A Spatiotemporal Wave of Turnover and Functional Maturation of Olfactory Receptor Neurons in the Spiny LobsterPanulirus argus

Abstract

Olfactory receptor neurons (ORNs) of crustaceans are housed in aesthetasc sensilla that are located on the lateral flagellum of the antennule. We used young adult spiny lobsters to examine turnover of aesthetascs and functional maturation of their ORNs after molting. The proliferation zone for new aesthetascs is located in the proximal part of the aesthetasc-bearing region and progressively moves along a distoproximal axis. Older aesthetascs are lost in the distal part of the aesthetasc-bearing region. As a result, an aesthetasc may be shed three to six molts after it differentiates. Taurine-like immunoreactivity is elevated in ORNs of aesthetascs that have yet to emerge on the cuticular surface and thereafter decreases gradually and asynchronously. ORNs from the distalmost-developing aesthetascs lose taurine-like immunoreactivity immediately before sensillar emergence, whereas ORNs from the most proximal and lateral new aesthetascs retain taurine-like immunoreactivity throughout the intermolt stage after sensillar emergence. Furthermore, taurine-like immunoreactivity is inversely correlated with odor responsiveness. These results suggest that taurine-like immunoreactivity reveals immature ORNs and that their functional maturation is not synchronized with molting and may not be completed until many weeks after sensillar emergence. Our data suggest successive spatiotemporal waves of birth, differentiation and functional maturation, and death of ORNs.

Adult neurogenesis and cell cycle regulation in the crustacean olfactory pathway: from glial precursors to differentiated neurons

“…As in most vertebrate taxa, proliferation in the central olfactory pathways of adult decapod crustaceans occurs in parallel with the continuous proliferation and turnover of ORNs in the olfactory organ (crustaceans: Sandeman and Sandeman, 1996;Steullet et al 2000;Harrison et al 2001;Derby et al 2003;vertebrates: Graziadei and Monti-Graziadei 1978;Farbman 1992;Byrd and Brunjes 2001;Beites et al 2005). Most decapod crustaceans, such as crayfish and lobsters, have indeterminate growth and continue to moult and grow throughout their lives (Hartnoll 1982).…”

“…The generation of new OSUs occurs at the proximal end of the olfactory organ within a restricted proliferation zone (Harrison et al 2001). The subsequent differentiation and maturation of newborn ORNs occurs over several weeks and is associated with elevated levels of taurine within the cytoplasm (Steullet et al 2000).…”

“…In adult, but not juvenile, crayfish and lobsters the proximal addition of new OSUs occurs in parallel with the loss of the oldest, distal-most OSUs, resulting in a continuous turnover and replenishment of ORNs (Sandeman and Sandeman 1996;Steullet et al 2000). In between the proximal (proliferation) and distal (senescence) regions of the olfactory organ, ORNs mature and become odor sensitive (Steullet et al 2000).…”

“…In between the proximal (proliferation) and distal (senescence) regions of the olfactory organ, ORNs mature and become odor sensitive (Steullet et al 2000). The birth, differentiation and death of ORNs, therefore, occur in a spatiotemporal wave along the length of the olfactory organ.…”

“…As the life-long addition of ORNs occurs in parallel with the continuous addition of olfactory interneurons in the brain, it has been proposed that these two processes are related functionally, with new olfactory interneurons being added to the central olfactory pathway to accommodate the ingrowing axons of new ORNs (Schmidt 1997;Sandeman et al 1998;Steullet et al 2000; see also reviews of vertebrate studies by Lledo and Saghatelyan 2005;Lindsey and Tropepe 2006). This hypothesis, however, has rarely been tested.…”