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

Abstract

Glomeruli are structural and functional units in the primary olfactory center in vertebrates and insects. In the cockroach Periplaneta americana, axons of different types of sensory neurons housed in sensilla on antennae form dorsal and ventral antennal nerves and then project to a number of glomeruli. In this study, we identified all antennal lobe (AL) glomeruli based on detailed innervation patterns of sensory tracts in addition to the shape, size, and locations in the cockroach. The number of glomeruli is approximately 205, and no sex-specific difference is observed. Anterograde dye injections into the antennal nerves revealed that axons supplying the AL are divided into 10 sensory tracts (T1-T10). Each of T1-T3 innervates small, oval glomeruli in the anteroventral region of the AL, with sensory afferents invading each glomerulus from multiple directions, whereas each of T4-T10 innervates large glomeruli with various shapes in the posterodorsal region, with a bundle of sensory afferents invading each glomerulus from one direction. The topographic branching patterns of all these tracts are conserved among individuals. Sensory afferents in a sub-tract of T10 had axon terminals in the dorsal margin of the AL and the protocerebrum, where they form numerous small glomerular structures. Sensory nerve branching pattern should reflect developmental processes to determine spatial arrangement of glomeruli, and thus the complete map of glomeruli based on sensory nerve branching pattern should provide a basis for studying the functional significance of spatial arrangement of glomeruli and its developmental basis.

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…After application of the fluorescent dye, the opening of the head was covered with a previously cut square of cuticle. Antennal afferents then underwent anterograde staining to visualize glomeruli as previously described (Nishino et al, 2009; Watanabe et al, 2010). The antennal nerve on the ipsilateral side was exposed and excised at the flagellar base.…”

“…In the male cockroach AL, all 203 ordinary glomeruli and two macroglomeruli can be unambiguously identified by the innervation patterns of T1 to T10 sensory tracts (Watanabe et al, 2010). The nomenclatures and detailed morphological features of glomeruli and glomerular groups were described in our previous studies (Watanabe et al, 2010, 2012b).…”

“…The nomenclatures and detailed morphological features of glomeruli and glomerular groups were described in our previous studies (Watanabe et al, 2010, 2012b). Specifically, ordinary glomeruli belonging to the T1-T4 groups were morphologically, functionally, and developmentally segregated from those belonging to the T5-T10 groups (Salecker and Boeckh, 1995; Watanabe et al, 2010, 2012b). We termed the former and latter groups the ‘antero-dorsal’ and ‘postero-ventral glomerular groups,’ respectively.…”

“…Using the standard glomeruli map in the male cockroach AL (Watanabe et al, 2010, 2012b), we colored glomeruli based on anatomical and physiological properties of innervating PNs.…”

“…In the cockroach Periplaneta americana , the AL equips two sex pheromone-sensitive glomeruli and 203 ordinary glomeruli which process general odors. The ordinary glomeruli have been classified into two glomerular groups: the antero-dorsal and postero-ventral groups (Watanabe et al, 2010). Because the antero-dorsal and postero-ventral group glomeruli receive olfactory inputs from OSNs in different types of sensilla that exhibit different odor spectra, they are morpho-functionally segregated (Fujimura et al, 1991; Watanabe et al, 2012a,b).…”