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John Allman (with colleague Atiya Hakeem at Caltech examining elephant brain specimens) is searching for one of the biological keys to human behavior. (Aaron Huey)

Brain Cells for Socializing

Does an obscure nerve cell help explain what gorillas, elephants, whales—and people—have in common?

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There was little chance of missing the elephant in the room. About a dozen years after Simba died at Cleveland Metroparks Zoo, a half-inch slab of her yellowish, wrinkled, basketball-size brain was laid out before John Allman, a neuroscientist at the California Institute of Technology in Pasadena.

Preserved in formaldehyde, it looked like half a pancake, frozen solid on a misting bed of dry ice. Allman carefully sliced it using the laboratory equivalent of a deli meat cutter. Taking well over an hour, he carved off 136 paper-thin sections.

Allman was searching for a peculiar kind of brain cell that he suspects is a key to how the African elephant—like a human being—manages to stay attuned to the ever-shifting nuances of social interplay. These spindle-shaped brain cells, called von Economo neurons—named for the man who first described them—are found only in human beings, great apes and a handful of other notably gregarious creatures. Allman, 66, compares the brains of people and other animals to gain insight into the evolution of human behavior.

"Neuroscience seems really reluctant to approach the question of what it is about our brains that makes us human, and John is doing exactly that," says Todd Preuss, a neuroanatomist and anthropologist at the Yerkes National Primate Research Center in Atlanta. "We know very, very little about how our brains differ from other animals', except that our brains are bigger."

The von Economo neurons are the most striking finding of recent years in comparative brain research, in which scientists tease out fine differences among species. Neuroanatomist Patrick Hof and his colleagues at the Mount Sinai School of Medicine in Manhattan first stumbled across the neurons in human brain specimens in 1995, in a region toward the front of the brain called the anterior cingulate cortex. Most neurons have cone- or star-shaped bodies with several branching projections, called dendrites, that receive signals from neighboring cells. But von Economo neurons are thin and elongated, with just one dendrite at each end. They are four times bigger than most other brain cells, and even in species that have the cells, they are rare.

The Manhattan team, it turned out, had rediscovered an obscure cell type first identified in 1881. Hof named the cells after a Vienna-based anatomist, Constantin von Economo, who precisely described the neurons in human brains in 1926; afterward the cells slipped into obscurity. Hof began looking in the brains of deceased primates, including macaque monkeys and great apes—chimps, bonobos, gorillas and orangutans—donated by zoos and sanctuaries. He contacted Allman, who had a collection of primate brains, and asked him to collaborate. In 1999, the scientists reported that all great ape species had von Economo cells, but lesser primates, such as macaques, lemurs and tarsiers, did not. That meant the neurons evolved in a common ancestor of all the great apes about 13 million years ago, after they diverged from other primates but well before the human and chimp lineages diverged about six million years ago.

Although Allman is renowned as a neuroanatomist, it's not surprising to find him delving into larger questions of what it means to be human. His doctorate, from the University of Chicago, was in anthropology, and he has long been fascinated with how the primate brain evolved. He conducted landmark studies with his colleague Jon Kaas, ident­ifying the parts of the owl monkey brain that analyze visual information and make sight possible. In 1974, Allman moved to Caltech, where he studied vision for 25 years. But he also itched to uncover how the basic workings of the human brain shape social behavior. The von Economo neurons immediately captured his interest.

Allman, who is divorced, lives in a 150-year-old brick house in San Marino that he shares with two Australian shepherd dogs, Luna and Lunita. Sepia-toned photographs of his suffragist grandmother hang on the living room wall. Being "notoriously nocturnal," as Allman puts it, he rarely gets to the lab before 1 p.m., leaves in the evening to continue working at home and usually stays up until 2 a.m. His Caltech office is dimly lit by a single window and a small desk lamp; it looks like a cave overrun with books and papers. Down the hall, glass slides of gorilla, bonobo and elephant brain tissue, stained blue and brown, lie drying on tables and counters.

From von Economo's work, Allman learned that the unusual cells seemed to reside only in the anterior cingulate cortex (ACC) and one other niche of the human brain, the frontal insula (FI). Brain-scanning studies have established that the ACC and FI are particularly active when people experience emotion. Both areas also seem to be important for "self-monitoring," such as noticing bodily sensations of pain and hunger or recognizing that one has made a mistake. The ACC seems broadly involved in nearly every mental or physical effort.

By contrast, the frontal insula may play a more specific role in generating social emotions such as empathy, trust, guilt, embarrassment, love—even a sense of humor. According to experiments that measure the workings of various brain regions, the area becomes active when a mother hears a crying baby, for instance, or when someone scrutinizes a face to determine the other person's intentions. The FI is where the brain monitors and reacts to "gut feelings" from bodily sensations or interactions within a social network, Allman says. It's the link between self-monitoring and awareness of others that makes it possible for us to understand the feelings of other people. "The basic proposition that I'm advancing," he says, "is the notion that self-awareness and social awareness are part of the same functioning, and the von Economo cells are part of that."

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