Nonapeptide Receptor Distributions in Promising Avian Models for the Neuroecology of Flocking

Abstract

Collective behaviors, including flocking and group vocalizing, are readily observable across a diversity of free-living avian populations, yet we know little about how neural and ecological factors interactively regulate these behaviors. Because of their involvement in mediating a variety of social behaviors, including avian flocking, nonapeptides are likely mediators of collective behaviors. To advance the neuroecological study of collective behaviors in birds, we sought to map the neuroanatomical distributions of nonapeptide receptors in three promising avian models that are found across a diversity of environments and widely ranging ecological conditions: European starlings, house sparrows, and rock doves. We performed receptor autoradiography using the commercially available nonapeptide receptor radioligands, 125I-ornithine vasotocin analog and 125I-linear vasopressin antagonist, on brain tissue sections from wild-caught individuals from each species. Because there is known pharmacological cross-reactivity between nonapeptide receptor subtypes, we also performed a novel, competitive-binding experiment to examine the composition of receptor populations. We detected binding in numerous regions throughout the brains of each species, with several similarities and differences worth noting. Specifically, we report that all three species exhibit binding in the lateral septum, a key brain area known to regulate avian flocking. In addition, sparrows and starlings show dense binding in the dorsal arcopallium, an area that has received scant attention in the study of social grouping. Furthermore, our competitive binding results suggest that receptor populations in sparrows and starlings differ in the lateral septum versus the dorsal arcopallium. By providing the first comprehensive maps of nonapeptide receptors in European starlings, house sparrows, and rock doves, our work supports the future use of these species as avian models for neuroecological studies of collective behaviors in wild birds.

Expression of oxytocin receptors in the zebra finch brain during vocal development

“…Leung et al (2009; reported that RA capsular labeling was absent in adult zebra finches; instead, the arcopallium labeling seen in adults resembled what we saw here in P75-95 juveniles. Notably, the distinctive 125 I-OVTA labeling in capsular RA that we see here in young zebra finches was previously described in adults of several seasonally breeding species, including canaries (Voorhuis et al, 1990), house sparrows (Ondrasek et al, 2018), European starlings (Ondrasek et al, 2018), dark-eyed juncos (Wilson et al, 2016), and white-throated sparrows (Leung et al, 2009). In seasonal species, song can become highly variable, not unlike plastic song, Fig.…”

“…Although the ligand is highly selective for OTR in rodents, it was more recently shown to bind to both OTR and vasopressin 1a receptors (V1aR) in primates (see Freeman & Young 2016). Its relative affinity for avian nonapeptide receptors has not been thoroughly investigated (but see Leung et al, 2009;Ondrasek et al, 2018;Voorhuis et al, 1990). Songbirds have at least three different nonapeptide receptors that are expressed in brain: OTR, V1aR, and vasopressin 2 receptors (V2R) (Leung et al, 2011).…”

Effects of oxytocin‐family peptides and substance P on locomotor activity and filial preferences in visually naïve chicks

“…Four avian nonapeptide receptors are known, and the nomenclature of the corresponding mammalian receptors based on homology is listed in Table . Notably, telencephalic brain nuclei that show greater activation with exposure to predisposed stimuli have also been documented to have enriched expression of mRNAs for nonapeptide receptors in the white‐throated sparrow and zebra finch (Leung et al., ) as well as in the rock dove, European starling and house sparrows (Ondrasek, Freeman, Bales, & Calisi, ).…”

“…In the domestic chick ( Gallus gallus), both the lateral septum and the avian partial homolog of the medial amygdala, the nucleus taeniae, are selectively responsive to features of predisposed stimuli (Lorenzi et al., ; Mayer, Rosa‐Salva, Loveland, & Vallortigara, ; Mayer, Rosa‐Salva, & Vallortigara, ) and these brain nuclei are known to express nonapeptide receptors in several species, including the chicken (Goodson, Schrock, Klatt, Kabelik, & Kingsbury, ; Leung et al., ; Ondrasek et al., ; Selvam, Jurkevich, & Kuenzel, ; Wilson et al., ). Therefore, it is reasonable to suggest that nonapeptide signalling in these brain nuclei may also be important for initiating the process of imprinting.…”

Social creatures: Model animal systems for studying the neuroendocrine mechanisms of social behaviour

“…Activation of nonapeptide receptors by endogenous mesotocin also promotes social behaviour (preferences for larger groups) and the preference for familiar social partners in the gregarious zebra finch . Antagonism of oxytocin receptors also reduces the preference for larger groups in finches .…”