In this study, we propose a novel methodology to model and analyze a circuit mechanism within the Fan-shaped body (FB), a core neuropil within the Central Complex of the fruit fly. Because the Fan-shaped body plays a crucial role in controlling both sleep and arousal, we hypothesize that specific neuronal circuits within the fruit fly’s FB act as loosely coupled oscillators and provide a control mechanism for opposing behaviors like sleep and arousal. To test our hypothesis in silico we created a multi-step framework of methods for identifying neurons of interest that perform as loosely coupled oscillators in the Central Complex using a statistical pathfinding analysis, graph analysis, and simulated signal analysis approaches. Our study also leverages publicly available computational tools to identify, visualize and simulate neuronal signals to advance the understanding of neural circuit dynamics and their implications for behavior and cognitive processes. The final results leverage the Wilson-Cowan model analysis between two neuron types, one excitatory and one inhibitory, from which we elucidate how stable points demonstrated by Wilson-Cowan analysis act as neuronal attractors to drive behavior. These results can be applied to Bayesian Brain theories like the Free Energy Principle. These results also imply experimental approaches that will help interpret the functionality of pathways identified in the fly brain connectome.