Highlights • Drosophila engage in a complex repertoire of aggressive behaviors. • Sensory cues from conspecific competitors, potential mates and food resources drive aggression in males. • Specific ...populations of aminergic and peptidergic neurons that modulate aggression have been identified. • P1 neurons trigger a persistent internal state that promotes both male courtship and aggression. • Social experience modifies aggressive behavior on short and long-term timescales.
Optogenetics allows the manipulation of neural activity in freely moving animals with millisecond precision, but its application in Drosophila melanogaster has been limited. Here we show that a ...recently described red activatable channelrhodopsin (ReaChR) permits control of complex behavior in freely moving adult flies, at wavelengths that are not thought to interfere with normal visual function. This tool affords the opportunity to control neural activity over a broad dynamic range of stimulation intensities. Using time-resolved activation, we show that the neural control of male courtship song can be separated into (i) probabilistic, persistent and (ii) deterministic, command-like components. The former, but not the latter, neurons are subject to functional modulation by social experience, which supports the idea that they constitute a locus of state-dependent influence. This separation is not evident using thermogenetic tools, a result underscoring the importance of temporally precise control of neuronal activation in the functional dissection of neural circuits in Drosophila.
How brains are hardwired to produce aggressive behavior, and how aggression circuits are related to those that mediate courtship, is not well understood. A large-scale screen for aggression-promoting ...neurons in Drosophila identified several independent hits that enhanced both inter-male aggression and courtship. Genetic intersections revealed that 8-10 P1 interneurons, previously thought to exclusively control male courtship, were sufficient to promote fighting. Optogenetic experiments indicated that P1 activation could promote aggression at a threshold below that required for wing extension. P1 activation in the absence of wing extension triggered persistent aggression via an internal state that could endure for minutes. High-frequency P1 activation promoted wing extension and suppressed aggression during photostimulation, whereas aggression resumed and wing extension was inhibited following photostimulation offset. Thus, P1 neuron activation promotes a latent, internal state that facilitates aggression and courtship, and controls the overt expression of these social behaviors in a threshold-dependent, inverse manner.
We introduce a method based on machine vision for automatically measuring aggression and courtship in Drosophila melanogaster. The genetic and neural circuit bases of these innate social behaviors ...are poorly understood. High-throughput behavioral screening in this genetically tractable model organism is a potentially powerful approach, but it is currently very laborious. Our system monitors interacting pairs of flies and computes their location, orientation and wing posture. These features are used for detecting behaviors exhibited during aggression and courtship. Among these, wing threat, lunging and tussling are specific to aggression; circling, wing extension (courtship 'song') and copulation are specific to courtship; locomotion and chasing are common to both. Ethograms may be constructed automatically from these measurements, saving considerable time and effort. This technology should enable large-scale screens for genes and neural circuits controlling courtship and aggression.
Males of most species are more aggressive than females, but the neural mechanisms underlying this dimorphism are not clear. Here, we identify a neuron and a gene that control the higher level of ...aggression characteristic of Drosophila melanogaster males. Males, but not females, contain a small cluster of FruM+ neurons that express the neuropeptide tachykinin (Tk). Activation and silencing of these neurons increased and decreased, respectively, intermale aggression without affecting male-female courtship behavior. Mutations in both Tk and a candidate receptor, Takr86C, suppressed the effect of neuronal activation, whereas overexpression of Tk potentiated it. Tk neuron activation overcame reduced aggressiveness caused by eliminating a variety of sensory or contextual cues, suggesting that it promotes aggressive arousal or motivation. Tachykinin/Substance P has been implicated in aggression in mammals, including humans. Thus, the higher aggressiveness of Drosophila males reflects the sexually dimorphic expression of a neuropeptide that controls agonistic behaviors across phylogeny.
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•A single class of neurons is identified that promotes aggression in male flies•These neurons are FruM+ and sexually dimorphic but do not control courtship•These neurons promote aggressive arousal via release of a neuropeptide, DTK•Tk is a neuropeptide gene that controls aggression in both flies and mammals
A small group of Drosophila neurons that are detectable in male, but not female, brains promote high levels of aggression via the release of a neuropeptide, Tachykinin. Homologs of this neuropeptide are implicated in mammalian aggression.
Threat displays are a universal feature of agonistic interactions. Whether threats are part of a continuum of aggressive behaviors or separately controlled remains unclear. We analyze threats in ...Drosophila and show they are triggered by male cues and visual motion, and comprised of multiple motor elements that can be flexibly combined. We isolate a cluster of ∼3 neurons whose activity is necessary for threat displays but not for other aggressive behaviors, and whose artificial activation suffices to evoke naturalistic threats in solitary flies, suggesting that the neural control of threats is modular with respect to other aggressive behaviors. Artificially evoked threats suffice to repel opponents from a resource in the absence of contact aggression. Depending on its level of artificial activation, this neural threat module can evoke different motor elements in a threshold-dependent manner. Such scalable modules may represent fundamental “building blocks” of neural circuits that mediate complex multi-motor behaviors.
