A role for descending auditory cortical projections in songbird vocal learning

Abstract

Many learned motor behaviors are acquired by comparing ongoing behavior with an internal representation of correct performance, rather than using an explicit external reward. For example, juvenile songbirds learn to sing by comparing their song with the memory of a tutor song. At present, the brain regions subserving song evaluation are not known. In this study, we report several findings suggesting that song evaluation involves an avian 'cortical' area previously shown to project to the dopaminergic midbrain and other downstream targets. We find that this ventral portion of the intermediate arcopallium (AIV) receives inputs from auditory cortical areas, and that lesions of AIV result in significant deficits in vocal learning. Additionally, AIV neurons exhibit fast responses to disruptive auditory feedback presented during singing, but not during nonsinging periods. Our findings suggest that auditory cortical areas may guide learning by transmitting song evaluation signals to the dopaminergic midbrain and/or other subcortical targets.

DOI: http://dx.doi.org/10.7554/eLife.02152.001

eLife digest

Most new skills, from playing a sport to learning a language, are acquired through a gradual process of trial and error. While some of this learning is driven by direct external rewards, such as praise, much of it occurs when the individual compares their current performance with their own impression of what a ‘correct’ performance should be. The way that the brain responds to external rewards is relatively well understood, but much less is known about the processes used by the brain to evaluate its own performance.

One way to study this process is to examine how songbirds learn their songs. While in the nest, young male birds memorize another bird's song, usually that of their father. They learn to sing by comparing their own vocals with this memorized template, tweaking their song until the two versions match. Now, Mandelblat-Cerf et al. have identified a pathway in the brain that enables the birds to make this comparison and to use any discrepancies to improve their subsequent attempts.

Anatomical labeling experiments revealed that a brain structure called the arcopallium has a key role in this process. The ventral part of this structure (known as AIV) receives inputs from the auditory cortex—meaning that it has access to the bird’s own song—and then forms connections with a specific group of neurons in the midbrain. These midbrain neurons, which communicate using the chemical transmitter dopamine, project to brain regions that ultimately control the movements involved in singing. This means that the AIV is ideally positioned to be able to evaluate and then adjust the song as required.

Consistent with this possibility, young zebra finches were less able to imitate a template song if their AIV was destroyed before they had started practicing. By contrast, destroying the AIV in adult birds who had already learned their song did not impair performance, indicating that the arcopallium circuit supports song learning rather than singing per se. Finally, recordings of neurons in the AIV made during singing revealed that this brain area sends signals about discrepancies between what the young bird tries to sing and what he hears himself sing.

In addition to providing further clues as to how the songbirds learn their songs, this work also highlights the fact that dopaminergic neurons in the midbrain—which are best known for being involved in our response to external rewards such as food and drugs—also contribute to learning that is driven internally.

DOI: http://dx.doi.org/10.7554/eLife.02152.002