The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations

Abstract

Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To address this question, we focused on the compact neural network of Caenorhabditis elegans animals for which the full wiring diagram is available, including the coordinates of individual synapses. We find that the positions of the chemical synapses along the neurites are not randomly distributed nor can they be explained by anatomical constraints. Instead, synapses tend to form clusters, an organization that supports local compartmentalized computations. In mutually synapsing neurons, connections of opposite polarity cluster separately, suggesting that positive and negative feedback dynamics may be implemented in discrete compartmentalized regions along neurites. In triple-neuron circuits, the nonrandom synaptic organization may facilitate local functional roles, such as signal integration and coordinated activation of functionally related downstream neurons. These clustered synaptic topologies emerge as a guiding principle in the network, presumably to facilitate distinct parallel functions along a single neurite, which effectively increase the computational capacity of the neural network.

MetaWorm: An Integrative Data-Driven Model SimulatingC. elegansBrain, Body and Environment Interactions

“…Also, as shown in Fig. 4F, the constructed connections tended to cluster together, which followed the clustered organization principle in published research 13,14 .…”

“…4A). For each connection, we randomly assigned a distance following the neurite centroids distance distributions of synapse/gap junction in experiment 13 (Fig. 4B).…”

“…Distribution of distances between centroids coordinates of neurites at connected synapse (upper) and gap junction (lower) locations. Experimental data (red/blue bars) from a published paper 13 is fitted by two inverse Gaussian distributions (black/red lines). Random data (yellow/green bars) is produced following the fitted inverse Gaussian distributions.…”

“…The neuron models were connected by graded synapses 8,11 and gap junctions 12 in C. elegans neural network. Graded synapses, include excitatory and inhibitory synapses, were modeled according to published C. elegans models 4,13,14 . The synaptic conductance is continuously changed with presynaptic membrane potential.…”