Social information changes stress hormone receptor expression in the songbird brain

Abstract

Social information is used by many vertebrate taxa to inform decision-making, including resource-mediated movements, yet the mechanisms whereby social information is integrated physiologically to affect such decisions remain unknown. Social information is known to influence the physiological response to food reduction in captive songbirds. Red crossbills (Loxia curvirostra) that were food reduced for several days showed significant elevations in circulating corticosterone (a "stress" hormone often responsive to food limitation) only if their neighbors were similarly food restricted. Physiological responses to glucocorticoid hormones are enacted through two receptors that may be expressed differentially in target tissues. Therefore, we investigated the influence of social information on the expression of the mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) mRNA in captive red crossbill brains. Although the role of MR and GR in the response to social information may be highly complex, we specifically predicted social information from food-restricted individuals would reduce MR and GR expression in two brain regions known to regulate hypothalamic-pituitary-adrenal (HPA) activity - given that reduced receptor expression may lessen the efficacy of negative feedback and release inhibitory tone on the HPA. Our results support these predictions - offering one potential mechanism whereby social cues could increase or sustain HPA-activity during stress. The data further suggest different mechanisms by which metabolic stress versus social information influence HPA activity and behavioral outcomes.

Keywords: Corticosterone; Food reduction; Glucocorticoid receptor; Mineralocorticoid receptor; Red crossbill.

Fig. 1

Experimental timeline. Daily food intake (dashed line) was measured for one week prior to the start of the experiment. Body condition and CORT (stars) were collected on days 0 and 14. Activity (camera beam) was filmed daily from days 8 to 14. Food was reduced (hashed box) in the food treatment group beginning on day 10, which marks the change from the pre-treatment to treatment phase of the experiment. Brains were collected on day 14 (open arrow).

Fig. 2

Relationship between body mass and activity during food treatment. The change in size-corrected body mass during food treatment negatively predicted the change in activity (F₃₁ = 8.5, P = 0.007, r² = 0.23). The outlier (open circle) did not influence the statistical significance of the pattern.

Fig. 3

Effect of food and social treatments on plasma corticosterone concentrations and glucocorticoid and mineralocorticoid receptor mRNA expression in captive red crossbills. Food reduction caused an increase in plasma corticosterone whereas social information had no effect (Panel A). There was a significant interaction between food and social treatment such that corticosterone increased hierarchically across groups (Panel B) and was significantly higher in food reduced birds if the social informant was similarly food reduced (i.e., F(f) group), but not significantly so if the social informant was fed ad libitum (i.e., F(a) group). Optical densities for hippocampal MR mRNA (Panels C, D) and paraventricular GR mRNA (Panels E, F) are summarized by food treatment only or social treatment only (Panels C, E). Food treatment had no influence on expression in the brain regions measured, whereas social treatment significantly influenced mRNA expression: birds with food-reduced neighbors had significantly lower MR mRNA expression in the hippocampus (HP) and GR mRNA expression in the paraventricular nucleus (PVN). There was no hierarchical effect or interaction between food and social treatment on either MR or GR expression (Panels D, F). Bars represent group averages with ± sem. Sample sizes given and letter groups denote significantly different groups by Wilcoxon or Kruskal Wallis rank sum test.

Fig. 4

Distribution maps (A & B) and representative photomicrographs of autoradiographs in bright field (C & D) of glucocorticoid receptor (GR) A & C and mineralocorticoid receptor (MR) B & D mRNA expression in the red crossbill brain. Hippocampus (HP), hyperstriatum ventrale (HV), lateral septum (LS), nucleus septalis medialis (NSM), nucleus medialis hypothalamic posterioris (PMH) and paraventricular nucleus (PVN). Commissura anterior (CA), third ventricle (V) and tectum optium (TeO) are provided for reference. Scale bars = 50 μm (C & D).