Jones Stephanie M, Sleiman Sarah Jo, McCann Katharine E, Jarmusch Alan K, Alexander Georgia M, Dudek Serena M
Neurobiology Laboratory, National Institute of Environmental Health Sciences, Division of Intramural Research, National Institute of Health, Research Triangle Park, NC, 27709, USA.
Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC, 27599, USA.
Neuropsychopharmacology. 2024 Dec;50(2):378-387. doi: 10.1038/s41386-024-01971-7. Epub 2024 Sep 5.
In the brain, the hippocampus is enriched with mineralocorticoid receptors (MR; Nr3c2), a ligand-dependent transcription factor stimulated by the stress hormone corticosterone in rodents. Recently, we discovered that MR is required for the acquisition and maintenance of many features of mouse area CA2 neurons. Notably, we observed that immunofluorescence for the vesicular glutamate transporter 2 (vGluT2), likely representing afferents from the supramammillary nucleus (SuM), was disrupted in the embryonic, but not postnatal, MR knockout mouse CA2. To test whether pharmacological perturbation of MR activity in utero similarly disrupts CA2 connectivity, we implanted slow-release pellets containing the MR antagonist spironolactone in mouse dams during mid-gestation. After confirming that at least one likely active metabolite crossed from the dams' serum into the embryonic brains, we found that spironolactone treatment caused a significant reduction of CA2 axon fluorescence intensity in the CA1 stratum oriens, where CA2 axons preferentially project, and that vGluT2 staining was significantly decreased in both CA2 and dentate gyrus in spironolactone-treated animals. We also found that spironolactone-treated animals exhibited increased reactivity to novel objects, an effect similar to what is seen with embryonic or postnatal CA2-targeted MR knockout. However, we found no difference in preference for social novelty between the treatment groups. We infer these results to suggest that persistent or more severe disruptions in MR function may be required to interfere with this type of social behavior. These findings do indicate, though, that developmental disruption in MR signaling can have persistent effects on hippocampal circuitry and behavior.
在大脑中,海马体富含盐皮质激素受体(MR;Nr3c2),这是一种在啮齿动物中受应激激素皮质酮刺激的配体依赖性转录因子。最近,我们发现MR对于小鼠CA2区神经元许多特征的获得和维持是必需的。值得注意的是,我们观察到,囊泡谷氨酸转运体2(vGluT2)的免疫荧光,可能代表来自乳头体上核(SuM)的传入神经,在胚胎期而非出生后的MR基因敲除小鼠CA2区被破坏。为了测试子宫内MR活性的药理学扰动是否同样会破坏CA2区的连接性,我们在妊娠中期给母鼠植入了含有MR拮抗剂螺内酯的缓释微丸。在确认至少一种可能的活性代谢物从母鼠血清进入胚胎大脑后,我们发现螺内酯处理导致CA2轴突在CA1层原层中的荧光强度显著降低,CA2轴突优先投射到该区域,并且在螺内酯处理的动物中,CA2区和齿状回中的vGluT2染色均显著降低。我们还发现,螺内酯处理的动物对新物体的反应性增加,这一效应与胚胎期或出生后靶向CA2区的MR基因敲除所见相似。然而,我们发现治疗组之间在对社交新奇性的偏好上没有差异。我们推断这些结果表明,可能需要MR功能的持续或更严重破坏才能干扰这种社交行为类型。不过,这些发现确实表明,MR信号的发育性破坏会对海马回路和行为产生持久影响。