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 and occurs primarily outside the synaptic connectome. We have mapped the putative monoamine connections, as well as a subset of neuropeptide connections, in C. elegans based on new and published gene expression data. The monoamine and neuropeptide networks exhibit distinct topological properties, with the monoamine network displaying a highly disassortative star-like structure with a rich-club of interconnected broadcasting hubs, and the neuropeptide network showing a more recurrent, highly clustered topology. Despite the low degree of overlap between the extrasynaptic (or wireless) and synaptic (or wired) connectomes, we find highly significant multilink motifs of interaction, pinpointing locations in the network where aminergic and neuropeptide signalling modulate synaptic activity. Thus, the C. elegans connectome can be mapped as a multiplex network with synaptic, gap junction, and neuromodulator layers representing alternative modes of interaction between neurons. This provides a new topological plan for understanding how aminergic and peptidergic modulation of behaviour is achieved by specific motifs and loci of integration between hard-wired synaptic or junctional circuits and extrasynaptic signals wirelessly broadcast from a small number of modulatory neurons.
Highlights
The new field of connectomics seeks to understand the brain by comprehensively mapping the anatomical and functional links between all its constituent neurons or larger scale brain regions [1]
Neural circuits depend on other types of signalling between neurons, such as extrasynaptic modulation by monoamines and peptides
The C. elegans nervous system has served as a prototype for analytical studies of connectome networks, since the synaptic connections made by each of its 302 neurons have been completely mapped at the level of electron microscopy [2, 3]
Summary
The new field of connectomics seeks to understand the brain by comprehensively mapping the anatomical and functional links between all its constituent neurons or larger scale brain regions [1]. The C. elegans nervous system has served as a prototype for analytical studies of connectome networks, since the synaptic connections made by each of its 302 neurons have been completely mapped at the level of electron microscopy [2, 3] Through this approach, the C. elegans nervous system has been found to share a number of topological features in common with most other real-world networks, from human brain networks through social networks to the internet [1, 4, 5]. One well-known example is the small-world phenomenon, whereby networks are simultaneously highly clustered (nodes that are connected to each other are likely to have many nearest neighbours in common) and highly efficient (the average path length between a pair of nodes is short) [6, 7]. For example hubs are known to play a privileged role in coordinating functions across a distributed network [11], while the short path lengths (often mediated by the hubs) help increase the efficiency of information transfer across the network [6]
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