Singing In The Brain

A neurobiologist's discoveries about the vocal learning talents of birds are yielding startling insights into the evolution of brains--including ours.
November 30, 2001

Erich Jarvis nestles himself into the thick green foliage of the Brazilian forest, just as the morning sun begins to drive vapor off the broad wet leaves. He has arrived just in time for the most important daily event in his scientific fieldwork--the "dawn chorus."

Songcatcher: Jarvis and his parabolic microphone, used for recording birdsong. Photo:Chris Hildreth

 

After a long, frustrating wait and too many missed opportunities, a prime target appears near his wire-cage trap. He aims a parabolic microphone at his small, quick quarry as his fellow scientist tracks it through binoculars. It takes four attentive eyes to track this lightning-fast creature--an absolute necessity, because if the scientists lose sight of it even for an instant, they cannot claim that they have gathered data on the same bird and the creature would be lost as a candidate for valid scientific study.

Jarvis barely manages to keep his flitting target framed in the video camera's sights. Then, to his utter gratification, the creature abruptly launches the performance he hoped for--emitting a raspy squeak so soft and high-pitched that Jarvis, when he first arrived in the forest, had taken for an insect's buzz. Again and again the creature sings, finally attaining the thirty-minute duration required for Jarvis' experiments. After zipping about, almost seeming to tease, his quarry flits into the trap to imbibe the sugar-water bait. Jarvis springs the trap and the tiny hummingbird is captured. Now he can measure the telltale changes in its brain produced by its obliging dawn chorus.

The hummingbird's half-hour of squeaky twitters has switched on a specific marker gene that the scientists know signals activity of the neural machinery underlying production of "learned vocalizations." Studying vocal learning is important because such learning of meaningful sounds is different from, say, the barking of a dog. Even though dog-lovers know that their pooch's bark is a form of communication, it is not learned but inborn. In contrast, vocal learning is imitative and rare in nature. It is found only in a few birds--songbirds, parrots, hummingbirds--and in just as few mammals, including whales, dolphins, bats, and, of course, humans.

Jarvis and his colleagues had already used their marker gene, with the faintly comical name of ZENK, to map the brain regions involved in vocal learning in songbirds and parrots, discovering that basically the same seven regions are involved. And once back at Duke, their analysis of the brains of the trapped hummingbirds resulted in a perfect scientific trifecta. As reported in August 2000 in the journal Nature, Jarvis and his colleagues discovered that hummingbirds also used the same seven brain structures to generate their song.

What's startling to biologists, says Jarvis, is that these three bird species occupy distant twigs on the bird family tree, each having closer relatives that are vocal nonlearners. The finding that these birds evolved to use a very similar set of structures for vocal learning offers a doorway to study a fascinating mystery of evolution. "One hypothesis is that the three orders evolved these structures independently over the last 65 million years in almost identical ways," says Jarvis.

This suggests that nature exerts some kind of external constraints other than genetics--called "epigenetic constraints"--on how complex brain structures evolve for complex behavior. "It's like the independent evolution of wings in both bats and birds. It is thought that the environment dictated that the wings had to be on either side of the body at the center of gravity for the least energy use, not one on the head and one on the foot."

Among the less likely evolutionary possibilities for the birds' song, says Jarvis, are that all modern birds had a common ancestor with vocal learning, and that many intervening orders lost the trait multiple, independent times. "If you apply that argument to mammals, then maybe some ancient mammal had the capability of speech, but it was lost multiple times at least between that ancestor and dolphins and humans." In both birds and mammals, such a multiple disappearance and then reappearance of this trait in one of many primates, humans, seems highly improbable, he says. Or all birds might have rudimentary, nonworking brain structures for vocal learning that are simply amplified in songbirds, parrots, and hummingbirds.

If such rudimentary brain structures exist, asks Jarvis, then why not have them in reptiles and dinosaurs? He and his colleagues can use modern techniques of genetic and molecular analysis to study the brains of "nonlearning" birds to answer such evolutionary questions. But more broadly, he says, his birds challenge all of us to rethink outmoded concepts of evolution, including our own place in it.

"Throughout our education, we have this concept of linear evolution instilled in us," he says. "We're told that there's this hierarchy of evolution, in which vertebrates evolved from some worm-like creature to fish, amphibians, reptiles, birds, mammals, and so forth, and that living vertebrates represent these stages in both body plan and brain intelligence. And once there were mammals, they evolved to primates, then humans, being last at the top of the hierarchy. But this concept of lower and higher in the vertebrate lineage is just completely false. Actually, evolution is a process in which each group of animals develops independent and diverse specializations. Songbirds have them, and we--as humans, mammals, and primates--have them."

