Read The Man Who Wasn't There: Investigations into the Strange New Science of the Self Online
Authors: Anil Ananthaswamy
It’s not just crickets. Similar single-neuron recordings of the mechanism of corollary discharge can be seen in nematode worms, songbirds, and even marmoset monkeys.
Within a decade of Irwin Feinberg’s 1978 proposal that a fault in the brain’s corollary-discharge mechanism might underlie the varied symptoms of schizophrenia, Chris Frith, a clinical psychologist who was then at the Northwick Park Hospital in Harrow, UK, developed his “comparator model” for how our sense of agency arises—the sense that makes us
feel
we are responsible for our actions. At the time, Frith argued that the disruption of this very basic aspect of our sense of self was behind the first-rank symptoms of schizophrenia: auditory verbal hallucinations, thought insertion, and delusions of control (the delusion that someone else is controlling one’s actions).
While the model has morphed somewhat over the years, its essence remains the same. Say you want to move your arm. The motor
cortex sends commands to the muscles in the arm. The motor cortex copies the command to other brain regions, which then use the copy to predict the sensory consequences of the arm movement. Meanwhile, the arm moves, which results in certain sensations (such as tactile, proprioceptive, or visual sensations). The “comparator” matches actual sensations with predicted sensations. If there is no mismatch, we feel that we performed the action—we
own
the action, giving us a sense of agency. A mismatch makes us feel that someone else, an external agency, is responsible.
It’s easy to see the appeal of this model. It allows the brain to dampen its response to self-generated sensations (for instance, the cricket’s deafness to its own chirps). It provides a mechanistic explanation for how the brain might distinguish between self and non-self, at least for motor actions. And there’s evidence that this ability is hampered in people with schizophrenia.
Take tickling.
It’s near impossible to tickle yourself. Frith, along with Sarah-Jayne Blakemore and Daniel Wolpert, showed why. In studies of healthy people, the researchers found that a couple of brain regions were far less active when people touched their left hands themselves compared with when the experimenter touched their left hands. The brain was stifling its response to self-generated touch sensations (explaining why we can’t tickle ourselves). Also, the brain region that is likely doing the stifling is the cerebellum, possibly by predicting the effects of self-generated movements.
Blakemore, Frith, and colleagues further showed that
people experiencing auditory hallucinations and delusions of control felt a touch on their left hand as equally intense, ticklish, and pleasant regardless of whether they themselves or the experimenter did the touching. In other words, many people with schizophrenia can tickle
themselves. This suggests an inability to tell apart self-generated actions from non-self actions.
There’s more evidence. Judith Ford and Daniel Mathalon, at the San Francisco VA Medical Center and the University of California, San Francisco, have shown that healthy people, just like crickets, can dampen down their response to self-generated sounds. Brain EEG signals in healthy people, just prior to them uttering a sound, show a synchrony that is suggestive of a copy of the command to move the vocal cords being sent to the auditory cortex. And then, an EEG signal called N1, indicative of auditory cortex activity, is damped down about 100 milliseconds after the healthy person makes the sound. This is possible evidence that the predicted sound has been compared with the actual sound, causing the external sound to be tagged as self-generated and thus ignored. N1, however, is not suppressed when the sound is external, which indicates that the person can hear it.
But this mechanism seems to be impaired in people with schizophrenia. This is evidence of a
possible disruption of the copy mechanism. For them the N1 signal is not suppressed to self-generated sounds, which means that the patients are hearing their own vocalizations in the same way they would hear external sounds (Sass suggests that this is a kind of hyperreflexivity—a propensity to take as an external object that which would usually be only tacitly experienced, and therefore be the very medium of selfhood). It is no great leap to think such disruptions of the comparator mechanism could blur the boundaries between self and non-self in schizophrenia.
At this point it’s worth getting subtler about what exactly might be going awry in schizophrenia. When I move my hands, I have two
feelings: a sense of owning my hands and a sense of agency that makes me feel that
I
am moving my hands. We saw in the previous chapter how BIID can be attributed to the loss of sense of ownership of body parts. While there is some evidence that schizophrenia results in somewhat perturbed feelings of body ownership, stronger evidence implicates an impaired sense of agency.
In 2008, cognitive neurologist Matthis Synofzik of the University of Tübingen, Germany; philosopher Gottfried Vosgerau of the Heinrich-Heine University in Düsseldorf, Germany; and their colleagues got even more picky. They argued that
one’s sense of agency should be subdivided into a nonconceptual (nonthinking and instinctive)
feeling
of agency and a more cognitive
judgment
of agency. Synofzik’s team says that while the
feeling
of agency relies on copies of motor signals and comparators that match predictions with actual sensory feedback, the
judgment
of agency depends on a cognitive analysis of the environment and our beliefs about it, which is called postdiction. “If you are alone in a room and something falls down from the table, your world knowledge will tell you that things do not fall by themselves, so you conclude that it must have been you, even if you don’t have a sensory motor feeling of having done anything,” Vosgerau told me during a phone conversation.
