Neural substrates of aggression and flight in the cat

Human aggression typologies largely correspond with those for other animals. While there may be no non-human equivalent of angry reactive aggression, we propose that human proactive aggression is similar to offense in other animals’ dominance contests for territory or social status. Like predation/hunting, but unlike defense, offense and proactive aggression are positively reinforcing, involving dopamine release in accumbens. The drive these motivational states provide must suffice to overcome fear associated with initiating risky fights. We term the neural activity motivating proactive aggression “non-angry aggressive arousal”, but use “angriffsberietschaft” for offense motivation in other animals to acknowledge possible differences. Temporal variation in angriffsberietschaft partitions fights into bouts; engendering reduced anti-predator vigilance, redirected aggression and motivational over-ride. Increased aggressive arousal drives threat-to-attack transitions, as in verbal-to-physical escalation and beyond that, into hyper-aggression. Proactive aggression and offense involve related neural activity states. Cingulate, insular and prefrontal cortices energize/modulate aggression through a subcortical core containing subnuclei for each aggression type. These proposals will deepen understanding of aggression across taxa, guiding prevention/intervention for human violence.

Agonistic interaction is important for establishing social hierarchy and determining access to limited resources. Although there are substantial studies investigating the neural mechanisms of aggressive or defensive behavior in male rodents, little attention has been paid to the mechanisms underlying agonistic behaviors in females. In the present study, we depicted patterns of agonistic behaviors in sexually naïve female Mongolian gerbils (Meriones unguiculatus) and examined the neuronal activation in the brain by Fos-immunoreactive (Fos-ir) staining. We found that the winner-loser relationship was established rapidly. Winners displayed higher levels of aggression, environmental exploration, scent marking, and self-grooming, but less defensive behavior, in comparison to losers. Several patterns of Fos-ir expression emerged following agonistic interactions. Winners had the number of Fos-ir cells in the ventrolateral subnucleus of the ventromedial hypothalamus (VMHvl) and dorsal periaqueductal grey (PAGd) more than the controls but less than the losers. Losers also had more Fos-ir cells in the paraventricular nucleus of the hypothalamus (PVN), anterior medial (BSTam) and anteriolateral (BSTal) subnuclei of the bed nucleus of the stria terminalis (BST), and the ventral subnucleus of the lateral septum (LSv), as well as less Fos-ir cells in the dentate gyrus of the hippocampus (DG), compared to the controls. In addition, the number of Fos-ir cells showed similar increases in the principal nucleus (BSTpr) and interfascicular nucleus (BSTif) of the BST and amygdala (AMYG) in both the winners and losers, compared to the controls. Together, these data illustrate the patterns of altered neuronal activation in a behavior-, social status-, and brain region-specific manner, implicating potential roles of the brain neural circuit in mediating agonistic interactions in female Mongolian gerbils.

Aggression is a crucial survival behavior: it is employed to defend territory, compete for food and mating opportunities, protect kin, and resolve disputes. Two highly conserved circuitries emerge as critical substrates for generating and modulating aggression. One circuitry centers on the medial hypothalamus, a brain region essential for driving the expression of aggressive behaviors. The other circuit involves the mesolimbic dopamine cells. Animal studies support essential roles of mesolimbic dopaminergic signaling in assessing the reward value of aggression and reinforcing aggressive behaviors. In this review, we will provide an overview regarding the functions of medial hypothalamus and dopaminergic system in mediating aggressive behaviors and the potential interactions between these two circuitries.

The interactions between predator and prey represent some of the most dramatic events in nature and constitute a matter of life and death for both sides. The hypothalamus has been implicated in driving predation and evasion; however, the exact hypothalamic neural circuits underlying these behaviors remain poorly defined. Here, we demonstrate that inhibitory and excitatory projections from the mouse lateral hypothalamus (LH) to the periaqueductal gray (PAG) in the midbrain drive, respectively, predation and evasion. LH GABA neurons were activated during predation. Optogenetically stimulating PAG-projecting LH GABA neurons drove strong predatory attack, and inhibiting these cells reversibly blocked predation. In contrast, LH glutamate neurons were activated during evasion. Stimulating PAG-projecting LH glutamate neurons drove evasion and inhibiting them impeded predictive evasion. Therefore, the seemingly opposite behaviors of predation and evasion are tightly regulated by two dissociable modular command systems within a single neural projection from the LH to the PAG.

Aggression is a prevalent behavior in the animal kingdom that is used to settle competition for limited resources. Given the high risk associated with fighting, the central nervous system has evolved an active mechanism to modulate its expression. Lesioning the lateral septum (LS) is known to cause “septal rage,” a phenotype characterized by a dramatic increase in the frequency of attacks. To understand the circuit mechanism of LS-mediated modulation of aggression, we examined the influence of LS input on the cells in and around the ventrolateral part of the ventromedial hypothalamus (VMHvl)—a region required for male mouse aggression. We found that the inputs from the LS inhibited the attack-excited cells but surprisingly increased the overall activity of attack-inhibited cells. Furthermore, optogenetic activation of the projection from LS cells to the VMHvl terminated ongoing attacks immediately but had little effect on mounting. Thus, LS projection to the ventromedial hypothalamic area represents an effective pathway for suppressing male aggression.

Aversive social interactions, such as social defeat, can alter a variety of behavioral and cognitive functions. In the present study, we examined the effects of social defeat and the subsequent housing on behavior as well as cell proliferation and cell survival in the solitary, male greater long-tailed hamster (Tscheskia triton). We found that three days of agonistic interactions reliably led to a subordinate-dominant relationship between pairs of male hamsters. However, such behavioral interactions did not alter cell proliferation in any of the brain areas examined. In addition, subordinate males housed in close proximity to the dominant male (separated by a wire screen) following social defeat did not display differences in agonistic behaviors, but had enhanced cell proliferation in the anterior hypothalamus, ventromedial hypothalamus (VMH), and amygdala as well as increased cell survival in the VMH, compared to subordinate males that were housed individually. Together, our data indicate distinct effects of agonistic interactions and the social housing condition on behavior as well as cell proliferation and survival in the brain of the greater long-tailed hamster.