Cilia directionality reveals a slow reverse movement of principal neurons for positioning and lamina refinement in the cerebral cortex.

IF 3.7 2区 生物学 Q1 DEVELOPMENTAL BIOLOGY
Development Pub Date : 2025-03-01 Epub Date: 2025-03-11 DOI:10.1242/dev.204300
Juan Yang, Soheila Mirhosseiniardakani, Liyan Qiu, Kostandina Bicja, Abigail Del Greco, Kevin JungKai Lin, Mark Lyon, Xuanmao Chen
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Abstract

Currently, not much is known about neuronal positioning and the roles of primary cilia in postnatal neurodevelopment. We show that primary cilia of principal neurons undergo marked changes in positioning and orientation, concurrent with postnatal neuron positioning in the mouse cerebral cortex. Primary cilia of early- and late-born principal neurons in compact layers display opposite orientations, while neuronal primary cilia in loose laminae are predominantly oriented toward the pia. In contrast, astrocytes and interneurons, and neurons in nucleated brain regions do not display specific cilia directionality. We further discovered that the cell bodies of principal neurons in inside-out laminated regions spanning from the hippocampal CA1 region to neocortex undergo a slow 'reverse movement' for postnatal positioning and lamina refinement. Furthermore, selective disruption of cilia function in the forebrain leads to altered lamination and gyrification in the retrosplenial cortex that is formed by reverse movement. Collectively, this study identifies reverse movement as a fundamental process for principal cell positioning that refines lamination in the cerebral cortex and casts light on the evolutionary transition from three-layered allocortices to six-layered neocortices.

纤毛方向性揭示了大脑皮层中主要神经元的缓慢反向运动,用于定位和层状细化。
目前,关于神经元定位和初级纤毛在出生后神经发育中的作用知之甚少。我们发现,主要神经元的初级纤毛在定位和方向上发生了显著的变化,与出生后小鼠大脑皮层神经元的定位同时发生。致密层中早生和晚生的主神经元的初级纤毛方向相反,而松散层中神经元的初级纤毛主要朝向绒毛。相反,星形胶质细胞、中间神经元和有核脑区的神经元不显示特定的纤毛方向性。我们进一步发现,从海马体CA1区到新皮层的内外层合区域的主要神经元的细胞体经历了一个缓慢的“反向运动”,用于产后定位和板层细化。此外,前脑纤毛功能的选择性破坏导致脾后皮层由反向运动形成的层压和旋回改变。总的来说,这项研究确定了反向运动是主要细胞定位的一个基本过程,它改善了大脑皮层的分层,并阐明了从三层异位皮质到六层新皮质的进化转变。
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来源期刊
Development
Development 生物-发育生物学
CiteScore
6.70
自引率
4.30%
发文量
433
审稿时长
3 months
期刊介绍: Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.
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