Mammal-Like Organization of the Avian Midbrain Central Gray and a Reappraisal of the Intercollicular Nucleus

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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...

Section: Discussionmentioning

confidence: 77%

“…Dominant waxbills show a very different pattern of Fos expression, with Fos expression in the lateral portion of intercollicularis correlating positively with displacements (38).…”

Section: Discussionmentioning

confidence: 99%

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

Goodson

Kelly

Kingsbury

et al. 2012

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“…This study goes a step further, by demonstrating the dissociability between the motivation to perform a complex social behavior and its quality as well as its coordination with relevant stimuli (the female). It is likely that T acting at neural substrates in multiple areas of the social behavior network (45,46) that includes the POM, as well as in the SCS itself (2), is required for the occurrence of the full suite of reproductive behaviors present in songbirds.…”

Section: Discussionmentioning

confidence: 99%

Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate

Alward

Balthazart

Ball

2013

117

144

Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a particular social context as well as the quality of song produced. The neural substrate(s) where T acts to regulate the motivation to sing as opposed to other aspects of song has not been definitively characterized. We show here that T implants in the medial preoptic nucleus (POM) of castrated male canaries (Serinus canaria) increase song rate but do not enhance acoustic features such as song stereotypy compared with birds receiving peripheral T that can act globally throughout the brain. Strikingly, T action in the POM increased song control nuclei volume, consistent with the hypothesis that singing activity induces neuroplasticity in the song control system independent of T acting in these nuclei. When presented with a female canary, POM-T birds copulated at a rate comparable to birds receiving systemic T but produced fewer calls and songs in her presence. Thus, POM is a key site where T acts to activate copulation and increase song rate, an appetitive sexual behavior in songbirds, but T action in other areas of the brain or periphery (e.g., HVC, dopaminergic cell groups, or the syrinx) is required to enhance the quality of song (i.e., stereotypy) as well as regulate context-specific vocalizations. These results have broad implications for research concerning how steroids act at multiple brain loci to regulate distinct sociosexual behaviors and the associated neuroplasticity.activity-driven plasticity | singing motivation | preoptic area S teroid hormones such as testosterone (T) can have multiple effects on physiology, morphology, and behavior (1-4). These pleiotropic effects of steroids allow coordinating suites of traits into an organized functional response (5, 6). In the case of the regulation of behavior, both motivational and performance aspects of behavior as well cognitive components are often activated by the same hormone (2, 7). The neural sites of steroid action coordinating these distinct aspects of an integrated behavioral response have not been well characterized. In this study, we investigated the site of hormone action in relation to the activation of different aspects of birdsong to illustrate how such an integrated regulation can occur.Birdsong is a species-typical, stereotypic set of usually long, learned, complex vocalizations produced in reproductive contexts (8). A discrete network of interconnected brain nuclei orchestrates song learning and production (from here on called the song control system or SCS) (3, 9-11). Areas such as HVC (acronym is proper name) and the robust nucleus of the arcopallium (RA) regulate the production of song, whereas areas such as Area X and LMAN are involved in song learning. These forebrain nuclei can undergo remarkable plasticity in response to seasonally changing T (12, 13; see refs. 2 and 14 for review). There is also evidence that other factors such as singing ac...

“…Thus, in both taxa significant activation is observed in the medial bed nucleus of the stria terminalis (BSTm), lateral septum (LS), paraventricular nucleus of the hypothalamus (PVN), anterior hypothalamus (AH), lateral portion of the ventromedial hypothalamus (VMH), and midbrain central gray (4-7; also see ref. 8). For the year-round territorial song sparrow, immediate early gene results are largely comparable in winter and summer (4,5), although microarray data suggest that hypothalamic responses to simulated intrusion are very different in winter and summer, perhaps reflecting the fact that luteinizing hormone is released during territorial challenges only in the breeding season (9).…”

mentioning

confidence: 99%

To flock or fight: Neurochemical signatures of divergent life histories in sparrows

Goodson

Wilson

Schrock

2012

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Many bird species exhibit dramatic seasonal switches between territoriality and flocking, but whereas neuroendocrine mechanisms of territorial aggression have been extensively studied, those of seasonal flocking are unknown. We collected brains in spring and winter from male field sparrows ( Spizella pusilla ), which seasonally flock, and male song sparrows ( Melospiza melodia ), which are territorial year-round in much of their range. Spring collections were preceded by field-based assessments of aggression. Tissue series were immunofluorescently multilabeled for vasotocin, mesotocin (MT), corticotropin-releasing hormone (CRH), vasoactive intestinal polypeptide, tyrosine hydroxylase, and aromatase, and labeling densities were measured in many socially relevant brain areas. Extensive seasonal differences are shared by both species. Many measures correlate significantly with both individual and species differences in aggression, likely reflecting evolved mechanisms that differentiate the less aggressive field sparrow from the more aggressive song sparrow. Winter-specific species differences include a substantial increase of MT and CRH immunoreactivity in the dorsal lateral septum (LS) and medial amygdala of field sparrows but not song sparrows. These species differences likely relate to flocking rather than the suppression of winter aggression in field sparrows, because similar winter differences were found for two other emberizids that are not territorial in winter—dark-eyed juncos ( Junco hyemalis ), which seasonally flock, and eastern towhees ( Pipilo erythropthalmus ), which do not flock. MT signaling in the dorsal LS is also associated with year-round species differences in grouping in estrildid finches, suggesting that common mechanisms are targeted during the evolution of different life histories.