Scientists map neural wiring of vocal circuits in songbirds

Researchers have mapped the long-range synaptic connections involved in vocal learning in zebra finches, uncovering new details about how the brain organises learned vocalisations such as birdsong. 

The study, published today as a Reviewed Preprint in eLife, is described by the editors as having fundamental significance and compelling evidence clarifying how four distinct inputs to a specific region of the brain act on three distinct cell types to facilitate the learning and production of birdsong.

Understanding how the brain integrates sensory and motor information to guide learned vocalisations is crucial for studying both birdsong and human speech. The courtship song of male zebra finches is a well-studied example of a naturally learned behaviour, and is controlled by a set of interconnected forebrain regions in the dorsal ventricular ridge (DVR) – the avian equivalent of the mammalian neocortex. Within this network, the premotor region HVC is essential for birds to both learn songs when they are young and to produce them when they are adults. Whilst the major pathways involved in guiding birdsongs have been established, the precise synaptic-level connections between different brain areas have remained difficult to establish due to technological limitations.

“Songbirds, like humans, learn their vocalisations through imitation and practice, relying on sensory feedback to refine their songs,” explains lead author Massimo Trusel, an Instructor in the Department of Neuroscience, UT Southwestern Medical Center, Texas, US. “We set out to uncover how different sensory inputs interact with HVC in the zebra finch song network to provide a framework for understanding how the brain organises learned vocal behaviour.” 

To map the synaptic connectivity of the HVC region, Trusel and colleagues used an optimised version of optogenetic circuit mapping, which allowed them to manipulate auditory and thalamic inputs from specific brain regions one-by-one, and record the activity of the HVC circuit. They could then trace how sensory and motor information converges on the circuits responsible for song production. They examined how inputs from four main sensory pathways interact with three key HVC cell types: HVC-RA neurons, which send signals to brain areas controlling movement for singing; HVC-AV neurons, which send motor signals to auditory areas involved in processing auditory feedback; and HVC-X neurons, which connect to the basal ganglia, a region that helps with learning and adjusting song patterns.

Their findings suggest HVC is organised into highly structured neural modules that contain both projection neurons and inhibitory interneurons, working together in tightly connected networks. This indicates that HVC acts as a hub for integrating sensory and motor information, with the three types of projection neurons receiving inputs tailored to their specific role in song learning and production. Put simply, HVC-RA neurons enable the production of stable, learned songs, and HVC-X neurons are responsible for learning and modifying the song. 

The researchers also found a previously unknown connection between HVC’s presynaptic partners mMAN (medial magnocellular nucleus of the anterior nidopallium) and Av (nucleus Avalanche). This suggests that mMAN, which was previously thought to play a role in early song learning only, may also help integrate auditory feedback with motor control, allowing young birds to fine-tune their songs as they develop.

While this study provides new insights into the HVC microcircuit, which eLife’s editors say is critical for informing models of song learning and production, there are some limitations to the work. These include a potential gap in understanding the functions of developmental song learning, as the research focused on analysing the neural connections in adult birds.

“Our study provides the most detailed synaptic map to date of how different brain regions connect to HVC, a crucial centre for song learning and production,” says senior author Todd Roberts, a professor at the Department of Neuroscience, UT Southwestern Medical Center. “By revealing these wiring patterns, we’ve highlighted the synaptic networks that allow birds to structure their songs and refine their vocal skills.  The optogenetics-based mapping technique we used provides a powerful tool to explore other neural circuits, bringing us closer to understanding how songbirds achieve their remarkable vocal imitation abilities. Furthermore, because birdsong and human speech may rely on similarly organised brain circuits, this work may also pave the way to understanding more about how our brains support the learning and production of speech and language.”

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