Effects of Mating and Social Exposure on Cell Proliferation in the Adult Male Prairie Vole (Microtus ochrogaster)

Abstract

Microtus ochrogaster is a rodent with a monogamous reproductive strategy characterized by strong pair bond formation after 6 h of mating. Here, we determine whether mating-induced pair bonding increases cell proliferation in the subventricular zone (SVZ), rostral migratory stream (RMS), and dentate gyrus (DG) of the hippocampus in male voles. Males were assigned to one of the four groups: (1) control: males were placed alone in a clean cage; (2) social exposure to a female (SE m/f): males that could see, hear, and smell a sexually receptive female but where physical contact was not possible, because the animals were separated by an acrylic screen with small holes; (3) social exposure to a male (SE m/m): same as group 2 but males were exposed to another male without physical contact; and (4) social cohabitation with mating (SCM): males that mated freely with a receptive female for 6 h. This procedure leads to pair bond formation. Groups 2 and 3 were controls for social interaction. Male prairie voles were injected with 5-bromo-2′-deoxyuridine (BrdU) during the behavioral tests and were sacrificed 48 h later. Brains were processed to identify the new cells (BrdU-positive) and neuron precursor cells (neuroblasts). Our principal findings are that in the dorsal region of the SVZ, SCM and SE m/f and m/m increase the percentage of neuron precursor cells. In the anterior region of the RMS, SE m/f decreases the percentage of neuron precursor cells, and in the medial region SE m/f and m/m decrease the number of new cells and neuron precursor cells. In the infrapyramidal blade of the subgranular zone of the DG, SE m/m and SCM increase the number of new neuron precursor cells and SE m/m increases the percentage of these neurons. Our data suggests that social interaction, as well as sexual stimulation, leads to pair bonding in male voles modulating cell proliferation and differentiation to neuronal precursor cells at the SVZ, RMS, and DG.

Plasticity of the paternal brain: Effects of fatherhood on neural structure and function

“…Moreover, as described above, exposure to pups for 20 min increases neurogenesis in the dentate gyrus of virgin male prairie voles, similar to effects of fatherhood (Ruscio et al., 2008). Neurogenesis in male prairie voles can also be affected by brief (6 hr) exposure to an ovariectomized, estrogen‐treated (i.e., sexually receptive but infertile) female, even when physical contact and mating are prevented, as well as by longer (48 hr) cohabitation with such a female (Castro et al., 2020). These findings suggest that different components of reproductive experience can affect different aspects of neural plasticity and, in some cases, may have redundant effects on the brain.…”

Brain functional networks associated with social bonding in monogamous voles

“…The NAcc–mPFC pathway has been widely characterized as modulating reward-seeking, goal-oriented behavior ( Gill et al, 2010 ), and the mPFC and the amygdala are extensively interconnected and tune the expression of fear and anxiety ( Liu et al, 2020 ; Marek et al, 2013 ). The involvement of the MeA–VP hints modulation of sex-related social interaction, particularly via chemosensory stimuli (MOB-DG) ( Castro et al, 2020 ; Liu et al, 2014 ).…”

Characterization of social behavior in the spiny mouse, Acomys cahirinus

“…obs.). For most species, social approach/investigation/recognition tests using stimulus chambers with 1‐cm diameter holes in one wall are sufficient to maintain the subject's interest in the stimulus animals (Castro et al, 2020; Kelly et al, 2020). In A .…”

“…obs.). For most species, social approach/investigation/recognition tests using stimulus chambers with 1-cm diameter holes in one wall are sufficient to maintain the subject's interest in the stimulus animals (Castro et al, 2020;Kelly et al, 2020). In A. cahirinus, however, we required access holes surrounding the entire stimulus container that were at least 2 cm in diameter in order for the animals to engage in the social investigation for more than a few seconds.…”