The multilayer connectome of Caenorhabditis elegans

TL;DR

This paper constructs a multilayer connectome for C. elegans, integrating synaptic, gap junction, and neuromodulatory networks to reveal complex topological properties and interaction modes, advancing understanding of neural communication.

Contribution

It introduces the first multilayer connectome including neuromodulatory layers, highlighting the role of extrasynaptic signalling in neural network structure and function.

Findings

Monoamine network has a disassortative star-like topology.

Rich-club of interconnected broadcasting hubs identified.

Significant interaction modes between layers modulate synaptic activity.

Abstract

Connectomics has focused primarily on the mapping of synaptic links in the brain; yet it is well established that extrasynaptic volume transmission, especially via monoamines and neuropeptides, is also critical to brain function. Here we present a draft monoamine connectome, along with a partial neuropeptide connectome, for the nematode C. elegans, based on new and published expression data for biosynthetic genes and receptors. Thus, the neuronal connectome can be represented as a multiplex network, with synaptic, gap junction, and neuromodulatory layers representing alternative modes of interneuronal interaction and with distinct network structures. In particular, the monoamine network exhibits novel topological properties, with a highly disassortative star-like structure and a rich-club of interconnected broadcasting hubs. Despite the low degree of overlap between layers, we find highly significant modes of interaction, pinpointing network locations and multilink motifs where aminergic and neuropeptide signalling modulate synaptic activity. The multilayer connectome of C. elegans represents a clear exemplar of a biological multiplex network and provides a prototype for understanding how extrasynaptic signalling can be integrated into the wired circuitry in larger brains.