What will surprise many, and even surprised Jarvis, is how little scientists really know about the language-fostering structures in our own brains. "After publication of the Nature paper on the hummingbirds, I started looking into the scientific literature on human speech more deeply than I ever had before," he says, waving a hand across an office floor piled with 800 or so scientific papers he has scrutinized. "I looked for any kind of brain differences or similarities with the bird vocal-learning and human-language literature. And the first thing I found is the human literature is a mess."

Of course, he notes, ethical constraints have prevented scientists from using the same rigorous techniques of dissection and experiment to study the human brain that they have with animals. It's understandable, then, that scientific understanding remains fragmentary of the language-related brain structures that sit between our very own ears. "Even the information in textbooks is not correct, because much of it doesn't come from studying human brains. Rather, it comes from extrapolating to humans studies of rats and nonhuman primates such as macaques."

Since neither of these species has been known to utter an intelligible learned vocalization, says Jarvis, "what's in textbooks is not reality, even though it's what students are learning as a mantra, and what professors are passing from generation to generation." In birds, vocal learners have different brain vocal pathways than vocal nonlearners. So it is impossible to extrapolate one to the other.

If Jarvis sounds like a man set to rattle some scientific cages, he is. Next year, he will help bring together at Duke a group of comparative neurobiologists, who will negotiate a renaming of the structures of bird brains from names given to them nearly a hundred years ago. The problem now, says Jarvis, is that names of all bird forebrain structures reflect an outmoded analogy to a basal structure in mammals called the "striatum," which scientists believed was a region involved in primitive, instinctual, and savage behaviors. Such invidious comparison doesn't reflect the reality that the striatum is involved in complex learned behaviors, and that a much larger proportion of the bird forebrain is instead analogous to the human cortex--an outer forebrain division that also manages complex behaviors. Although humans are taught to be inordinately proud of our cerebral cortex, it is actually the interaction of different parts of the forebrain, including the striatum, that manages complex processes as thought. Likewise, says Jarvis, birds have comparable brain divisions that manage their complex behavioral processes, among them several of the seven vocal learning nuclei in each of these parts.

photo:Maria Amélia Maciel

 

Besides renaming bird-brain structures, Jarvis proposes renaming some mammalian brain structures to be less mammalian-centric. "We're going to ask neuroscientists, or anybody talking about the mammalian brain, to stop using terms like 'neocortex' and 'neostriatum.' Those names are based on false ideas of mammalian brains being supreme."

Once the nomenclature is corrected, says Jarvis, he and his colleagues can proceed with developing more realistic comparisons of bird and human brains. "I believe that the difference, really, between humans and songbirds, besides the general brain organization of mammals and birds, is that humans have more of what the birds have," he says. "But in order to explain this hypothesis of parallels between vocal imitation structures in the bird brain and language structures in human brains, I first have to get around this hundred-year-old dogma that their brains are so very different."

As a proselytizer for new paradigms in brain science, Jarvis himself is perhaps a new--or at least rare--"paradigm" for a brain scientist. For one thing, he came from a family of performing artists (his early hero was not Einstein but Houdini), and his childhood ambition was to become a magician. Naturally, he entered the High School of Performing Arts in Manhattan, eventually leaving his magic days behind to emerge as a modern dancer.

To Jarvis, however, the leap from dance to science was not a strenuous one. "Between high school and college, I decided I wanted to do something that I felt would have more impact in the world, and I decided that was science. So, I took the discipline I learned as a dancer, as well as the imagination that I got as a magician, and tried to combine them into doing scientific research." Since his father had shared with his son an interest in science, Jarvis perceived science not as a dry cookbook enterprise, but just as creative as any art.

 
 

His ethnic heritage--African American, Native American, and European--qualified him for an affirmative-action program at Hunter College, where he launched his research in molecular biology. However, heeding his mother's inspiration that he should always go for his dream, he decided to think big and choose between two diverse and ambitious scientific endeavors. "One was the study of the origins of the universe, and the other was the study of the brain," he recalls. "I figured those two were challenging enough, and I wanted something very challenging. Since my intuition and upbringing were more connected to biology--to the Earth rather than to the sky--I figured in that case, I'll study the brain."

As a premier undergraduate researcher--he published six professional scientific papers on his discoveries--he had his pick of top-ranked graduate programs. He decided, he says, that he wanted to link the precise techniques of molecular biology to understanding animal behavior. But he confesses that he himself harbored a typical mammal's evolutionary chauvinism. "I thought I'd study mammals because that's the closest you're going to get to humans, and I thought mammals were the most intelligent species."

