Excitation and inhibition onto central courtship neurons biases Drosophila mate choice

Abstract

The ability to distinguish males from females is essential for productive mate selection and species propagation. Recent studies in Drosophila have identified different classes of contact chemosensory neurons that detect female or male pheromones and influence courtship decisions. Here, we examine central neural pathways in the male brain that process female and male pheromones using anatomical, calcium imaging, optogenetic, and behavioral studies. We find that sensory neurons that detect female pheromones, but not male pheromones, activate a novel class of neurons in the ventral nerve cord to cause activation of P1 neurons, male-specific command neurons that trigger courtship. In addition, sensory neurons that detect male pheromones, as well as those that detect female pheromones, activate central mAL neurons to inhibit P1. These studies demonstrate that the balance of excitatory and inhibitory drives onto central courtship-promoting neurons controls mating decisions.DOI: http://dx.doi.org/10.7554/eLife.11188.001

Genetically expressed voltage sensor ArcLight for imaging large scale cortical activity in the anesthetized and awake mouse

“…With recent advances in GEVIs, there is a large demand to determine the in vivo functional limitations and capabilities for each new voltage probe. Since the initial discovery and publication; 1 to our knowledge, ArcLight has been predominantly adopted as a tool for neuroscience research in Drosophila 14,15,16,58,59 and has not been widely utilized in mammals. Other FRET-based GEVIs such as Butterfly 1.2, and VSFP 2.3 have been shown to measure widefield cortical responses in vivo; however, the monochromatic fluorophore ArcLight has yet been tested in in vivo cortical systems.…”

Dopaminergic Circuitry Underlying Mating Drive

“…Much of this progress has followed from gaining genetic access to neurons expressing the sexually dimorphic transcription factor Fruitless (Ito et al, 1996;Ryner et al, 1996;Stockinger et al, 2005). Fruitless expression is thought to delineate circuitry extending from the sensory neurons that detect females to the motor output neurons that execute the various aspects of the courtship ritual (Cachero et al, 2010;Clowney et al, 2015;Kallman et al, 2015;Manoli et al, 2005;Ruta et al, 2010;Stockinger et al, 2005;Yu et al, 2010). The ability to target and manipulate small groups of neurons within the Fruitless circuit has begun providing insight into how sensory information is translated into motor output in the context of a goal-oriented behavior (Clowney et al, 2015;Coen et al, 2016;Fan et al, 2013;Kallman et al, 2015;Kimura et al, 2008;Kohatsu et al, 2011;Pan et al, 2012;von Philipsborn et al, 2011;Ruta et al, 2010;Zhou et al, 2015).…”

“…The dopamine signal is sensed and interpreted by a group of $40 Fruitless neurons called P1 (Kimura et al, 2008) (also known as pMP4; Yu et al, 2010; or as a subset of pC1; Pan et al, 2012;Zhou et al, 2015). P1 neurons receive stimulatory input from female-derived sensory information (Clowney et al, 2015;Kallman et al, 2015;Kohatsu et al, 2011) and project to motor command neurons (Kohatsu et al, 2011;von Philipsborn et al, 2011). Dopaminergic internal state input therefore gates courtship initiation through a numerically compact neuronal node that lies at the transition between sensory input and motor output.…”

Targeted manipulation of neuronal activity in behaving adult flies

“…The upstream neuron is then optogenetically activated while the downstream neuron expressing GCaMP6 is monitored for changes in fluorescence (Figure 6c). These experiments can be done with the nervous system kept in the body or using a dissected brain (Kallman et al 2015;Zhou et al 2015;Clowney et al 2015;Hampel et al 2015;Cohn et al 2015;Shirangi et al 2016). The functional connectivity between neurons that is demonstrated by measuring GECI responses cannot indicate whether the connections are direct, and it is always possible that intermediate neurons are involved.…”