Wing structure and neural encoding jointly determine sensing strategies in insect flight

PLoS Comput Biol. 2021 Aug 11;17(8):e1009195. doi: 10.1371/journal.pcbi.1009195. eCollection 2021 Aug.

Abstract

Animals rely on sensory feedback to generate accurate, reliable movements. In many flying insects, strain-sensitive neurons on the wings provide rapid feedback that is critical for stable flight control. While the impacts of wing structure on aerodynamic performance have been widely studied, the impacts of wing structure on sensing are largely unexplored. In this paper, we show how the structural properties of the wing and encoding by mechanosensory neurons interact to jointly determine optimal sensing strategies and performance. Specifically, we examine how neural sensors can be placed effectively on a flapping wing to detect body rotation about different axes, using a computational wing model with varying flexural stiffness. A small set of mechanosensors, conveying strain information at key locations with a single action potential per wingbeat, enable accurate detection of body rotation. Optimal sensor locations are concentrated at either the wing base or the wing tip, and they transition sharply as a function of both wing stiffness and neural threshold. Moreover, the sensing strategy and performance is robust to both external disturbances and sensor loss. Typically, only five sensors are needed to achieve near-peak accuracy, with a single sensor often providing accuracy well above chance. Our results show that small-amplitude, dynamic signals can be extracted efficiently with spatially and temporally sparse sensors in the context of flight. The demonstrated interaction of wing structure and neural encoding properties points to the importance of understanding each in the context of their joint evolution.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Biological Evolution
  • Biomechanical Phenomena
  • Computational Biology
  • Computer Simulation
  • Feedback, Sensory / physiology
  • Flight, Animal / physiology*
  • Insecta / anatomy & histology*
  • Insecta / physiology*
  • Manduca / anatomy & histology
  • Manduca / physiology
  • Mechanoreceptors / physiology
  • Models, Biological*
  • Models, Neurological
  • Rotation
  • Wings, Animal / anatomy & histology*
  • Wings, Animal / innervation*
  • Wings, Animal / physiology

Grants and funding

This work was supported by the Washington Research Foundation (AIW); the eScience Institute at the University of Washington (AIW); and the Air Force Office of Scientific Research awards FA9550-18-1-0114 (BWB) and FA9550-19-1-0386 (BWB, TLD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.