Graph-theoretic analysis on the bilateral symmetry and asymmetry in the nervous system

Abstract

This study investigates the intricate balance between bilateral symmetry and asymmetry in the nervous system, exploring the tradeoff between redundancy and functional diversity. Focusing on the nematode roundworm Caenorhabditis elegans and Drosophila larvae as model systems due to its well-specified and thoroughly studied neural connectome, our research employs a three-phase approach: 1. Graph-Theoretic Analysis of Redundancy Measures: Examination of graph-theoretic measures associated with redundancy in the C. elegans connectome. 2. Quantification of Symmetry and Classification of Functional Asymmetries: Utilization of degeneracy measures to quantify symmetry and classify functional asymmetries within the C. elegans connectome. 3. Redundancy Analysis Across Networks: Analysis of redundancy in C. elegans sub-network connectomes and Drosophila larvae connectome. Our findings reveal a high degree of bilateral symmetry in the connectomes, facilitating contralateral compensation for global information flow and promoting similar functionalities between neuron pairs. Simultaneously, network asymmetry prevents complete redundancy, preserving the capacity for diverse functions and suggesting a mechanism of high degeneracy in the network, ensuring robustness and diversity in neural wiring. Subsystem analysis indicates interneuron systems exhibit high bilateral redundancy, sensory systems display lateralization, and the motor system remains unbiased. Furthermore, the application of degeneracy measures has successfully classified functionally asymmetric neurons, notably ASE and AWC, in both sexes of C. elegans. Our analysis has revealed both commonalities, such as IL1D and AIM, and differences in the classification of asymmetric neurons between hermaphrodite (HSN) and male (BAG) C. elegans connectomes. To assess the significance of these asymmetric connections, we conducted a vulnerability analysis, shedding light on potential biological roles for the classified asymmetric neurons. This comprehensive analysis provides valuable insights into the design principles of neural networks, emphasizing the delicate balance between symmetry and asymmetry in achieving adaptability and functionality. Furthermore, the study suggests a deeper understanding of the role of asymmetry in neural processes and unveils previously unknown asymmetric functions.