Octopaminergic neurons have multiple targets in Drosophila larval mushroom body calyx and can modulate behavioral odor discrimination

Abstract

Discrimination of sensory signals is essential for an organism to form and retrieve memories of relevance in a given behavioral context. Sensory representations are modified dynamically by changes in behavioral state, facilitating context-dependent selection of behavior, through signals carried by noradrenergic input in mammals, or octopamine (OA) in insects. To understand the circuit mechanisms of this signaling, we characterized the function of two OA neurons, sVUM1 neurons, that originate in the subesophageal zone (SEZ) and target the input region of the memory center, the mushroom body (MB) calyx, in larval Drosophila. We found that sVUM1 neurons target multiple neurons, including olfactory projection neurons (PNs), the inhibitory neuron APL, and a pair of extrinsic output neurons, but relatively few mushroom body intrinsic neurons, Kenyon cells. PN terminals carried the OA receptor Oamb, a Drosophila α1-adrenergic receptor ortholog. Using an odor discrimination learning paradigm, we showed that optogenetic activation of OA neurons compromised discrimination of similar odors but not learning ability. Our results suggest that sVUM1 neurons modify odor representations via multiple extrinsic inputs at the sensory input area to the MB olfactory learning circuit.

Mushroom body output neurons MBONa1/a2 define an odor intensity channel that regulates behavioral odor discrimination learning in larvalDrosophila

“…Brains were immunolabeled to visualize glomeruli by anti-DLG (Lahey et al, 1994), GFP by rat monoclonal anti-GFP, and subsets of synaptic sites were visualized by anti-octopamine (OA) for MBONa1/a2-KC or MBONa1/a2-PN connectivity, and anti-GABA for MBONa1/a2-APL connectivity. KC-MBONa1/a2 GRASP showed a diffuse pattern with some GRASP signals localized in the vicinity of OA boutons, suggesting a synaptic localization for some of the signals, consistent with the MBONa1/a2 contacts seen previously using GRASP (Wong, Wan et al, 2021). These were in the calyx core, or interglomerular space (Fig.…”

“…1C). MBONa1/a2 innervation of the calyx is mainly postsynaptic as shown by expression of the dendritic marker DenMark::mCherry (Nikolai et al, 2010), driven by OK263-GAL4 (Wong, Wan et al 2021), only a few puncta were seen using Syt::GFP; however, strong Syt::GFP labeling but not DenMark was observed around the region of the ML (Fig. 1D), implying that these MBONa1/a2 projections are presynaptic.…”

“…MBs are centers for associative learning in the insect brain, and the calyx is the dendritic input region with a role in odor discrimination. The calyx receives stereotypic input from projection neurons (PNs) and is innervated by a feedback inhibitory neuron, the larval APL (Masuda-Nakagawa et al, 2005, and two octopaminergic neurons called sVUM1 originating in the SEZ, which can modulate behavioral odor discrimination (Wong, Wan et al, 2021). Two output neurons, named MBONa-1 and MBONa-2, arborize in the MB calyx (Saumweber et al, 2018).…”

Pharmacological Properties and Function of the PxOctβ3 Octopamine Receptor in Plutella xylostella (L.)

“…Octopamine (OA) is a multifunctional biogenic amine found at high concentrations only in invertebrates [ 7 ]. Octopamine plays a vital role in a wide range of physiological processes, including fighting, motivation, aggression, muscle regulation and performance, ovulation, glycogen decomposition, fat metabolism, desensitization, learning and memory, and the circadian rhythm [ 8 , 9 , 10 , 11 ].…”

Knockdown of a β-Adrenergic-Like Octopamine Receptor Affects Locomotion and Reproduction of Tribolium castaneum

“…High concentrations of OA have been found in the neuronal and nonneuronal tissues of most invertebrate species [ 2 ]. OA acts as a neurohormone, neuromodulator, and neurotransmitter in invertebrates [ 3 ], with essential functions and regulation of many physiological processes, including olfactory sensitivity [ 4 , 5 , 6 ], endocrine regulation [ 7 ], learning and memory [ 8 , 9 ], locomotion [ 10 , 11 , 12 , 13 ], sleep [ 14 ], induction of germline stem cell increase [ 15 ], and ovulation [ 16 , 17 , 18 , 19 ].…”