Schulz Julia, Franz Hanna R, Deimel Stephan H, Widmann Annekathrin
Department of Molecular Neurobiology of Behavior, University of Göttingen, Göttingen, Germany.
Front Physiol. 2024 Mar 14;15:1363943. doi: 10.3389/fphys.2024.1363943. eCollection 2024.
Neonicotinoid insecticides, the fastest-growing class in recent decades, interfere with cholinergic neurotransmission by binding to the nicotinic acetylcholine receptor. This disruption affects both targeted and non-targeted insects, impairing cognitive functions such as olfaction and related behaviors, with a particular emphasis on olfactory memory due to its ecological impact. Despite the persistent presence of these chemicals in the environment, significant research gaps remain in understanding the intricate interplay between cognitive function, development, neuronal activity, and neonicotinoid-induced toxicity. This study focuses on the fruit fly , chosen for its genetic tractability, well-characterized neural circuitry, and remarkable parallels with bees in neurotransmitter systems and brain structures. Our aim is to establish the fruit fly as a valuable model organism for studying the effects of neonicotinoids on behavior and neuronal circuitry, with particular attention to olfactory memory and associated brain circuitries. To achieve this aim, we conducted experiments to investigate the effects of short-term exposure to sublethal doses of the neonicotinoid imidacloprid, mimicking realistic environmental insecticide exposure, on the formation of odor memories. Additionally, we evaluated synaptic contacts and cholinergic neurotransmission within the mushroom body, the primary memory network of insects. Our results showed significant impairments in odor memory formation in flies exposed to imidacloprid, with exposure during the adult stage showing more pronounced effects than exposure during the larval stage. Additionally, functional studies revealed a decrease in synaptic contacts within the intrinsic olfactory projection neurons and the mushroom body. Furthermore, another experiment showed an odor-dependent reduction in cholinergic neurotransmission within this network. In summary, employing as a model organism provides a robust framework for investigating neonicotinoid effects and understanding their diverse impacts on insect physiology and behavior. Our study initiates the establishment of the fruit fly as a pivotal model for exploring neonicotinoid influences, shedding light on their effects on olfactory memory, neuronal integrity, and synaptic transmission.
新烟碱类杀虫剂是近几十年来增长最快的一类杀虫剂，它通过与烟碱型乙酰胆碱受体结合来干扰胆碱能神经传递。这种干扰会影响目标昆虫和非目标昆虫，损害嗅觉等认知功能以及相关行为，由于其对生态的影响，尤其着重于嗅觉记忆。尽管这些化学物质在环境中持续存在，但在理解认知功能、发育、神经元活动和新烟碱类诱导的毒性之间复杂的相互作用方面，仍存在重大研究空白。本研究聚焦于果蝇，因其具有遗传易处理性、特征明确的神经回路，以及在神经递质系统和脑结构方面与蜜蜂有显著相似之处。我们的目标是将果蝇确立为一种有价值的模式生物，用于研究新烟碱类对行为和神经回路的影响，特别关注嗅觉记忆和相关脑回路。为实现这一目标，我们进行了实验，以研究短期暴露于亚致死剂量的新烟碱类杀虫剂吡虫啉（模拟现实环境中的杀虫剂暴露）对气味记忆形成的影响。此外，我们评估了昆虫主要记忆网络蘑菇体内的突触联系和胆碱能神经传递。我们的结果表明，暴露于吡虫啉的果蝇在气味记忆形成方面有显著损伤，成年期暴露比幼虫期暴露表现出更明显的影响。此外，功能研究显示，内在嗅觉投射神经元和蘑菇体内的突触联系减少。此外，另一项实验表明，该网络内胆碱能神经传递存在气味依赖性降低。总之，将果蝇用作模式生物为研究新烟碱类的影响以及理解它们对昆虫生理和行为的多种影响提供了一个有力的框架。我们的研究开启了将果蝇确立为探索新烟碱类影响的关键模式的进程，揭示了它们对嗅觉记忆、神经元完整性和突触传递的影响。
