Neural mechanisms underlying the emergence of rhythmic and stereotyped vocalizations in juvenile songbirds

Abstract

Complex motor behaviors in humans, such as speech, are not innate, but instead are learned. How does the brain construct neural circuits that generate these motor behaviors during learning? To understand the neural mechanisms underlying learned motor skills, I use vocal learning in songbirds as a model. While previous studies have shown that a premotor area in the songbird brain, HVC, is important for stereotyped adult song, the role of HVC in juvenile song is less known. This thesis characterizes how activity in HVC develops during song learning in juvenile birds. Early in song learning, temporal structure emerged in HVC. During the earliest vocalization of juvenile birds (subsong), HVC neurons exhibit bursts of action potentials. However, only half of the neurons show bursts that are temporally aligned to syllables, and most of these bursts are clustered around onsets of subsong syllables. Over several days, as the bird starts producing the earliest stereotyped vocalization called protosyllables, HVC neurons start exhibiting rhythmic bursts at 5-10 Hz. These rhythmic bursts are aligned to protosyllables, and bursts from different neurons are active at different latencies relative to protosyllables. Thus, as a population, HVC neurons start forming a rhythmic neural sequence. As the bird matures, multiple distinct syllable types emerge from a protosyllable. During this process, some neurons are active only during a specific syllable type ('specific neurons') while others are active during both syllable types ('shared neurons'). These shared neurons are active at similar latencies for both syllable types, and therefore form a shared neural sequence. Over development, fraction of shared neurons decrease and more neurons become specific. These results demonstrate that splitting of a neural sequence into multiple sequences underlies the emergence of a multiple syllable types. Moreover, this sequence splitting is observed during different song learning strategies, suggesting that this is a fundamental neural mechanism for song learning. This work demonstrates how the growth of a rhythmic neural sequence and its subsequence splitting gives rise to complex vocalization in songbirds. This may be a general neural mechanism in which the brain constructs neural circuits during learning of a complex motor behavior.