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 OT homologue). Most drug effects appear 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.

Vertebrate animals exhibit a spectacular diversity of social behaviors, yet a variety of basic social behavior processes are essential to all species. These include social signaling; discrimination of conspecifics and sexual partners; appetitive and consummatory sexual behaviors; aggression and dominance behaviors; and parental behaviors (the latter with rare exceptions). These behaviors are of fundamental importance and are regulated by an evolutionarily conserved, core social behavior network (SBN) of the limbic forebrain and midbrain. The SBN encodes social information in a highly dynamic, distributed manner, such that behavior is most strongly linked to the pattern of neural activity across the SBN, not the activity of single loci. Thus, shifts in the relative weighting of activity across SBN nodes can conceivably produce almost limitless variation in behavior, including diversity across species (as weighting is modified through evolution), across behavioral contexts (as weights change temporally) and across behavioral phenotypes (as weighting is specified through heritable and developmental processes). Individual neural loci may also express diverse relationships to behavior, depending upon temporal variations in their functional connectivity to other brain regions ("neural context"). We here review the basic properties of the SBN and show how behavioral variation relates to functional connectivity of the network, and discuss ways in which neuroendocrine factors adjust network activity to produce behavioral diversity. In addition to the actions of steroid hormones on SBN state, we examine the temporally plastic and evolutionarily labile properties of the nonapeptides (the vasopressin-and oxytocin-like neuropeptides), and show how variations in nonapeptide signaling within the SBN serve to promote behavioral diversity across social contexts, seasons, phenotypes and species. Although this diversity is daunting in its complexity, the search for common "organizing principles" has become increasingly fruitful. We focus on multiple aspects of behavior, including sexual behavior, aggression and affiliation, and in each of these areas, we show how broadly relevant insights have been obtained through the examination of behavioral diversity in a wide range of vertebrate taxa. Keywords evolution; sociality; hypothalamus; amygdala; preoptic area; lateral septum; bed nucleus of the stria terminalis; songbird; oxytocin; vasotocin; vasopressin; sexual behavior *Correspondence: James L. Goodson, Department of Biology, Indiana University, Bloomington IN 47405 USA w, phone: (812) 856-4756, fax: (812) 855-6705, e-mail: jlgoodso@indiana.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process erro...

Mesolimbic dopamine (DA) circuits mediate a wide range of goaloriented 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 noncourting 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.song ͉ evolution ͉ periaqueductal gray ͉ vocalization A ffiliation behaviors such as courtship, pair bonding, grouping, and parental care can vary dramatically across individuals and species. However, despite the fact that we now know a good deal about the neurobiology of affiliation behaviors (1, 2), we still know very little about the phenotypic variations in neural mechanisms that underlie phenotypic differences in behavior. In fact, nonapeptide systems (the vasopressin-and oxytocin-like peptides) arguably provide the only examples from tetrapod vertebrates in which neural mechanisms have been systematically studied in relation to species-specific social structure (e.g., mating system and sociality) and individual differences in affiliation (3, 4).Among the many other neurochemical systems that regulate motivational and behavioral states, mesolimbic dopamine (DA) circuits are perhaps the strongest candidates as generators of phenotypic diversity. DA influences numerous affiliation behaviors such as pair bonding (5), sexual communication (6-8), and copulation (9-11). Of particular interest are DA cells in the ventral tegmental area (VTA), which are well known to regulate incentive and reward-related processes (12, 13). These cells project o...

Previous comparisons of territorial and gregarious finches (family Estrildidae) suggest the hypothesis that arginine vasotocin (VT) neurons in the medial bed nucleus of the stria terminalis (BSTm) and V 1a -like receptors in the lateral septum (LS) promote flocking behavior. Consistent with this hypothesis, we now show that intraseptal infusions of a V 1a antagonist in male zebra finches (Taeniopygia guttata) reduce gregariousness (preference for a group of 10 versus 2 conspecific males), but have no effect on the amount of time that subjects spend in close proximity to other birds ("contact time"). The antagonist also produces a profound increase in anxiety-like behavior, as exhibited by an increased latency to feed in a novelty-suppressed feeding test. Bilateral knockdown of VT production in the BSTm using LNA-modified antisense oligonucleotides likewise produces increases in anxiety-like behavior and a potent reduction in gregariousness, relative to subjects receiving scrambled oligonucleotides. The antisense oligonucleotides also produced a modest increase in contact time (irrespective of group size). Together, these combined experiments provide clear evidence that endogenous VT promotes preferences for larger flock sizes, and does so in a manner that is coupled to general anxiolysis. Given that homologous peptide circuitry of the BSTm-LS is found across all tetrapod vertebrate classes, these findings may be predictive for other highly gregarious species.Central nonapeptide circuits play phylogenetically widespread roles in the modulation of social behaviors and stress responses and often exert their effects in a species-specific manner (Engelmann et al., 2004;De Vries and Panzica, 2006;Donaldson and Young, 2008;Veenema and Neumann, 2008;Choleris et al., 2009;Goodson and Thompson, 2010). These circuits arise primarily from magnocellular and parvocellular neurons in the preoptic area and hypothalamus that produce either arginine vasotocin (VT; in nonmammalian vertebrates) or arginine vasopressin (VP; in mammals), plus a single oxytocin-like peptide form in any given species. In addition to these cell groups, virtually all tetrapods, including humans, exhibit VT/VP neurons in the medial extended amygdala, primarily within the medial bed nucleus of the stria terminalis (BSTm) (De Vries and Panzica, 2006;Goodson and Thompson, 2010). Unlike the various hypothalamic VT/VP cell groups, the BSTm neurons and their projections to basal forebrain sites such as the lateral septum (LS), medial preoptic area and habenula Absil et al., 2002) are typically sexually

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.