Animals rely on olfaction to navigate through complex olfactory landscapes, but the mechanisms that allow an animal to encode the spatial structure of an odorous environment remain unclear. To acquire information about the spatial distribution of an odorant, animals may rely on bilateral olfactory organs and compare side differences of odor intensity and timing [1-6] or may perform spatial and temporal signal integration of subsequent samplings [7]. The American cockroach can efficiently locate a source of sex pheromone even after the removal of one antenna, suggesting that bilateral comparison is not a prerequisite for odor localization in this species [8, 9]. Cognate olfactory sensory neurons (OSNs) originating from different locations on the flagellum, but bearing the same olfactory receptor, converge onto the same glomerulus within the antennal lobe, which is thought to result in a loss of spatial information. Here, we identified 12 types of pheromone-responsive projection neurons (PNs), each with spatially tuned receptive field. The combination of (1) the antennotopic organization of OSNs terminals and (2) the stereotyped compartmentalization of PNs' dendritic arborization within the macroglomerulus (MG), allows encoding the spatial position of the pheromone. Furthermore, each PN type innervates a different compartment of the mushroom body, providing the means for encoding spatial olfactory information along the olfactory circuit. Finally, MG PNs exhibit both excitatory and inhibitory spatial receptive fields and modulate their responses based on changes in stimulus geometry. In conclusion, we propose a mechanism for encoding information on the spatial distribution of a pheromone, expanding both our understanding of odor coding and of the strategies insects adopt to localize a sexual mate.
In many insect species, sex pheromone is processed by specific, enlarged glomeruli in the antennal lobes of males. In the male American cockroach, two closely located glomeruli (A and B) are responsible for processing the major pheromone components (periplanone-A and -B, respectively), and these collectively form the macroglomerular complex. Afferents originating from the dorsal and ventral surfaces of the antenna tend to project to the anterior and posterior regions of the macroglomerular complex via the dorsal and ventral antennal nerves, respectively. This topographic segregation of afferents is seen only in the macroglomerular complex, and not in other glomeruli that process normal environmental odors. Using differential, anterograde dye injection into the two antennal sensory nerves, we show that the macroglomerular complex is not formed by fusion of several glomeruli, as suggested in previous studies. but that the precursors of the A- and B-glomeruli already exist in the first larval instar. The volume of afferents in the macroglomerular complex precursor increases nearly exponentially with molting times. 430-fold from the first instar to the adult. The A- and B-glomeruli both undergo continuous growth during postembryonic development, but peak growth rates occur in different larval stages. The growth rate of the B-glomerulus peaked in the mid-developmental stage then declined, while growth of A-glomerulus was maintained at low level in early- to mid-developmental stages but increased greatly in later stages. These results suggest perception of sex pheromone occurs in early instars, and that PA and PB have distinct roles in different developmental stages
In most insects, sex pheromone is processed by an enlarged glomerular complex (macroglomerular complex, MGC) in the male antennal lobe (first-order olfactory center). The MGC of the American cockroach consists of two closely located A- and B-glomeruli which are responsible for processing the major sex pheromone components, periplanone-A and -B, respectively. Using anterograde dye injection, we investigated sexual dimorphism in sensory afferents and interneuron. The A- and B-glomeruli exist in the first larval instar of both sexes. The female MGC homolog grows at a relatively constant rate (1.2-1.8-fold growth per molt) throughout development, whereas the male MGC shows a period of accelerated growth between the 5th and 9th instars, where volume can be more than double in a single molt. These different growth patterns resulted in a 1:30 ratio in glomerular complex volumes of adult females versus males. In the female MGC-homolog, afferents originating from the dorsal and ventral antennal surfaces were biased toward anterior and posterior regions, and segregation of these afferents was less clear compared to the adult male. The staining of interneurons projecting to the protocerebrum revealed that projection patterns characteristic of sex pheromone processing appear in the late 8th instar in males, while possibly homologous projections in the female were far fewer in number. These results suggest that the glomerular complexes in pre-8th larval males, and probably females, are not differentiated for specific detection of sex pheromone. Male-specific projections for sex pheromone detection may be formed by modification of pre-existing neural circuitry
Antennae are one of the major organs to detect chemo- and mechanosensory cue in crickets. Little is known how crickets process and integrate different modality of information in the brain. We thus used a number of different anatomical techniques to gain an understanding of the neural pathways extending from the antennal sensory neurons up to centers in the brain. We identified seven antennal sensory tracts (assigned as T1–7) utilizing anterograde dye filling from the antennal nerve. Tracts T1–T4 project into the antennal lobe (AL), while tracts T5 and T6 course into the dorsal region of the deutocerebrum or the suboesophageal ganglion, and finally, tract T7 terminates in the ventral area of flagellar afferent (VFA). By analyzing autofluorescence images of the AL, we identified 49 sexually isomorphic glomeruli on the basis of shape, relative position and size. On the basis of our sensory-tract data, we assigned the glomeruli into one of four separate groups. We then three-dimensionally reconstructed the internal structures in the AL (glomeruli) and the VFA (layers). Next in the protocerebrum, we identified both the tracts and their terminations from the AL and VFA. We found that 10 tracts originate in the AL, whereas there are at least eight tracts from the VFA. Several tracts from the AL share their routes with those from the VFA, but their termination areas are segregated. We now have a better anatomical understanding of the pathways for the antennal information in cricket
BackgroundFacultative parthenogenesis, seen in many animal phyla, is a reproductive strategy in which females are able to generate offspring when mating partners are unavailable. In some subsocial and eusocial insects, parthenogenesis is often more prevalent than sexual reproduction. However, little is known about how social cooperation is linked to the promotion of parthenogenesis. The domiciliary cockroach Periplaneta americana is well-suited to addressing this issue as this species belongs to the superfamily Blattoidea, which diverged into eusocial termites and shows facultative parthenogenesis.ResultsWe studied environmental factors that influence asexual production of ootheca using behavioral assays in P. americana. When more than three virgin females immediately after the imaginal molt were kept together in a small sealed container, they tended to produce egg cases (oothecae) via parthenogenesis earlier than did isolated females, resulting in apparent synchronization of ootheca production, even among females housed in different containers. In contrast, virgin females housed with genitalia-ablated males or group-housed females with antennae ablated did not significantly promote ootheca production compared to isolated females. Daily addition of the primary sex pheromone component to the container did not promote ootheca production in isolated females. Another line of study showed that grouped females make parthenogenesis more sustainable than previously known; a founder colony of 15 virgin females was sufficient to produce female progeny for a period of more than three years.ConclusionsGroup-housed females promote and stabilize asexual ootheca production compared to isolated females, and that this promotion is triggered by female-specific chemosensory signals (other than sex pheromone) primarily detected by antennae. Promotion of ootheca production between females is likely to be an early stage of social cooperation, reminiscent of the foundation and maintenance of a colony by female pairs in the eusocial termite Reticulitermes speratus.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-017-0063-x) contains supplementary material, which is available to authorized users.
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