Mesoscopic organization reveals the constraints governing C. elegans nervous system

TL;DR

This study investigates the mesoscopic modular organization of the C. elegans nervous system, revealing that its structure is shaped by functional processing needs rather than solely by resource or efficiency constraints.

Contribution

The paper demonstrates that neuronal modules in C. elegans are influenced by functional requirements, not just by wiring cost or efficiency, and links structure to sensory-motor processing.

Findings

Modules cannot be explained by wiring cost or efficiency alone.

Neuronal network forms a distinct class compared to other efficient transport networks.

Functionally critical neurons are identified through modular connection patterns.

Abstract

One of the biggest challenges in biology is to understand how activity at the cellular level of neurons, as a result of their mutual interactions, leads to the observed behavior of an organism responding to a variety of environmental stimuli. Investigating the intermediate or mesoscopic level of organization in the nervous system is a vital step towards understanding how the integration of micro-level dynamics results in macro-level functioning. In this paper, we have considered the somatic nervous system of the nematode Caenorhabditis elegans, for which the entire neuronal connectivity diagram is known. We focus on the organization of the system into modules, i.e., neuronal groups having relatively higher connection density compared to that of the overall network. We show that this mesoscopic feature cannot be explained exclusively in terms of considerations, such as optimizing for resource constraints (viz., total wiring cost) and communication efficiency (i.e., network path length). Comparison with other complex networks designed for efficient transport (of signals or resources) implies that neuronal networks form a distinct class. This suggests that the principal function of the network, viz., processing of sensory information resulting in appropriate motor response, may be playing a vital role in determining the connection topology. Using modular spectral analysis, we make explicit the intimate relation between function and structure in the nervous system. This is further brought out by identifying functionally critical neurons purely on the basis of patterns of intra- and inter-modular connections. Our study reveals how the design of the nervous system reflects several constraints, including its key functional role as a processor of information.