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

Abstract

The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths – of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male-specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons’ wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition – however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

Functional map of the macroglomerular complex of male Helicoverpa armigera

“…These findings are consistent with previous studies examining the function of Cu from OSNs and PNs using calcium imaging and intracellular recording (Wu et al ., 2013; 2015; Kymre et al ., 2021). Z 11‐16:Ald evokes strong calcium ion activity in the Cu unit, and Z 11‐16:Ald‐sensitive PNs extend dense dendritic arborizations throughout the whole glomerulus (Wu et al ., 2013; Wu et al ., 2015; Kymre et al ., 2021). This, coupled with the findings relating to the input and output neurons responding to Z 11‐16:Ald, indicates that there is a correspondence between the primary pheromone input to and output from the Cu unit.…”

“…(2016), and intracellular recording was performed following the protocol described in Zhao and Berg (2010) and Kymre et al . (2021). In the single sensillum recording experiments, the stimulus cartridge for each compound was prepared by loading 10 μ L of 10 μ g/ μ L diluted solution onto a filter paper strip (0.8 cm × 2.6 cm), which was then placed in a glass pipette (23 cm in length) after the solvent evaporated.…”

“…Intracellular recording and staining experiments were referred to as intracellular recording and retrograde filling, which is opposite of the single sensillum recording and anterograde filling experiments mentioned above, and were performed following previously described procedures (Zhao & Berg, 2010; Kymre et al ., 2021; Sun et al ., 2022). Briefly, H. armigera was restrained in a plastic pipette with the head exposed.…”

“…Calcium imaging and intracellular recording in the MGC output neurons, projection neurons (PNs), have recently been used to elucidate the central pathway for encoding sex pheromones in H. armigera (Kymre et al ., 2021). The OSNs housed in the pheromone‐sensitive sensilla send information to the MGC units and serve as odor signal inputs for those PNs.…”

Stage-specific expression of an odorant receptor underlies olfactory behavioral plasticity in Spodoptera littoralis larvae

“…Together, they house olfactory sensory neurons (OSNs) that express the chemosensory receptors responsible for olfaction: odorant receptors (ORs) and ionotropic receptors (IRs) [13]. The axons from these OSNs innervate one or several glomeruli in the antennal lobe, before the signals are projected into the higher brain center [15,16]. Lepidoptera larvae generally have fewer sensilla and OSNs on their chemosensory organs than adults and a smaller repertoire of expressed ORs [17][18][19][20][21].…”