•Fly threat displays are comprised of multiple motor elements•Modular AIP neurons control threat displays independently of other aggressive behaviors•AIP neuron activation can mimic bimodal sensory cues and evoke variable motor output•Threat displays promote, but are not required for, conspecific target repulsion
Duistermars et al. characterize threat displays in flies and the sensory cues required for this behavior. They also identify a compact neural module that controls flexible threat behavior according to its level of activity.
Diffuse neuromodulatory systems such as norepinephrine (NE) control brain-wide states such as arousal, but whether they control complex social behaviors more specifically is not clear. Octopamine ...(OA), the insect homolog of NE, is known to promote both arousal and aggression. We have performed a systematic, unbiased screen to identify OA receptor-expressing neurons (OARNs) that control aggression in Drosophila. Our results uncover a tiny population of male-specific aSP2 neurons that mediate a specific influence of OA on aggression, independent of any effect on arousal. Unexpectedly, these neurons receive convergent input from OA neurons and P1 neurons, a population of FruM+ neurons that promotes male courtship behavior. Behavioral epistasis experiments suggest that aSP2 neurons may constitute an integration node at which OAergic neuromodulation can bias the output of P1 neurons to favor aggression over inter-male courtship. These results have potential implications for thinking about the role of related neuromodulatory systems in mammals.
•OAR+ aSP2 neurons control aggression independently of arousal in Drosophila•Octopamine receptor Oamb in aSP2 neurons modulates aggression in response to OA•aSP2 neurons receive input from P1 neurons, which promote courtship and aggression•aSP2 neurons integrate input from OANs and P1 neurons to promote aggression
Watanabe et al. describe a circuit mechanism by which the neuromodulator octopamine regulates an output relay from a multifunctional social behavior network to control the balance between aggression and courtship in Drosophila.
Aggression involves both sexually monomorphic and dimorphic actions. How the brain implements these two types of actions is poorly understood. We have identified three cell types that regulate ...aggression in Drosophila: one type is sexually shared, and the other two are sex specific. Shared common aggression-promoting (CAP) neurons mediate aggressive approach in both sexes, whereas functionally downstream dimorphic but homologous cell types, called male-specific aggression-promoting (MAP) neurons in males and fpC1 in females, control dimorphic attack. These symmetric circuits underlie the divergence of male and female aggressive behaviors, from their monomorphic appetitive/motivational to their dimorphic consummatory phases. The strength of the monomorphic → dimorphic functional connection is increased by social isolation in both sexes, suggesting that it may be a locus for isolation-dependent enhancement of aggression. Together, these findings reveal a circuit logic for the neural control of behaviors that include both sexually monomorphic and dimorphic actions, which may generalize to other organisms.
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•Sexually dimorphic attack is controlled by sexually dimorphic neurons in Drosophila•Shared cells that control aggressive approach activate the dimorphic attack neurons•The transition from approach to attack occurs at a higher threshold than approach•Isolation enhances shared → dimorphic functional connectivity to promote aggression
Chiu et al. uncover how a sexually dimorphic behavior is wired in the brains of male and female flies. Looking for neuronal components controlling aggressive behaviors, they find a single type of neuron that controls aggressive approach in both sexes connected hierarchically to different neurons in males versus females that control dimorphic attack responses (lunge versus headbutt, respectively). They then show that social isolation, known to augment aggressive behaviors in both sexes, strengthens the connections between the monomorphic and dimorphic neurons.
Axon pruning is widely used for the refinement of neural circuits in both vertebrates and invertebrates, and may also contribute to the pathogenesis of neurodegenerative diseases. However, little is ...known about the cellular and molecular mechanisms of axon pruning. We use the stereotyped pruning of γ neurons of the
Drosophila mushroom bodies (MB) during metamorphosis to investigate these mechanisms. Detailed time course analyses indicate that MB axon pruning is mediated by local degeneration rather than retraction and that the disruption of the microtubule cytoskeleton precedes axon pruning. In addition, multiple lines of genetic evidence demonstrate an intrinsic role of the ubiquitin-proteasome system in axon pruning; for example, loss-of-function mutations of the ubiquitin activating enzyme (E1) or proteasome subunits in MB neurons block axon pruning. Our findings suggest that some forms of axon pruning during development may share similarities with degeneration of axons in response to injury.
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