Neural distribution of nonapeptide binding sites in two species of songbird.
ABSTRACT Vasotocin (VT) and its mammalian homologue, vasopressin (VP), modulate many social behaviors in a variety of vertebrate species. In songbirds, the effects of centrally administered VT vary according to species, which may reflect species-specific distributions of VT binding sites. Different radioligands used to map receptors in previous autoradiographical studies have revealed nonoverlapping distributions of VT binding, suggesting a heterogeneous population of more than one type of VT receptor. For two model songbird species, the white-throated sparrow (Zonotrichia albicollis) and zebra finch (Taeniopygia guttata), we labeled putative VT receptors with two radioligands, [(125)I]ornithine vasotocin analog ([(125)I]OVTA) and [(125)I]linear VP antagonist ([(125)I]HO-LVA). Competitive binding assays in the lateral septum showed that both ligands were effectively displaced by both VT and a related nonapeptide, mesotocin (MT), showing that these radioligands, which were developed to label mammalian nonapeptide receptors, label at least one population of related receptors in songbirds. [(125)I]OVTA labeled receptors throughout the telencephalon, diencephalon, midbrain, and brainstem, with a similar distribution in both species. In contrast, the binding of [(125)I]HO-LVA was restricted to the septal area, dorsal arcopallium, and optic tectum in sparrow and was essentially undetectable in zebra finch. Because the avian brain is likely to express multiple types of VT receptors, we hypothesize that the binding patterns of these radioligands represent a heterogeneous receptor population.
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ABSTRACT: Of the major vertebrate taxa, Class Aves is the most extensively studied in relation to the evolution of social systems and behavior, largely because birds exhibit an incomparable balance of tractability, diversity, and cognitive complexity. In addition, like humans, most bird species are socially monogamous, exhibit biparental care, and conduct most of their social interactions through auditory and visual modalities. These qualities make birds attractive as research subjects, and also make them valuable for comparative studies of neuroendocrine mechanisms. This value has become increasingly apparent as more and more evidence shows that social behavior circuits of the basal forebrain and midbrain are deeply conserved (from an evolutionary perspective), and particularly similar in birds and mammals. Among the strongest similarities are the basic structures and functions of avian and mammalian nonapeptide systems, which include mesotocin (MT) and arginine vasotocin (VT) systems in birds, and the homologous oxytocin (OT) and vasopressin (VP) systems, respectively, in mammals. We here summarize these basic properties, and then describe a research program that has leveraged the social diversity of estrildid finches to gain insights into the nonapeptide mechanisms of grouping, a behavioral dimension that is not experimentally tractable in most other taxa. These studies have used five monogamous, biparental finch species that exhibit group sizes ranging from territorial male-female pairs to large flocks containing hundreds or thousands of birds. The results provide novel insights into the history of nonapeptide functions in amniote vertebrates, and yield remarkable clarity on the nonapeptide biology of dinosaurs and ancient mammals. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.Hormones and Behavior 01/2012; 61(3):239-50. · 3.87 Impact Factor
Article: Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty.[show abstract] [hide abstract]
ABSTRACT: 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.Hormones and Behavior 02/2011; 60(1):12-21. · 3.87 Impact Factor
Article: Oxytocin and social motivation.[show abstract] [hide abstract]
ABSTRACT: Humans are fundamentally social creatures who are ‘motivated’ to be with others. In this review we examine the role of oxytocin (OT) as it relates to social motivation. OT is synthesized in the brain and throughout the body, including in the heart, thymus, gastrointestinal tract, as well as reproductive organs. The distribution of the OT receptor (OTR) system in both the brain and periphery is even more far-reaching and its expression is subject to changes over the course of development. OTR expression is also sensitive to changes in the external environment and the internal somatic world. The OT system functions as an important element within a complex, developmentally sensitive biobehavioral system. Other elements include sensory inputs, the salience, reward, and threat detection pathways, the hypothalamic-pituitary-gonadal axis, and the hypothalamic-pituitary-adrenal stress response axis. Despite an ever expanding scientific literature, key unresolved questions remain concerning the interplay of the central and peripheral components of this complex biobehavioral system that dynamically engages the brain and the body as humans interact with social partners over the course of development.Developmental cognitive neuroscience. 10/2011; 1(4):471-93.