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Drosophila melanogaster produce different communication sounds during interactions with conspecifics by vibrating their wings. Males sing a pre-copulatory courtship song with pulse and sine elements. Females sing a structurally different song during copulation. Both sexes also produce a third type of sound pulses during agonistic interactions, i.e. during sexual rejection and inter-male aggression. It is well established that male courtship song increases female receptivity to mating. Female copulation song depends on male inseminate composition and might influence the transfer of the latter. The behavioural effect and function of agonistic sounds are not yet fully understood. Male courtship song production relies on sex specific neurons. As a precisely quantifiable and very specific element of courtship with defined motor parameters, it is an ideal model system for behavioural circuit neuroscience and has provided basic insight to how the nervous system generates, modulates and patterns adaptive behaviour. Central brain networks integrate multimodal sensory information and flexibly control the initiation and maintenance of singing. The circuits generating the species-specific song pattern and shaping motor control of the wing are mainly located in the ventral nerve cord. First studies have started to address how other Drosophila species with divergent sound producing behaviour differ on the level of neuronal circuits from D. melanogaster. In the future, advances in connectomics are expected to greatly facilitate neuronal circuit analysis in general and allow for a comprehensive synthesis of described circuit motifs for different aspects of sound production and its coordination in behavioural context.

Females communicate sexual receptivity in various ways. Drosophila signal that they are mated and ovulating, and resistive to mating again, by extruding their egg-laying organ (ovipositor). Connectome-aided circuit analysis reveals how this break up message is computed and differs from an acceptance response in virgins.

Foraging animals have to evaluate, compare and select food patches in order to increase their fitness. Understanding what drives foraging decisions requires careful manipulation of the value of alternative options while monitoring animals choices. Value-based decision-making tasks in combination with formal learning models have provided both an experimental and theoretical framework to study foraging decisions in lab settings. While these approaches were successfully used in the past to understand what drives choices in mammals, very little work has been done on fruit flies. This is despite the fact that fruit flies have served as model organism for many complex behavioural paradigms. To fill this gap we developed a single-animal, trial-based decision making task, where freely walking flies experienced optogenetic sugar-receptor neuron stimulation. We controlled the value of available options by manipulating the probabilities of optogenetic stimulation. We show that flies integrate reward history of chosen options and forget value of unchosen options. We further discover that flies assign higher values to rewards experienced early in the behavioural session, consistent with formal reinforcement learning models. Finally, we also show that the probabilistic rewards affect walking trajectories of flies, suggesting that accumulated value is controlling the navigation vector of flies in a graded fashion. These findings establish the fruit fly as a model organism to explore the genetic and circuit basis of reward foraging decisions.

In most animal species, males and females communicate during sexual behavior to negotiate reproductive investments. Pre-copulatory courtship may settle if copulation takes place, but often information exchange and decision-making continue beyond that point. Here, we show that female Drosophila sing by wing vibration in copula. This copulation song is distinct from male courtship song and requires neurons expressing the female sex determination factor DoublesexF. Copulation song depends on transfer of seminal fluid components of the male accessory gland. Hearing female copulation song increases the reproductive success of a male when he is challenged by competition, suggesting that auditory cues from the female modulate male ejaculate allocation. Our findings reveal an unexpected fine-tuning of reproductive decisions during a multimodal copulatory dialog. The discovery of a female-specific acoustic behavior sheds new light on Drosophila mating, sexual dimorphisms of neuronal circuits and the impact of seminal fluid molecules on nervous system and behavior., Male fruitflies sing a patterned wing song during courtship. Here, the authors show that females sing a distinct song during copulation, which is controlled by sex-specific neurons, depends on seminal fluid from the male accessory gland and modulates latency of female remating with subsequent males.

Multifunctional motor systems produce distinct output patterns that are dependent on behavioral context, posing a challenge to underlying neuronal control. Flies use their wings for flight and the production of a patterned acoustic signal, the male courtship song, employing in both cases a small set of wing muscles and corresponding motor neurons. We took first steps toward elucidating the neuronal control mechanisms of this multifunctional motor system by live imaging of muscle ensemble activity patterns during song and flight, and we established the functional role of a comprehensive set of wing muscle motor neurons by silencing experiments. Song and flight rely on distinct configurations of neuromuscular activity, with most, but not all, flight muscles and their corresponding motor neurons contributing to song and shaping its acoustic parameters. The two behaviors are exclusive, and the neuronal command for flight overrides the command for song. The neuromodulator octopamine is a candidate for selectively stabilizing flight, but not song motor patterns.

