A sublethal dose of a neonicotinoid insecticide disrupts visual processing and collision avoidance behaviour in Locusta migratoria

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.

The cholinergic pesticide imidacloprid impairs contrast and direction sensitivity in motion detecting neurons of an insect pollinator

“…Imidacloprid, in fact, did not abolish the stimulus-evoked responses in our case as 364 seen previously in projection neurons (Andrione et al, 2016) and in the visual pre-365 motor neuron in locusta (Parkinson et al, 2017). Why then we do not observe a shut 366 down of the responses?…”

“…The dearth of studies on the effects of IMI on the visual system is surprising given 50 that many parts of the insect visual system are known potential targets for cholinergic 51 agonists. Both cholinergic neurons and nAChRs are widely expressed in the insect 52 optic lobes -both peripherally and centrally (Kreissl and Bicker, 1989;Brotz et al, 53 3 activity in intact animals previously injected with a sub-lethal dose of imidacloprid 59 compared to animals injected with its vehicle (Parkinson et al, 2017). This study is of 60 particular interest as it represents the first and only evidence of impairment in vivo in 61 the visual nervous system of an insect due to imidacloprid exposure, although where 62 and how this deficit arises in the upstream optic lobes remains unknown.…”

Modality-specific impairment of learning by a neonicotinoid pesticide

“…In the honeybee, imidacloprid can impair odour coding in antennal lobes, the first odour processing centre of the bee brain [41], and may even impair detection of volatiles upstream in antennal sensilla through action on odorant-binding proteins [42]. To our knowledge, the effects of imidacloprid on the bee visual system at an analogous peripheral or central level have not been determined (but see [43]).…”

Extremely low neonicotinoid doses alter navigation of pest insects along pheromone plumes

“…Sublethal doses of the neonicotinoid imidacloprid impair the motion-sensitive visual network of Locusta migratoria L. affecting their escape response 23 . Similarly, sublethal exposure to imidacloprid alters the motion-detection neural system of a hoverfly pollinator 30 .…”