关键词: Brain-derived neurotrophic factor Estradiol Gliogenesis Neurogenesis Oxytocin Pair bond Progesterone Prolactin Sociosexual behavior

Mesh : Animals Female Male Sex Characteristics Brain-Derived Neurotrophic Factor / metabolism Oxytocin / metabolism Grassland Prolactin / metabolism Progesterone Neurons / metabolism Brain / metabolism Neural Stem Cells / metabolism Arvicolinae / metabolism Cell Proliferation Estradiol / metabolism DNA-Binding Proteins / metabolism

来  源:   DOI:10.1186/s13293-023-00563-2   PDF(Pubmed)

Abstract:
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.
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.
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. Highlights 1. Sociosexual experiences that promote pair bonding (social exposure and social cohabitation with mating) induce changes in the properties of neural stem/progenitor cells isolated from the SVZ in adult prairie voles. 2. Social interactions lead to increased proliferation and induce a bias in the differentiation potential of SVZ-isolated cells in both male and female voles. 3. The differentiation potential of SVZ-isolated cells is conserved under in vitro conditions, suggesting a commitment to a neuronal lineage under a sociosexual context. 4. Hormonal and growth factors treatments (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone) affect the generation and differentiation of neurospheres, with dependencies on sex and sociosexual context. 5. Proliferation and neurogenesis in the SVZ may play a crucial role in establishing, enhancing, maintaining, or accelerating pair bond formation.
In this study, researchers evaluated whether social interactions and copulation induce changes in the proliferation and differentiation of neural progenitor cells in adult male and female voles using an in vitro neurosphere formation assay. The following groups were assigned: control animals without any exposure to another vole outside their litter, another group with social exposure consisting of sensory exposure to a vole of the opposite sex and a third group with social cohabitation and copulation. Forty eight hours after social interactions, cells were isolated from the neurogenic niche subventricular zone (SVZ) and cultured to assess their self-renewal and proliferation abilities to form neurospheres. The results showed in the social interaction groups, a greater number and growth of neurospheres in both males and females. Differentiation capacity was assessed by immunodetection of MAP2 and GFAP to identify neurons or glia, respectively, arise from neurospheres, with an increase in neuronal fate in groups with social interaction. In the second part of the study, the researchers analyzed the effect of different hormone and growth factor treatments and found that the response in both proliferation and differentiation potential may vary depending on the sociosexual context or sex. This study suggests that social interactions leading to pair bond formation alter the properties of SVZ cells, whereby proliferation and neurogenesis may have an impact on the establishment and maintenance of pair bonding.
摘要:
背景:草原田鼠(Microtusochogaster)是一种社会一夫一妻制的啮齿动物,在同居后建立持久的配对关系,有(6小时)或没有(24小时)交配。以前,我们报告说,在雄性田鼠的神经源性壁龛中,社会互动和交配增加了细胞增殖和向神经元命运的分化。我们假设神经发生可能是参与交配诱导的配对键形成的神经可塑性机制。这里,我们评估了从雌性和雄性成年田鼠脑室下区(SVZ)分离出的神经祖细胞(NPCs)的分化潜能,并将其作为社会性经历的函数.将动物分配到以下组中的一组:(1)对照(Co),性天真的雌性和雄性田鼠,与另一个异性田鼠没有接触;(2)社会暴露(SE),暴露于嗅觉的男性和女性,听觉,和来自异性田鼠的视觉刺激,但没有身体接触;和(3)与交配的社会同居(SCM),雄性和雌性田鼠交配以诱导配对形成。随后,从SVZ中分离出NPC,维护,并补充生长因子以在体外形成神经球。
结果:值得注意的是,我们在SE和SCM田鼠中检测到,神经球源性巢蛋白+细胞的增殖更高,以及成熟神经元(MAP2)的增加和神经胶质(GFAP)分化细胞的减少,具有一些性别差异。这些数据表明,当田鼠暴露于导致配对的社交经历时,SVZ的未分化细胞获得了对神经元谱系的承诺,尽管在体外条件下进行了适应,但确定的神经球潜力仍得到保留。最后,我们在不同激素和因子(脑源性神经营养因子,雌二醇,催乳素,催产素,和孕酮);SVZ分离的细胞响应激素或因子而产生神经球并在体外分化成神经元或神经胶质谱系的能力也取决于性别和社会性别。
结论:促进田鼠配对的社会相互作用改变了从SVZ分离的细胞的特性。因此,SE或SCM诱导两性分化潜能的偏见,而SE足以促进男性大脑中SVZ分离细胞的增殖。在女性中,进行交配时增殖增加。下一个问题是,SVZ细胞的增殖和神经发生的增加是否是建立必不可少的可塑性过程,增强,维护,或加速配对键的形成。亮点1.促进配对结合(社会暴露和社会同居与交配)的社会性经历会引起成年草原田鼠从SVZ分离的神经干/祖细胞特性的变化。2.社会相互作用导致雄性和雌性田鼠中SVZ分离细胞的增殖增加并诱导分化潜能的偏差。3.SVZ分离细胞的分化潜能在体外条件下是保守的,表明在社会性背景下对神经元谱系的承诺。4.激素和生长因子治疗(脑源性神经营养因子,雌二醇,催乳素,催产素,和孕酮)影响神经球的产生和分化,依赖于性和社会性背景。5.SVZ中的增殖和神经发生可能在建立中起关键作用,增强,维护,或加速配对键的形成。
在这项研究中,研究人员使用体外神经球形成试验评估了社会交往和交配是否会引起成年雄性和雌性田鼠神经祖细胞增殖和分化的变化.分配了以下组:对照动物,它们的窝外没有任何暴露于另一只田鼠,另一组有社会暴露,包括对异性田鼠的感官暴露,第三组有社会同居和交配。社交互动48小时后,从神经源性小生境脑室下区(SVZ)分离细胞并进行培养以评估其形成神经球的自我更新和增殖能力。结果显示,在社会交往群体中,男性和女性神经球的数量和增长。通过免疫检测MAP2和GFAP以鉴定神经元或神经胶质细胞来评估分化能力,分别,来自神经球,随着社会互动群体中神经元命运的增加。在研究的第二部分,研究人员分析了不同激素和生长因子治疗的效果,发现增殖和分化潜能的反应可能因社会背景或性别而异。这项研究表明,导致配对键形成的社会互动改变了SVZ细胞的特性,其中增殖和神经发生可能对配对的建立和维持有影响。
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