Coincidence of pheromone and plant odor leads to sensory plasticity in the heliothine olfactory system

Abstract

Male moths possess a highly specialized olfactory system comprised of two segregated sub-arrangements dedicated to processing information about plant odors and pheromones, respectively. Communication between these two sub-systems has been described at the peripheral level, but relatively little is known about putative interactions at subsequent synaptic relays. The male moth faces the challenge of seeking out the conspecific female in a highly dynamic odor world. The female-produced pheromone blend, which is a limited resource serving as guidance for the male, will reach his antennae in intermittent pockets of odor filaments mixed with volatiles from various plants. In the present study we performed calcium imaging for measuring odor-evoked responses in the uni-glomerular antennal-lobe projection neurons (analog to mitral cells in the vertebrate olfactory bulb) of Helicoverpa armigera. In order to investigate putative interactions between the two sub-systems tuned to plant volatiles and pheromones, respectively, we performed repeated stimulations with a selection of biologically relevant odors. We found that paired stimulation with a plant odor and the pheromone led to suppressed responses in both sub-systems as compared to those evoked during initial stimulation including application of each odor stimulus alone. The fact that the suppression persisted also after pairing, indicates the existence of a Hebbian-like plasticity in the primary olfactory center established by temporal pairing of the two odor stimulation categories.

A novel major output target for pheromone-sensitive projection neurons in male moths

“…Totally, 16 males (age: 2-3 days) were used to measure pheromone-evoked responses from the MGC by means of calcium imaging. Selective staining of projection neurons in H. armigera was described elsewhere (Ian et al, 2017). Briefly, the head capsule was opened after the moth was immobilized in a small plastic tube.…”

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

“…Totally, 8 males (2-3 days) were used in calcium-imaging experiments. Retrograde selective staining of MGC PNs has been reported elsewhere (Chu et al, 2020a;Ian et al, 2017;Sachse & Galizia, 2002;Sachse & Galizia, 2003). A glass electrode tip coated with Fura-2 dextran (potassium salt, 10,000 MW, Molecular Probes) was inserted into the calyces to selectively label the medial-tract PNs.…”

Plasticity and modulation of olfactory circuits in insects

“…When the two odors are presented with a time shift, the responses of AL neurons to the sex pheromone are delayed as compared to a simultaneous application (Dupuy et al 2017 ), which correlates with delayed behavioral responses. In another noctuid moth, Helicoverpa armigera , calcium imaging revealed a reduced increase of intracellular calcium levels when stimulated with a blend of sex pheromone and complex plant odors as compared to individual odor application (Ian et al 2017 ). On the other hand, synergistic responses to a mixture of sex pheromone and a volatile originating from the larval host plant, pear ester, were reported in the AL of the codling moth Cydia pomonella and well correlated with behavioral responses (Trona et al 2013 ).…”