Voluntary amputation and extra phantom limbs

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.

image
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

More like this

Any chance that librarian with the phantom limb was named Hamilton?

Really interesting post, btw!

Very interesting post, thank you. The subject of phantom limbs has intrigued me ever since I read about the phenomenon in V.S. Ramachandran's seminal book Phantoms In The Brain.

I recently saw an old episode of Jerry Springer (I know, I know, it was a moment of madness, what can I say?) and it was rather saddening to see the audience hoot with laughter at an individual who seemed to have a pathological hatred of his legs (below the knee) and exhibited an intense desire to have them amputated. Clearly he was a sufferer of Body Dysmorphic Disorder (BDD, similar to the BIDD you mention).

Another TV program I caught actually featured an pre-amputee (is that the correct term?) who actually met Ramachandran and his team and was treated with the "mirror trick" that Ramachandran discovered. Unfortunately his psychological distress was so intense that, despite the treatment, he ended up having his limb amputated anyway.

It really is an interesting condition deserving of further research.

Hmm... I wonder how this relates to transgendered people. This in combination with some other things might explain the feelings of having the "wrong" body.

If the brain's body-map is being constantly updated with sensory information, but a real limb feels like it doesn't belong, does that suggest there's something wrong with the updating mechanism, as well as the map?

The sensory impressions are experienced - the limb isn't numb or invisible - but the experiences don't "filter through" to the body-map.

Fascinating article, as always.

If cell death destroys the original architectural basis for certain body representations causing BIID, why doesn't cortical reorganisation shift neural correlates of the deleted representations to regions of the brain still intact instead of making a hack job with weird distortions from the remaining cells?

Great post, holmes! I wonder if there is a relationship between these phenomena and the weird feeling you sometimes get when you have a bad fever where your limbs feel like they are much much bigger than they really are?

Rr, the fellow I mentioned on the Jerry Springer show was also a transvestite. So it was pretty easy to see why the audience hooted with laughter at an old man dressed as a very bad drag queen and talking about how badly he wanted his legs cut off. I am personally saddened by such things and I don't think that people like this should be on exhibition, especially on such an inappropriate forum as Jerry Springer.

I agree with you and Mo about underlying neurological reasons for these conditions (BDD, BIID, etc.), they could very well explain these things, if they haven't already done so to some extent.

This is really cool stuff. Thanks for writing about it. Do you know if this type of work has been extended to the more common delusions? Do Schizophrenics' command hallucinations register on their auditory cortex? What about the visual cortices of people tripping on LSD or shrooms?

By Stagyar zil Doggo (not verified) on 28 Mar 2009 #permalink

This is exciting news for those of us who have BIID.

One thing Dr. McGeoch hasn't really explored is the relationship between the "amputee BIID" and the "paraplegic BIID". There are people who have BIID that don't need to be amputees, but rather need to be paraplegic, or to be blind, or deaf.

More studies are definitely required.

You may be interested in BIID-info.org which offers a lot of the current literature on BIID, or transabled.org which is a multi-author blog talking about the experience of living with BIID.

I wonder if a few stem cells in the right place could help the BIID brain to form an image of a limb that is there. Oliver Sacks described a similar feeling in his book A Leg to Stand On . After an injury, one of his legs was paralyzed for a while, and while it was neither receiving nor sending messages, it seemed as foreign and grotesque as a dinner plate mysteriously attached to his body. (I'm paraphrasing--it's been a few years.)

For the phantom limbs, a shot of Botox in the right place might work wonders. But those don't seem to be so upsetting.

It would be interesting to know if transsexualism came from distortions in body image, as it could be dismissed as a stereotyped view of gender-appropriate behavior.

Hi, Answer to Stagyar:

Hallucinations have been demonstrated to correspond to activation to areas of sensory cortex corresponding to the type of hallucination. So, they seem to be generated "from the ground up" at least, in part.

@NeuroWhoa: I have a theory that people with eating disorders suffer from BDD. At least, in extreme cases, sufferers may have an altered perception of their on bodies. But there are probably also psychosocial factors at play.

@Rr: I think the transgender phenomenon is more likely to be hormonal in origin, and related to the sexually dimorphic regions of the brain.

Kapitano: Yes, the patients in the first study do feel tactile stimuli applied to their affected limbs, but that information isn't relayed to the higher order association areas which construct the body image.

ylang: Good question. Synaptic/ neural plasticity is driven by sensory experience, so perhaps this doesn't occur in BIID because the body image generator doesn't receive the required sensory information directly.

PhysioProf: Wow! You actually like a neuroimaging study? The phenomenon you are referring to is macrosomatognosia, or Alice in Wonderland Syndrome. This is a hallucination experienced by a minority of migraine sufferers, during the aura which precedes the headache. I believe it is caused by waves of abnormal electrical activity sweeping across the visual cortex, but it seems perfectly reasonable to think that the SPL is also involved.

