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

THE MIRROR-NEURON HYPOTHESIS does a good job of accounting for the defining features of autism: lack of empathy, pretend play, imitation, and a theory of mind.⁴ However, it is not a complete account, because there are some other common (though not defining) symptoms of autism that mirror neurons do not have any apparent bearing on. For example, some autistics display a rocking to-and-fro movement, avoid eye contact, show hypersensitivity and aversion to certain sounds, and often engage in tactile self-stimulation—sometimes even beating themselves—which seems intended to dampen this hypersensitivity. These symptoms are common enough that they too need to be explained in any full account of autism. Perhaps beating themselves is a way of enhancing the salience of the body, thereby helping anchor the self and reaffirming its existence. But can we put this idea in the context of the rest of what we have said so far about autism?

In the early 1990s our group (in collaboration with Bill Hirstein, my postdoctoral colleague; and Portia Iversen, cofounder of Cure Autism Now, an organization devoted to autism) thought a lot about how to account for these other symptoms of autism. We came up with what we called the “salience landscape theory”: When a person looks at the world, she is confronted with a potentially bewildering sensory overload. As we saw in Chapter 2 when we considered the two branches of the “what” stream in the visual cortex, information about the world is first discriminated in the brain’s sensory areas and then relayed to the amygdala. As the gateway to the emotional core of your brain, the amygdala performs an emotional surveillance of the world you inhabit, gauges the emotional significance of everything you see, and decides whether it is trivial and humdrum or something worth getting emotional over. If the latter, the amygdala tells the hypothalamus to activate the autonomic nervous system in proportion to the arousal worthiness of the triggering sight—it could be anything from mildly interesting to downright terrifying. Thus the amygdala is able to create a “salience landscape” of your world, with hills and valleys corresponding to high and low salience.

It is sometimes possible for this circuit to go haywire. Your autonomic response to something arousing manifests as increased sweating, heart rate, muscular readiness, and so on, to prepare your body for action. In extreme cases this surge of physiological arousal can feed back into your brain and prompt your amygdala to say, in effect, “Wow, it’s even more dangerous than I thought. We’ll need more arousal to get out of this!” The result is an autonomic blitzkrieg. Many adults are prone to such panic attacks, but most of us, most of the time, are not in danger of getting swept away by such autonomic maelstroms.

With all this in mind, our group explored the possibility that children with autism have a distorted salience landscape. This may be partially due to indiscriminately enhanced (or reduced) connections between sensory cortices and the amygdala, and possibly between limbic structures and the frontal lobes. As a result of these abnormal connections, every trivial event or object sets off an uncontrollable autonomic storm, which would explain autistics’ preference for sameness and routine. If the emotional arousal is less florid, on the other hand, the child might attach abnormally high significance to certain unusual stimuli, which could account for their strange preoccupations, including their sometimes savant-like skills. Conversely, if some of the connections from the sensory cortex to the amygdala are partially effaced by the distortions in salience landscape, the child might ignore things, like eyes, that most normal children find highly attention grabbing.

To test the salience landscape hypothesis we measured galvanic skin response (GSR) in a group of 37 autistic and 25 normal children. The normal children showed arousal for certain categories of stimuli as expected but not for others. For example, they had GSR responses to photos of parents but not of pencils. The children with autism, on the other hand, showed a more generally heightened autonomic arousal that was further amplified by the most trivial objects and events, whereas some highly salient stimuli such as eyes were completely ineffective.