Fatherhood reduces the survival of adult‐generated cells and affects various types of behavior in the prairie vole (Microtus ochrogaster )

Abstract

Motherhood has profound effects on physiology, neuronal plasticity, and behavior. We conducted a series of experiments to test the hypothesis that fatherhood, similarly to motherhood, affects brain plasticity (such as cell proliferation and survival) and various behaviors in the highly social prairie vole (Microtus ochrogaster). In Experiment 1, adult males were housed with their same-sex cage mate (control), single-housed (isolation), or housed with a receptive female to mate and produce offspring (father) for 6 weeks. Fatherhood significantly reduced cell survival (assessed by bromodeoxyuridine labeling), but not cell proliferation (assessed by Ki67 labeling), in the amygdala, dentate gyrus of the hippocampus, and ventromedial hypothalamus, suggesting that fatherhood affects brain plasticity. In Experiment 2, neither acute (20 min) nor chronic (20 min daily for 10 consecutive days) pup exposure altered cell proliferation or survival in the brain, but chronic pup exposure increased circulating corticosterone levels. These data suggest that reduced cell survival in the brain of prairie vole fathers was unlikely to be due to the level of pup exposure and display of paternal behavior, and may not be mediated by circulating corticosterone. The effects of fatherhood on various behaviors (including anxiety-like, depression-like, and social behaviors) were examined in Experiment 3. The data indicated that fatherhood increased anxiety- and depression-like behaviors as well as altered aggression and social recognition memory in male prairie voles. These results warrant further investigation of a possible link between brain plasticity and behavioral changes observed due to fatherhood.

Adult Hippocampal Neurogenesis in Natural Populations of Mammals

“…The reduction in AHN is not necessarily limited to the lactating mother. In Californian mice in which females and males are engaged in the care for pups, both parents show reduced AHN, notably without showing decreased performance in behavioral tests (Glasper et al 2011), similar to the AHN reduction in the social prairie vole fathers (Lieberwirth et al 2013). In wild Namaqua rock mice, previous reproduction led to a permanent reduction in AHN.…”

The birth of new neurons in the maternal brain: Hormonal regulation and functional implications

“…In the California mouse and the prairie vole, fatherhood has been shown to reduce neurogenesis in the DG without affecting neurogenesis in the SVZ or OB (Glasper et al, 2011; Lieberwirth et al, 2013). The reduction in fathers was shown to be specific to cell survival (Lieberwirth et al, 2013; Hyer et al, 2016) and thus suggests that parenthood in general impairs hippocampal neurogenesis by reducing cell proliferation and/or survival.…”

“…The reduction in fathers was shown to be specific to cell survival (Lieberwirth et al, 2013; Hyer et al, 2016) and thus suggests that parenthood in general impairs hippocampal neurogenesis by reducing cell proliferation and/or survival. No studies to date have looked at the potential hormonal mediators reducing neurogenesis during fatherhood.…”

Chemical olfactory signals and parenthood in mammals

“…The functional significance of these reduced proliferation and maturation processes in the MOB in mothers interacting with their lambs remains unknown. It may accentuate a survival-promoting effect by eliminating newborn neurons that are not functional and thus promoting the maturation and integration of new neurons which Lieberwirth et al (2013) participate in learning by reducing cell competition. Computational studies support this hypothesis by showing that the rate of cell proliferation and cell survival contribute to the stability of the neural activity in the network (Butz et al, 2006;Lehmann et al, 2005).…”

“…The prairie vole is a socially monogamous species that displays spontaneous biparental behavior toward its offspring (Lonstein and De Vries, 1999). After six weeks of cohabitation with a female to mate and produce offspring, male prairie voles did not show any change in cell survival in the MOB (Lieberwirth et al, 2013). However, because the phenotype of survival cells was not characterized, significant changes in either neuroblasts or mature neurons cannot be ruled out.…”