Dominance hierarchy influences adult neurogenesis in the dentate gyrus

Abstract

Many mammalian species form dominance hierarchies, but it remains unknown whether differences in social status correspond to structural differences in the brain. Stressful experiences may arise naturally during the establishment of dominance, and stress has been linked to adult neurogenesis in the hippocampus. To determine whether position in a dominance hierarchy leads to changes in adult neurogenesis in the hippocampus, we examined the brains of rats housed in a visible burrow system (VBS), a seminaturalistic environment with opportunities for social interaction. Dominance hierarchies emerged among the males in all colonies within 3 d of living in the VBS. Although cell proliferation in the dentate gyrus did not differ between the groups, more new neurons were observed in the dentate gyrus of the dominant males compared with both subordinates and controls. Dominant and subordinate animals showed similar basal, stress, and recovery from stress levels of corticosterone, as well as similar thymus, adrenal gland, and body weights, suggesting that variables other than stress are responsible for the observed changes in adult neurogenesis. The differences in brain structure persisted among the animals that had no access to the burrow system after the dominance hierarchy stabilized, suggesting that social status rather than living in a complex environment accounts for the effect of dominance on adult neurogenesis.

Figure 1.

A, Diagram of the visible burrow system, a seminaturalistic environment for the rat: a large enclosure (in gray), surrounded by tunnels and chambers of different size (in purple). B, New cells in the dentate gyrus of subordinate (top left) and dominant (bottom left) animals. More BrdU-labeled cells were observed in the dentate gyrus of dominant relative to subordinate and control animals (controls not shown). Confocal laser-scanning images of cells in the GCL of animals living in the VBS. Double-labeling of BrdU (red) with a neuronal marker NeuN (green). Another BrdU-labeled cell is positive for TUJ1 (green), a marker of both immature and mature neurons. The majority of BrdU-labeled cells colabeled with one of the neuronal markers, and the rate of colabeling did not vary across groups. Proliferating cells in the GCL of animals living in the VBS. No differences were detected in the number of cells expressing endogenous markers of cell proliferation, Ki-67, or phosphorylated-histone-H3. Scale bar, 10 μm. C, BrdU counts in the dentate gyrus of dominant, subordinate, and cage control animals. Two weeks after a single BrdU injection, dominant animals had more BrdU-labeled cells in the dentate gyrus compared with subordinate animals and cage controls. This difference was maintained in animals whether or not they had access to a more enriched environment during the survival time after BrdU injection. Bars represent mean ± SEM. Asterisks represent significant difference from subordinates and controls; p < 0.05. D, Plasma corticosterone (CORT) response to restraint stress. Samples were collected before restraint, after 0.5 hr long restraint, and after 3.5 hr of recovery. Corticosterone values did not differ between dominant and subordinate animals. Bars represent mean ± SEM.