Drosophila melanogaster sexual behaviour relies on well-studied genetically determined neuronal circuits. At the same time, it can be flexible and is modulated by multiple external and internal factors. This review focuses on how physiological state, behavioural context and social experience impact sexual circuits in the two sexes. We discuss how females tune receptivity and other behaviours depending on mating status and how males adjust courtship intensity based on sexual satiety, age and the conflicting drive for aggression. Neuronal mechanisms for behavioural modulation include changes in sensory and central processing. Activity of modulatory neurons can enhance, suppress or reverse the behavioural response to sensory cues. In summary, fly sexual behaviour is an excellent model to study mechanisms of neuromodulation of complex innate behaviour on the circuit level.

Genetic hardwiring during brain development provides computational architectures for innate neuronal processing. Thus, the paradigmatic chick retinotectal projection, due to its neighborhood preserving, topographic organization, establishes millions of parallel channels for incremental visual field analysis. Retinal axons receive targeting information from quantitative guidance cue gradients. Surprisingly, novel adaptation assays demonstrate that retinal growth cones robustly adapt towards ephrin-A/EphA forward and reverse signals, which provide the major mapping cues. Computational modeling suggests that topographic accuracy and adaptability, though seemingly incompatible, could be reconciled by a novel mechanism of coupled adaptation of signaling channels. Experimentally, we find such ‘co-adaptation’ in retinal growth cones specifically for ephrin-A/EphA signaling. Co-adaptation involves trafficking of unliganded sensors between the surface membrane and recycling endosomes, and is presumably triggered by changes in the lipid composition of membrane microdomains. We propose that co-adaptative desensitization eventually relies on guidance sensor translocation into cis-signaling endosomes to outbalance repulsive trans-signaling. DOI: http://dx.doi.org/10.7554/eLife.25533.001, eLife digest The human brain contains roughly 100 billion neurons, which are organized into complex networks. But how does the brain establish these networks in the first place? Neurons have long projections known as axons and, in the developing brain, these axons form structures called growth cones at their tips. The growth cones possess finger-like appendages that probe their surroundings in search of signals displayed on the surface of other cells. These signals guide the growth cones to their targets and move the axon tip into a position where it can form connections with other neurons within a particular network. The signals that growth cones follow are often distributed in concentration gradients so that the levels of a signal may be low at one end of a brain structure and gradually increase to a maximum level at the other end. In the developing visual system, for example, about one million axons from the retina reach their proper targets in visual regions of the brain by reading gradients of signals called ephrins and Ephs. However, when Fiederling et al. studied retinal neurons in a petri dish, they found that the axons became much less sensitive to both signals upon prolonged exposure to them. This unexpected finding raised a new question. If neurons rely upon these gradients for navigation, how do they continue to find their way if they also become less sensitive to those signals over time? Fiederling et al. used a computer to simulate the events occurring in the developing brain. The simulations were based on the idea that navigating growth cones sense the ratio of ephrins to Ephs, instead of sensing the individual concentrations of these signals. Thus, by keeping the amounts of all involved sensors in strict proportion to each other while continuously re-adjusting them, the axons could still be accurately guided to their targets even though the neurons would become less sensitive to the signals. Experiments in neurons grown in petri dishes confirmed that retinal growth cones do exactly this and regulate the amounts of ephrin and Eph sensors on their outer membranes in a highly coordinated manner using a previously unknown mechanism. Given that signaling requires energy, the brain may have evolved this system to reduce the costs associated with wiring itself up. The system also offers greater flexibility than guidance based on the absolute concentrations of the signals. If other regions of the brain use a similar mechanism to establish their own wiring patterns, then understanding such basic mechanisms might eventually provide insights into diseases of miswiring such as schizophrenia and autism. DOI: http://dx.doi.org/10.7554/eLife.25533.002

SummaryThe courtship song of the Drosophila male serves as a genetically tractable model for the investigation of the neural mechanisms of decision-making, action selection, and motor pattern generation. Singing has been causally linked to the activity of the set of neurons that express the sex-specific fru transcripts, but the specific neurons involved have not been identified. Here we identify five distinct classes of fru neuron that trigger or compose the song. Our data suggest that P1 and pIP10 neurons in the brain mediate the decision to sing, and to act upon this decision, while the thoracic neurons dPR1, vPR6, and vMS11 are components of a central pattern generator that times and shapes the song's pulses. These neurons are potentially connected in a functional circuit, with the descending pIP10 neuron linking the brain and thoracic song centers. Sexual dimorphisms in each of these neurons may explain why only males sing.