Mesoscopic organization reveals the constraints governing C. elegans nervous system
arXiv:0905.3887 · doi:10.1371/journal.pone.0009240
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.
Published version, Minor modifications, 16 pages, 9 figures
References in corpus (28)
- Fast unfolding of communities in large networks
- Statistical mechanics of complex networks
- The structure and function of complex networks
- Community structure in social and biological networks
- Modularity and community structure in networks
- Fast algorithm for detecting community structure in networks
- Efficient Behavior of Small-World Networks
- Assortative mixing in networks
- The architecture of complex weighted networks
- Functional cartography of complex metabolic networks
- Synchronization in complex networks
- Mixing patterns in networks
- Specificity and stability in topology of protein networks
- Comparing community structure identification
- The worldwide air transportation network: Anomalous centrality, community structure, and cities' global roles
- Dynamical and correlation properties of the Internet
- Community structure in directed networks
- Large-scale topological and dynamical properties of Internet
- Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems
- Extracting the hierarchical organization of complex systems
- Classes of complex networks defined by role-to-role connectivity profiles
- Betweenness centrality correlation in social networks
- Topology of biological networks and reliability of information processing
- Performance of networks of artificial neurons: The role of clustering
- Wiring cost in the organization of a biological network
- Predicting the connectivity of primate cortical networks from topological and spatial node properties
- Modularity produces small-world networks with dynamical time-scale separation
- Modular networks emerge from multiconstraint optimization
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- Developmental trajectory of Caenorhabditis elegans nervous system governs its structural organization
- Modular structure in C. elegans neural network and its response to external localized stimuli
- Modular organization enhances the robustness of attractor network dynamics
- Communities in C.elegans connectome through the prism of non-backtracking walks
- A distance constrained synaptic plasticity model of C. elegans neuronal network
- Mesoscopic architecture enhances communication across the Macaque connectome revealing structure-function correspondence in the brain
- Multiple dynamical time-scales in networks with hierarchically nested modular organization
- Closed-loop control of a modular neuromorphic biohybrid