Do you remember the first time you played tennis? Before even picking up a racket, you probably watched somebody else hit the ball and imagined all of the movements that you needed to make in order to do this yourself. The process by which we learn through observation of others has been associated with the acquisition of a range of complex skilled behaviors in humans as well as some animal species. Zebra finches, for instance, learn to produce their songs by listening to and trying to imitate a tutor, usually their father. In a recently published report (Vallentin et al., 2016), we examined the changes in the songbird brain that occur throughout development, and we discovered a synaptic mechanism that is critical for shaping observational learning for singing behavior.

In our study, we used juvenile zebra finches that were still learning their songs and carefully tracked their performance by comparing the songs that they produced with that of their tutor. Some birds learned quickly and imitated their tutor at an early age, while others needed more time to acquire this skill. We performed in vivo recordings while the juvenile birds listened to their tutor’s song. We focused on the HVC, a cortical region that is important for song production and contains premotor neurons that influence song-related musculature and a range of local circuit inhibitory interneurons. Simply hearing the father’s song activates the same premotor neurons that the zebra finch will eventually use to produce his own song. Once the song had been mastered, however, premotor neurons stopped responding to the tutor song. In further experiments, we found that the responses to the tutor song were being actively suppressed by synaptic inhibition.

To learn more about this inhibitory suppression, we directly measured the activity of inhibitory interneurons within the HVC and used two-photon targeted voltage-clamp recordings to measure inhibitory currents onto premotor neurons. In both cases, we found that the suppression of the tutor song through HVC inhibition was more strongly correlated with learning rather than developmental age. As the bird acquires his song and establishes his ideal motor program, this circuit became increasingly protected from any outside influences.

To address whether this inhibition can be localized to specific pieces of the song, we trained zebra finches with a synthetic tutor song consisting of four identical syllables “AAAA.” After the birds managed to copy syllable “A” well, we extended the tutor song by adding syllable “B” (“ABAB”). At that point, the bird will be fluent in “A” but still clumsy in his production of “B.” We found that inhibition was selectively stronger during syllable “A” versus syllable “B,” suggesting that inhibition suppresses individual pieces of a motor sequence that the juvenile zebra finch has already mastered and protecting them from further parental influence.

Our findings strongly implicate a specific inhibitory synaptic contact as a “gate” for motor learning in the songbird, suggesting a possible target to make these brain circuits available once again for the learning of new songs.

—Daniela Vallentin, PhD

Read the paper “Inhibition protects acquired song segments during vocal learning in zebra finches” in Science, published January 15, 2016.