Monoaminergic Systems in Flight-Induced Potentiation of Phonotactic Behavior in Female Crickets

We have recently shown that experience of flight remarkably enhanced subsequent terrestrial phonotaxis in females in response to the male calling song. Here, we elucidated the possible roles of octopamine and serotonin in the enhancing effect of flying on phonotactic behavior. Octopamine is known to be released into the hemolymph during flight in insects; however, the octopamine receptor antagonist epinastine did not abolish the effects of flight in our study. On the contrary, the drug significantly potentiated the influence of flying on phonotactic behavior. The octopamine receptor agonist chlordimeform, at a concentration of 2 mM, which was previously found to activate aggression in crickets, dramatically reduced the phonotactic response. However, at a 10-times-lower dose, chlordimeform produced a light but significant decrease in the time that females took to reach the source of the calling song. A similar effect was produced by octopamine itself, which hardly passes the blood-brain barrier in insects. The effect of flight was completely abolished in female crickets treated with alpha-methyl tryptophan (AMTP). AMPT suppresses the synthesis of serotonin, decreasing its content in the nervous systems of insects, including crickets. An activation of the serotonin synthesis with 5-hydroxytryptophan mimicked the effect of flight by increasing the number of visits to and the time spent in the zone near the source of the calling song. The 5-HT content in the third thoracic ganglion was significantly higher in flyers compared to the control group. In contrast, no changes in the octopamine level were observed in the third thoracic ganglion, which is known to play a crucial role in decision-making involved in intraspecific interactions. Therefore, the results suggest that although octopamine is known to be released into the hemolymph during flight, it is likely to inhibit rather than activate the central mechanisms related to phonotaxis. The weak facilitating effect of a low dose of chlordimeform can be attributed to the activation of peripheral octopaminergic receptors. Our results suggest that the serotoninergic system may contribute to the facilitation of female phonotactic behavior by flying. We suggest that both flying and serotonin enhance sexual motivation in females and, by these means, impact their behavioral response to the male calling song.