David Kabelik

Mesotocin and nonapeptide receptors promote estrildid flocking behavior.

Why Birds of a Feather Flock Together The biological determination of sociality, that is, why one might choose to associate with others and how many, has been unclear. Goodson et al. (p. 862) show that in gregarious finches, oxytocin-like receptors and their cognate ligand, mesotocin, are associated with group size choices. Receptor distributions clearly differentiate territorial species from flocking species. Furthermore, these compounds appear to play a role in affecting choice in affiliation in mammals, and thus may be conserved across evolutionary distant taxa. Oxytocin and oxytocin-like receptors control group size preference in a songbird, suggesting an evolutionarily conserved role in social affiliation. Proximate neural mechanisms that influence preferences for groups of a given size are almost wholly unknown. In the highly gregarious zebra finch (Estrildidae: Taeniopygia guttata), blockade of nonapeptide receptors by an oxytocin (OT) antagonist significantly reduced time spent with large groups and familiar social partners independent of time spent in social contact. Opposing effects were produced by central infusions of mesotocin (MT, avian homolog of OT). Most drug effects appeared to be female-specific. Across five estrildid finch species, species-typical group size correlates with nonapeptide receptor distributions in the lateral septum, and sociality in female zebra finches was reduced by OT antagonist infusions into the septum but not a control area. We propose that titration of sociality by MT represents a phylogenetically deep framework for the evolution of OT’s female-specific roles in pair bonding and maternal functions.

Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship

Mesolimbic dopamine (DA) circuits mediate a wide range of goal-oriented behavioral processes, and DA strongly influences appetitive and consummatory aspects of male sexual behavior. In both birds and mammals, mesolimbic projections arise primarily from the ventral tegmental area (VTA), with a smaller contribution from the midbrain central gray (CG). Despite the well known importance of the VTA cell group for incentive motivation functions, relationships of VTA subpopulations to specific aspects of social phenotype remain wholly undescribed. We now show that in male zebra finches (Estrildidae: Taeniopygia guttata), Fos activity within a subpopulation of tyrosine hydroxylase-immunoreactive (TH-ir; presumably dopaminergic) neurons in the caudal VTA is significantly correlated with courtship singing and coupled to gonadal state. In addition, the number of TH-ir neurons in this caudal subpopulation dichotomously differentiates courting from non-courting male phenotypes, and evolves in relation to sociality (flocking vs. territorial) across several related finch species. Combined, these findings for the VTA suggest that divergent social phenotypes may arise due to the differential assignment of “incentive value” to conspecific stimuli. TH-ir neurons of the CG (a population of unknown function in mammals) exhibit properties that are even more selectively and tightly coupled to the expression of courtship phenotypes (and appetitive courtship singing), both in terms of TH-ir cell number, which correlates significantly with constitutive levels of courtship motivation, and with TH-Fos colocalization, which increases in direct proportion to the phasic expression of song. We propose that these neurons may be core components of social communication circuits across diverse vertebrate taxa.

Endogenous Vasotocin Exerts Context-Dependent Behavioral Effects in a Semi-Naturalistic Colony Environment

Arginine vasotocin (VT), and its mammalian homologue arginine vasopressin (VP), are neuropeptides involved in the regulation of social behaviors and stress responsiveness. Previous research has demonstrated opposing effects of VT/VP on aggression in different species. However, these divergent effects were obtained in different social contexts, leading to the hypothesis that different populations of VT/VP neurons regulate behaviors in a context-dependent manner. We here use VP antagonists to block endogenous VT function in male zebra finches (Taeniopygia guttata) within a semi-natural, mixed-sex colony setting. We examine the role of VT in the regulation of aggression and courtship, and in pair bond formation and maintenance, over the course of three days. Although our results confirm previous findings, in that antagonist treatment reduces aggressive mate competition during an initial behavioral session during which males encounter novel females, we find that the treatment effects are completely reversed within hours of colony establishment, and the antagonist treatment instead facilitates aggression in later sessions. This reversal occurs as aggression shifts from mate competition to nest defense, but is not causally associated with pairing status per se. Instead, we hypothesize that these divergent effects reflect context-specific activation of hypothalamic and amygdalar VT neurons that exert opposing influences on aggression. Across contexts, effects were highly specific to aggression and the antagonist treatment clearly failed to alter latency to pair bond formation, pair bond stability, and courtship. However, VT may still potentially influence these behaviors via promiscuous oxytocin-like receptors, which are widely distributed in the zebra finch brain.

