Abstract

Neonicotinoids are known to affect insect navigation and vision, however the mechanisms of these effects are not fully understood. A visual motion sensitive neuron in the locust, the Descending Contralateral Movement Detector (DCMD), integrates visual information and is involved in eliciting escape behaviours. The DCMD receives coded input from the compound eyes and monosynaptically excites motorneurons involved in flight and jumping. We show that imidacloprid (IMD) impairs neural responses to visual stimuli at sublethal concentrations, and these effects are sustained two and twenty-four hours after treatment. Most significantly, IMD disrupted bursting, a coding property important for motion detection. Specifically, IMD reduced the DCMD peak firing rate within bursts at ecologically relevant doses of 10 ng/g (ng IMD per g locust body weight). Effects on DCMD firing translate to deficits in collision avoidance behaviours: exposure to 10 ng/g IMD attenuates escape manoeuvers while 100 ng/g IMD prevents the ability to fly and walk. We show that, at ecologically-relevant doses, IMD causes significant and lasting impairment of an important pathway involved with visual sensory coding and escape behaviours. These results show, for the first time, that a neonicotinoid pesticide directly impairs an important, taxonomically conserved, motion-sensitive visual network.

Highlights

  • Neonicotinoid insecticides (NIs) dominate a quarter of the global pesticide market[1]

  • The lobula giant movement detector (LGMD)/descending contralateral movement detector (DCMD) pathway responds robustly to objects approaching on a direct collision course[29], with peak firing rates occurring when the object surpasses an angular threshold on the retina[30]

  • We estimated the male 48 h LD50 at 2,500 ng/g, whereas for females it could be as high as 10,000 ng/g, females were not tested over an adequate range of doses to confirm this

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Summary

Introduction

Neonicotinoid insecticides (NIs) dominate a quarter of the global pesticide market[1]. Collision avoidance behaviours and possess tractable motion-sensitive visual neurons Two of these neurons are the lobula giant movement detector (LGMD), which receives encoded visual information from retinotopic units (photoreceptors and corresponding optic lobe interneurons), and its postsynaptic partner, the descending contralateral movement detector (DCMD)[28]. The LGMD/DCMD pathway responds robustly to objects approaching on a direct collision course (looming)[29], with peak firing rates occurring when the object surpasses an angular threshold on the retina[30] These neurons encode trajectory changes[31] and maintain robust responses with the addition of complex backgrounds[32, 33]. Inhibitory synapses between neighboring retinotopic units (lateral inhibition) and between retinotopic units and the LGMD (feed forward inhibition) act to modulate and shape responses to object motion[36]

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