As a first step toward such mammalian studies, he joined Rockefeller University, planning to study the molecular biology of rat or primate behavior. He quickly realized the lack of good natural-behavioral studies in such species. He then joined the research team of the famed biologist Fernando Nottebohm, renowned for his pioneering studies of the neural basis of birdsong and the discovery of making new neurons in adult vertebrates' brains. Jarvis says he was especially intrigued by Nottebohm's "ethological" approach--that is, studying animals under conditions of natural behavior. "I decided that, okay, for my graduate training, I'll do some research in the bird brain-the 'lower' form of animals. And after I learned some ethological approaches and applied my molecular biology to them, then I'll go to the 'higher' form, the mammalian system, and eventually maybe study humans."

photo:Maria Amélia Maciel

 

 

One scientific bias he quickly encountered was against mixing molecules and behavior in research. His advisers cautioned him about trying to measure molecular-level changes resulting from natural behavior, "because natural behavior was viewed as something very complex and difficult to study, particularly if you're going to use molecular biology," he says. But he persisted. Working with colleagues Claudio Mello and David Clayton, he and the young scientists found that the ZENK gene--whose role in learning is now being proven--was dramatically switched on during listening and producing learned vocalizations in songbirds. Using this approach, they managed to map the brain regions involved.

Such discoveries and comparisons with mammals began to change Jarvis' outlook toward "mere" bird brains. "I started to get rid of this idea of mammals being highly specialized, and started to think more globally," he says. "I wanted to explore just what the relationship was among all animals that have a brain. I couldn't study all animals, but I wanted to know whether the brain function Clayton, Mello, and I were discovering in songbirds was unique. After all, many neurobiologists thought of the songbird brain as an exotic branch of evolution, and that it was doing some fancy things that weren't relevant to vertebrate brain function in general."

So, for their next experiments, Jarvis and Mello made their way to the local pet store and obtained some budgerigars, commonly known as parakeets. Their studies of these small parrots revealed that they also used the same seven brain structures as songbirds in vocal learning. The identity of their next experimental subjects became obvious because Mello is Brazilian; Brazil is known as the hummingbird capital of the world.

Given a chance to enjoy field research in his native land, Mello joined with Jarvis and Brazilian colleagues to study whether hummingbirds sang from the same neural "songbook" as songbirds and parrots. Jarvis, Mello, and colleagues soon found themselves immersed in a fluttering cloud of wings at a nature reserve in EspÌrito Santo, Brazil, where for six decades hummingbirds had been lured with feeders.

Beyond hunkering down in the forest to study hummingbird behavior, Jarvis and his Duke colleagues are now hunkering down in high-tech genomics laboratories to explore the cellular machinery underlying vocal learning behavior. They even plan to tinker with it. One of Jarvis' key tools will be the "gene chip"--arrays of thousands of genes spotted onto small glass squares that enable researchers to detect which genes are switched on during cell processes. "Such chips will help us understand how behavior sets in motion molecular pathways," says Jarvis. "And then, we'll try to find out what those molecular pathways are doing to the brain; and then, in turn, how they affect behavior."

Jarvis plans to compare the "gene expression profiles" of those hummingbird species that learn song to those that don't. Then, just maybe, he will attempt experiments that sound like science fiction: engineering song-learning birds from nonlearners. "If we can figure just which genes are specifically activated in vocal learners, we can use transgenic experiments to put those genes into a nonlearning species and convert a vocal nonlearner into a vocal learner."

Such genetic experiments, even with an animal as seemingly distant from humans as the hummingbird, could help us understand human language, Jarvis says. "We're finding with these DNA chips that somewhere between 70 and 80 percent of the genes that we get from the songbird brain have a homologous counterpart in humans and mammals in general."

Beyond implications for humans, Jarvis' insights have fueled his imaginative speculations about evolution on other planets, taking him back to his interest in cosmology. "When I pulled out a bunch of physics books from my student days and started reading them, I came across this idea that certain physical constants are the same throughout the universe. And I wondered whether, if these physical constants apply to all things, they must apply to the brain. So, I'm coming closer and closer to thinking that such epigenetic constraints might well mean that--even though there is likely a diversity of life on other planets--there are also constancies. So, I would not be surprised if brains like ours might have evolved on other planets."

The lesson, says Jarvis, is that we humans need to think of ourselves not as inherently supreme ruling creatures on this planet, but as privileged members of an elegant web of evolution--one that might even reach to the stars.