Low doses of a neonicotinoid insecticide modify pheromone response thresholds of central but not peripheral olfactory neurons in a pest insect

Abstract

Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids, leaving residues in the environment. There is now evidence that low doses of insecticides can have positive effects on pest insects by enhancing various life traits. Because pest insects often rely on sex pheromones for reproduction, and olfactory synaptic transmission is cholinergic, neonicotinoid residues could modify chemical communication. We recently showed that treatments with different sublethal doses of clothianidin could either enhance or decrease behavioural sex pheromone responses in the male moth, Agrotis ipsilon. We investigated now effects of the behaviourally active clothianidin doses on the sensitivity of the peripheral and central olfactory system. We show with extracellular recordings that both tested clothianidin doses do not influence pheromone responses in olfactory receptor neurons. Similarly, in vivo optical imaging does not reveal any changes in glomerular response intensities to the sex pheromone after clothianidin treatments. The sensitivity of intracellularly recorded antennal lobe output neurons, however, is upregulated by a lethal dose 20 times and downregulated by a dose 10 times lower than the lethal dose 0. This correlates with the changes of behavioural responses after clothianidin treatment and suggests the antennal lobe as neural substrate involved in clothianidin-induced behavioural changes.

An Insecticide Further Enhances Experience-Dependent Increased Behavioural Responses to Sex Pheromone in a Pest Insect

“…ipsilon males to the pheromone after a treatment with 10 ng of clothianidin are correlated with increased sensitivity of AL neurons [11]. We can therefore speculate that similar modulatory mechanisms might be involved in the two processes.…”

“…The behavioural increase of sex pheromone responses after clothianidin treatment has previously been shown to be linked with increased sensitivity of central olfactory neurons [11]. This sensitivity change could be due to the presence of specific nAchR subunits in inhibitory neurons of the olfactory pathway, which might desensitize through clothianidin treatment [47, 48].…”

“…This sensitivity change could be due to the presence of specific nAchR subunits in inhibitory neurons of the olfactory pathway, which might desensitize through clothianidin treatment [47, 48]. Alternatively clothianidin might indirectly act via modulation of dopamine levels in the brain ([11] and references therein).…”

“…The clothianidin dose of 10 ng, which corresponds to the LD20, was chosen because this dose elicited an increase in behavioural and central nervous pheromone responses in 5 day-old A . ipsilon males, treated at day 4 [11, 12]. To study age-dependence of clothianidin treatments, 1 day-old and 4 day-old males were fed 10 μl of the clothianidin solution or the corresponding DMSO solution as a control and submitted to behavioural tests 24 h later (Fig 1).…”

“…This hormetic-like effect was found to be correlated with an increase in pheromone sensitivity within the central, but not the peripheral olfactory system [11, 12]. As insect behaviour is highly plastic and depends on physiological state, i.e.…”