Postembryonic development of sexually dimorphic glomeruli and related interneurons in the cockroach Periplaneta americana

Abstract

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

Sensillum‐specific, topographic projection patterns of olfactory receptor neurons in the antennal lobe of the cockroach Periplaneta americana

“…The orientation and position of the brain is shown with reference to the body axis, which is more convenient when working with appendages (Nishino et al, 2009, 2010, 2011). The coordinates based on the neuraxis used in some of previous studies on the cockroach brain were converted to body axis coordinates in this work.…”

Complete mapping of glomeruli based on sensory nerve branching pattern in the primary olfactory center of the cockroach Periplaneta americana

“…The procedures for staining antennal afferents were described previously (Nishino and Mizunami, 2007;Nishino et al, 2009aNishino et al, , 2010. After the animals had been anesthetized with carbon dioxide, the head with antennae was detached from the body and fixed on a dish with low-melting-point wax.…”

“…In the cockroach, anterograde staining of antennal sensory afferents showed that the sensory axon terminals ramify throughout the glomerulus, making synaptic connection with projection neurons and local interneurons (Boeckh and Tolbert, 1993;Distler and Boeckh, 1997a,b), whose dendritic trunks enter from the periphery (Malun et al, 1993). In the cockroach, a hemimetabolous insect, the basic structure of the AL is formed during embryogenesis (Salecker and Boeckh, 1995), with the volume of individual glomeruli increasing during postembryonic development (Prillinger, 1981;Nishino et al, 2009aNishino et al, , 2010: axon terminals of newly emerged sensory afferents are assumed to be added in the proximal region to the axonal entry side of each glomerulus at every molt (Nishino and Mizunami, 2007). However, in holometabolous insects, such as moths, honeybees, and flies, the axons of olfactory receptor neurons enter the AL at the beginning of pupal ecdysis, and they grow first along the periphery of the glomerular precursor structure and then proceed toward the center (Salecker and Malun, 1999).…”

“…Immediately after entering the deutocerebrum, mechanosensory and contact-chemosensory afferents run posterodorsally and give off collaterals in the dorsal lobe and descend to the subesophageal ganglion to give off some terminal branches (Nishino et al, 2005). On the other hand, olfactory and hygrosensory and thermosensory afferents project to given glomeruli in the AL (Boeckh and Tolbert, 1993;Nishikawa et al, 1995;Mizunami, 2006, 2007;Nishino et al, 2009aNishino et al, , 2010. Some aspects of the structurerelated functional properties of the AL glomeruli have been reported for the cockroach (Burrows et al, 1982;Malun et al, 1993;Nishikawa et al, 1995;Strausfeld and Li, 1999;Nishino et al, 2003).…”

Group-housed females promote production of asexual ootheca in American cockroaches

“…Ablation of the largest chemosensory organs, antennae, resulted in a delay in ootheca production compared to that in intact females, although complete ablation of the antennae may have side-effects related to loss of sensory input [34]. Unexpectedly, a typical female-specific odor, the primary sex pheromone component (periplanone-B), did not promote ootheca production, despite the fact that the female P. americana is equipped with a specific olfactory glomerulus in its first-order olfactory center that processes periplanone-B [35, 36]. …”