Acetylcholine‐mediated axon‐glia signaling in the developing insect olfactory system

Abstract

In the olfactory system of the sphinx moth Manduca sexta, migration of neuropil glial cells is triggered by olfactory receptor axons and depends on intraglial Ca(2+) signaling. It is not known, however, how receptor axons and glial cells communicate and whether Ca(2+) signaling is a consequence of this communication. We studied Ca(2+) increases in glial cells in vivo and in situ, evoked by electrical stimulation of olfactory receptor axons in pupae and by odor stimulation of receptor neurons in adult moths. Axonal activity leads to Ca(2+) increases in neuropil glial cells that are blocked by nicotinic acetylcholine receptor antagonists and can be mimicked by acetylcholine and carbachol application. In addition, Ca(2+) transients were abolished by removal of external Ca(2+) and blockage of voltage-gated Ca(2+) channels. During development, acetylcholine-mediated Ca(2+) signaling could first be elicited at stage 6, the time when neuropil glial cells start to migrate. Glial migration was reduced after injection of nicotinic antagonists into pupae. The results show that Ca(2+) signaling can be induced by acetylcholine release from olfactory receptor axons, which activates nicotinic acetylcholine receptors and leads to voltage-gated Ca(2+) influx. The results further suggest that cholinergic signaling in the olfactory system is required for glial cell migration in Manduca.

Antennal Lobe Processing Increases Separability of Odor Mixture Representations in the Honeybee

“…Therefore the participation of LNs or PNs in the compound signal is thought to be negligible (Galizia and Vetter 2005). A significant part of the signal may come from glial cells surrounding each glomerulus because in the hawkmoth Manduca sexta, bath application of Calcium Green was shown to mainly stain periglomerular glial cells in adults and odors trigger activity in these cells (Heil et al 2007). Even so, it is clearly established that release of acetylcholine (ACh) from ORN axons leads to activation of nicotinic receptors (nAChRs) in these glial cells, which depolarizes the cell membrane and thereby opens voltage-gated calcium channels (VGCCs).…”

Recognition, presence, and survival of locust central nervous glia in situ and in vitro

“…A reason for this variability lies in the lack of universal glia-specific markers. Although a number of antibodies, lectins, and other molecular markers specifically label insect glial cells, none of the currently available markers universally labels all types of glia through all developmental stages of a given species (Boyan and Williams, 2004;Gibson et al, 2004;Halter et al, 1995;Heil et al, 2007;Hä hnlein and Bicker, 1996;Meyer et al, 1987;Parker and Auld, 2006). The most commonly used antibody for labeling glial cells in the developing and adult CNS of Drosophila is directed against the homeodomain-containing transcription factor Reversed polarity (Repo).…”

Olfactory coding in five moth species from two families

“…The dye was accumulated by OSNs that contribute largely to the neural circuits of a glomerulus but are shown to actively expel dye molecules (Manzini and Schild, 2003), and also by glial cells that tightly surround each glomerulus and retain the fluorescent dye. Glial cells respond with an influx of Ca 2+ upon odorant stimulation of OSNs projecting to the respective glomerulus (Heil et al, 2007), thus leading to an increase of fluorescence at the site and reflecting the activity of OSNs. After incubation for 90min, the brain was rinsed several times with physiological saline to remove excessive dye.…”