Neural Distribution of Vasotocin Receptor mRNA in Two Species of Songbird

Abstract

The neurohypophyseal hormones vasopressin and oxytocin are produced and released within the mammalian brain, where they act via multiple receptor subtypes. The neural distributions of these receptors, for example, V1a and oxytocin receptors, have been well described in many mammals. In birds, the distribution of binding sites for the homologous neuropeptides, vasotocin (VT) and mesotocin, has been studied in several species by using synthetic radioligands designed to bind to mammalian receptors. Such binding studies, however, may not reveal the specific distributions of each receptor subtype. To identify and map the receptors likely to bind VT and mesotocin, we generated partial cDNA sequences for four VT receptor subtypes, VT1, VT2 (V1b), VT3 (oxytocin-like), and VT4 (V1a), in white-throated sparrow (Zonotrichia albicollis) and zebra finch (Taeniopygia guttata). These genes shared high sequence identity with the homologous avian and mammalian neurohypophyseal peptide receptors, and we found evidence for VT1, VT3, and VT4 receptor mRNA expression throughout the brains of both species. As has been described in rodents, there was striking interspecific and intraspecific variation in the densities and distribution of these receptors. For example, whereas the VT1 receptor mRNA was more widespread in zebra finch brain, the VT3 (oxytocin-like) receptor mRNA was more prevalent in the sparrow brain. Although VT2 (V1b) receptor mRNA was abundant in the pituitary, it was not found in the brain. Because of their association with brain regions implicated in social behavior, the VT1, VT3, and VT4 receptors are all likely candidates for mediating the behavioral effects of VT.

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

“…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.…”

“…For instance, isotocin promotes social approach in goldfish (Carassius auratus) [25] and administration of a non-selective nonapeptide antagonist reduces intersexual affiliation in the convict cichlid [20]. In zebra finches, flocking behaviour and preferences for familiar social partners are reduced, following administration of an OTA [26] that probably binds to the oxytocic VT3 receptor [27]. Furthermore, variation in affiliative behaviour between pairs in tamarins (Saguinus oedipus) is correlated with variation in urinary OT levels [28].…”

Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches

“…Interestingly, unlike voles, zebra finches and other socially monogamous songbirds do not express OTR or V1aR mRNA at detectable levels in either the ventromedial striatum (including the nucleus accumbens) or ventral pallidum (31). In contrast, they do express high densities of OTRs in the LS (18,31), an area where both OTRs and V1aRs are required for VP-mediated effects on pair bonding in male prairie voles (10).…”

“…In contrast, they do express high densities of OTRs in the LS (18,31), an area where both OTRs and V1aRs are required for VP-mediated effects on pair bonding in male prairie voles (10). Comparable experiments have not been conducted in female voles.…”

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

“…Optical densities (ODs) of immunolabeling were measured in the medial preoptic nucleus, several hypothalamic areas (PVN, AH, and lateral and medial divisions of the VMH); anterior and posterior medial amygdala (MeA); BSTm; lateral BST; central gray; nucleus intercollicularis; rostral and caudal VTA; and nucleus accumbens. In addition, we quantified labeling in subnuclei of the septal complex that are differentiated on the basis of chemoarchitecture, peptide receptor distributions, and/or transcriptional responses to social stimuli (4,10,11,25,26). These are the nucleus of the pallial commissure; caudocentral septum (CcS); rostral LS subdivision (LSr); and both pallial and subpallial portions of the caudal LS subdivision, which are denoted here as LSc.d and subpallial LSc (includes both ventral and ventrolateral subnuclei).…”