Social information changes the brain

Abstract

Social animals live in complex physical and social environments requiring them to attend and rapidly respond to social and environmental information by changing their behavior. A key social influence is rank or status, a ubiquitous element in animal societies. Rank typically regulates access to reproduction and other resources, among other consequences for individuals. Because reproduction is arguably the most important event in any animals' life, understanding how reproduction is regulated by social status and related physiological factors can instruct our understanding of evolutionary change. This article reviews evidence from a model social system in which reproduction is tightly controlled by social status. Surprisingly, changes in social status have rapid and profound effects over very short time scales and radically alter overt behavior, as well as physiological, cellular, and molecular factors that regulate reproductive capacity.

Fig. 1.

Body patterns for typical dominant (territorial; Upper Left) and nondominant (nonterritorial; Lower Left) A. burtoni males, and sexually receptive, gravid (Upper Right) and mouthbrooding (Lower Right) females. Dominant males have a bright basic color (yellow or blue), with distinct yellow-orange egg-spots on their anal fins, dark forehead stripes, a dark opercular spot on the caudal edge of the gill cover, a dark lachrymal stripe or eye-bar extending from the eye to the lower jaw, and a bright orange-red patch on the humeral scales. Subordinate males are pale and similar in color to females. Females cycle between a gravid and receptive phase, in which they develop distended abdomens from growing oocytes, and a mouthbrooding phase, in which their mouths distend to accommodate the developing young inside the mouth. Modified from ref. .

Fig. 2.

Rapid increase in mRNA expression of the immediate early gene egr-1 in GnRH1 neurons and throughout the nuclei of the SBN in males transitioning from subordinate to dominant status. (A) Photomicrograph of egr-1 silver grains (small black dots; in situ hybridization) on GnRH1 neurons (arrows) in the anterior parvocellular preoptic nucleus (aPPn) of a male A. burtoni. (Scale bar, 10 μm.) (B) Egr-1 silver grain density (mean ± SE) of the entire aPPn in subordinate (Sub), ascending (Ascend), and dominant (Dom) males shows greater egr-1 staining at 20 min after social opportunity in ascending males compared with the stable social states. (C) GnRH1 neuron number (open circles) and egr-1 silver grain density (filled circles) (mean ± SE) within adjacent sections of the aPPn to show the greater egr-1 staining in sections that have more GnRH1 neurons. Modified from ref. .

Fig. 3.

Schematic illustration of the HPG axis showing genes and peptides regulated in males by the occasion of social opportunity. Information about social status is processed by the brain, which, in turn communicates with the gonads via the HPG axis. Physiological signals regulated by the ascent in status are indicated in the table on the right. All these are up-regulated as a male becomes dominant (D) and down-regulated when a male becomes nondominant. For more detail, see ref. .

Fig. 4.

Social opportunity rapidly increases egr-1 mRNA levels (measured by quantitative PCR in nuclei of the SBN. Relative mRNA levels (normalized to the geometric mean of the reference genes 18s and g3pdh) were higher in ascending males compared with the stable subordinate and dominant male states. Different letters indicate significant differences among social groups at P < 0.05. ns, not significant. ATn, anterior tuberal nucleus; Ce, cerebellum; Dm, medial part of the dorsal telencephalon; Dl, lateral part of the dorsal telencephalon; Pit, pituitary; POA, preoptic area; Vs, supracommissural nucleus of the ventral telencephalon; VTn, ventral tuberal nucleus; Vv, ventral nucleus of the ventral telencephalon. Reproduced from ref. .

Fig. 5.

Relative levels of mRNA expression of cfos (A) and egr-1 (B) for each of the six nodes of the SBN, plotted as a function of whether females saw their preferred males win (filled bars) or lose (open bars) a fight. Asterisks above pairs of values (mean + SE) indicate significant differences (t tests, corrected for multiple comparisons). Between A and B is a schematic sagittal section of the A. burtoni brain showing the approximate locations of the microdissected brain regions sampled. AH, anterior hypothalamus; Cce, cerebellum; Dm, medial part of the dorsal telencephalon; Dl, lateral part of the dorsal telencephalon; LS, lateral septum; PAG, periaqueductal gray; R, raphe nucleus; Vm, ventromedial hypothalamus. Modified from ref. .