Experience-dependent modulation of antennal sensitivity and input to antennal lobes in male moths (Spodoptera littoralis) pre-exposed to sex pheromone

Abstract

SUMMARYSex pheromones are intraspecific olfactory signals emitted by one sex to attract a potential mating partner. Behavioural responses to sex pheromones are generally highly stereotyped. However, they can be modulated by experience, as male moths previously exposed to female sex pheromone respond with a lower threshold upon further detection, even after long delays. Here, we address the question of the neural mechanisms underlying such long-term modulation. As previous work has shown increased responses to pheromone in central olfactory neurons, we asked whether brief exposure to the pheromone increases input activity from olfactory receptor neurons. Males pre-exposed to sex pheromone exhibited increased peripheral sensitivity to the main pheromone component. Among nine antennal genes targeted as putatively involved in pheromone reception, one encoding a pheromone-binding protein showed significant upregulation upon exposure. In the primary olfactory centre (antennal lobe), the neural compartment processing the main pheromone component was enlarged after a brief pheromone exposure, thus suggesting enduring structural changes. We hypothesise that higher peripheral sensitivity following pre-exposure leads to increased input to the antennal lobe, thus contributing to the structural and functional reorganization underlying a stable change in behaviour.

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

“…In mammals oxytocin promotes a variety of social behaviors, including sexual behavior, and sexually experienced male rats have higher levels of brain oxytocin receptors as well as shorter copulation latencies compared to naïve males [7]. Prior exposure to opposite sex pheromones also can change an animal’s olfactory sensory threshold [8], [9], which may allow more rapid mate detection and increase the probability of mating success. A social environment in which there is competition for mates can have different effects on mate choice depending upon the circumstances [2], and learning via social interactions has the potential to affect sexual selection and speciation [10].…”

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

“…In S . littoralis , pre-exposure experiments and behavioural pheromone tests were performed only with sexually mature 2- to 3-day-old males and it was suggested that pre-exposure elicits a sensitization to the pheromone by enhancing peripheral and central neuron sensitivity [25, 26, 28, 39]. Here we show that the behavioural pheromone pre-exposure effect is age-independent in A .…”

“…Such a type of olfactory plasticity based on non-associative learning has been unveiled in the moth Spodoptera littoralis : a brief pre-exposure to sex pheromone enhances behavioural responses to sex pheromone 15 min and 24 h later [25, 26]. Pheromone exposure was also shown to enhance peripheral pheromone detection, central nervous pheromone responses, and to induce an increase in the volume of certain glomeruli and specifically the size of the biggest glomerulus processing the main pheromone component within the antennal lobe (AL), the primary olfactory centre, as well as in a secondary olfactory centre, the calyces of the mushroom bodies [25, 27, 28]. It is so far unknown if such pre-exposure effects are also present in other insects and if they depend on the physiological state of the insect.…”

Neurophysiological mechanisms underlying sex- and maturation-related variation in pheromone responses in honey bees (Apis mellifera)

“…Plasticity in olfactory pathway responsiveness can be an underlying factor that modulates behavioral variation over the course of an individual's life (Davis and Takahashi 1980;Davis 1984;Gadenne and Anton 2000;Gadenne et al 2001;Anderson et al 2007;Anton et al 2007; Barrozo et al 2010Barrozo et al , 2011George et al 2011;Guerrieri et al 2012;Cator et al 2013). Plasticity in the response to chemosensory cues can ensure appropriate, context-dependent responses, i.e., only responding to sex pheromones at certain times of the day or night or otherwise only when capable of mating (Shorey et al 1968).…”

“…Olfactory cues are detected, processed and classified by the olfactory system, which is similarly modularly organized in both vertebrates and invertebrates (Hansson 1999;Wyatt 2014). Modulation of behavioral responses to olfactory cues can be driven by alterations in the sensitivity of olfactory sensory neurons (OSNs) in the peripheral nervous system, as in flies and mosquitoes (Davis and Takahashi 1980;Davis 1984;Crnjar et al 1990;George et al 2011;Cator et al 2013) or noctuid moths (Anderson et al 2007; Barrozo et al 2011;Guerrieri et al 2012). Alterations can also occur in the central nervous system, during the processing and integration of odorant cue information in the antennal lobe and its neurons projecting to protocerebral neuropils, such as occurs in the moth, Agrotis ipsilon (Gadenne and Anton 2000;Gadenne et al 2001).…”