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

Think of what this means. It is almost as if there are two Jasons trapped inside one body: the Jason on the phone, who is fully alert and conscious, and the Jason in person, who is a barely conscious zombie. How can this be? The answer has to do with how the accident affected the visual and auditory pathways in Jason’s brain. To a surprising extent, the activity of each pathway—vision and hearing—must be segregated all the way up to the critically important anterior cingulate. This collar of tissue, as we shall see, is where your sense of free will partly originates.

If the anterior cingulate is extensively damaged, the result is the full picture of akinetic mutism; unlike Jason, the patient is in a permanent twilight state, not interacting with anyone under any circumstances. But what if the damage to the anterior cingulate is more subtle—say, the visual pathway to the anterior cingulate is damaged selectively at some stage, but the auditory pathway is fine. The result is telephone syndrome: Jason springs to action (speaking metaphorically!) when chatting on the phone but lapses into akinetic mutism when his father walks into the room. Except when he is on the telephone, Jason is no longer a person.

I am not making this distinction arbitrarily. Although Jason’s visuomotor system can still track and automatically attend to objects in space, he cannot recognize or attribute meaning to what he sees. Except when he is on the phone with his father, Jason lacks the ability to form rich, meaningful metarepresentations, which are essential to not only our uniqueness as a species but also our uniqueness as individuals and our sense of self.

Why is Jason a person when he is on the phone but not otherwise? Very early in evolution the brain developed the ability to create first-order sensory representations of external objects that could elicit only a very limited number of reactions. For example a rat’s brain has only a first-order representation of a cat—specifically, as a furry, moving thing to avoid reflexively. But as the human brain evolved further, there emerged a second brain—a set of nerve connections, to be exact—that was in a sense parasitic on the old one. This second brain creates metarepresentations (representations of representations—a higher order of abstraction) by processing the information from the first brain into manageable chunks that can be used for a wider repertoire of more sophisticated responses, including language and symbolic thought. This is why, instead of just “the furry enemy” that it is for the rat, the cat appears to you as a mammal, a predator, a pet, an enemy of dogs and rats, a thing that has ears, whiskers, a long tail, and a meow; it even reminds you of Halle Berry in a latex suit. It also has a name, “cat,” symbolizing the whole cloud of associations. In short, the second brain imbues an object with meaning, creating a metarepresentation that allows you to be consciously aware of a cat in a way that the rat isn’t.

Metarepresentations are also a prerequisite for our values, beliefs, and priorities. For example, a first-order representation of disgust is a visceral “avoid it” reaction, while a metarepresentation would include, among other things, the social disgust you feel toward something you consider morally wrong or ethically inappropriate. Such higher-order representations can be juggled around in your mind in a manner that is unique to humans. They are linked to our sense of self and enable us to find meaning in the outside world—both material and social—and allow us to define ourselves in relation to it. For example, I can say, “I find her attitude toward emptying the cat litter box disgusting.”

The visual Jason is essentially dead and gone as a person, because his ability to have metarepresentations of what he sees is compromised.¹ But the auditory Jason lives on; his metarepresentations of his father, his self, and their life together are largely intact as activated via the auditory channels of his brain. Intriguingly, the hearing Jason is temporarily switched off when Mr. Murdoch appears in person to talk to his son. Perhaps because the human brain emphasizes visual processing, the visual Jason stifles his auditory twin.

Jason presents a striking case of a fragmented self. Some of the “pieces” of Jason have been destroyed, yet others have been preserved and retain a surprising degree of functionality. Is Jason still Jason if he can be broken into fragments? As we shall see, a variety of neurological conditions show us that the self is not the monolithic entity it believes itself to be. This conclusion flies directly in the face of some of our most deep-seated intuitions about ourselves—but data are data. What the neurology tells us is that the self consists of many components, and the notion of one unitary self may well be an illusion.