1While the ventromedial hypothalamus, ventrolateral area (VMHvl) is now well established as a 2 critical locus for the generation of conspecific aggression, its role is complex, with populations of 3 neurons responding during the motivational, sensory, and action phases of aggression, and also 4 during social interactions with the opposite sex. It has been previously unclear how the brain 5 uses this complex multidimensional signal and generates a discrete action: the attack. Here we 6 find that the largest posterior target of the VMHvl, the lateral periaqueductal gray (lPAG) 7 encodes a simplified attack-selective signal during aggression. Single units in the lPAG exhibit 8 greater selectivity for the attack action during aggression than VMHvl neurons and a 9 subpopulation of neurons in the PAG exhibit short-latency, time-locked spiking relative to the 10 activity of jaw muscles for biting during attack. In addition, channelrhodopsin assisted circuit 11 mapping reveals a preferential projection from VMHvl glutamatergic cells to lPAG glutamatergic 12 cells. Using projection-specific fiber photometry, we find that this excitatory projection conveys 13 male-biased signals from the VMHvl to downstream glutamatergic PAG neurons that integrate 14 ongoing male-related activity over several seconds, which suggests that action-selectivity is 15 generated by a combination of both pre and postsynaptic filtering mechanisms. 16 17 18 muscle 19 20The VMHvl has emerged as a clearing house for socially relevant information, 21 responding during attack, but also exhibiting increased activity during sensory investigation of 22 males and females and during the preparatory phase prior to attack (Falkner et al. 2016(Falkner et al. , 2014 23 Remedios et al. 2017; Lin et al. 2011). In addition, suppression of VMHvl activity decreases not 24 only the frequency of attack, but also investigatory, sexual, and aggression-seeking 25 behaviors (Yang et al. 2013; Lee et al. 2014; Falkner et al. 2016). How then do neurons 26 3 downstream of the VMHvl interpret this complex code to drive aggression? Pharmacological 27 manipulation of PAG circuits have been shown affect the efficacy of hypothalamic-mediated 28 conspecific aggression, strongly indicating that the PAG's actions are downstream of the 29 hypothalamus (Zalcman and Siegel 2006; Gregg and Siegel 2003), though its precise role in 30 this transformation has remained unclear. The emerging role of the PAG in the expression of 31 other innate behaviors, such as stimulus-induced flight, appears to be that of a split-second 32 action (Evans et al. 2018; Wang et al. 2019). We reasoned that a parallel circuit in the PAG 33 might perform a similar function during conspecific attack. 34We reversibly suppressed the activity of the PAG during freely moving interactions with 35 males and females using the GABAA agonist muscimol and tested whether inactivation altered 36 conspecific social behaviors, including attack and investigation. We found that inactivation of 37 the PAG produced action-s...
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