Neural Control of Action Selection Among Innate Behaviors

Abstract

Nervous systems must not only generate specific adaptive behaviors, such as reproduction, aggression, feeding, and sleep, but also select a single behavior for execution at any given time, depending on both internal states and external environmental conditions. Despite their tremendous biological importance, the neural mechanisms of action selection remain poorly understood. In the past decade, studies in the model animal Drosophila melanogaster have demonstrated valuable neural mechanisms underlying action selection of innate behaviors. In this review, we summarize circuit mechanisms with a particular focus on a small number of sexually dimorphic neurons in controlling action selection among sex, fight, feeding, and sleep behaviors in both sexes of flies. We also discuss potentially conserved circuit configurations and neuromodulation of action selection in both the fly and mouse models, aiming to provide insights into action selection and the sexually dimorphic prioritization of innate behaviors.

Asexuality in Drosophila juvenile males is organizational and independent of juvenile hormone

“…To compare synaptic connections more systematically among courtship regulatory neurons in juvenile and mature males, we next examined syb‐GRASP signals between NPF/TH and all dsx neurons, including dsx pC1 neurons that largely overlap with P1 neurons (Jiang & Pan, 2022). We first examined dsx expression in juvenile and adult males.…”

“…Such kind of activation experiment is sufficient to support stimulatory function of these neurons in male courtship, but insufficient to test the integrity of the whole circuit, for example whether the sex circuitry in juvenile males is developmentally or functionally intact. For example, sex circuitries in male and female animals are organizationally different and encode sex‐specific behaviors, but activation of some neurons can induce the sex‐specific behavior in both sexes (Clyne & Miesenbock, 2008; Rezaval et al , 2016; Wei et al , 2018; Deutsch et al , 2020; Jiang & Pan, 2022). Artificial activation of dsx pC1 neurons induced courtship‐like tracking behavior and even wing extension in adult female flies (Rezaval et al , 2016; Deutsch et al , 2020); similarly, optogenetic activation of the medial preoptic area (mPOA) elicits both male‐typical and female‐typical sexual behaviors in both male and female mice (Wei et al , 2018).…”

“…***P < 0.001, Mann-Whitney U-test. examined syb-GRASP signals between NPF/TH and all dsx neurons, including dsx pC1 neurons that largely overlap with P1 neurons (Jiang & Pan, 2022). We first examined dsx expression in juvenile and adult males.…”

“…The execution of courtship behaviors in isolated males by activating fru M neurons directly indicates the functionality of the sex circuitry. Furthermore, a subset of fru M ‐expressing male‐specific P1 neurons, the majority of which also express doublesex ( dsx ), integrate internal and external cues to initiate male courtship and are recognized as a center for sex drive (Kimura et al , 2008; Pan et al , 2012; Clowney et al , 2015; Kallman et al , 2015; Wu et al , 2019; Jiang & Pan, 2022). Artificial activation of P1 neurons promotes tracking behavior to visual objects in mature males (Pan et al , 2012; Hindmarsh Sten et al , 2021).…”

Molecular and neuronal mechanisms governing sexually dimorphic prioritization of innate behaviors

“…Our study provides a framework to investigate multiple innate behaviors and their prioritizations in both sexes. Future studies would reveal how DH44 exerts the sex-specific and state-dependent functions in pC1 neurons in molecular details, and whether such a mechanism would apply to high-order animals as counterparts for both the DH44 peptide and pC1 neurons exist in mammals[24, 28, 35].…”