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

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 pollinat...

Full description

Bibliographic Details
Main Authors: Elisa Rigosi, David C. O’Carroll
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2021.682489/full
id doaj-3b0cf53f106c4580950171b8ddf2e108
record_format Article
spelling doaj-3b0cf53f106c4580950171b8ddf2e1082021-07-09T15:14:59ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2021-07-011210.3389/fphys.2021.682489682489Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect PollinatorElisa RigosiDavid C. O’CarrollCholinergic 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.https://www.frontiersin.org/articles/10.3389/fphys.2021.682489/fullpesticidesmotion detectioncontrast sensitivityinsect visionlobula plate tangential cellsnicotinic acetylcholine receptors
collection DOAJ
language English
format Article
sources DOAJ
author Elisa Rigosi
David C. O’Carroll
spellingShingle Elisa Rigosi
David C. O’Carroll
Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
Frontiers in Physiology
pesticides
motion detection
contrast sensitivity
insect vision
lobula plate tangential cells
nicotinic acetylcholine receptors
author_facet Elisa Rigosi
David C. O’Carroll
author_sort Elisa Rigosi
title Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
title_short Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
title_full Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
title_fullStr Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
title_full_unstemmed Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator
title_sort acute application of imidacloprid alters the sensitivity of direction selective motion detecting neurons in an insect pollinator
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2021-07-01
description 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.
topic pesticides
motion detection
contrast sensitivity
insect vision
lobula plate tangential cells
nicotinic acetylcholine receptors
url https://www.frontiersin.org/articles/10.3389/fphys.2021.682489/full
work_keys_str_mv AT elisarigosi acuteapplicationofimidaclopridaltersthesensitivityofdirectionselectivemotiondetectingneuronsinaninsectpollinator
AT davidcocarroll acuteapplicationofimidaclopridaltersthesensitivityofdirectionselectivemotiondetectingneuronsinaninsectpollinator
_version_ 1721310136634441728