Diverging network architecture of the $\textit{C. elegans}$ connectome and signaling network

Abstract

The connectome describes the complete set of synaptic contacts through which neurons communicate. While the architecture of the $\textit{C. elegans}$ connectome has been extensively characterized, much less is known about the organization of causal signaling networks arising from functional interactions between neurons. Understanding how effective communication pathways relate to or diverge from the underlying structure is a central question in neuroscience. Here, we analyze the modular architecture of the $\textit{C. elegans}$ signal propagation network, measured via calcium imaging and optogenetics, and compare it to the underlying anatomical wiring measured by electron microscopy. Compared to the connectome, we find that signaling modules are not aligned with the modular boundaries of the anatomical network, highlighting an instance where function deviates from structure. However, we find that some of the most striking features of the anatomical network are preserved, as exemplified by the pharynx, which is delineated into a separate community in both anatomy and signaling. We analyze the cellular compositions of the signaling architecture and find that its modules are enriched for specific cell types and functions, suggesting that the network modules are neurobiologically relevant. Lastly, we identify a "rich club" of hub neurons in the signaling network. The membership of the signaling rich club differs from the rich club detected in the anatomical network, challenging the view that structural hubs occupy positions of influence in functional (signaling) networks. Our results provide new insight into the interplay between brain structure, in the form of a complete synaptic-level connectome, and brain function, in the form of a system-wide causal signal propagation atlas.