The Tell-Tale Brain: A Neuroscientist's Quest for What Makes Us Human

Frankly, I find these psychological explanations unconvincing. The condition usually begins early in life, and it is unlikely that a ten-year-old would desire a giant penis (although an orthodox Freudian wouldn’t rule it out). Moreover, the subject can point to the specific line—say, two centimeters above the elbow—along which she desires amputation. It isn’t simply a vague desire to eliminate a limb, as one would expect from a psychodynamic account. Nor can it be a desire to attract attention, for if that were the case, why be so particular about where the cut should be made? Finally, the subject usually has no other psychological issues of any consequence.

There are also two other observations I made of these patients that strongly suggest a neurological origin for the condition. First, in more than two-thirds of cases the left limb is involved. This disproportionate involvement of the left arm reminds me of the decidedly neurological disorder of somatoparaphrenia (described later), in which the patient, who has a right-hemisphere stroke, not only denies the paralysis of his left arm but also insists that the arm doesn’t belong to him. This is rarely seen in those with left-hemisphere strokes. Second, my students Paul McGeoch and David Brang and I have found that touching the limb below the line of the desired amputation produces a big jolt in the patient’s GSR (galvanic skin response), but touching above the line or touching the other limb does not. The patient’s alarm bells really and truly go off when the affected limb is touched below the line. Since it’s hard to fake a GSR, we can be fairly sure of a neurological basis for the disorder.

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.