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Brain damage pops woman's personal bubble

Not Exactly Rocket Science
By Ed Yong
Aug 30, 2009 10:00 PMNov 5, 2019 12:13 AM


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We all have a personal bubble, an invisible zone of privacy around our bodies. When strangers cross this boundary, it makes us feel uncomfortable. But not all of us - Daniel Kennedy from the California Institute of Technology has been studying a woman known only as SM, who lacks any sense of personal space.

SM suffers from a rare genetic disorder called Urbach-Wiethe disease, that causes parts of the brain's temporal lobes to harden and waste away. This brain damage has completely destroyed SM's amygdalae, a pair of small, almond-shaped structures that help us to process emotions.

Kennedy asked her to say when she felt most comfortable as a female experimenter walked towards her. On average, she preferred a distance of around a foot, about half the usual two-foot gap that 20 other normal people demanded. SM's lack of boundaries remained whether she walked towards her partner or vice versa, whether they were looking away or at each other, and whether they started close by or far apart.

The fact that SM had a boundary at all was probably because at close distances, it's hard to see people. She said time and time again that she was actually comfortable at any distance, and during one trial, she actually walked all the way to her partner until they were actually touching. Even when they were making direct eye contact and touching nose-to-nose, she only rated the experience as 1 on a comfort scale of 1 to 10, where 1 is perfectly comfortable and 10 is a level of discomfort that only the British can survive. When a male stranger talked to her up close, she again rated the chat as a 1 (even though he gave it a 7).

SM has been working with this group of researchers, led by Ralph Adolphs, for over a decade but her comfort didn't stem from simply knowing her partner well. When Kennedy tested two other people who also knew the scientists equally well, but didn't have damaged amygdalae, they were much less accommodating with their personal space than SM was. Nor did SM simply put her discomfort to heel - she knew that Kennedy was "up to something", but so did the male stranger and that did nothing to allay his discomfort.

In fact, it was clear that SM understood the concept of personal space. She thought it was smaller than most people's, and she said that she didn't want to make other people too uncomfortable by standing too close to them. She estimated that people feel most comfortable about 1.5 feet apart - that's an underestimate but it's still larger than her own preference.

Kennedy's experiments suggest that our sense of personal space comes from the amydgala. Indeed, when he scanned the brains of a small group of volunteers, their amygdalae were more active when someone was standing close to the scanner than when they were keeping their distance.

Kennedy thinks that the amygdala, with its pivotal role in emotional processing, governs the emotional kick we feel when people enter our personal zone. Without it, we remain unfazed by close proximity. What's less clear is how this affect changes as we get to know people better. Why is it that friends and loved ones are allowed (or positively encouraged) to stay nearer than strangers are?

Other aspects of SM's ability to deal with emotions are off-kilter too. For a start, she knows no fear - not in a Batman way, but in the sense that she can't recognise the emotion in the eyes of others Way back in 1994, Adolphs' group showed that SM can reasonably recognise the emotions in most facial expressions, but she falters when the face in question is afraid. And even though she's a talented artist, she can't draw a scared face, once claiming that she didn't know what such a face would look like.

Now, Naotsugu Tsuchiya, working in Adolphs' team, has found that SM's knowledge of fear is a little more complicated. When asked to classify angry and fearful faces, or threatening and harmless scenes, SM did so completely normally when she had to do it quickly. Even though she felt that the scared faces were less intense than volunteers with intact amygdalae, she classified them correctly, with similar reaction times.

In a similar experiment, Tsuchiya showed SM faces that had been gradually morphed from fearful to neutral expressions. When she had unlimited time, it took much more severe expressions for her to recognise a face as fearful. But when she had to quickly pick scared faces from a set, her performances were indistinguishable from other people.

This means that the amygdala isn't always necessary to know fear. It's not needed for the earliest stages where our brain starts to process fearful images below the level of our consciousness. Instead, Tsuchiya suggests that after this first level of analysis is over, the amygdala helps us to use the results to make social judgments - to explicitly recognise fear for what it is and to assess the relevance of those first subconscious twinges.

Reference: Nature Neurosciencedoi:10.1038/nn.2381 and 10.1038/nn.2380

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