American Scientist

THE TELL-TALE BRAIN: A Neuroscientist’s Quest for What Makes Us Human. V. S. Ramachandran. xxvi + 357 pp. W. W. Norton and Company, 2011. $26.95.

In his new book, The Tell-Tale Brain, V. S. Ramachandran takes us on a fascinating tour of his research regarding a wide range of neurological conditions. These include acquired atypical phenomena such as phantom limbs, innate atypical phenomena such as synesthesia, neurodevelopmental disabilities such as autism, and psychiatric syndromes such as Capgras syndrome. Writing mostly in the first person, he describes how he and his colleagues puzzled over how to explain each unusual phenomenon or syndrome. The result is a highly readable journey into his lab, and into his mind. By showing how talented neuroscientists like Ramachandran set out to make sense of the brain’s mysteries, the book will educate the wider public about those mysteries and inspire a new generation of students to move into neuroscience.

The book covers a broad range of conditions. But in this review I will focus on the author’s account of autism and the theory he proposes to explain it. According to Ramachandran, in autism the mirror-neuron system is broken. Is this true?

Mirror neurons are a highly appealing concept. As Ramachandran explains, they were first discovered in monkeys in 1992, when Giacomo Rizzolatti and colleagues at the University of Parma in Italy noticed that the same neurons that fired when a monkey reached for an object also fired when the monkey saw another monkey reaching for an object. Since then, scientists have hypothesized that mirror neurons are the building blocks of a number of important human cognitive skills, including imitation, mind-reading and even empathy. Given that children with autism have difficulty with all three of these skills, it seems highly plausible that their mirror-neuron systems might be underdeveloped or malfunctioning.

By January 2006, two compelling pieces of evidence for the “broken mirror” theory of autism had been published. In March 2005, with Lindsay M. Oberman as first author, Ramachandran’s group at the University of California, San Diego, published a paper in Cognitive Brain Research reporting the results of a study that used electroencephalography (EEG) to measure the brain waves of 10 high-functioning children with autism and 10 age- and gender-matched control subjects. The researchers analyzed the EEG data looking for suppression of mu waves (those with a frequency of 8 to 13 hertz). Mu-wave suppression normally occurs both when a person performs an action and when he or she observes someone else performing an action. The study found that mu waves were suppressed in the children with autism only when they performed an action themselves, not when they observed others acting. The experiment, which is described in The Tell-Tale Brain, is an important plank in the mirror-neuron theory of autism.

Shortly afterward, Mirella Dapretto and colleagues at the University of California, Los Angeles, reported in the January 2006 issue of Nature Neuroscience the results of an fMRI study in which 10 high-functioning children with autism and 10 control subjects were asked to watch and imitate facial expressions that showed such emotions as anger, fear, happiness or sadness. The children with autism could imitate the faces but had difficulty recognizing their meaning; these children showed reduced activity in the pars opercularis of the inferior frontal gyrus, which is held to be part of the mirror-neuron system. Ramachandran notes that other researchers, including Riitta Hari and Michele Villalobos, have corroborated his hypothesis.

However, the results of a study published in Neuron in 2010 suggest that the mirror-neuron system in people with autism may in fact work normally. In typical people, mirror neurons are known to fire more weakly when a movement is repeated than when it is initially made. So Ilan Dinstein at the Weizmann Institute in Rehovot, Israel, together with colleagues at New York University, set out to test whether this was also the case in adults with autism. They asked 13 high-functioning adults with autism and 10 control subjects to perform hand movements, or to watch others perform them, while undergoing fMRI. In some trials the same hand movement was performed repeatedly, and in others the movements varied. The researchers found that both in the people with autism and in the control group, the anterior intraparietal sulcus and the ventral premotor cortex (components of the mirror-neuron system) were active not only while a person was making the hand movements, but also when he or she was watching them being performed by someone else. And in both groups, these mirror-neuron areas showed less activity when the same movements were performed or observed over and over again, but not when a series of novel movements was being performed.

Another recent study also challenges the “broken mirror” theory of autism. Jean Decety at the University of Chicago, working with Yang-Teng Fan and others in Taiwan, used EEG to look for mu-wave suppression in 20 males with autism and 20 controls while they were watching or performing hand movements. The findings, published in the Journal of Child Psychology and Psychiatry in 2010, failed to replicate those of Ramachandran’s 2005 study: In Decety’s subjects, mu-wave suppression while actions were being observed did not differ significantly between the two groups. Neither of these two studies that challenge Ramachandran’s theory are discussed in the book.

There are also clinical and experimental reasons for being skeptical of the broken-mirror theory of autism. First, it has been noted from the earliest accounts that when children with autism speak, they often echo other people’s speech (so-called echolalia), repeating what is said verbatim and faithfully reproducing the intonation, tempo, precise articulation and accent of the other person. Is this not excellent imitation? Would it be possible for someone to do this whose mirror-neuron system was impaired?

In addition, although autism is certainly a social disability, it also has nonsocial features that reveal a different cognitive or information-processing style. For example, people with autism have excellent attention to detail and are able to memorize not just other people’s words but also inanimate information such as car license plates or railway timetables. And finally, people with autism often develop obsessions, becoming immersed in a single topic to the exclusion of all else. How can a single factor like a broken mirror-neuron system explain these nonsocial features? In recognition of this latter point, Ramachandran has come up with a second theory (the “salience landscape theory”) to account for the nonsocial features. And in fairness, I should mention that he does acknowledge in a note that the evidence for mirror-neuron dysfunction in autism is “compelling but not conclusive.”

Nevertheless, Ramachandran argued in a TED talk he gave in November 2009 that 100,000 years ago mirror neurons evolved and enabled imitation, tool use, theory of mind, empathy, emulation, culture and civilization. He puts a huge weight of importance on these neurons, even though they have not really been measured in humans; this is because the single-cell recordings of brain cells that have been done in experimental animals such as monkeys cannot ethically be done in humans. All we really have are indirect or crude measures of mirror-neuron activity, using technologies such as fMRI. In an essay on the Edge website (http://www.edge.org/3rd_culture/ramachandran/ramachandran_p1.html) Ramachandran wrote, “I predict that mirror neurons will do for psychology what DNA did for biology: they will provide a unifying framework and help explain a host of mental abilities that have hitherto remained mysterious and inaccessible to experiments.” Whether he has overstated the importance of mirror neurons and will decide to retract this statement remains to be seen. As an explanation of autism, the theory offers some tantalizing clues; however, some problematic counterevidence challenges the theory and particularly its scope.

But none of these debatable scientific issues diminished my enjoyment of this book, which is important as a record of its author’s restless mind and seemingly infinite curiosity. Ramachandran is without doubt one of the world’s most stimulating neuroscientists, and his bold ideas offer not just food for thought but explanations of what makes us human.

Simon Baron-Cohen is professor of developmental psychopathology at the University of Cambridge and director of the Autism Research Centre in Cambridge. He is the author of a number of books, including The Science of Evil: On Empathy and the Origins of Cruelty (Basic Books, 2011), Prenatal Testosterone in Mind (The MIT Press, 2005) and The Essential Difference: Men, Women and the Extreme Male Brain (Basic Books, 2003).