The hourglass organization of the C. elegans connectome

Abstract

We approach the C. elegans connectome as an information processing network that receives input from about 90 sensory neurons, processes that information through a highly recurrent network of about 80 interneurons, and it produces a coordinated output from about 120 motor neurons that control the nematodes muscles. We focus on the feedforward flow of information from sensory neurons to motor neurons, and apply a recently developed network analysis framework referred to as the "hourglass effect". The analysis reveals that this feedforward flow traverses a small core ("hourglass waist") that consists of 10-15 interneurons. These are mostly the same interneurons that were previously shown (using a different analytical approach) to constitute the "rich-club" of the C. elegans connectome. This result is robust to the methodology that separates the feedforward from the feedback flow of information. The set of core interneurons remains mostly the same when we consider only chemical synapses or the combination of chemical synapses and gap junctions. The hourglass organization of the connectome suggests that C. elegans has some similarities with encoder-decoder artificial neural networks in which the input is first compressed and integrated in a low-dimensional latent space that encodes the given data in a more efficient manner, followed by a decoding network through which intermediate-level sub-functions are combined in different ways to compute the correlated outputs of the network. The core neurons at the hourglass waist represent the information bottleneck of the system, balancing the representation accuracy and compactness (complexity) of the given sensory information. Author SummaryThe C. elegans nematode is the only species for which the complete wiring diagram ("connectome") of its neural system has been mapped. The connectome provides architectural constraints that limit the scope of possible functions of a neural system. In this work, we identify one such architectural constraint: the C. elegans connectome includes a small set (10-15) of neurons that compress and integrate the information provided by the much larger set of sensory neurons. These intermediate-level neurons encode few sub-functions that are combined and re-used in different ways to activate the circuits of motor neurons, which drive all higher-level complex functions of the organism such as feeding or locomotion. We refer to this encoding-decoding structure as "hourglass architecture" and identify the core neurons at the "waist" of the hourglass. We also discuss the similarities between this property of the C. elegans connectome and artificial neural networks. The hourglass architecture opens a new way to think about, and experiment with, intermediate-level neurons between input and output neural circuits.