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.

Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird

“…This effect is not due to general memory impairments, as no deficits are observed in tests of nonsocial memory [40]. Because the medial amygdala in birds (formerly nucleus taeniae [43,44]) exhibits at least a modest level of OTA binding [34], the amygdala could be another site of action that by itself, or together with the LS, mediates the effects of OTA observed here.…”

“…Because autoradiographic data show that the distribution of OTA binding sites in birds is virtually identical to that of VT3 mRNA expression [26,27,34], it is likely that the OTA effects observed here are mediated via the oxytocic VT3 receptor. Notably, competitive binding experiments show that MT and VT have a comparable ability to displace radiolabelled OTA [34], and, similarly, mammalian nonapeptides are also somewhat promiscuous in their receptor binding.…”

“…However, nonapeptides may potentially influence pair bonding via actions at multiple other receptor types, including the VT1 receptor (a V 2b receptor [35]), which is distributed in numerous brain areas [27], and the OT-like VT3 receptor. Because the VT3 receptor appears to be promiscuous [34], the OTA effects observed in the present study may reflect the actions of endogenous MT, VT or both.…”

“…Notably, competitive binding experiments show that MT and VT have a comparable ability to displace radiolabelled OTA [34], and, similarly, mammalian nonapeptides are also somewhat promiscuous in their receptor binding. Despite this promiscuity, OTA effects on zebra finch social preferences are reversed with administration of MT, but not VT [26], perhaps owing to differential binding of VT and MT to the three nonapeptide receptor types present in the brain.…”

“…Zebra finches also exhibit no VT4 (V1aR) expression in the ventral pallidum [27], the site most extensively studied in relation to pair bonding in male voles. However, VP promotes pair bond formation in male prairie voles by binding to both OTRs and V1aRs in the LS [16], and the zebra finch VT3 receptor is heavily expressed in the LS [26,27,34]. Administration of either OTA or a V 1a antagonist into the LS blocks pair bond formation in male prairie voles, whereas administration of VP induces pair bond formation in the absence of mating [16].…”