Mesotocin and Nonapeptide Receptors Promote Estrildid Flocking Behavior

Abstract

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.

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

“…Estrildid finches that are gregarious year-round exhibit nonapeptide binding sites in the rostral LSc.d (pallial LS) at much higher densities than do territorial estrildids (10,11). The relevance of these binding sites to flocking is supported by the demonstrations that intraventricular and intraseptal infusions of nonapeptide receptor antagonists (V 1a and oxytocin receptor antagonists) reduce preferences for larger groups in the highly gregarious zebra finch (11, 13), as does antisense knockdown of VT-ir neurons in the BSTm (13)-neurons that seem to provide the majority of VT-ir innervation to the LS (28,29).…”

“…These studies show that multiple neurochemical systems have evolved in relation to grouping behavior, particularly within the LS and associated subnuclei of the posterior septum. Receptor densities for vasotocin (VT; homolog of the mammalian nonapeptide vasopressin), mesotocin (MT; homolog of the mammalian nonapeptide oxytocin), corticotropin-releasing hormone (CRH), and vasoactive intestinal polypeptide (VIP) all exhibit patterns of parallel and divergent evolution that closely track species-typical group size (10,11). Furthermore, VT neurons in the BSTm that project to the LS are sensitive to social valence and exhibit differential Fos responses in territorial and flocking species (12).…”

“…Furthermore, VT neurons in the BSTm that project to the LS are sensitive to social valence and exhibit differential Fos responses in territorial and flocking species (12). Antisense knockdown of VT production in those cells potently reduces gregariousness in the highly social zebra finch (Taeniopygia guttata) (13), and antagonism of V 1a -like and oxytocic receptors in the septum likewise reduces preferred group sizes (11,13). The relative distribution of nonapeptide receptors across LS subnuclei may also be relevant to species differences in grouping, because flocking species have proportionally higher receptor binding in the dorsal (pallial) LS, whereas territorial species exhibit proportionally more binding in the subpallial LS (10,11).…”

“…Antisense knockdown of VT production in those cells potently reduces gregariousness in the highly social zebra finch (Taeniopygia guttata) (13), and antagonism of V 1a -like and oxytocic receptors in the septum likewise reduces preferred group sizes (11,13). The relative distribution of nonapeptide receptors across LS subnuclei may also be relevant to species differences in grouping, because flocking species have proportionally higher receptor binding in the dorsal (pallial) LS, whereas territorial species exhibit proportionally more binding in the subpallial LS (10,11). Consistent with these findings, septal VT infusions reduce territorial aggression in emberizid sparrows and estrildid finches (14,15).…”

“…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).…”