Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin

Abstract

SUMMARYIn the male moth, Agrotis ipsilon, mating induces a transient inhibition of behavioural and central nervous responses to sex pheromone. Newly mated males are not attracted to sex pheromone, and the sensitivity of their antennal lobe (AL) neurons is lower than in virgin males. This rapid transient olfactory inhibition prevents them from re-mating unsuccessfully until they have refilled their sex glands. We hypothesized that this olfactory 'switch off' might be controlled by neuromodulators such as biogenic amines. To test our hypothesis, we studied the effects of octopamine (OA) and serotonin (5-hydroxytryptamine, 5-HT) on the coding properties of pheromone-sensitive AL neurons in virgin and newly mated males. We show that AL neuron sensitivity increased in newly mated males after injection of OA or 5-HT, but only OA treatment affected certain response characteristics of AL neurons in virgin males. Whereas all measured AL neuron response characteristics were different between virgin and newly mated males, amine treatment in newly mated males restored only the latency and spike frequency, but not the duration of excitatory and inhibitory phases, which were initially found in virgin males. Additionally, we investigated the behavioural effects of OA and 5-HT treatments in virgin and mated males. Although OA and 5-HT enhanced the general flight activity of newly mated males, amine treatments did not restore the behavioural pheromone response of mated moths. Altogether, these results show that, although biogenic amines modulate the olfactory system in moths, OA and 5-HT are probably not involved in the post-mating inhibition of responses to sex pheromone in A. ipsilon males.

Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect

“…Interestingly, by detailed analysis of MGC neuron responses to sex pheromone, we found a clear pheromone response threshold of 1ng, indicating that at this level the pheromone starts to elicit a response in the brain of newly mated males. We have recently shown that mating indeed induced drastic changes in the responses of AL neurons to the pheromone in mated males; together with changes in spike frequency, the latency, and durations of excitatory and inhibitory phases were also changed as compared with virgin males (Barrozo et al, 2010). This could explain the observed lack of response of newly mated males in the wind tunnel: below a specific threshold, males do not detect the pheromone and therefore do not respond; above this threshold, males do detect the pheromone, which has become inhibitory.…”

“…Although biogenic amines have been shown to be involved in the modulation of pheromone sensitivity in animals including insects, octopamine and serotonin are probably not involved in the transient post-mating olfactory switch-off in A. ipsilon males (Barrozo et al, 2010). As an analogy to what is known for the lack of receptivity and pheromonostasis following mating in females, we will test the hypothesis that there could be either an inhibitory factor present or a stimulatory factor lacking in the sex accessory glands or in some part of the brain in newly mated A. ipsilon males.…”

“…Pairing experiments were performed as previously described (Barrozo et al, 2010;Gadenne et al, 2001). Briefly, virgin 5-dayold sexually mature males and virgin 3-day-old sexually mature females were individually paired in cylindrical plastic containers before the onset of scotophase in a mating room under a 16h:8h light:dark photoperiod and at 22±1°C.…”

“…The behaviour of virgin and newly mated 5-day-old male moths was observed in a 2m-long wind tunnel under the same conditions as for the mating observations (inversed 16h:8h light:dark photoperiod, 22±1°C) (Barrozo et al, 2010;Gadenne et al, 2001). Newly mated males were transferred into the wind tunnel room in the darkness (both the mating room and wind tunnel room were under inversed light regimes and separated by a dark corridor).…”

“…Each experimental male was tested only once to one stimulus and at a single dose, and then the animal was discarded. Assays were performed during 3min, and partial flight, complete flight and landing on the pheromone source were considered as an oriented response (Barrozo et al, 2010;Jarriault et al, 2009a). The proportion of males performing an oriented flight was analysed.…”