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Circuit modules linking internal states and social behaviour in flies and mice

Key Points

  • Mouse and fly brains contain relatively small populations of neurons that control both mating and aggression. In mice, these neurons are located within the oestrogen receptor 1-positive population in the ventrolateral part of the ventromedial hypothalamic nucleus (VMHvl); in flies, these neurons are located within the P1 population of male-specific Fruitless-expressing interneurons in the central brain.

  • Whether the same or different neurons within each of the two systems control mating and aggression remains to be established. Also, it is not yet certain whether these neurons control both behaviours in a direct or indirect manner; for example, P1 neurons, which directly promote courtship, may trigger aggression indirectly, through a rebound from inhibition.

  • Optogenetic activation of these neuron populations evokes mating or aggressive behaviours at different threshold levels of photostimulation. However, in the two species the thresholds are reversed; whether this reflects biological or technical factors is uncertain.

  • Both populations of neurons promote persistent internal 'π' states (related to motivation, arousal or drive) that impel the animal to engage in social behaviours. Whether these states have identical functions in the two species is not yet clear.

  • Both populations receive inputs from pheromone-processing pathways, suggesting that they may transform these chemosensory cues into representations of conspecific sexual identity, internal state or behavioural decisions.

  • While the similarities between the VMHvl and the P1 cluster may be superficial and coincidental, it is attractive to think that these neuron populations represent a conserved or analogous module for the high-level control of sex and aggression. Nevertheless, there are important differences between the two systems.

Abstract

Goal-directed social behaviours such as mating and fighting are associated with scalable and persistent internal states of emotion, motivation, arousal or drive. How those internal states are encoded and coupled to behavioural decision making and action selection is not clear. Recent studies in Drosophila melanogaster and mice have identified circuit nodes that have causal roles in the control of innate social behaviours. Remarkably, in both species, these relatively small groups of neurons can influence both aggression and mating, and also play a part in the encoding of internal states that promote these social behaviours. These similarities may be superficial and coincidental, or may reflect conserved or analogous neural circuit modules for the control of social behaviours in flies and mice.

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Figure 1: P1 and VMHvl neurons control multiple social behaviours.
Figure 2: Effects of P1 neuron activation on social behaviour in flies.
Figure 3: P1a neurons promote a persistent internal state of social arousal or motivation.
Figure 4: VMHvl neurons promote aggressive motivation or arousal.
Figure 5: P1 and VMHvl neurons receive ascending inputs from multiple chemosensory systems.

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Acknowledgements

The author thanks D. Tsao, E. Hoopfer and members of the Anderson laboratory, and an anonymous reviewer for helpful discussions and critical feedback, and V. Chiu for fly drawings in figures 1 and 3. The author apologizes to all of those authors whose primary research papers could not be cited owing to restrictions on the number of references. This work was supported by grants from the US National Institutes of Health and National Institute of Mental Health, the Paul G. Allen Family Foundation, the Simons Foundation, the Ellison Medical Foundation, the Moore Foundation, the Guggenheim Foundation and the California Institute of Technology. D.J.A. is an investigator of the Howard Hughes Medical Institute.

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PowerPoint slides

Glossary

π states

A generic term, introduced for the purposes of this Review, denoting persistent and scalable internal brain states.

Appetitive phases

The phases of a goal-directed activity that involve seeking or investigative actions; in social behaviour, these include approach and ano-genital or head-directed sniffing.

Consummatory phases

In aggression, the phase that involves overt attack behaviours such as biting; in mating, the phase that includes intromission (pelvic thrusting with vaginal penetration) and ejaculation.

Scalability

In the context of this Review, the property of a π state to exhibit graded and time-varying changes in its intensity, such as escalation during a social encounter.

Gal4 lines

Inbred lines of transgenic flies in which the expression of the yeast transcriptional activator Gal4 is restricted to specific neuron subsets by regulatory DNA fragments.

Split Gal4 system

Intersectional labelling of neurons by expressing the DNA-binding and transcriptional activation domains of GAL4 from two separate transgenes under the control of different but overlapping promoters.

Wing extension

A social behaviour in which a male fly extends one wing towards another fly and vibrates it at specific frequencies to generate a courtship 'song'.

Fos

An immediate early gene, the transcription of which is rapidly induced by elevated intracellular free calcium and therefore serves as a surrogate marker of neuronal activation.

Fibres of passage

Axons that pass through a given brain region en route to a distant target without forming local synapses; such axons can nevertheless be electrically stimulated.

Compartment analysis of temporal activity by fluorescence in situ hybridization

(catFISH). A method for comparing immediate-early gene activation in the same neuron in response to two sequential stimuli.

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Anderson, D. Circuit modules linking internal states and social behaviour in flies and mice. Nat Rev Neurosci 17, 692–704 (2016). https://doi.org/10.1038/nrn.2016.125

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