A comprehensive anatomical map of the peripheral octopaminergic/tyraminergic system of Drosophila melanogaster

Abstract

The modulation of an animal’s behavior through external sensory stimuli, previous experience and its internal state is crucial to survive in a constantly changing environment. In most insects, octopamine (OA) and its precursor tyramine (TA) modulate a variety of physiological processes and behaviors by shifting the organism from a relaxed or dormant condition to a responsive, excited and alerted state. Even though OA/TA neurons of the central brain are described on single cell level in Drosophila melanogaster, the periphery was largely omitted from anatomical studies. Given that OA/TA is involved in behaviors like feeding, flying and locomotion, which highly depend on a variety of peripheral organs, it is necessary to study the peripheral connections of these neurons to get a complete picture of the OA/TA circuitry. We here describe the anatomy of this aminergic system in relation to peripheral tissues of the entire fly. OA/TA neurons arborize onto skeletal muscles all over the body and innervate reproductive organs, the heart, the corpora allata, and sensory organs in the antennae, legs, wings and halteres underlining their relevance in modulating complex behaviors.

Endocrine fine-tuning of daily locomotor activity patterns under non-starving conditions in Drosophila

“…OA is produced by octopaminergic neurons (OANs) located mostly along the midline in the brain and ventral nerve cord [18]. Among other functions, OA exerts myotropic effects on skeletal muscles [19] and mediates the adaptation of muscle metabolism to the physiological demands of locomotion [20][21][22].Both AKH and OA are crucial for starvation-induced hyperactivity, as this behaviour is absent in flies with impaired AKH or OA signalling [4,5,[7][8][9]. AKH activates a subset of OANs which are required for starvation-induced hyperactivity [5,9].…”

“…OA is produced by octopaminergic neurons (OANs) located mostly along the midline in the brain and ventral nerve cord [18]. Among other functions, OA exerts myotropic effects on skeletal muscles [19] and mediates the adaptation of muscle metabolism to the physiological demands of locomotion [20][21][22].…”

Drosophilainsulin-like peptide 8 (DILP8) in ovarian follicle cells regulates ovulation and metabolism

“…Thus DILP8 could act both in a paracrine fashion directly on follicle cells to induce rupture and subsequent ovulation and act systemically on neurons innervating the oviduct muscle that regulate ovulation. Since octopaminergic neurons innervating the oviduct have been implicated in regulation of ovulation (Monastirioti, 2003;Lee et al, 2009;Rubinstein and Wolfner, 2013;Sun and Spradling, 2013;Deady et al, 2015;Pauls et al, 2018), and follicle cell maturation [see (Knapp et al, 2020)], we tested whether octopaminergic neurons express the Lgr3 receptor.…”

“…Rabbit anti-leucokinin (Nässel et al, 1992) at 1:2000; rabbit anti-ion transport peptide (Galikova et al, 2018) at 1:1500; rabbit anti-DILP3 (Veenstra et al, 2008) at 1:2000 provided by J. A. Veenstra, Bordeaux, France, rabbit anti-tyrosine decarboxylase-2 (Tdc2; pab0822-P, Covalab, Cambridge, UK; at 1:200 [see (Pauls et al, 2018)] obtained from D. Pauls, Leipzig, Germany; Rhodamine-phalloidin was used at 1:1000 to stain muscle. The following secondary antisera were used: goat anti-rabbit Alexa 546, goat anti-rabbit Alexa 488 and goat anti-mouse Alexa 488 (all from Invitrogen).…”

“…Since it is known that the ovaries and oviduct are innervated by octopaminergic neurons (Monastirioti, 2003;Rubinstein and Wolfner, 2013;Pauls et al, 2018), we performed double labeling with Lgr3-Gal4-driven GFP and immunostaining with antiserum to TDC2, a biosynthetic enzyme catalyzing the production of octopamine (OA) and tyrosine (Tyr). We detected TDC2-immunlabeled axons running posteriorly from abdominal neuromeres ( Fig.…”