The songbird connectome (OSCINE-NET.ORG): structure-function organization beyond the canonical vocal control network.

Abstract

Background: Understanding the neural basis of behavior requires insight into how different brain systems coordinate with each other. Existing connectomes for various species have highlighted brain systems essential to various aspects of behavior, yet their application to complex learned behaviors remains limited. Research on vocal learning in songbirds has extensively focused on the vocal control network, though recent work implicates a variety of circuits in contributing to important aspects of vocal behavior. Thus, a more comprehensive understanding of brain-wide connectivity is essential to further assess the totality of circuitry underlying this complex learned behavior.

Results: We present the Oscine Structural Connectome for Investigating NEural NETwork ORGanization (OSCINE-NET.ORG), the first interactive mesoscale connectome for any vocal learner. This comprehensive digital map includes all known connectivity data, covering major brain superstructures and functional networks. Our analysis reveals that the songbird brain exhibits small-world properties, with highly connected communities functionally designated as motor, visual, associative, vocal, social, and auditory. Moreover, there is a small set of significant connections across these communities, including from social and auditory sub-communities to vocal sub-communities, which highlight ethologically relevant facets of vocal learning and production. Notably, the vocal community contains the majority of the canonical vocal control network, as well as a variety of other nodes that are highly interconnected with it, meriting further evaluation for their inclusion in this network. A subset of nodes forms a "rich broker club," highly connected across the brain and forming a small circuit amongst themselves, indicating they may play a key role in information transfer broadly. Collectively, their bidirectional connectivity with multiple communities indicates they may act as liaisons across multiple functional circuits for a variety of complex behaviors.

Conclusions: OSCINE-NET.ORG offers unprecedented access to detailed songbird connectivity data, promoting insight into the neural circuits underlying complex behaviors. This data emphasizes the importance of brain-wide integration in vocal learning, facilitating a potential reevaluation of the canonical vocal control network. Furthermore, we computationally identify a small, previously unidentified circuit-one which may play an impactful role in brain-wide coordination of multiple complex behaviors.