Dynamic neuromodulation of aggression by vasotocin: influence of social context and social phenotype in territorial songbirds

The homologous neuropeptides vasotocin (VT) and vasopressin (VP) influence agonistic behaviours across many taxa, but peptide–behaviour relationships are complex and purportedly species-specific. Putative species-specific effects in songbirds are confounded with context, however, such that territorial species have been tested only in resident–intruder paradigms and gregarious species have been tested only in a mate competition paradigm. Using the territorial violet-eared waxbill (Estrildidae: Uraeginthus granatina), we now show that a V1a receptor antagonist reduces male aggression during mate competition (as in gregarious finches), but does not affect resident–intruder aggression in dominant males. However, the V1a antagonist disinhibits aggression in less aggressive (typically subordinate) males. These results are consistent with recent data on the activation of different VT cell groups during positive and negative social interactions. Thus, VT influences aggression similarly across territorial and gregarious species, but in context- and phenotype-specific ways that probably reflect the differential activation of discrete VT cell groups.

Steroid hormone mediation of limbic brain plasticity and aggression in free-living tree lizards, Urosaurus ornatus

The neural mechanisms by which steroid hormones regulate aggression are unclear. Although testosterone and its metabolites are involved in both the regulation of aggression and the maintenance of neural morphology, it is unknown whether these changes are functionally related. We addressed the hypothesis that parallel changes in steroid levels and brain volumes are involved in the regulation of adult aggression. We examined the relationships between seasonal hormone changes, aggressive behavior, and the volumes of limbic brain regions in free-living male and female tree lizards (Urosaurus ornatus). The brain nuclei that we examined included the lateral septum (LS), preoptic area (POA), amygdala (AMY), and ventromedial hypothalamus (VMH). We showed that the volumes of the POA and AMY in males and the POA in females vary with season. However, reproductive state (and thus hormonal state) was incompletely predictive of these seasonal changes in males and completely unrelated to changes in females. We also detected male-biased dimorphisms in volume of the POA, AMY, and a dorsolateral subnucleus of the VMH but did not detect a dimorphism between alternate male morphological phenotypes. Finally, we showed that circulating testosterone levels were higher in males exhibiting higher frequency and intensity of aggressive display to a conspecific, though brain nucleus volumes were unrelated to behavior. Our findings fail to support our hypothesis and suggest instead that plasma testosterone level covaries with aggression level and in a limited capacity with brain nucleus volumes but that these are largely unrelated relationships.

Dopaminergic regulation of mate competition aggression and aromatase-Fos colocalization in vasotocin neurons.

Recent experiments demonstrate that aggressive competition for potential mates involves different neural mechanisms than does territorial, resident-intruder aggression. However, despite the obvious importance of mate competition aggression, we know little about its regulation. Immediate early gene experiments show that in contrast to territorial aggression, mate competition in finches is accompanied by the activation of neural populations associated with affiliation and motivation, including vasotocin (VT) neurons in the medial bed nucleus of the stria terminalis (BSTm) and midbrain dopamine (DA) neurons that project to the BSTm. Although VT is known to facilitate mate competition aggression, the role of DA has not previously been examined. We now show that in male zebra finches (Taeniopygia guttata), mate competition aggression is inhibited by the D(2) agonist quinpirole, though not the D(1) agonist SKF-38393 or the D(4) agonist PD168077. The D(3) agonist 7-OH-DPAT also inhibited aggression, but only following high dose treatment that may affect aggression via nonspecific binding to D(2) receptors. Central VT infusion failed to restore D(2) agonist-inhibited aggression in a subsequent experiment, demonstrating that D(2) does not suppress aggression by inhibiting VT release from BSTm neurons. In a final experiment, we detected D(2) agonist-induced increases in immunofluorescent colocalization of the product of the immediate early gene c-fos and the steroid-converting enzyme aromatase (ARO) within VT neurons of the BSTm. Thus, although VT and DA appear to influence mate competition aggression independently, BSTm VT neurons are clearly influenced by the activation of D(2) receptors, which may modify future behaviors.

Cryptic Regulation of Vasotocin Neuronal Activity but Not Anatomy by Sex Steroids and Social Stimuli in Opportunistic Desert Finches

In most vertebrate species, the production of vasotocin (VT; non-mammals) and vasopressin (VP; mammals) in the medial bed nucleus of the stria terminalis (BSTm) waxes and wanes with seasonal reproductive state; however, opportunistically breeding species might need to maintain high levels of this behaviorally relevant neuropeptide year-round in anticipation of unpredictable breeding opportunities. We here provide support for this hypothesis and demonstrate that these neurons are instead regulated ‘cryptically’ via hormonal regulation of their activity levels, which may be rapidly modified to adjust VT signaling. First, we show that combined treatment of male and female zebra finches (Estrildidae: Taeniopygia guttata) with the androgen receptor antagonist flutamide and the aromatase inhibitor 1,4,6-androstatriene-3,17-dione does not alter the expression of VT immunoreactivity within the BSTm; however, both hormonal treatment and social housing environment (same-sex versus mixed-sex) alter VT colocalization with the immediate early gene product Fos (a proxy marker of neural activation) in the BSTm. In a second experiment, manipulations of estradiol (E2) levels with the aromatase inhibitor letrozole (LET) or subcutaneous E2 implants failed to alter colocalization, suggesting that the colocalization effects in experiment 1 were solely androgenic. LET treatment also did not affect VT immunoreactivity in a manner reversible by E2 treatment. Finally, comparisons of VT immunoreactivity in breeding and nonbreeding individuals of several estrildid species demonstrate that year-round stability of VT immunoreactivity is found only in highly opportunistic species, and is therefore not essential to the maintenance of long-term pair bonds, which are ubiquitous in the Estrildidae.

