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For young canaries learning their song, freedom in youth gives way to rules in adulthood


Young canaries can learn atypical songs but recast them into adult canary syntax as they mature

For some kinds of birds, learning to sing is as much a part of growing up as learning to talk is for human children. They listen to their parents and other adults, memorize, imitate, practice, and in time are able to chirp a tune characteristic of their species that will help attract a mate.

Now Rockefeller University scientists have found that young canaries can learn to accurately imitate a computer-generated song that sounds nothing like a canary. But as the birds mature, they edit their song, dropping some elements, rearranging others, and adding repetitions and phrasing typical of an adult canary melody. The results appear in the May 13 issue of Science.

"This kind of reprogramming is reminiscent of the flexibility of phoneme rearrangement in human speech and is an aspect of vocal prowess in birds that had not been described before," says Fernando Nottebohm, Ph.D., Rockefeller’s Dorothea L. Leonhardt Professor and head of the Laboratory of Animal Behavior.

Young canaries normally learn their songs by closely copying a nearby adult, a process that takes six to eight months. However, even birds raised without a singing tutor develop a song with canary-like syllables and phrasing. Under those conditions the juveniles are thought to be guided by an innate program that leads to the development of normal adult song.

But Timothy Gardner, Ph.D., at the time a postdoctoral fellow in the Nottebohm lab, had heard anecdotal evidence of canaries singing outside the range of normal imitations, of canaries that imitated zebra finches, for example.

With the exception of well-known mimics, such as the mockingbird, songbirds in nature rarely imitate the song of other species; they only imitate older birds of their own kind. The researchers wondered whether this preference results from innate knowledge about what the adult song should sound like, and if so, how that innate knowledge steers the learning process. They also wanted to study how the integration of innate and learned knowledge comes about.

"Canaries seemed good material for probing these questions," says Nottebohm. "The method we chose was to tutor canaries with synthetic computer-generated song that violated a specific ’rule’ of adult canary song. Sometimes by trying to see how far you can push an organism to do things it would not normally do you can learn more about the underlying mechanisms."

"The song of canaries is characterized by a successive repetition of sounds, each sound repeated many times forming a phrase," Nottebohm explains, "for example, AAAAA BBBBB CCCCC and so on, where each letter stands for a sound repeated many times. In this notation a string of As is called a ’phrase,’ and one phrase follows another." The researchers wondered whether young canaries would imitate songs that lacked this repetition, songs made up of a string of single nonrepeated sounds such as ABCDE. So they composed two kinds of songs that never occur in the repertoire of an adult canary.

"We synthesized a song, using a computer, in which each sound is slightly-and randomly-different from the one preceding it, and we call that a random walk," says Nottebohm. In another synthesized song each successive note was identical to the previous one except for a slight drop in pitch, a downward swooping glissando that canaries never make.

The scientists studied 16 male canaries that were never exposed to normal canary song. The birds were reared by their mothers, who at that time did not sing. Then, when they were 25 days old, they were housed individually out of earshot of other canaries. A recording of the random walk song was played to 10 of the canaries every two hours during daylight; the remaining six birds heard the glissando instead. The birds heard the recordings every day for a year. At the same time, sounds made by the birds were recorded continuously and analyzed by a computer program that edited out brief calls and cage noises.

Six of the 10 birds exposed to the random walk song learned to imitate the first 10 seconds of the song-a remarkable achievement, considering that all the unique sounds of a canary raised in an aviary add up to only about 2.7 seconds of song.

In the normal course of learning their song, canaries begin to organize syllables into phrases by the time they are two months old. But the birds growing up listening to the random walk and glissando songs instead did their best to imitate the atypical, synthetic songs of their tutors for several months, producing long sequences of dissimilar sounds.

Then puberty hit. As the birds’ testosterone levels rose, their style of singing started to change.

"At sexual maturity, when the song would be important for courting females, rules interfered," says Nottebohm. "The freedom of youth was superceded by adult rules, and phrased song took over."

The change took place at different rates, and with varying degrees of completeness in different individuals. All the birds that at first sang a detailed imitation of their tutor, however, reprogrammed their songs as they approached sexual maturity. They dropped many of the learned syllables and those that persisted were now repeated in the phrased manner that characterizes adult canary song. In addition, the researchers pushed two of the birds raised with the random-walk song into hormonal adulthood with a treatment of testosterone. These canaries reprogrammed their songs more abruptly.

"The individual differences among birds are probably as widespread and dramatic as the individual differences in human speech learning," says Gardner, who wrote the software that allowed the researchers to objectively compare the songs. Throughout the study, approximately 15,000 songs were recorded and analyzed for each bird. This analysis required the continuous running for one week of 16 computers in Rockefeller’s Center for Studies in Physics and Biology. Felix Naef, Ph.D., a third author on the Science paper, also contributed to the programming and analysis.

Adds Gardner, "One reason these kinds of observations have not made it into the scientific literature before is that they are very difficult to quantify. But this computationally intensive process made for more robust results."

From time to time some of the birds sang, as adults, fragments of the songs they learned as juveniles. Apparently these birds retained two programs for singing that shared common material: the juvenile slavish imitation of an atypical, phraseless song, and the adult song that reworked a subset of sounds into a different syntax.

"Clearly, learning song and the rules for adult song can be uncoupled," says Nottebohm. "The song acquired during the freedom of youth and the song with adult rules imposed can be quite different. Yet in the adult bird the two can coexist side by side."

"We have no idea how the brain manages to do this, but the outcome is reminiscent of people speaking two languages, like German and English, with different grammars -- not a small feat for birds."

Joseph Bonner | EurekAlert!
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