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

Rigosi, Elisa LU and O’Carroll, David C. LU (2021) In Frontiers in Physiology 12.
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... (More)

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.

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author
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organization
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type
Contribution to journal
publication status
published
subject
keywords
contrast sensitivity, insect vision, lobula plate tangential cells, motion detection, neonicotinoid, nicotinic acetylcholine receptors, pesticides
in
Frontiers in Physiology
volume
12
article number
682489
publisher
Frontiers Media S. A.
external identifiers
  • scopus:85111270325
  • pmid:34305640
ISSN
1664-042X
DOI
10.3389/fphys.2021.682489
language
English
LU publication?
yes
id
76cd94cc-ad54-4577-913b-488dab42734a
date added to LUP
2021-08-30 16:54:59
date last changed
2024-04-20 10:24:39
@article{76cd94cc-ad54-4577-913b-488dab42734a,
  abstract     = {{<p>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.</p>}},
  author       = {{Rigosi, Elisa and O’Carroll, David C.}},
  issn         = {{1664-042X}},
  keywords     = {{contrast sensitivity; insect vision; lobula plate tangential cells; motion detection; neonicotinoid; nicotinic acetylcholine receptors; pesticides}},
  language     = {{eng}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Physiology}},
  title        = {{Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator}},
  url          = {{http://dx.doi.org/10.3389/fphys.2021.682489}},
  doi          = {{10.3389/fphys.2021.682489}},
  volume       = {{12}},
  year         = {{2021}},
}