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

Abstract

In vertebrates and many invertebrates, olfactory signals detected by peripheral olfactory receptor neurons (ORNs) are conveyed to a primary olfactory center with glomerular organization in which odor-specific activity patterns are generated. In the cockroach, Periplaneta americana, ORNs in antennal olfactory sensilla project to 205 unambiguously identifiable antennal lobe (AL) glomeruli that are classified into 10 glomerular clusters (T1-T10 glomeruli) innervated by distinct sensory tracts. In this study we employed single sensillum staining techniques and investigated the topographic projection patterns of individual ORNs to elucidate the relationship between sensillum types and glomerular organization in the AL. Axons of almost all ORNs projected to individual glomeruli. Axons of ORNs in perforated basiconic sensilla selectively innervated the anterodorsal T1-T4 glomeruli, whereas those in trichoid and grooved basiconic sensilla innervated the posteroventral T5-T9 glomeruli. About 90% of stained ORNs in trichoid sensilla sent axons to the T5 glomeruli and more than 90% of ORNs in grooved basiconic sensilla innervated the T6, T8, and T9 glomeruli. The T5 and T9 glomeruli exclusively receive sensory inputs from the trichoid and grooved basiconic sensilla, respectively. All investigated glomeruli received convergent input from a single type of sensillum except F11 glomerulus in the T6 glomeruli, which was innervated from both trichoid and grooved basiconic sensilla. These results suggest that ORNs in distinct sensillum types project to glomeruli in distinct glomerular clusters. Since ORNs in distinct sensillum types are each tuned to distinct subsets of odorant molecules, the AL is functionally compartmentalized into groups of glomeruli.

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…Segregation of axon terminals between type1 and type2 PNs was observed in all dual intracellular staining specimens ( n = 5). In previous cockroach studies, OSNs in antennal perforated basiconic sensilla were reported to terminate specifically in the antero-dorsal group glomeruli, whereas those in the trichoid and grooved basiconic sensilla terminated in postero-ventral group glomeruli ( Figure 2E ; Watanabe et al, 2012b). Thus, type1 and type2 PNs appear to receive sensory inputs from different types of antennal sensilla ( Figure 2E ).…”

“…(E) Schematic drawing of parallel pathways from the periphery to higher brain center in the cockroach brain. OSNs in perforated basiconic sensilla ( single-walled A [ sw -A] and sw -B) selectively terminate in antero-dorsal group glomeruli (AD glomeruli), whereas those in trichoid sensilla ( sw- C) and grooved basiconic sensilla ( double-walled A [ dw -A]) projects to the postero-ventral group glomeruli (PV glomeruli: Watanabe et al, 2012b). Therefore, type1 PNs with dendrites in PV glomeruli and type2 PNs with dendrites in AD glomeruli form two segregated parallel pathways from the periphery to higher brain centers.…”

“…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.…”

“…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). The current study revealed that olfactory signals processed in postero-ventral and antero-dorsal group glomeruli are relayed by two morphologically distinct types of uniglomerular PNs, termed type1 and type2 PNs, respectively (Strausfeld and Li, 1999a; Watanabe et al, 2012a).…”