Mechanical and morphological features of the cockroach antenna confer flexibility, reveal a kinematic chain system and predict strain information for proprioception

Abstract

A broad class of animals rely on touch sensation for perception. Among insects, the American cockroach P. americana is a touch specialist that uses a pair of soft antennae with distributed sensors to touch its environment to guide decision making. During touch, forces on the antenna can activate thousands of mechanosensors. To understand the content of this sensory information, it is critical to understand how antenna mechanics shape the transmission of contact forces. Here, we investigate the mechanical behavior and morphology of the American cockroach antenna at the individual segment level through experiments, mathematical modeling, imaging with Micro-Computed Tomography (Micro-CT), 3D reconstruction of antenna morphology, and finite element modeling (FEM). Our experimental results and model predictions reveal that the antenna flagellum bends according to a kinematic chain model, with rigid segments connected by joints. Whereas the middle region of the antenna consistently fractured under cyclic bending, the tip region remained intact under large deformations, revealing mechanical specialization along the antenna. Micro-CT imaging revealed an invagination of the exocuticle at segment intersections of the tip. To test the hypothesis that this structure can enhance flexibility and robustness, we used FEM and confirmed that the invagination allows for larger bending without structural failure (buckling). Applying FEM to a morphologically accurate kinematic chain model of the flagellum revealed the relationship between the local strain at the location of marginal sensilla and intersegment angle, predicting the information available for antenna proprioception. Taken together, these findings reveal biomechanical adaptations of insect antennae and provide a critical step toward a mechanistic understanding of touch sensation in a touch specialist. SUMMARY STATEMENTBy combining experiments, imaging and modeling, we demonstrate distinct mechanical features in the cockroach antenna and provide a framework to model the neuromechanics of the antenna in an insect touch specialist.