Friday, June 19, 2009

Smithsonian - Brain Cells for Socializing

The neuroscience of social behavior is a new and emerging field, and one that may change a lot of how we conceptualize our need for social connection

Brain Cells for Socializing

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

  • By Ingfei Chen
  • Photographs by Aaron Huey
  • Smithsonian magazine, June 2009

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."

Allman thinks that the neurons expedite communication from the ACC and FI to the rest of the brain. The cells are unusually large, and in the nervous system, size often correlates with speed. "They're big neurons, which I think do a very fast read of something and then relay that information elsewhere quickly," he says. He speculates that as our primate ancestors evolved bigger and bigger brains, they needed high-speed connections to send messages across greater distances. "Large brain size necessarily carries with it a slowing down of communication within the brain," he adds. "So one way of dealing with that is to have a few specialized populations of cells that are pretty fast."

Given that the neurons live in the brain's social hot spots, Allman theorizes that the von Economo cell system allows a rapid, intuitive read on emotionally charged, volatile situations. The neurons "would enable one to quickly adjust to changing social contexts," he speculates. In the ancient past, this neural wiring might have conferred a survival edge to our ancestors by enabling them to make accurate, split-second judgments, especially about whom they could trust or not.

Allman, Hof and their colleagues have looked for von Economo neurons in more than 100 animal species, from sloths to platypuses. Only a few of them, other than primates and elephants, are known to have the cells: humpback whales, sperm whales, fin whales, orcas and bottle-nosed dolphins. The cells presumably evolved in now extinct species that gave rise to those marine mammals some 35 million years ago.

As I watched him section the elephant brain at Caltech, Allman, with colleagues Atiya Hakeem and Virginie Goubert, finally reached the FI of Simba's left hemisphere. Three days later, microscope examination of the brain slices revealed it to be dotted with the distinctive spindle-shaped cells. That confirmed their previous sighting of similar neurons in the FI of Simba's right hemisphere. The elephant cells are larger than human and primate ones, about the size of whale neurons, but the size and shape are unmistakably von Economo neurons.

From counting the von Economo cells in 16 slides—an eye-glazing chore—Hakeem and Allman estimate that there are roughly 10,000 of them in the postage-stamp-size FI on the right side of the elephant brain, or about 0.8 percent of the FI's 1.3 million neurons. Von Economo neurons are more plentiful in the human FI, averaging about 193,000 cells and accounting for about 1.25 percent of all neurons there. In absolute numbers, the human brain has roughly half a million von Economo neurons, far more than the brains of elephants, whales or great apes. Allman and his colleagues have found none in the elephant's closest kin: the anteater, armadillo and rock hyrax. The cells' absence in these species supports Allman's theory that the neurons are a feature of big brains.

Allman speculates that such cells readily evolve from a small set of neurons in the insular cortex that are found in all mammals and regulate appetite. He thinks that while von Economo cells likely evolved to speed information around a big brain, they got co-opted by the demands of social interactions. If he's right, smart, social animals such as whales and elephants might have the same specialized wiring for empathy and social intelligence as human beings.

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