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Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear.
Brain, Behavior and Evolution ( IF 2.1 ) Pub Date : 2018-11-09 , DOI: 10.1159/000494050
Christine Köppl 1, 2 , Viviane Wilms 3 , Ian John Russell 4 , Hans Gerd Nothwang 5, 6
Affiliation  

The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K+) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K+) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K+) relative to the perilymph. Yet only in land vertebrates does (K+) exceed (Na+). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K+) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans.

中文翻译:

脊椎动物内耳内淋巴分泌的演变和内淋巴电位的产生。

现存脊椎动物的耳朵反映了多个独立的进化轨迹。例子包括中耳或哺乳动物耳蜗的独特特化。脊椎动物内耳之间的另一个显着差异涉及内淋巴电位大小的差异。这在内耳的前庭和听觉部分之间以及不同脊椎动物的听觉外围之间都不同。在这里,我们比较了脊椎动物不同内脏器官的细胞和分子机制。我们从侧线和前庭系统开始,因为它们可能代表多形性条件,然后回顾不同脊椎动物听觉内器官的情况。所有三个系统都包含沐浴在高 (K+) 环境中的毛细胞。浅表侧线神经瘤沐浴在由复杂的凝胶状杯状体提供的电保持高 (K+) 微环境中。这与正的内电势有关。这是否是侧线的特殊或普遍特征以及可能的前庭杯状体仍有待发现。前庭系统代表具有内淋巴的封闭系统,其特征在于相对于外淋巴增强的 (K+)。然而,只有在陆地脊椎动物中,(K+) 才超过 (Na+)。内淋巴电位范围从 +1 到 +11 mV,尽管我们注意到有趣的报告,即半规管壶腹壶腹中高达 +70 mV 的显着更高的电位。类似地,在听觉系统中,观察到高 (K+)。然而,与前庭系统相比,正内淋巴电位在脊椎动物之间变化更大,范围从接近 0 mV 到大约 +100 mV。在内耳中产生内淋巴的组织在细胞类型和位置上表现出相当大的差异。鱼中所谓的暗细胞和可能同源的离子细胞似乎是常见的元素,但总是至少存在一种额外的细胞类型。为了激发该领域的研究,我们提出了对这些细胞类型的分类并讨论了潜在的进化关系。它们的分子库在很大程度上是未知的,为未来的研究提供了进一步的沃土。最后,我们建议增加内淋巴潜能的最终选择压力,如在哺乳动物中观察到的,在鸟类中观察到的程度较小,是专门维持高频率的毛细胞受体电位的交流分量。总之,我们为未来研究内耳不同隔室中内淋巴的分子和细胞基础的方向确定了有趣的问题。这些答案将为包括人类在内的许多物种所必需的感觉器官的进化和发育过程提供重要的见解。
更新日期:2019-11-01
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