The Neural Basis for a Persistent Internal State inDrosophilaFemales

Abstract

Sustained changes in mood or action require persistent changes in neural activity, but it has been difficult to identify and characterize the neural circuit mechanisms that underlie persistent activity and contribute to long-lasting changes in behavior. Here, we focus on changes in the behavioral state of Drosophila females that persist for minutes following optogenetic activation of a single class of central brain neurons termed pC1. We find that female pC1 neurons drive a variety of persistent behaviors in the presence of males, including increased receptivity, shoving, and chasing. By reconstructing cells in a volume electron microscopic image of the female brain, we classify 7 different pC1 cell types and, using cell type specific driver lines, determine that one of these, pC1-Alpha, is responsible for driving persistent female shoving and chasing. Using calcium imaging, we locate sites of minutes-long persistent neural activity in the brain, which include pC1 neurons themselves. Finally, we exhaustively reconstruct all synaptic partners of a single pC1-Alpha neuron, and find recurrent connectivity that could support the persistent neural activity. Our work thus links minutes-long persistent changes in behavior with persistent neural activity and recurrent circuit architecture in the female brain.

Neural Network Organization for Courtship Song Feature Detection inDrosophila

“…2), we could then determine all synaptic connections (via automated synapses (Buhmann et al, 2019)) between these neurons and earlier neurons in the pathway. We also examined connections to higher-order neurons shown to be pulse-preferring (vpoEN (Wang et al) and pC2l (Deutsch et al, 2019)), to drive a persistent internal state in females (pC1d/e (Deutsch et al, 2020)), and descending neurons that drive song-responsive behaviors (pMN1/DNp13 (Wang et al) and pMN2/vpoDN (Deutsch et al, 2019; Wang et al, 2020b)) (Fig. 9A).…”

“…We used FAFB reconstructions corresponding to previously known auditory neurons (Dorkenwald et al 2020), higher-order auditory neurons (Deutsch et al, 2020; Wang et al, 2020b), and all auditory WED/VLP neurons for which we found EM reconstructions. We then found all automatically detected synapses between every pair of individual neurons (Buhmann et al, 2019).…”

Cell types and neuronal circuitry underlying female aggression in Drosophila

“…The five cell types that make up the pC1 group express dsx and have been implicated in female receptivity, oviposition, male courtship, and both male and female aggression (Deutsch et al 2020;Fathy, 2016;Hoopfer et al, 2015;Ishii et al, 2020;Koganezawa et al, 2016;Palavicino-Maggio et al, 2019;Rideout et al, 2010;Wang et al, 2020a,b;Wohl et al, 2020;Zhou et al, 2014). In previous work, the lack of cell-type specific genetic reagents has made it difficult to elucidate the relative contribution of the five pC1 cell types in females to each of these behaviors.…”

“…A complementary study by Deutsch et al (2020) found that combined activation of pC1d and pC1e using ReaChR resulted in a persistent phenotype lasting for minutes. Using lines labeling aIPg cells, we did observe head butting and fencing behaviors after the cessation of the optogenetic stimulus that lasted for a shorter, but ethologically relevant (Bath et al, 2017;Yuan et al, 2014), time period on the order of 10s of seconds.…”

“…Genes involved in sexual differentiation, including doublesex (dsx) and fruitless (fru), contribute to social behaviors (Dickson, 2008;Koganezawa et al, 2016;Pavlou and Goodwin, 2013;Siwicki and Kravitz, 2009;Yamamoto, 2007;Yamamoto and Koganezawa, 2013;Zhou et al, 2014). Recent work has revealed the involvement of the dsx-expressing pC1 cluster, a group of 5 cell types, in promoting aggressive phenotypes in female flies (Deutsch et al, 2020;Fathy, 2016;Palavicino-Maggio et al, 2019). As in the VMHvl of mice, cells within this cluster can be divided into multiple subtypes and particular subtypes are also involved in other female behaviors, including mating and egg laying (Wang et al, 2020a,b).…”