electrical activity of cells in the parietal cortex – towards the back of the monkeys' brains – through electrodes.

As long ago as 1911, the parietal cortex was implicated as the seat of body image when neurologists Henry Head and Gordon Holmes observed cases of parietal lobe damage in which patients rejected their own body parts, and speculated that the feather in the hat of an Edwardian lady became integrated into her so-called body schema.

Iriki found that the monkey's parietal cortex contains cells that respond to both visual and touch input, and he suggests that these neurons 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 – 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 rake.

In other words, those neurons were firing in response to the sight of the rake in the same way that they would to the monkey's own hand. Yet, intriguingly, when there was no fruit reward, and the monkeys were allowed to play with the rake as a toy rather than as a tool, the receptive fields showed no such adaptation. "This use-dependent expansion occurred only when the monkeys held a tool and intended to use it as an extension of their hand," says Iriki.

The plasticity of the parietal response recorded by the Japanese group fits with findings reported by Graziano two years ago, that neurons in one region of the parietal lobe, area five, encoded not only the position of a monkey's arm while it was covered from view, but also the position of a visible, realistic false arm – although they did not respond to an unrealistic false arm that the monkey could see.

However, says Graziano, the fact that a monkey can cleverly manipulate a rake does not on its own imply that the monkey has a sense of self or that the tool is integrated into it. The animal could just be learning that a certain action brings a desired response – a form of association that even very simple organisms are capable of. He points out that many groups before Iriki's have succeeded in training monkeys to move a cursor on a computer screen.

One such example was described in Nature magazine last March by Mijail Serruya of Brown University, Rhode Island, and colleagues, who devised an algorithm that translates the activity of a monkey's motor neurons, which control movement, into a signal that allows the animal to control a cursor just as quickly and accurately as if it were controlling it with its own hands – a device they hope to adapt to help paralysed patients to communicate and operate machinery.

Yet Iriki believes that he has strong evidence to suggest that monkeys do have a body image that they can dissociate from their physical beings, mentally rotate and still recognise as self. When he prevented his rake-wielding monkeys from seeing their own hand, and presented them instead with a video image of the hand, rake and fruit reward, he found that they were able to operate just as skilfully. Moreover, 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 of the hand.

In his latest experiments, Iriki has tested the monkeys' brains for levels of different brain chemicals as the animals learn. His analyses showed an increase in a substance called brain-derived neurotrophic factor (BDNF), which promotes neuronal growth, and of the receptor molecules that interact with it. He saw these increases in the monkey's two-week training period, but not once it had acquired the skill.

Iriki says that the macaque's body image matches that of a nine-year-old child. In infancy, a child's sense of his own body is very sketchy, being derived purely from the immediate sensory consequences of his actions. As he grows, so his body image becomes more sophisticated. By the age of nine, says Iriki, a child has a set of visual images of his body that don't need to be supported by actions, and it is this capacity that allows the monkey to manipulate the rake via the video image.

Later in human development, the mental representation becomes "totally free from physical constraints of the actual world to become a symbolic one", he says. And the emergence of this symbolic representation in hominid evolution might have marked the precursors of higher cognitive functions – the neural mechanisms of which his work might now help to uncover. "It does look like there are many similarities at a fundamental level between the self-representational capacities of primates – and probably mammals in general – and humans," says Patricia Churchland, chair of philosophy at the University of California, San Diego.

But Iriki's work might also throw light on those bizarre cases of body image gone wrong, says Salvatore Aglioti, a neuropsychologist at the Universities of Rome and Verona. In 1996, Aglioti reported the case of the "lady of the rings" – a woman who, following injury to the right side of her brain including the parietal cortex, denied ownership of the rings on her left hand (as well as the hand itself), though she had no hesitation in claiming them as her own when she saw them on her right hand.

"The studies carried out by Iriki et al may help to get close to the mystery of delusional beliefs, like supernumerary limbs, and feelings of non-belonging, in brain-damaged patients," Aglioti concludes.