Of course, it’s all happening in the blink of an eye, so to speak. Nonetheless, it’s possible to tease apart these mechanisms. Researchers have shown that people with schizophrenia have a disturbed
feeling
of agency, and to compensate
they tend to rely more on their
judgment
of agency, which depends on external factors such as visual feedback. This means that, on the experiential level, they are likely to experience themselves almost as if from outside themselves, again manifesting a kind of hyperreflexivity and an absence of a more basic sense of existing. This
could also explain the split-second delay Sophie said she experiences between moving her hands and feeling that she initiated the action—a delay that makes her question whether her hands are her own.
None of this negates the comparator model. In fact, Synofzik and colleagues acknowledge that their results “
support the notion of a dysfunction of the comparator mechanism in schizophrenia.” Indeed, it’s because of this dysfunction that people with schizophrenia have to rely more heavily on their judgments about the external environment to augment their sense of agency.
So, if a person with schizophrenia picks up a television remote and switches on the TV, he might not feel that he initiated that action. The television nonetheless comes on, so the patient infers someone else made him do it. In Laurie’s case, she didn’t feel like she cut herself after an evening of watching fireworks on Bonfire Night. “Although it appears to be my decision, it was not my decision, or my volition, to do such a thing,” she told me. “So [there is a] loss of agency, yes.”
Given she
knew
she didn’t decide to cut herself, the alternative was obvious: somebody else must be responsible. “I think it’s a natural search for meaning. This is happening to me, so I want an explanation, just like any other human being would do,” she said. “So, then you have an enemy, a conspiracy.” Paranoia is often the outcome.
In a way, the comparator model and its variants help us understand why a person with schizophrenia may feel like his actions are controlled by an external agency and how it might lead to paranoia. Or why the sounds one utters may seem like they were spoken by someone else. But what if no one is speaking, not even you, and yet you hear voices?
Judith Ford has spent the past decade and a half thinking about auditory verbal hallucinations (AVHs), science-speak for hearing voices. In the late 1990s, Ford made the switch from studying aging and Alzheimer’s to studying these voices. In the beginning, she’d analyze data collected by other researchers and write papers. “I was raising small children, and it worked for me,” she said. But soon she realized she had to talk to her patients, pay attention to their individual experiences. It’s these discussions that highlighted the nuances of what she was trying to study. For example, one of her patients told her that before he started taking an antipsychotic drug called Zyprexa, the devil talked to him. Once he was on Zyprexa, God began talking to him. He was still hearing voices, but they had gone from being negative to positive.
Such insights have informed Ford’s work. Healthy people hear voices too, but they tend largely to be positive, and the individuals have some semblance of control over the voices. Not so for people with schizophrenia, about 75 percent of whom hear voices. The voices sound real and are often spoken by “specific non-self voices.” They are usually negative, inciting violence toward oneself (as in Laurie’s case) or others, at times leading to suicide or even homicide.
This phenomenon of voices inciting violence against others is captured vividly by Anne Deveson, an Australian writer and documentary filmmaker, in her book
Tell Me I’m Here
, in which she chronicles her teenage son Jonathan’s devastating schizophrenia and the toll it took on Jonathan, Deveson, and her family. Suffering severely, Jonathan had long taken to disappearing from home, and reappearing suddenly. He could become violent.
In one harrowing section of her book, Deveson describes the scene when she and Jonathan’s probation officer, Brenda (who had just been summoned), confront him:
When Brenda arrived Jonathan was lying on the big couch that faced the sea. He was nodding to himself as if he were listening to voices, but he did not speak aloud. We asked if he were hearing voices. Jonathan looked suspiciously at both of us, then said, “No voices.” He said something else but his voice trailed away. Brenda leaned forward and said she could not hear him.
“I said only Anne’s voice,” he shouted.
“Where’s Anne’s voice?”
“Plotting against me. Inside my head.”
“Jonathan, I’m not plotting against you. And I’m not inside your head. I’m here.”
He looked at me, his eyes darting everywhere, and still that racing energy which seemed to fill the whole room, bouncing off the ceiling and the walls, jangling my own energy, so that I felt I was receiving an electric shock.
“God has said that I should kill you Anne, and Brenda too if she doesn’t shut up.”
He stalked out of the room, waving his arms. A few seconds later he returned, looked at us both, muttered something and left again. This time he didn’t return.
There is something deeply unsatisfactory about trying to find mechanistic explanations for Jonathan’s complex auditory hallucinations. But science has to begin somewhere. One theory tries to explain such auditory verbal hallucinations as misperceived inner speech or inner speech that somehow is not tagged as belonging to the self. We are all familiar with inner speech—it’s our internal monologue, externally inaudible, sometimes clear enough to ourselves, even if it does
not have an auditory quality, and at other times experienced in a more implicit manner (in all likelihood, you are experiencing it as you read this sentence). But Ford argues that auditory verbal hallucinations are not like the willed kind of inner speech, they are more like unbidden thoughts (the stuff of daydreaming or mind wandering). The question then is: how can mind wandering turn into AVHs?
Ralph Hoffman of Yale University and his team have found that in people with schizophrenia,
there is hyperconnectivity between language areas of the brain and the putamen, a deep-brain region that has been linked to the conscious perception of sound. Hoffman argues that this hyperconnectivity is what allows activity in the language areas to enter one’s consciousness as voices.