Synaptic Connectivity of Sensorimotor Circuits for Vocal Imitation in the Songbird

Abstract

Birdsong is a complex and volitionally produced skilled behavior that, like speech and language, is dependent on forebrain circuits for its fluent production. The well delineated neural circuits associated with song provide a powerful system in which to study how synaptically linked networks of neurons control a natural and complex behavior. The premotor cortical analog HVC is necessary for song production and for song learning. Although the main input and output pathways of HVC have in most cases been known for decades, we still lack a detailed synaptic wiring diagram of this core circuit. Here we report our progress in building this wiring diagram. HVC has at least three non-overlapping classes of projection neurons and receives input from at least five song associated regions, totaling 15 potential synaptic pathways. Combining optogenetic stimulation of axon terminals from HVCs different afferent pathways with targeted whole-cell patch-clamp recordings of HVC projection neurons, we now provide an initial synaptic connectivity map of 12 of these potential pathways. We report on 435 whole-cell patch-clamp recordings from the 3 classes of HVC projection neurons, examining 4 different input pathways, from NIf, Uva, mMAN, Av, and mapping the polysynaptic and monosynaptic connections in each pathway. We find that the synaptic connectivity of HVCs input-output pathways is complex. Each class of projection neuron receives monosynaptic input from three of the four afferents and all in different combinations. At this stage, only one input pathway, NIf, appears to monosynaptically project onto all three classes of HVC projection neurons. We provide this initial synaptic mapping as an update for the field and will build on this wiring diagram, by updating this bioRxiv manuscript, as more data is collected, and additional pathways are characterized.

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“…The song nucleus HVC (acronym used as proper name), which is located within the NCL (Matsunaga et al., 2008), is of particular interest as it feeds information into both pathways. On the one hand, it sends projections to Area X within the striatum (AFP), and on the other hand, it sends projections to the robust nucleus (RA) within the arcopallium (PMP) (Düring et al., 2020; Trusel et al., 2022) (Figure 1).…”