How does one explain this strange disorder in terms of the known anatomy? As we saw in Chapter 1, nerves for touch, muscle, tendon, and joint sensation project to your primary (S1) and secondary (S2) somatosensory cortices in and just behind the postcentral gyrus. Each of these areas of the cortex contains a systematic, topographically organized map of bodily sensations. From there, somatosensory information gets sent to your superior parietal lobule (SPL), where it gets combined with balance information from your inner ear and visual feedback about the limbs’ positions. Together these inputs construct your body image: a unified, real-time representation of your physical self. This representation of the body in the SPL (and probably its connections with the posterior insula) is partly innate. We know this because some patients with arms missing from birth experience vivid phantom arms, implying the existence of scaffolding that is hardwired by genes.6 It doesn’t require a leap of faith to suggest that this multisensory body image is organized topographically in the SPL the same way it is in S1 and S2.
If a particular body part such as an arm or a leg failed to be represented in this hardwired scaffolding of your body image, the result could conceivably be a sense of strangeness or possibly revulsion toward it. But why? Why is the patient not merely indifferent to the limb? After all, patients with nerve damage to the arm resulting in a complete loss of sensation don’t say they want their arm removed.
The answer to this question lies in the key concept of mismatch aversion, which as you will see plays a crucial role in many forms of mental illness. The general idea is that lack of coherence, or mismatch, between the outputs of brain modules can create alienation, discomfort, delusion, or paranoia. The brain abhors internal anomalies—such as the mismatch between emotion and identification in Capgras syndrome—and will often go to absurd lengths to deny them or explain them away. (I emphasize “internal” because generally speaking, the brain is more tolerant of anomalies in the external world. It may even enjoy them: Some people love the thrill of solving baffling mysteries.) It isn’t clear where the internal mismatch is detected to create unpleasantness. I suggest it’s done by the insula (especially the insula in the right hemisphere), a small patch of tissue which receives signals from S2 and sends outputs to the amygdala, which in turn sends sympathetic arousal signals down to the rest of the body.
In the case of nerve damage, the input to S1 and S2 itself is lost, so there is no mismatch or discrepancy between S2 and the multisensory body image in the SPL. In apotemnophilia, by contrast, there is normal sensory input from the limb to the body maps in S1 and S2, but there is no “place” for the limb signals to output to in the SPL body image maintained by the SPL.7 The brain does not tolerate this mismatch well, and so this discrepancy is crucial for creating the feelings of “overpresence” and mild aversiveness of the limb, and the accompanying desire for amputation. This explanation of apotemnophilia would account for the heightened GSR and also the essentially ineffable and paradoxical nature of the experience: part of the body and not part of the body at the same time.
Consistent with this overall framework I have noticed that merely having the patient look at his affected limb through a minifying lens to optically shrink it makes the limb feel far less unpleasant, presumably by reducing the mismatch. Placebo-controlled experiments are needed to confirm this.
Finally, my lab conducted a brain-scanning study on four patients with apotemnophilia and compared the results with four normal control subjects. In the controls, touching any part of the body activated right SPL. In all four patients, touching the part of the limb each one wanted removed evoked no activity in the SPL—the brain’s map of the body didn’t light up, so to speak, on the scans. But touching the unaffected limb did. If we can replicate this finding with a larger number of patients, our theory will be well supported.
One curious aspect of apotemnophilia that is unexplained by our model is the associated sexual inclinations in some subjects: desire for intimacy with another amputee. These sexual overtones are probably what misled people to propose a Freudian view of the disorder.
Let me suggest something different. Perhaps one’s sexual “aesthetic preference” for certain body morphology is dictated in part by the shape of the body image as represented—and hardwired—in the right SPL and possibly insular cortex. This would explain why ostriches prefer ostriches as mates (presumably even when smell cues are eliminated) and why pigs prefer porcine shapes over humans.
Expanding on this, I suggest that there is a genetically specified mechanism that allows a template of one’s body image (in the SPL) to become transcribed into limbic circuitry, thereby determining aesthetic visual preference. If this idea is right, then someone whose body image was congenitally armless or legless would be attracted to people missing the same limb. Consistent with this view, people who wish to have their leg amputated are almost always attracted to leg amputees, not arm amputees.
SOMATOPARAPHRENIA: DOCTOR, THIS IS MY MOTHER’S ARM
Distortion of body-part ownership also occurs in one of the strangest syndromes in neurology, which has the tongue-twisting name “somatoparaphrenia.” Patients with a left-hemisphere stroke have damage to the band of fibers issuing from the cortex down into the spinal cord. Because the left side of the brain controls the right side of the body (and vice versa), this leaves the right side of their bodies paralyzed. They complain about their paralysis, asking the doctor whether the arm will ever recover, and not surprisingly they are often depressed.
When the stroke is in the right hemisphere, the paralysis is on the left. The majority of such patients are troubled by the paralysis as expected, but a small minority deny the paralysis (anosognosia), and an even smaller subset actually deny ownership of the left arm, ascribing it to the examining physician or to a spouse, sibling, or parent. (Why a particular person is chosen isn’t clear, but it reminds me of the manner in which the Capgras delusion often also involves a specific individual.)
In this subset of patients there is usually damage to the body maps in S1 and S2. In addition to this, the stroke has destroyed the corresponding body-image representation in the right SPL, which would ordinarily receive input from S1 and S2. Sometimes there is also additional damage to the right insula—which receives input the directly from S2 and also contributes to the construction of the person’s body image. The net result of this combination of lesions—S1, S2, SPL, and insula—is a complete sense of disownership of the arm. The ensuing tendency to ascribe it to someone else may be a desperate, unconscious attempt to explain the alienation of the arm (shades of Freudian “projection” here).
Why is somatoparaphrenia only seen when the right parietal is damaged but not when the left one is? To understand this we have to invoke the idea of division of labor between the two hemispheres (hemispheric specialization), a topic I will consider in some detail later in this chapter. Rudiments of such specialization probably exist even in the great apes, but in humans it is much more pronounced and may be yet another factor contributing to our uniqueness.