Seasonal Variation in Group Size Is Related to Seasonal Variation in Neuropeptide Receptor Density

Abstract

In many species, seasonal variation in grouping behavior is widespread, with shifts towards territoriality in the breeding season and grouping in the winter. Compared to the hormonal and neural mechanisms of seasonal territorial aggression, the mechanisms that promote seasonal grouping have received little attention. We collected brains in spring and winter from wild-caught males of two species of emberizid sparrows that seasonally flock (the field sparrow, Spizella pusilla, and the dark-eyed junco, Junco hyemalis) and two species that do not seasonally flock (the song sparrow, Melospiza melodia, and the eastern towhee, Pipilo erythrophthalmus). We used receptor autoradiography to quantify seasonal plasticity in available binding sites for three neuropeptides known to influence social behavior. We examined binding sites for ¹²⁵I-vasoactive intestinal polypeptide (VIP), ¹²⁵I-sauvagine (SG, a ligand for corticotropin-releasing hormone receptors) and ¹²⁵I-ornithine vasotocin analog (OVTA, a ligand for the VT3 nonapeptide). For all species and ligands, brain areas that exhibited a seasonal pattern in binding density were characterized by a winter increase. Compared to nonflocking species, seasonally flocking species showed different binding patterns in multiple brain areas. Furthermore, we found that winter flocking was associated with elevated winter ¹²⁵I-VIP binding density in the medial amygdala, as well as ¹²⁵I-VIP and ¹²⁵I-OVTA binding density in the rostral arcopallium. While the functional significance of the avian rostral arcopallium is unclear, it may incorporate parts of the pallial amygdala. Our results point to this previously undescribed area as a likely hot spot of social modulation.

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.…”

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

“…There is evidence, however, that in zebra finches, vasotocin (AVT) neurons in the BSTM strongly promote the tendency of these birds to prefer large groups (Kelly et al., ). Moreover, density of the vasotocin receptor subtype 3 / Oxytocin‐like receptor (VT3) receptor (see Table ) increases in the winter in the field sparrow and dark‐eyed junco, species that flock during this season (Wilson, Goodson, & Kingsbury, ). All together, although in male chickens BSTM AVT neurons respond to social stimuli of positive valence this appears to be restricted to courtship, and VT3 receptor density increases during seasonal flocking in songbirds and this relies on affiliative behaviour, whether and how these findings relate to early affiliative social experiences is unknown.…”

“…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 .…”

“…Grouping behaviour follows seasonal variation in many bird species, with shifts towards territoriality in the breeding season and grouping in the winter. The receptor densities in various brain regions vary seasonally, particularly the densities of receptors for the neuropeptides vasotocin, corticotrophin‐releasing hormone and vasoactive intestinal polypeptide (VIP), and VIP receptor density is associated with seasonal flocking …”