Aggression- and sex-induced neural activity across vasotocin populations in the brown anole

Activity within the social behavior neural network is modulated by the neuropeptide arginine vasotocin (AVT) and its mammalian homologue arginine vasopressin (AVP). However, central AVT/AVP release causes different behavioral effects across species and social environments. These differences may be due to the activation of different neuronal AVT/AVP populations or to similar activity patterns causing different behavioral outputs. We examined neural activity (assessed as Fos induction) within AVT neurons in male brown anole lizards (Anolis sagrei) participating in aggressive or sexual encounters. Lizards possess simple amniote nervous systems, and their examination provides a comparative framework to complement avian and mammalian studies. In accordance with findings in other species, AVT neurons in the anole paraventricular nucleus (PVN) were activated during aggressive encounters; but unlike in other species, a positive correlation was found between aggression levels and activation. Activation of AVT neurons within the supraoptic nucleus (SON) occurred nonspecifically with participation in either aggressive or sexual encounters. Activation of AVT neurons in the preoptic area (POA) and bed nucleus of the stria terminalis (BNST) was associated with engagement in sexual behaviors. The above findings are congruent with neural activation patterns observed in other species, even when the behavioral outputs (i.e., aggression level) differed. However, aggressive encounters also increased activation of AVT neurons in the BNST, which is incongruous with findings in other species. Thus, some species differences involve the encoding of social stimuli as different neural activation patterns within the AVT/AVP network, whereas other behavioral differences arise downstream of this system.

Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch.

Steroid-induced changes in dopaminergic activity underlie many correlations between gonadal hormones and social behaviors. However, the effects of steroid hormones on the various behaviorally relevant dopamine cell groups remain unclear, and ecologically relevant species differences remain virtually unexplored. We examined the effects of estradiol (E2) manipulations on dopamine (DA) neurons of male and female zebra finches (Taeniopygia guttata), focusing on numbers of tyrosine hydroxylase-immunoreactive (TH-ir) cells in the A8-A15 cell groups, and on TH colocalization with Fos, conducted in the early A.M., in order to quantify basal transcriptional activity. TH is the rate-limiting enzyme for catecholamine synthesis, and specifically DA in the A8-A15 cell groups. In contrast to other examined birds and mammals, reducing E2 levels with the aromatase-inhibitor Letrozole failed to alter TH-ir neuron numbers within the ventral tegmental area (VTA; A10), while increasing neuron numbers in the central gray (CG; A11) and caudal midbrain A8 populations. Consistent with findings in other birds, but not mammals, we also found no effects of E2 manipulations (Letrozole or Letrozole plus E2 replacement) on TH-Fos colocalization in any location. In accordance with previous observations in both mammals and birds, E2 treatment decreased the number of TH-ir neurons in the A12 population of the tuberal hypothalamus, a cell group that inhibits the release of prolactin. In general, males and females exhibited similar TH-ir neuron numbers, although males exhibited significantly more TH-ir neurons in the A11 CG population than did females. These results suggest partial variability in E2 regulation of DA across species.

Steroid hormones alter neuroanatomy and aggression independently in the tree lizard

Steroid hormones effect changes in both neuroanatomy and aggressive behavior in animals of various taxa. However, whether changes in neuroanatomy directly underlie changes in aggression is unknown. We investigate this relationship among steroid hormones, neuroanatomy, and aggression in a free-living vertebrate with a relatively simple nervous system, the tree lizard (Urosaurus ornatus). Weiss and Moore [1] manipulated testosterone and progesterone levels in adult male tree lizards and found that both hormones facilitated aggressive behavior toward a conspecific. In this study, we examined the brains of a subset of these animals to determine whether changes in limbic morphology were associated with hormone-induced changes in aggressive behavior. Specifically, we tested the hypothesis that testosterone and/or progesterone cause changes in neural morphology that are necessary for the expression of testosterones effects on aggressive behavior. We found that both hormones increased aggression; however, only testosterone induced changes in neuroanatomy. Testosterone increased the size of both the amygdala and nucleus sphericus. However, we could detect no individual correlations between neuroanatomy and aggression levels suggesting that the observed large-scale changes in neuroanatomy are not precisely reflective of changes in mechanisms underlying aggression.