Two types of sensory proliferation patterns underlie the formation of spatially tuned olfactory receptive fields in the cockroach Periplaneta americana

Abstract

In the cockroach Periplaneta americana, to represent pheromone source in the receptive space, axon terminals of sex pheromone-receptive olfactory sensory neurons (pSNs) are topographically organized within the primary center, the macroglomerulus, according to the peripheral locations of sex pheromone-receptive single walled (sw)-B sensilla. In this study, we sought to determine when and where pSNs emerge in the nymphal antenna. We revealed two different pSN proliferation patterns that underlie the formation of topographic organization in the macroglomerulus. In nymphal antennae, which lack sw-B sensilla, pSNs are identified in the shorter sensilla, termed sw-A sensilla. Because new sw-A sensilla emerge on the proximal antenna at every molt, topographic organization in the macroglomerulus must be formed by adding axon terminals of newly emerged pSNs to the lateral region in the macroglomerulus at each molt. At the final molt, a huge number of new sw-B sensilla appeared throughout the whole antenna. Sw-B sensilla in the proximal part of the adult antenna were newly formed during the last instar stage, whereas those located in the distal antenna were transformed from sw-A sensilla. This transformation was accompanied by an increase in the number of pSNs. Axon terminals of newborn pSNs in new sw-B sensilla were recruited to the lateral part of the macroglomerulus, whereas those of newborn pSNs in transformed sw-B sensilla were recruited to the macroglomerulus according to the sensillar location. These mechanisms enable an increase in sensitivity to sex pheromone in adulthood while retaining the topographic map formed during the postembryonic development.

Sensory neurons that respond to sex and aggregation pheromones in the nymphal cockroach

“…Although the antennae of nymphal cockroaches lack sw-B sensilla 17,27,28 , previous studies suggested that nymphal cockroaches sense sex pheromones as follows. First, the A-and B-glomeruli are formed during early development, and the volumes of these glomeruli gradually increase at every moult concomitantly with the elongation of the antennae [28][29][30] . Second, the nymphal antennae exhibit weak but reliable electroantennogram responses to sex pheromones [31][32][33] .…”

“…Third, later instar nymphs have PB-PNs that have dendrites in the nymphal B-glomerulus 34 . Finally, a large majority of nymphal sw-A sensilla are transformed into sw-B sensilla at the final moult, and some OSNs in the nymphal sw-A sensilla extend their axon terminals into the A-and B-glomeruli 28 . Therefore, nymphal sw-A sensilla may be able to detect sex pheromones.…”

Coding of odour and space in the hemimetabolous insect Periplaneta americana

“…Even if not statistically significant, this observation is coherent with previous electrophysiological observations, which showed that uPNs responsive to distal pheromone stimuli respond with about 60% (Hosl 1990) or 75% (Nishino 2018) of the intensity of uPNs responsive to proximal stimuli. This effect is likely due to a decrease in sensillar density along the cockroach antenna, thus to a smaller population of responsive neurons (Hösl, 1990; Watanabe et al, 2018).…”

“…With calcium imaging analysis, we could detect a clear response to a plume of odorant localized a few millimetres from the head, but almost no activity when the odour plume was presented to a more distal antennal section. This effect can be explained only partially by the decrease in sensillar density along the antenna from proximal to distal (Hösl, 1990; Watanabe et al, 2018). Indeed, olfactory sensilla density may explain up to 2-fold decrease in sensitivity along the antenna, but not the 5-to-10-fold signal decrease that we observed ( Fig.…”

“…Hence, the basic structures of the brain are established during embryogenesis, and gradually increase in volume during multiple post-embryonic moults. At each moult, new antennal segments are added proximally to the head, together with new OSNs (Schafer and Sanchez, 1973; Watanabe et al, 2018). As shown for the macroglomerulus (Nishino et al, 2018) and suggested for common glomeruli (Nishino and Mizunami, 2007), OSNs axons descend along the antennal nerve and terminate onto the antennal lobe glomeruli, forming segment (thus age)-specific layers of OSNs terminals from the core to the cortex of each glomerulus, producing an antennotopic innervation (Nishino et al, 2018).…”