Abstract

To maintain their speeds during navigation, insects rely on feedback from their visual and mechanosensory modalities. Although optic flow plays an essential role in speed determination, it is less reliable under conditions of low light or sparse landmarks. Under such conditions, insects rely on feedback from antennal mechanosensors but it is not clear how these inputs combine to elicit flight-related antennal behaviours. We here show that antennal movements of the honeybee, Apis mellifera, are governed by combined visual and antennal mechanosensory inputs. Frontal airflow, as experienced during forward flight, causes antennae to actively move forward as a sigmoidal function of absolute airspeed values. However, corresponding front-to-back optic flow causes antennae to move backward, as a linear function of relative optic flow, opposite the airspeed response. When combined, these inputs maintain antennal position in a state of dynamic equilibrium.

Highlights

  • When flying in unpredictable conditions, sensory cues from a single modality are often unreliable measures of the ambient environmental parameters

  • This feedback is transduced primarily by two sets of mechanosensors - the chordotonal Johnston’s organ (JO) (Gewecke, 1974) which senses a wide range of stimuli from high-frequency antennal vibrations to low-frequency ambient airflow or gravity (Yorozu et al, 2009; Dieudonneet al., 2014), and the antennal hair plates which are involved in the reflexive positioning of antennae during flight (Krishnan et al, 2012)

  • The above study provides us with insights into how the insect antennomotor system integrates the multiple sensory cues that it encounters during flight

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Summary

Introduction

When flying in unpredictable conditions, sensory cues from a single modality are often unreliable measures of the ambient environmental parameters. Reliance on optic flow may be problematic under dimly lit or overcast conditions, or when flying over lakes or deserts which present sparse visual feedback In such situations, sampling from multiple sensory cues reduces the ambiguity arising from variability in feedback from single modalities (Wehner, 2003; Sherman and Dickinson, 2004; Wasserman et al, 2015). Mechanosensory feedback from antennae has emerged as a key sensory input for insect flight (Sane et al, 2007; Yorozu et al, 2009; Krishnan et al, 2012; Fuller et al, 2014). This feedback is transduced primarily by two sets of mechanosensors - the chordotonal Johnston’s organ (JO) (Gewecke, 1974) which senses a wide range of stimuli from high-frequency antennal vibrations to low-frequency ambient airflow or gravity (Yorozu et al, 2009; Dieudonneet al., 2014), and the antennal hair plates (or Bohm’s bristles) which are involved in the reflexive positioning of antennae during flight (Krishnan et al, 2012)

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