If someone told you that they wanted to have a perfectly good leg amputated, or that they have three arms, when they clearly do not, you would probably be inclined to think that they are mentally disturbed. Psychiatrists, too, considered such conditions to be psychological in origin. Voluntary amputation, for example, was regarded as a fetish, perhaps arising because an amputee's stump resembles a phallus, whereas imaginary extra limbs were likely to be dismissed as the products of delusions or hallucinations.

However, these bizarre conditions - named body integrity identity disorder (BIID) and supernumerary phantom limb, respectively - are now widely believed to have a neurological basis. Two forthcoming studies confirm this, by providing strong evidence that both conditions occur as a result of abnormal activity in a part of the brain which is known to be involved in constructing a mental representation of the body, or body image.

In BIID, or apotemnophilia, individuals express a strong desire to have a healthy limb amputated at a very specific location. People with this condition usually describe the affected limb as being "intrusive" or "over-present", and report that they have had the desire to remove since early childhood, but do not understand why. This desire can be so strong that sufferers sometimes resort to damaging the affecting limb irreparably, thus forcing doctors to amputate it. The vast majority of BIID sufferers have no other psychological disturbances, and almost always say that they feel much happier when the limb is eventually amputated.

A growing body of literature suggests that body awareness disorders such as BIID occur as a result of abnormal activity in the right parietal lobe, which is known to be essential for constructing a mental representation of the body. Specifically, this body image is constructed in the superior parietal lobule (SPL), which performs a function referred to as multisensory integration, whereby different types of sensory information entering the brain are brought together. Thus, information from the visual parts of the brain and the primary somatosensory cortex, which processes tactile sensations and proprioceptive information relating to the position of the body within space, is sent to the superior parietal lobule. There, it is combined with information from the motor cortex, which controls movement, and all is processed further to generate an internal model of the body. If these processes are perturbed, the body image is compromised.

Paul McGeoch of the Brain and Perceptual Process Laboratory at UCSD and his colleagues therefore postulated that the desire to have an otherwise healthy limb amputated occurs as a result of abnormal activity in the right superior parietal lobule, and recruited four male BIID sufferers (or apotemnophiles) from internet support groups to test their hypothesis. Three of these expressed a desire to have their left leg amputated, while the fourth wanted both legs removed. For their study, the researchers simply tapped the participants' feet with a bundle of fibre-optic filaments, and at the same time, recorded the electrical activity of their brains using magnetoencephalography (MEG). Their responses to the tactile stimulation were compared to those of four controls.

In all four controls, tapping either foot caused an almost instantaneous activation of the right SPL. In the three apotemnophiles who wanted one leg amputated, tapping the unaffected foot evoked a response in the right SPL, but tapping the affected one did not, and in the fourth apotemnophile, who sought amputation of both legs, neither foot evoked a response. These findings confirm the researchers' hypothesis that BIID arises as a result of abnormal function in the right parietal lobe. The brain does not register the limb as a part of the body, and contains no representation of it, so it is not incorporated into the body image. As a result, the apotemnophile has no sense of ownership over the limb, and feels strongly that it does not "belong" to him. It feels extraneous or redundant, so he wishes to have it removed.

FreeSurfer reconstructions of the right hemisphere of one control (a, b) and one apotemnophile (c, d), viewed from the top. In the control, touch to both feet causes an increase in SPL activity (outlined in black). In the apotemnophile subject A.O., touch to the unaffected foot evokes a response in the SPL (c), but touch to the affected foot does not (d) (From McGeoch et al, 2009)





Supernumerary phantom limb is a much rarer condition, in which the patient experiences the presence of an extra limb, usually following a stroke. Mostly this feels much the same as the phantom limbs of amputees - an illusion, from which sensations sometimes emanate. But in a small number of cases the patient reports that they can also see the limb, and some even say that they can feel and use it. This phenomenon of "multimodal" extra phantom limb has not been investigated thoroughly, because there are so few reported cases. Now though, a team of clinical neuropsychologists from the Geneva University Hospitals describe what they believe to be the second documented case of such a patient.

The researchers report the case a 64 year-old librarian who was admitted to hospital following a subcortical haemorrhage. Four days after being hospitalized, the patient began to experience a supernumerary phantom limb, and spontaneously reported it to her physicians. This phantom, she said, started from the elbow of her left arm (which had been paralyzed by the stroke). It felt "just like a real hand", but was "weightless", "transparent" and "thinner" than her actual arms. The patient also told the doctors that the phantom was not experienced permanently, but only when she intentionally "triggered" it. Furthermore, it was anatomically correct and functional - she said that it had flexible joints at the elbow wrist and fingers, all of which she could move independently, and claimed that she could not only see it, but also feel it and purposefully move it. The patient was of perfectly sound mind, but could not explain her condition and so was co-operative.

The doctors placed her into a brain scanner, and asked her to scratch her cheek with her phantom limb. Remarkably, the scan confirmed the patient's subjective reports of her experience. When she willed the phantom limb into action, the doctors observed an increase in the activity of the right motor cortex; when she said that the phantom was approaching her face, they observed an increase in visual cortical activity; and when she told them that the limb had made contact, they observed increased activity in the region of somatosensory cortex corresponding to the cheek. The patient's brain had generated a virtual simulation of a fully functional arm, which had been incorporated into the body image and which ran alongside the neural representations of her real arms. In her mind, this virtual arm was just as real as her actual arms.

Extraordinary as they are, the findings of both these studies fit perfectly with the current view that the brain constructs a mental representation of the body by integrating different types of sensory information. In both conditions, the body image is grossly distorted, and this distortion has bizarre consequences. In the case of supernumerary phantom limb, the distortion is obviously acquired - it occurs as the result of a stroke. The parts of the brain which relay body image-related sensory information to the SPL have been starved of oxygen. Cell death occurs, so the SPL is deprived of some the information it normally processes. This perturbs SPL function, and so distorts the body image. In this case, the brain's representation of the left arm has been duplicated, and incorporated into the mental scheme of the body.

In BIID, the situation is apparently reversed: the body image is missing a representation of the affected limb. But the body image distortion seen in BIID is almost certainly congenital. Children born with missing arms or legs sometimes experience phantom limb syndrome, suggesting that there is a representation of the limb in the brain, even though it has never existed. The body image is, therefore, probably "hard wired" during development. The experience of BIID sufferers is consistent with this, as they typically report that they have had the desire to have a limb amputated since early on in their lives. It seems the brains of apotemnophiles fail to generate a representation of the affected limb, because of some aberrant developmental mechanism. The limb has never been a component of the body image, so the afflicted person grows up believing that it feels "wrong", but cannot explain why.

Related:

McGeoch, P.D. et al (2009). Apotemnophilia - the neurological basis of a 'psychological' disorder. Nature Precedings DOI: 10101/npre.2009.2954.1.

Khateb, A., et al (2009). Seeing the phantom: A functional MRI study of a supernumerary phantom limb Ann. Neurol. DOI: 10.1002/ana.21647