Development of ocular dominance columns across rodents and other species: revisiting the concept of critical period plasticity

IF 3.4 3区 医学 Q2 NEUROSCIENCES
Toru Takahata
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Abstract

The existence of cortical columns, regarded as computational units underlying both lower and higher-order information processing, has long been associated with highly evolved brains, and previous studies suggested their absence in rodents. However, recent discoveries have unveiled the presence of ocular dominance columns (ODCs) in the primary visual cortex (V1) of Long-Evans rats. These domains exhibit continuity from layer 2 through layer 6, confirming their identity as genuine ODCs. Notably, ODCs are also observed in Brown Norway rats, a strain closely related to wild rats, suggesting the physiological relevance of ODCs in natural survival contexts, although they are lacking in albino rats. This discovery has enabled researchers to explore the development and plasticity of cortical columns using a multidisciplinary approach, leveraging studies involving hundreds of individuals—an endeavor challenging in carnivore and primate species. Notably, developmental trajectories differ depending on the aspect under examination: while the distribution of geniculo-cortical afferent terminals indicates matured ODCs even before eye-opening, consistent with prevailing theories in carnivore/primate studies, examination of cortical neuron spiking activities reveals immature ODCs until postnatal day 35, suggesting delayed maturation of functional synapses which is dependent on visual experience. This developmental gap might be recognized as ‘critical period’ for ocular dominance plasticity in previous studies. In this article, I summarize cross-species differences in ODCs and geniculo-cortical network, followed by a discussion on the development, plasticity, and evolutionary significance of rat ODCs. I discuss classical and recent studies on critical period plasticity in the venue where critical period plasticity might be a component of experience-dependent development. Consequently, this series of studies prompts a paradigm shift in our understanding of species conservation of cortical columns and the nature of plasticity during the classical critical period.
啮齿动物和其他物种眼球优势柱的发育:重新审视关键期可塑性的概念
皮质柱被认为是低阶和高阶信息处理的基础计算单元,它的存在长期以来一直与高度进化的大脑有关,以前的研究表明啮齿类动物中不存在皮质柱。然而,最近的研究发现,在长-埃文斯大鼠的初级视觉皮层(V1)中存在眼优势柱(ODCs)。这些区域显示出从第 2 层到第 6 层的连续性,证实了它们是真正的 ODC。值得注意的是,在与野生大鼠亲缘关系密切的挪威褐鼠身上也观察到了ODCs,这表明ODCs在自然生存环境中的生理意义,尽管白化大鼠体内缺乏ODCs。这一发现使研究人员能够采用多学科方法,利用涉及数百个个体的研究来探索皮质柱的发育和可塑性--这在食肉动物和灵长类动物中是一项具有挑战性的工作。值得注意的是,发育轨迹因研究内容的不同而不同:基因-皮层传入终端的分布表明,在睁眼之前,ODCs 就已经成熟,这与食肉动物/灵长类动物研究中的主流理论一致;而对皮层神经元尖峰活动的研究则显示,直到出生后第 35 天,ODCs 才发育成熟,这表明功能性突触的延迟成熟依赖于视觉经验。在以往的研究中,这一发育间隙可能被认为是眼优势可塑性的 "关键期"。在本文中,我总结了大鼠眼支配突触和基因皮层网络的跨物种差异,然后讨论了大鼠眼支配突触的发育、可塑性和进化意义。我讨论了临界期可塑性的经典研究和最新研究,临界期可塑性可能是经验依赖性发育的一个组成部分。因此,这一系列研究促使我们对大脑皮层柱的物种保护和经典关键期可塑性本质的理解发生了范式转变。
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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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