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.

Keywords: grouping behavior; mesotocin; neuroecology; oxytocin; vasopressin; vasotocin.

FIGURE 1

Representative photomicrographs of ¹²⁵I-ornithine vasotocin analog (¹²⁵I-OVTA; A,C,E,G,I,K,M) or ¹²⁵I-linearized vasopressin antagonist (¹²⁵I-LVA; B,D,F,H,J,L,N) binding in the brain of a house sparrow (images correspond to individual “B” in Table 2).

FIGURE 2

Representative photomicrographs of ¹²⁵I-ornithine vasotocin analog (¹²⁵I-OVTA; A,C,E,G,I,K,M,O) or ¹²⁵I-linearized vasopressin antagonist (¹²⁵I-LVA; B,D,F,H,J,L,N,P) binding in the brain of a European starling (images correspond to individual “B” in Table 3).

FIGURE 3

Representative photomicrographs of ¹²⁵I-ornithine vasotocin analog (¹²⁵I-OVTA; A,C,E,G,I,K,M) or ¹²⁵I-linearized vasopressin antagonist (¹²⁵I-LVA; B,D,F,H,J,L,N) binding in the brain of a rock dove (images correspond to individual “B” in Table 4).

FIGURE 4

Photomicrographs showing diverse binding patterns of ¹²⁵I-ornithine vasotocin analog (¹²⁵I-OVTA) in medial striatum of two female rock doves. For the bird represented by the right panel (B), incubation with ¹²⁵I-linearized vasopressin antagonist (¹²⁵I-LVA) produced similar ring-like binding in the medial striatum, although the signal was less intense. Images in the left (A) and right (B) panels correspond with individuals “B” and “C,” respectively, in Table 4. HA, apical hyperpallium; HD, densicellular hyperpallium.

FIGURE 5

Effects of a competitor, Manning Compound (MC) on mean optical binding density (+SEM) for ¹²⁵I-OVTA and ¹²⁵I-LVA in the lateral septum of a house sparrow (A, ¹²⁵I-OVTA alone; B, ¹²⁵I-OVTA plus MC; C, ¹²⁵I-LVA alone; D, ¹²⁵I-LVA plus MC). (A–D) Correspond to individual “C” in Table 2. Symbols above brackets in the chart (E) indicate significant and near significant differences between binding conditions (^∗∗∗P < 0.001, ^∗∗P < 0.01, ^‡P = 0.05).

FIGURE 6

Effects of a competitor, Manning Compound (MC) on mean optical binding density (+SEM) for¹²⁵I-OVTA and ¹²⁵I-LVA in the lateral septum of a European starling (A, ¹²⁵I-OVTA alone; B, ¹²⁵I-OVTA plus MC; C, ¹²⁵I-LVA alone; D, ¹²⁵I-LVA plus MC). (A–D) Correspond to individual “B” in Table 3. Asterisks above brackets in the chart (E) indicate significant differences between binding conditions (^∗∗∗P < 0.001, ^∗P < 0.05).

FIGURE 7

Effects of a competitor, MC on mean optical binding density (+SEM) for¹²⁵I-OVTA and ¹²⁵I-LVA in the lateral septum of a rock dove (A, ¹²⁵I-OVTA alone; B, ¹²⁵I-OVTA plus MC; C, ¹²⁵I-LVA alone; D, ¹²⁵I-LVA plus MC). (A–D) Correspond to individual “C” in Table 4. Asterisks above brackets in the chart (E) indicate significant differences between binding conditions (^∗∗∗P < 0.001, ^∗∗P < 0.01).

FIGURE 8

Effects of a competitor, MC on mean optical binding density (+SEM) for¹²⁵I-OVTA and ¹²⁵I-LVA in the arcopallium of a house sparrow (A, ¹²⁵I-OVTA alone; B, ¹²⁵I-OVTA plus MC; C, ¹²⁵I-LVA alone; D, ¹²⁵I-LVA plus MC). (A–D) Correspond to individual “B” in Table 2. Asterisks above brackets in the chart (E) indicate significant differences between binding conditions (^∗∗P < 0.01, ^∗P < 0.05).

FIGURE 9

Effects of a competitor, MC on mean optical binding density (+SEM) for ¹²⁵I-OVTA and ¹²⁵I-LVA in the arcopallium of a European starling (A, ¹²⁵I-OVTA alone; B, ¹²⁵I-OVTA plus MC; C, ¹²⁵I-LVA alone; D, ¹²⁵I-LVA plus MC). (A–D) Correspond to individual “B” in Table 3. Asterisks above brackets in the chart (E) indicate significant differences between binding conditions (^∗∗P < 0.01).