Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator.

Elisa Rigosi,David C O’Carroll

doi:10.3389/fphys.2021.682489

Abstract

Cholinergic pesticides, such as the neonicotinoid imidacloprid, are the most important insecticides used for plant protection worldwide. In recent decades, concerns have been raised about side effects on non-target insect species, including altered foraging behavior and navigation. Although pollinators rely on visual cues to forage and navigate their environment, the effects of neonicotinoids on visual processing have been largely overlooked. To test the effect of acute treatment with imidacloprid at known concentrations in the brain, we developed a modified electrophysiological setup that allows recordings of visually evoked responses while perfusing the brain in vivo. We obtained long-lasting recordings from direction selective wide-field, motion sensitive neurons of the hoverfly pollinator, Eristalis tenax. Neurons were treated with imidacloprid (3.9 μM, 0.39 μM or a sham control treatment using the solvent (dimethylsulfoxide) only. Exposure to a high, yet sub-lethal concentration of imidacloprid significantly alters their physiological response to motion stimuli. We observed a general effect of imidacloprid (3.9 μM) increasing spontaneous activity, reducing contrast sensitivity and giving weaker directional tuning to wide-field moving stimuli, with likely implications for errors in flight control, hovering and routing. Our electrophysiological approach reveals the robustness of the fly visual pathway against cholinergic perturbance (i.e., at 0.39 μM) but also potential threatening effects of cholinergic pesticides (i.e., evident at 3.9 μM) for the visual motion detecting system of an important pollinator.

Highlights

Major ongoing debate concerns the off-target effects on animal populations of widely used agrichemicals including neonicotinoid pesticides, such as imidacloprid
An inclusion criterion for our classification of recorded neurons as lobula plate tangential cells (LPTCs) was that they were motion opponent i.e., their spontaneous activity was inhibited by stimuli in the antipreferred direction (Figure 2)
We observed a large increase in the response to anti-preferred direction stimuli only for the units exposed to 3.9 μM IMI

Summary

Introduction

Major ongoing debate concerns the off-target effects on animal populations of widely used agrichemicals including neonicotinoid pesticides, such as imidacloprid (recently reviewed in bees in Alkassab and Kirchner, 2017; Wood and Goulson, 2017; Sgolastra et al, 2020). Prior work on the neurophysiological effects of these chemicals have primarily utilized cultured cells and isolated brain preparations (see for example: Buckingham et al, 1997; Déglise et al, 2002; Jepson et al, 2006; Barbara et al, 2008; Palmer et al, 2013; Wilson et al, 2013; Benzidane et al, 2017) While these in vitro approaches certainly help in identify effective sites of action, they provide little information on how neuronal function is affected in the whole living organism in the presence of relevant external sensory stimuli. There had been only few attempts to redress this deficiency in vivo, for example, a calcium imaging study recorded odor-evoked responses from the antennal lobe of the intact honey bee and revealed impaired odor processing when the brain was exposed to an acute dose of IMI (Andrione et al, 2016)

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Conclusion