Cross-species conservation in the regulation of parvalbumin by perineuronal nets

IF 3.4 3区 医学 Q2 NEUROSCIENCES Frontiers in Neural Circuits Pub Date : 2023-11-29 DOI:10.3389/fncir.2023.1297643
Angela S. Wang, Xinghaoyun Wan, Daria-Salina Storch, Vivian Y. Li, Gilles Cornez, Jacques Balthazart, J. Miguel Cisneros-Franco, Etienne de Villers-Sidani, Jon T. Sakata
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Abstract

Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.

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神经元周围网对副白蛋白的跨物种调控保护
副发光素(PV)神经元在调节神经动态和可塑性方面发挥着不可或缺的作用。因此,了解调控PV表达的因素对于揭示大脑功能的调节因子非常重要。虽然人们已经研究了哺乳动物中 PV 神经元对神经过程的贡献,但对非哺乳动物物种中 PV 功能的了解相对较少,而辨别不同物种中 PV 调控的相似性可以深入了解 PV 神经元作用的进化保护。在这里,我们研究了影响鸣禽和啮齿类动物感觉和运动回路中PV神经元中PV丰度的因素。特别是,我们研究了优先环绕 PV 神经元的细胞外基质--神经元周围网(PNN)--对 PV 丰度的调节程度,以及 PV 和 PNN 表达之间的关系在不同脑区和物种间的差异和发育过程中的变化。我们普遍发现,在啮齿动物和鸣禽中,被 PNNs 包围的皮层 PV 神经元(PV+PNN 神经元)比没有 PNNs 的 PV 神经元(PV-PNN 神经元)富含更多的 PV。有趣的是,鸣禽基底神经节发声部分(X 区)的 PV 和 PNN 表达关系与其他区域不同,PV+PNN 神经元的 PV 表达低于 PV-PNN 神经元。这些关系在鸣禽大脑发声运动回路的发育过程中保持一致。最后,我们发现 PNN 对鸣禽的 PV 表达有因果关系,因为 PNN 的退化会导致 PV 神经元中 PV 表达的减少。这些发现揭示了在鸣禽和啮齿类动物的感觉和运动皮层中,PV和PNN表达之间的保守关系,并表明在鸣禽和啮齿类动物中,PV神经元能以类似的方式调节可塑性和神经动力学。
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来源期刊
CiteScore
6.00
自引率
5.70%
发文量
135
审稿时长
4-8 weeks
期刊介绍: Frontiers in Neural Circuits publishes rigorously peer-reviewed research on the emergent properties of neural circuits - the elementary modules of the brain. Specialty Chief Editors Takao K. Hensch and Edward Ruthazer at Harvard University and McGill University respectively, are supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics and the public worldwide. Frontiers in Neural Circuits launched in 2011 with great success and remains a "central watering hole" for research in neural circuits, serving the community worldwide to share data, ideas and inspiration. Articles revealing the anatomy, physiology, development or function of any neural circuitry in any species (from sponges to humans) are welcome. Our common thread seeks the computational strategies used by different circuits to link their structure with function (perceptual, motor, or internal), the general rules by which they operate, and how their particular designs lead to the emergence of complex properties and behaviors. Submissions focused on synaptic, cellular and connectivity principles in neural microcircuits using multidisciplinary approaches, especially newer molecular, developmental and genetic tools, are encouraged. Studies with an evolutionary perspective to better understand how circuit design and capabilities evolved to produce progressively more complex properties and behaviors are especially welcome. The journal is further interested in research revealing how plasticity shapes the structural and functional architecture of neural circuits.
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