Increased proliferation and neuronal fate in prairie vole brain progenitor cells cultured in vitro: effects by social exposure and sexual dimorphism

• Authors: Daniela Ávila-González, Universidad Nacional Autónoma de México; Italo Romero-Morales, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes; Lizette Caro, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes; Alejandro Martínez-Juárez, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes; Larry Young, Emory University; Francisco Camacho-Barrios, Universidad Nacional Autónoma de México; Omar Martínez-Alarcón, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes; Analía E. Castro, Universidad Nacional Autónoma de México; Raúl G. Paredes, Universidad Nacional Autónoma de México; Néstor F Díaz, Instituto Nacional de Perinatología Isidro Espinosa de los Reyes; Wendy Portillo, Universidad Nacional Autónoma de México
• Journal Title: Biology of Sex Differences
• Volume: Volume 14
• Publisher: Springer Nature | 2023-11-02, Pages 77-None
• Type of Work: Article | Final Publisher PDF
• Publisher DOI: http://doi.org/10.1186/s13293-023-00563-2
• Subjects: Biology, Neuroscience
• Keywords: Pair bond; Neurogenesis; Gliogenesis; Sociosexual behavior; Estradiol; Brain-derived neurotrophic factor; Prolactin; Oxytocin; Progesterone

Abstract

Background The prairie vole (Microtus ochrogaster) is a socially monogamous rodent that establishes an enduring pair bond after cohabitation, with (6 h) or without (24 h) mating. Previously, we reported that social interaction and mating increased cell proliferation and differentiation to neuronal fate in neurogenic niches in male voles. We hypothesized that neurogenesis may be a neural plasticity mechanism involved in mating-induced pair bond formation. Here, we evaluated the differentiation potential of neural progenitor cells (NPCs) isolated from the subventricular zone (SVZ) of both female and male adult voles as a function of sociosexual experience. Animals were assigned to one of the following groups: (1) control (Co), sexually naive female and male voles that had no contact with another vole of the opposite sex; (2) social exposure (SE), males and females exposed to olfactory, auditory, and visual stimuli from a vole of the opposite sex, but without physical contact; and (3) social cohabitation with mating (SCM), male and female voles copulating to induce pair bonding formation. Subsequently, the NPCs were isolated from the SVZ, maintained, and supplemented with growth factors to form neurospheres in vitro. Results Notably, we detected in SE and SCM voles, a higher proliferation of neurosphere-derived Nestin + cells, as well as an increase in mature neurons (MAP2 +) and a decrease in glial (GFAP +) differentiated cells with some sex differences. These data suggest that when voles are exposed to sociosexual experiences that induce pair bonding, undifferentiated cells of the SVZ acquire a commitment to a neuronal lineage, and the determined potential of the neurosphere is conserved despite adaptations under in vitro conditions. Finally, we repeated the culture to obtain neurospheres under treatments with different hormones and factors (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone); the ability of SVZ-isolated cells to generate neurospheres and differentiate in vitro into neurons or glial lineages in response to hormones or factors is also dependent on sex and sociosexual context. Conclusion Social interactions that promote pair bonding in voles change the properties of cells isolated from the SVZ. Thus, SE or SCM induces a bias in the differentiation potential in both sexes, while SE is sufficient to promote proliferation in SVZ-isolated cells from male brains. In females, proliferation increases when mating is performed. The next question is whether the rise in proliferation and neurogenesis of cells from the SVZ are plastic processes essential for establishing, enhancing, maintaining, or accelerating pair bond formation.