Abstract
The sensitivity of neurons from the honey bee olfactory system to pyrethroid insecticides was studied using the patch-clamp technique on central ‘antennal lobe neurons’ (ALNs) in cell culture. In these neurons, the voltage-dependent sodium currents are characterized by negative potential for activation, fast kinetics of activation and inactivation, and the presence of cumulative inactivation during train of depolarizations. Perfusion of pyrethroids on these ALN neurons submitted to repetitive stimulations induced (1) an acceleration of cumulative inactivation, and (2) a marked slowing of the tail current recorded upon repolarization. Cypermethrin and permethrin accelerated cumulative inactivation of the sodium current peak in a similar manner and tetramethrin was even more effective. The slow-down of channel deactivation was markedly dependent on the type of pyrethroid. With cypermethrin, a progressive increase of the tail current amplitude along with successive stimulations reveals a traditionally described use-dependent recruitment of modified sodium channels. However, an unexpected decrease in this tail current was revealed with tetramethrin. If one considers the calculated percentage of modified channels as an index of pyrethroids effects, ALNs are significantly more susceptible to tetramethrin than to permethrin or cypermethrin for a single depolarization, but this difference attenuates with repetitive activity. Further comparison with peripheral neurons from antennae suggest that these modifications are neuron type specific. Modeling the sodium channel as a multi-state channel with fast and slow inactivation allows to underline the effects of pyrethroids on a set of rate constants connecting open and inactivated conformations, and give some insights to their specificity. Altogether, our results revealed a differential sensitivity of central olfactory neurons to pyrethroids that emphasize the ability for these compounds to impair detection and processing of information at several levels of the bees olfactory pathway.
Highlights
In social bees, olfaction is a key function that underlies many activities such as nursing, defense against parasites and predators, foraging, and orientation
Whereas the action of pyrethroid insecticides on voltage-gated sodium channels has already been investigated in invertebrates [22,23,24,33,34,35], data on beneficial insects such as bees are lacking, while precise molecular actions of these insecticides are needed to interpret and predict their sublethal effects, as well as those of insecticides with a similar mode of action
In antennal lobe neurons (ALNs), the first observation made with all 3 pyrethroids is a marked slowing of the tail current
Summary
Olfaction is a key function that underlies many activities such as nursing, defense against parasites and predators, foraging, and orientation. From a toxicological point of view, the study of sublethal effects of pyrethroids is a priority since subtle modifications can strongly affect highly complex organizations such as those exhibited by social bees In the honeybee, these sublethal effects include impairment of olfaction and learning performances [8,9], behavioral changes such as disorientation and desertion from the hive [10,11] that would globally lead to colony disturbance. These sublethal effects include impairment of olfaction and learning performances [8,9], behavioral changes such as disorientation and desertion from the hive [10,11] that would globally lead to colony disturbance Whereas some of these sublethal effects (especially the so called ‘knockdown’ effect) have been ascribed to their deleterious action on the peripheral nervous system, little direct evidence has been so far obtained in honeybees [12]. Some sublethal effects of pyrethroids (e.g., decrease of queen’s egg-laying) have been attributed to their action on the central nervous system [14], and in particular on neurons from the olfactory pathway, such as ALN neurons
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