An aggression-specific cell type in the anterior hypothalamus of finches

Abstract

The anterior hypothalamus (AH) is a major integrator of neural processes related to aggression and defense, but cell types in the AH that selectively promote aggression are unknown. We here show that aggression is promoted in a very selective and potent manner by dorsal AH neurons that produce vasoactive intestinal polypeptide (VIP). Fos activity in a territorial finch, the violet-eared waxbill (Estrildidae: Uraeginthus granatina) is positively related to aggression in the dorsal AH, overlapping a population of VIP-producing neurons. VIP is known to promote territorial aggression in songbirds, and thus we used antisense oligonucleotides to selectively block AH VIP production in male and female waxbills. This manipulation virtually abolishes aggression, reducing the median number of displacements in a 3-min resident-intruder test from 38 in control subjects to 0 in antisense subjects. Notably, most antisense and control waxbills exhibit an agonistic response such as a threat or agonistic call within 2 s of intrusion. Thus, antisense subjects clearly classify intruders as offensive, but fail to attack. Other social and anxiety-like behaviors are not affected and VIP cell numbers correlate positively with aggression, suggesting that these cells selectively titrate aggression. Additional experiments in the gregarious zebra finch (Estrildidae: Taeniopygia guttata) underscore this functional specificity. Colony-housed finches exhibit significant reductions in aggression (primarily nest defense) following AH VIP knockdown, but no effects are observed for social preferences, pair bonding, courtship, maintenance behaviors, or anxiety-like behaviors. To our knowledge, these findings represent a unique identification of an aggression-specific cell type in the brain.neuropeptide | reproduction T he anterior hypothalamus (AH) is a hub of neural processes related to aggression and agonistic communication in taxa ranging from fish to mammals (1-9). The AH is strongly interconnected with the ventrolateral subnucleus of the ventromedial hypothalamus (VMHvl) (10), and both areas are overlapped by the "hypothalamic attack area," a region from which aggressive behavior is elicited by electrical stimulation in mammals (7,9,11,12). A comparable organization is found in birds, as demonstrated by both electrical stimulation (1, 8) and immediate early gene expression (13,14). The AH and VMHvl integrate information from many socially relevant forebrain regions and project to midbrain areas that regulate motivation and motor processes (10,(15)(16)(17). However, whereas recent studies in male mice show that overlapping but distinct neuronal populations of the VMHvl regulate fighting and mating (18), the neurochemical phenotypes of aggression-related neurons in the VMHvl and AH are largely unknown (7). AH vasopressin neurons that promote aggression in voles also influence affiliation (5), and the AH further regulates stress response and defense (12,14,19). Thus, the identification of AH neurons that selectively promote aggression requires t...

The neurobiology of offensive aggression: Revealing a modular view

“…In hamsters, local injection of vasopressin receptor antagonists in the AHA increased the attack latency and decreased the number of attacks [46], while in monogamous voles AHA vasopressin-containing neurons were causally linked to aggression [47]. In zebra finches, Vasoactive Intestinal Polypeptide (VIP)-expressing cell types in the AHA were demonstrated to be specifically involved in aggression [48].…”

Social descent with territory loss causes rapid behavioral, endocrine, and transcriptional changes in the brain

“…Therefore, transcriptional changes that alter outputs of aggressive signaling in the ATn could contribute to reduced dominance and increased subordination in descending male A. burtoni. Further, increased egr-1 levels in the VTn of descending males may serve a related function, as this homolog of the anterior hypothalamus also plays a role in aggression in other vertebrates (Goodson et al, 2012). The POA is composed of many nuclei with a multitude of functions including regulation of sexual behavior, reproductive physiology, aggression, parental care, stress-coping, energy homeostasis, thermoregulation, sleep and arousal (O'Connell and Hofmann, 2011).…”

Seasonal Variation in Group Size Is Related to Seasonal Variation in Neuropeptide Receptor Density

“…We quantified binding in numerous forebrain areas known to be involved in regulating grouping behavior, affiliation, stress processes and other social behaviors in birds and/or mammals. These areas include the MeA (level 1, capping the solid band of the ventral amygdalofugal tract; level 2, ventromedial to the fascicles of the ventral amygdalofugal tract; level 3, ventral to the robust nucleus of the arcopallium (RA) [Goodson et al, 2012b]), BSTm/lateral BST (BSTl) (supracommissural), medial preoptic area (MPA; rostral, medial to the septomesencephalic tract ), medial preoptic nucleus (MPO; caudal, ventral to the anterior commissure), anterior hypothalamus (delineated as in Goodson et al [2012a]), VMH, PVN, tuberal hypothalamus (TH) and various subnuclei of the septal complex (as differentiated by chemoarchitecture , receptor distributions and/or transcriptional responses to social stimuli). We also quantified binding within the dorsal and lateral divisions of the rostral arcopallium (Arco-r.d and Arco-r.l), as this forebrain area showed high levels of specific binding, particularly for 125 I-OVTA.…”