A General Odorant Background Affects the Coding of Pheromone Stimulus Intermittency in Specialist Olfactory Receptor Neurones

Abstract

In nature the aerial trace of pheromone used by male moths to find a female appears as a train of discontinuous pulses separated by gaps among a complex odorant background constituted of plant volatiles. We investigated the effect of such background odor on behavior and coding of temporal parameters of pheromone pulse trains in the pheromone olfactory receptor neurons of Spodoptera littoralis. Effects of linalool background were tested by measuring walking behavior towards a source of pheromone. While velocity and orientation index did drop when linalool was turned on, both parameters recovered back to pre-background values after 40 s with linalool still present. Photo-ionization detector was used to characterize pulse delivery by our stimulator. The photo-ionization detector signal reached 71% of maximum amplitude at 50 ms pulses and followed the stimulus period at repetition rates up to 10 pulses/s. However, at high pulse rates the concentration of the odorant did not return to base level during inter-pulse intervals. Linalool decreased the intensity and shortened the response of receptor neurons to pulses. High contrast (>10 dB) in firing rate between pulses and inter-pulse intervals was observed for 1 and 4 pulses/s, both with and without background. Significantly more neurons followed the 4 pulses/s pattern when delivered over linalool; at the same time the information content was preserved almost to the control values. Rapid recovery of behavior shows that change of perceived intensity is more important than absolute stimulus intensity. While decreasing the response intensity, background odor preserved the temporal parameters of the specific signal.

Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth

“…The resolution of pulsed pheromone stimuli further improved when heptanal was added, especially for A2 neurons, because of the shortening of the E1 phase and the lengthening of the following inhibition. In S. littoralis, an improvement of pulse resolution in pheromone specific ORNs was also found when pheromone stimuli were applied in a plant odour background (Party et al, 2009;Rouyar et al, 2011). The contrast enhancement between the single spike trains emitted in response to the discontinuous mixture signal in A2 neurons in A. ipsilon is amplified at the neuron population scale.…”

“…In virgin males of the noctuid moth Agrotis ipsilon, an increase of responses to the flower volatile heptanal was found in AL neurons of the OG when adding the sex pheromone (Barrozo et al, 2010). Most of these studies [except on the peripheral level (Party et al, 2009;Rouyar et al, 2011)] on mixtures of sex pheromone and plant odours were performed using individual stimulations of odours, thus revealing static aspects (e.g. synergy and inhibition) of odour mixture perception.…”

Glomerular interactions in olfactory processing channels of the antennal lobes

“…In this case, plant odorants interfere with the signaling process of the major sex-pheromone component at the receptor level indicating that plant odorants in the environment can reduce the activity of pheromone-specific olfactory receptor cells and might also impair mate finding. Similarly, in Spodoptera littoralis , linalool as a background (i.e., nonspecific) odorant reduces the maximum firing rate of pheromone-sensitive olfactory receptor cells in response to a pheromone pulse (Party et al 2009; Rouyar et al 2011). However, the odorant background ensures preservation of temporal character of a pulsed olfactory signal, irrespective of effects on response intensity which can enhance mate location at high pheromone density close to a pheromone source (Rouyar et al 2011).…”

“…Similarly, in Spodoptera littoralis , linalool as a background (i.e., nonspecific) odorant reduces the maximum firing rate of pheromone-sensitive olfactory receptor cells in response to a pheromone pulse (Party et al 2009; Rouyar et al 2011). However, the odorant background ensures preservation of temporal character of a pulsed olfactory signal, irrespective of effects on response intensity which can enhance mate location at high pheromone density close to a pheromone source (Rouyar et al 2011). This confirms findings that pheromone detection by moth olfactory receptor cells is influenced by odorant compounds in the environment and these odorants can affect the ability of pheromone-sensitive olfactory receptor cells to code temporal parameters of the pheromone signal.…”

“…This confirms findings that pheromone detection by moth olfactory receptor cells is influenced by odorant compounds in the environment and these odorants can affect the ability of pheromone-sensitive olfactory receptor cells to code temporal parameters of the pheromone signal. The most frequent type of interaction between general odorants and pheromone appears to be mixture suppression (Party et al 2009; Rouyar et al 2011). Even in situations where a cognate pheromone component and a non-cognate odorant (other conspecific/heterospecific pheromone component or host plant volatile) are used as stimuli, mixture suppression can occur as in H. virescens (Hillier and Vickers 2011).…”