The C. elegans Connectome Consists of Homogenous Circuits with Defined Functional Roles

Abstract

A major goal of systems neuroscience is to decipher the structure-function relationship in neural networks. Here we study network functionality in light of the common-neighbor-rule (CNR) in which a pair of neurons is more likely to be connected the more common neighbors it shares. Focusing on the fully-mapped neural network of C. elegans worms, we establish that the CNR is an emerging property in this connectome. Moreover, sets of common neighbors form homogenous structures that appear in defined layers of the network. Simulations of signal propagation reveal their potential functional roles: signal amplification and short-term memory at the sensory/inter-neuron layer, and synchronized activity at the motoneuron layer supporting coordinated movement. A coarse-grained view of the neural network based on homogenous connected sets alone reveals a simple modular network architecture that is intuitive to understand. These findings provide a novel framework for analyzing larger, more complex, connectomes once these become available.

Structural and developmental principles of neuropil assembly inC. elegans

“…The lineage, morphology and synaptic connectivity of all 181 neurites is known 3,8 . While connectomic analyses have revealed network principles and circuit motifs [9][10][11][12][13][14][15][16][17][18][19][20][21][22] , we still lack an understanding of the design principles that underlie nerve ring neuropil architecture and function, and the developmental sequence that forms this functional architecture.…”

Phase transitions in evolutionary dynamics

“…This seems particularly appealing for biological networks like brain and protein-protein interaction networks, but also in the tumor initiation process within healthy tissues as proposed in [17]. Most graph structures reduce in a very slight amount the advantage of a invading mutant, but some suppression mechanisms could be amplified by repetitive rules (such as those described in [18] and [19] for neuronal networks) involved in the modular architecture of many biological networks.…”

Hub connectivity, neuronal diversity, and gene expression in theC. elegansconnectome

“…The chemical synapse network is both directed (i.e., the pre-synaptic and post-synaptic neurons are identified) and weighted (as the number of synapses from one neuron to another), while gap junctions are conventionally represented as weighted (as the number of electrical synapses connecting two neurons), undirected connections. Previous investigations of C. elegans neuronal connectivity have used differently processed versions of these data, including: (i) only chemical synapses [48]; (ii) a combination of chemical and electrical synapses as a directed network (electrical synapses represented as reciprocal connections) [49,50]; (iii) a combination of chemical and electrical synapses as an undirected network (representing unidirectional and reciprocal chemical connections equivalently) [28,51,52,53]; or (iv) comparing multiple connectome representations [54]. Our analysis here focuses on the combined directed, binary network, treating gap junctions as bidirectional connections.…”

“…Fig. S1 of [49]). Unlike network analyses of mammalian brains, where all neurons are confined to a spatially contiguous organ, neurons of the C. elegans nervous system are distributed throughout the entire organism, forming a dense cluster of 147 neurons in the head (all within 130 µm), 105 sparser neurons in the body (spanning 1.02 mm), which are predominantly motor neurons (75%), and another dense cluster of 27 neurons in the tail (all within 90 µm of each other), as plotted in Fig.…”

“…3 for each combination of source and target neuron labels, across 10 equiprobable distance bins (with exponential fits added for visualization). Distinguishing connections by source and target neuron types uncovers clear spatial relationships (that are obscured when all connections are grouped, as in [49]), that differ across connection classes. From the very short distance scale of 100 µm of head→head and tail→tail connections to the very longest-range head→tail and tail→head connections ( 1 mm), connection probability decreases with separation distance (Fig.…”