Stagyar: As Frank points out, schizophrenics' hallucinations are associated with activity in the corresponding sensory areas. You might like to read this recent post about delusions.

Monado: Neither stem cells nor botox seems plausible; let me think and I'll get back to you.

Frank & Mo: Thanks.
Mo: The link to the delusions post does not work.

By Stagyar zil Doggo (not verified) on 31 Mar 2009 #permalink

Hi,

At the beginning you say the problems where considered to be psychological, but now appear to have a neurological basis. Could you say, in simple terms, what the difference is? As a lay person in this field I'd have thought all 'psychological' problems would have a neurological basis. I was under the impression psychology was pretty much a guessing game waiting for neuroscience to provide more concrete answers, pretty much the way science provides answers for what were once philosophical speculations.

ronmurp: Of course all psychological phenomena are based on brain activity. Here, a psychological condition is one that is not caused by observable brain damage or dysfunction.

Very interesting!

But Ronmurp has a good point. It is important not to confuse the cause with a symptom. Any psychological abnormality is bound to have abnormal activation somewhere down the line! The person has an abnormal body image, so you can pretty much take an abnormality in activation in the body image region for granted. It doesn't demonstrate that the cause is (even partially) genetic, and the current neuroscience establishment has too much of a tendency to jump to that conclusion, which leads to hopelessness on the part of the patient.

Citing patient's beliefs about their childhood experiences is also a misleading argument, as memories are very easily altered (or completely dreamt up) when ruminated upon.

Also, this sort of information does nothing to explain why this abnormality eventually results in such distress and in some cases in amputation efforts. That will almost certainly be the result of years of confusion and attempts to rationalise the situation, and should be treated with CBT, part of which is showing the patient that this is an objective and recognised phenomenon, and they're not 'just going insane'.

Regarding neural plasticity/compensation: your body can mend a broken bone, but it must be directed with a plaster cast. Same with the brain, which organises itself by and large with neuronal-scale local learning rules, not a central director. Stem cells are not going to work if the correct contextual learning processes are not taking place. Maybe instigating those processes is all that's needed? I am convinced that the only way that will happen is through introspective therapies, encouraging feeling whatever related sensation is there, and gradually deepening that. Think of the blind people who train themselves to echolocate, ie 'see' sound. Evidently this occurs by encouraging an abnormal linkage between the auditory system and the parietal spatial system. From the patient's perspective, it simply involves trying to 'feel things out'. Neurophysiological insight will help of course, but I think attempts can be started now.

Hi, Well, I'm a BIID sufferer who had my hand amputated about 4 years ago. I can attest to the feelings of lack of possession of the affected body part and elation when it was finally gone. Moreover, my brain seemed to be perfectly adapted to a one-handed way of doing things immediately after my amputation...as if I had been an amputee from birth.

In spite of the normalcy I feel about losing my hand I realize that I exist in a different reality from the people around me...that it's not "natural" to amputate a perfectly healthy limb...so, I don't expect to ever have understanding for my BIID from the general population. I was asked to appear on a major West Coast radio talk show (with voice disguised), and considered it at length, thinking I might be able to raise awareness of BIID, and maybe do something which could bring a route to safe hospital amputations for sufferers. In the end, I decided it would just be an opportunity for berating the freak, and declined.

I am very concerned though, because BIID brings about an anxiety so great that sufferers become disfunctional, and some, myself included, stage accidents to remove the affected part. Unskillful actions can cause terrible trauma, pain or death, yet hospital surgery is denied because of lack of recognition of BIID as a valid condition.

I find the foregoing unsensational discussion of our condition very heartening, and only hope that amputation can rapidly be accepted as a valid treatment for BIID so that no one else will have to endure the torment and danger that the internal battle between the normal revulsion against self-injury and the overwhelming need to lose a limb brings about.

Peace, Jason

By Jason Bonner (not verified) on 17 May 2009 #permalink

Thank you very much for writing this. I feel a little bit better knowing that I'm not crazy.

I am currently suffering symptoms very similar to the ones you've described. About 5 months ago I had an episode of muscular spasms in my face, which were similar to lockjaw. It only happened once but since then I've been having:

involuntary movements in my limbs (mostly my left arm)
episodes of paralysis on my left side
loss of speech

I also have a persistent feeling that my left arm is somehow foreign to the rest of my body. It feels more present than my other limbs and in my mind it stands out more. If all of my limbs could talk my left arm would be shouting while the other 3 could only whisper.

These feelings make me reluctant to use my left arm because it feels very awkward. I work with computers so typing has become a great struggle.

Just this morning this same feeling has spread to the rest of my left side, from head to toe. I find myself wanting to bandage up or paint the left side of my face because I feel like its wrong somehow. This is very distressing to me and I don't know what to do.

By Martin Riley (not verified) on 13 Oct 2009 #permalink

Absolutely fascinating. My heart goes out to those who suffer from this condition. Thank you, Mo, for an excellent post.

By Catharine (not verified) on 13 Oct 2009 #permalink