Structure and mechanics of cockroach antennae confer flexibility and shape strain transmission for proprioception

ABSTRACT A broad class of animals rely on touch sensation for perception. Among insects, the American cockroach (Periplaneta americana) 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 investigated the structure and mechanics of antennae of the American cockroach at the individual annulus level through experiments, modeling, imaging with micro-computed tomography (micro-CT), 3D reconstruction of antenna morphology and finite element modeling (FEM). Our data and model predictions revealed that the antenna flagellum bends according to a kinematic chain model, with annuli connected by softer joints. Whereas the middle region of the antenna consistently fractured under cyclic bending, the tip region remained intact, revealing mechanical specialization along the antenna. Micro-CT imaging revealed an invagination of the exocuticle at annulus intersections of the tip. To test the hypothesis that this structure could 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 campaniform sensilla, 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.