Stratified Palliobulbar and Midbrain Circuits Control the Timing and Acoustics of Learned Vocalizations

Abstract

In mammals and birds, production of learned vocalizations depends on prominent projections from the pallium to the brainstem. Although pallial and cortical coding mechanisms for speech and birdsong are becoming increasingly clear, understanding how palliobulbar projections supervise brainstem circuits has remained challenging. Here we identify the functional organization of pallial and brainstem control of learned song in the zebra finch, a songbird in which genetic control of neuronal pathways is now feasible. We find that palliobulbar projections to the medulla and midbrain periaqueductal gray (PAG) arise from largely non-overlapping neuronal populations. Genetic silencing of these pathways reveals that projections to the medulla control the learned acoustic content defining individual song syllables, while projections to the PAG control the respiratory timing needed to sequence syllables. Using large-scale neuronal recordings, we find that song and innate calls are uniquely encoded within the PAG. Dual recordings from the palliobulbar neurons and the PAG suggest hierarchical encoding of expiratory and inspiratory events along this pathway. Lastly, genetic silencing reveals that PAG projections to the medulla are needed for birds to generate learned song and innate calls. Thus, stratified palliobulbar pathways control respiratory-timing and acoustics for song. Yet, without the PAG, they are insufficient to produce any vocalizations.