P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila
authors: Eric D Hoopfer, Yonil Jung, Hidehiko K Inagaki, Gerald M Rubin, David J Anderson
doi: 10.7554/eLife.11346
CITATION
Hoopfer, E. D., Jung, Y., Inagaki, H. K., Rubin, G. M., & Anderson, D. J. (2015). P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife, 4, e11346. https://doi.org/10.7554/eLife.11346
ABSTRACT
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.
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For most animals, mating and fighting are critical for survival and reproduction. These behaviors are also closely related and share similar actions. How are such complex behaviors hard-wired into the brain? A fruit fly called Drosophila melanogaster is an excellent system to investigate this problem, because flies mate and fight, and powerful genetic tools are available to probe the circuits of neurons that control these behaviors.
A great deal has been learned recently about the neural circuits that control mating, but much less was known about how the circuits for aggression are organized. Hoopfer et al. systematically activated different sets of neurons in thousands of male flies to try to find the circuits that trigger aggression. While this identified some neurons that specifically promoted aggression, it also uncovered a cluster – called P1 neurons – that promoted both aggression and courtship. This was unexpected, because P1 neurons were previously thought to only control courtship behavior.
The P1 neurons produced different behaviors at different stimulation thresholds, with the neurons requiring a stronger level of activation to promote courtship instead of aggression. Moreover, the P1 neurons triggered a lasting change in the internal state of the male that increased his tendency to engage in aggression or courtship. These results are reminiscent of observations made in mice, suggesting small groups of neurons that control mating and fighting may represent an evolutionarily conserved neural circuit “motif” for the control of social behavior.
The next step is to figure out how P1 neurons trigger a persistent internal state of arousal or motivation, and to determine whether and how this circuitry participates in the “decision” to engage in mating or fighting.